Pathways in the Emergence of Developmental Neuroethology: Antecedents to Current Views of Neurobehavioral Ontogeny Ronald W. Oppenheim Department of Neurobiology and Anatomy and Neuroscience Program, Bowman Gray School of Medicine, Wake Forest University, Winston-Salem, North Carolina 27103

SUMMARY The historical forces that have contributed to our current views of neurobehavioral development (and thus to the fields of developmental psychobiology and neuroethology) are many and varied. Although similar statements might be made about almost any field of science, it is in particular true of this field, which represents a kind of mongrel discipline derived from at least three major sources (psychology, embryology, and neuroscience) and several more minor ones (including developmental psychology and psychiatry, psychoanalysis, education, zoology, ethology, and sociology). Although I attempt to demonstrate here how each of these sources may have influenced the emergence of a unified field of developmental psychobiology or developmental neuroethology, because the present article represents the first attempt of which I am aware to trace the history of these fields I am certain that there is considerable room for improvement, correction, and revision of the views expressed here. Accordingly, I consider this inaugural effort a kind of reconnaissance intended to trace a necessarily imperfect historic path for others to follow and im-

prove upon. In the final analysis, I will be satisfied if this article only serves to underscore two related points: first is the value derived from historical studies of contemporary issues in development, and the second concerns the extent to which our current ideas and concepts about neurobehavioral development, ideas often considered new and contemporary, were already well known to those who came before us. The first point underscores the arguments expressed in the Introduction that the present must always be reconciled with the past, for the past is never entirely past. The second point returns full circle to an important thought expressed in the opening quotation to this article, namely, that even though our historic predecessors lacked much of the empirical facts available to us they were nonetheless able to attain a surprisingly deep understanding of neurobehavioral ontogeny. o 1992

. . . the ruling modes of thought of our own age, which some among us are prone to regard as clear and coherent and firmly grounded and final, are unlikely to appear in the eyes of posterity to have any ofthese attributes. The adequate record of even the confusions of our forbears may help not only to clarify those confusions, but to engender a salutary doubt whether we are wholly im-

mune from different but equally great confusions. For though we have more empirical information at our disposal we have not different or better minds; and it is, after all, the action of the mind upon facts that makes both philosophy and science-and, indeed, largely makes ‘facts.’ (Lovejoy, 1936, p. 17)

Received August 12, 1991 ; accepted August 12, 1991 Journal of Neurobiology, Vol. 23, No. 10, pp. 1370-1403 ( 1992) 0 1992 John Wiley & Sons, Inc. CCC 0022-3034/92/101370-34

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John Wiley & Sons, Inc.

Keywords: history, developmental neurobiology, develop-

mental psychobiology, child psychology, developmental psychology.

INTRODUCTION An Historical Perspective In learning a new discipline or body of facts, it can often be exceedingly helpful if one understands

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how, as well as why, the issues, questions, and problems that are of current interest attained their present status. When one becomes familiar with prior controversies, learns of the pivotal conceptual and technical advances, and is introduced to the individuals who have influenced the development of a field, the present often becomes more meaningful. Further, as often noted, history can serve to invoke humility in the sense that one often discovers the germ, if not the full-blown expression, of ideas that one had previously considered new and original. As Andr6 Gide is reputed to have said, “Everything that needs to be said has already been said. But since no one was listening, everything must be said again and again.” Although when viewed in retrospect history appears as a record of the inevitable, in fact there is little in history that could not have been done differently. Thus, one of the functions of the study of history is to serve as a guide or touchstone for the future. Perhaps this point is nowhere more succinctly stated than in the quote from Shakespeare’s “The Tempest,” inscribed on the National Archives Building in Washington, which says, “What is Past is Prologue.” Although the present account of this field focuses on the contributions of individuals, this is not meant to imply that great men make history in isolation. Rather, I have chosen this format as a convenient way of discussing trends, movements, and ideas, always recognizing, however, that it is great ideas (and their transformation over time), interacting with the general social and scientific milieu, that, in the final analysis, makes intellectual history.

Neuroethology and Development The field of neuroethology is concerned with understanding naturally occurring behaviors and their underlying neural structure and function in such a way that it becomes possible to relate the activity of interconnected nerve cells to coordinated patterns of movement (behavior). It has often been noted that a major difference between the neurobiological vs. neuroethological approach is that the neurobiologist focuses on a “bottom-up” analysis whereas the neuroethologist prefers a “top-down’’ analysis, beginning with an adaptively significant behavior pattern and then proceeding to neurobiological investigations of the behavior. Although the term neuroethology first came into use in the 1960s, the conceptual framework that

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continues to guide the field even today can be traced in a rather direct line back to the work of E. von Holst in the 1930s and later (Ewert, 1980). However, this is only one of many lineages that fostered the development of modern neuroethology. Neuroethology was not the simple outgrowth of the ideas of a specific school or individual but rather represents a unique interdisciplinary field whose roots can be traced to influences arising from several different and separate fields. However, because my goal in this essay is to discuss the origins of developmental neuroethology (which can be considered a separate field) the history of neuroethology, per se, is not my focus here. Except for its strong conceptual and historic ties to ethology, developmental neuroethology represents an even stronger example of a field that is not merely the outgrowth of a particular individual or group, or of particular controversies, methods, or schools. In fact, despite the title of this special issue it seems to me to be somewhat of an exaggeration to even consider it a separate field at the present time. Except for the present volume, the only time I recall seeing the term developmental neuroethology used was in an article by Lang, Costello, Govind, and Greene ( 1977). Notwithstanding these comments, I believe the present volume could play an important role in fostering developmental studies in neuroethology. By coopting the name developmental neuroethology, by providing case histories of how the issues to be addressed can be studied, and by creating challenges for the future, the present volume may be remembered as the midwife that gave birth to a new discipline in behavioral biology. If this were to occur, it would certainly be cause for celebration. However, there would still remain the nagging question of why it has taken so long for neuroethology as a whole to realize the value of a developmental approach. Although I shall discuss this question further below, I feel compelled to comment here that, in the past, with a few notable exceptions (e.g., Bekoff, 1981; Provine, 1984; Heiligenberg, 1991 and this volume; Fentress, this volume), neuroethologists have, by and large, ignored developmental issues. The literature on developmental studies in neuroethology is sparse and many popular textbooks and review articles in the field fail to discuss developmental problems at all (e.g., Alcock, 1979; Camhi, 1984; Hoyle, 1984; Young, 1989). In light ofthese comments concerning the apparent lack of any speciJc antecedents to developmental neuroethology, one may reasonably ask what I

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could possibly write about in this essay. The answer is simple. To paraphrase an old aphorism, “no field of neuroscience is an island in and of itself.” To the extent that a field of developmental neuroethology exists today (and, more importantly, to the extent that it will remain viable and prosper in the future), the field has been inexorably guided and influenced by ideas, concepts, theories, and data derived from diverse sources extending back a long time in history. It is these sources that I discuss and evaluate in the present essay.

THE “PREMODERN” PERIOD: ANTIQUITY TO THE 20TH CENTURY

Early Philosophical and Educational Influences

It has been said of psychology that it has a long past but only a short history (Ebbinghaus, 1909). By this, it is meant that many of the basic issues in psychology have been the subject of intellectual and philosophical inquiry since antiquity, whereas the scientific (i.e., experimental) approach to psychology only began in earnest in the last century. The same is true of developmental disciplines, including the study of neurobehavioral development. The modern period of scientific inquiry into behavioral development has its roots, in part at least, in the changing attitudes and concepts of human infancy and childhood in Western civilization. Only when this period of life began to be Valued as important in its own right, in the sense that it was thought to make fundamental contributions to later behavior, could there be any notable progress in our understanding of the details of early stages of behavioral development. The current scientific and cultural belief of Western civilization that infants and children are not merely miniature biologic or psychological replicas of adults is of relatively recent origin (Oppenheim, 1981, 1984). We presently conceive of infancy and childhood as qualitatively special and separate periods or stages that are adaptively distinct and that, in part, follow different psychological rules, obey unique neurobiological laws, and are organized according to different guidelines from those of later stages (Hall and Oppenheim, 1987). Although this view of childhood has been slowly developing over the past 400 years, it is nonetheless true that prior to the latter part of the 19th century Western soci-

ety (especially most intellectuals and scientists of this period ) would have found our present concern for early behavioral development rather curious. Accordingly, infancy and early childhood was often considered a period to be ignored or, at best, tolerated as a necessary but relatively unimportant step in the path to adulthood. But, to study or examine this period of life as one might study astronomy, medicine, or philosophy was seldom senously considered. Perhaps one of the most pervasive and long-lasting philosophical ideas that influenced the establishment of this attitude in Western civilization, in particular with regard to the systematic educational training of young children, stems from ancient Greece. As originally stated by Plato and Aristotle, the Greeks held that prior to the onset of intellectual reasoning (thought to begin at about age 7 ) any attempt at formal education or systematic training was a waste of effort (Ulich, 1959; Lodge, 1970). Although the Roman educator Quintillian later promoted the view that systematic education of children should begin in infancy (Smail, 1938), the Platonic approach proved to be the more popular and consequently dominated Western attitudes toward infancy, childhood, and early behavioral development for centuries. It is also worth noting that the pervasive belief in Western culture that the early years-in this case beginning at ages 6 or 7-are critically formative also stems from Plato. In The Republic, Plato states, And the first step, as you know, is always what matters most, particularly when we are dealing with those who are young and tender. That is the time when they are taking shape and when any impression we choose to make leaves a permanent mark.

It has been argued that during this long premodern period even the infants and children of the privileged classes were apparently provided with little more than caretaking attention, and even this was usually assumed by slaves, servants, or other surrogates rather than by parents. According to this view, the high rate of infant mortality made it necessary for a child to “prove” itself, so to speak, by surviving for a few years before parents and other adults felt compelled to devote any significant attention to its education or training (Aries, 1962;de Mause, 1974; Stone, 1976). This is not to imply that in the past many, perhaps most, parents did not love their children or recognize their special physical and emotional needs (e.g., Shahar, 1991) but rather only serves to emphasize the different

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intellectual conceptions of this developmental period that were held at different times in history. Even after having survived to the age of 6 or 7 years, however, childhood was seldom dealt with as a special or unique stage in the life cycle. Although it was obviously recognized that, with regard to size, strength, experience, etc., the child was different from grown men and women, for all practical purposes the child of 6 or 7 was often viewed as an undersized adult. Children were dressed as adults and forced, or expected, to partake of adult activities. Such attitudes and practices were not conducive to serious inquiries into the nature of behavioral development, especially development during infancy and early childhood. By the close of the 17th century, this perspective of early childhood was beginning to show signs of change, especially among the wealthy aristocrats and the better educated middle class. John Locke’s influential book, On Education, published in 1693, for instance, was written for the son of Locke’s lawyer friend, Edward Clark, and was intended specifically as a guide for the rearing and education of children of the English country gentry. Although there is presently an increasing interest among scholars in the history of attitudes toward infancy and childhood, it is still not entirely clear why our views of these early developmental stages began to change in the late 17th and early 18th centuries. It seems likely, however, that this trend was part of the more general movement, known as the Enlightenment, that swept across Europe in the 18th century and was especially influential in France. The new doctrine of individual rights, an integral part of the Enlightenment philosophy, brought forth a plethora of reform ideas that extended to all aspects of society, including the inauguration of debates and struggles over the proper role of education and the amelioration of societies ills, such as child abuse. Other factors that may have contributed to this changing perspective of childhood were an increasing economic prosperity, a decrease in infant mortality, and the growing influence of Christian beliefs stressing the duty ofparents to safeguard the innocence and weakness of children. The general philosophical trend of the Enlightenment, when coupled with these other factors, was probably responsible for the gradual emergence of more consistent and loving parentchild relationships, which in turn may have fostered an intellectual interest in this period of life. Whatever the specific reasons, the 18th century marks an important watershed in attitudes toward

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childhood and in the study of behavioral development.

Rousseau and Educational Philosophy: A New Conception of Ontogeny The changing perspective of childhood that began to emerge in the 18th century is perhaps nowhere better exemplified than in the revolutionary book by the French philosopher, Jean-Jacques Rousseau, entitled Emile, Or On Education, and published in 1762. For the first time in history, an influential intellectual was proposing that, behaviorally, the infant and child are qualitatively different from the adult. According to Rousseau, childhood is a time important in itself, a period when the behavior of the child is especially appropriate to the demands and needs of his own world and not merely an incomplete or incipient form of adult behavior. Rousseau believed that nature endowed the child with an order and scheme of development that ensured its healthy growth (“maturation”). Intellectual guidance, formal education, and training of all kinds were considered necessary and important for healthy growth, but they must always be subservient to, and carried out within, the framework of the child’s natural, biologic development. Because of such beliefs, Rousseau has often been mistakenly viewed as a nativist or “predeterminist” concerning the role of the environment and experience. In fact, his views were not so different from those proposed by modern interactionist, epigenetic conceptions of behavioral development. In some respects, our present views of human behavioral development largely reflect an elaboration, rather than a refutation, of Rousseau’s original ideas on these matters. A careful reading of Emile reveals that Rousseau recognized many of the central issues and problems of behavioral development. He proposed, for example, that all children develop naturally by passing through a number of stages that follow one another in a stereotyped sequence, that for behavior to develop normally each behavioral stage requires exercise, and that the functioning or exercise of one behavior may be necessary for the development and normal manifestation of a different, later appearing, behavior; and, finally, he proposed that there are important self-regulatory mechanisms that “nature” provides to each child for guiding development. Notwithstanding the originality and importance of Rousseau’s ideas on childrearing, there is no evi-

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dence that his book had any immediate influence on the childrearing practices of Western society in general. Because they were expressed more in the framework of philosophy or educational theory rather than as a practical how-to-do-it of childrearing for parents, the ideas of Rousseau, and to a lesser extent those of J. Locke, tended to have a greater influence on educational theorists than on social attitudes and practices. The important ideas of F. Froebel-founder of the kindergarten-and other educational theorists such as J. Herbart, H. Spencer, and J. Pestalozzi, in the 18th and 19th centuries, were largely elaborations on Rousseau and, in fact, all four authors explicitly acknowledge the influence of Rousseau (Ulich, 1959). Perhaps the greatest impact of Rousseau on educational theorists concerns his belief in the uniqueness of childhood. Following Rousseau, Froebel and other educational pioneers recognized that there were qualitative differences between children and adults and even between the different stages of childhood. If they differed from Rousseau at all, it was with regard to their belief in the inordinate importance of the earliest stages of development. As Froebel stated . . . the neonatal period, the first stage of development, is of the utmost importance for the present and later life of the human being. If the child is injured at this period, if the germinal leaves of the future tree of life are marred at this time, he will only with the greatest difficulty and the utmost effort grow into strong manhood . . . and escape in his further development the stunting effects of the injury. . . . (Froebel, 1887, p. 574)

As I discuss in more detail below, this view, that the period of infancy and early childhood are more important and influential for adult behavior than other developmental stages, was perhaps the most pervasive and persistent notion in the entire history of this field. Although its validity has recently been challenged (e.g., Cairns, 1979), it continues to be an integral part of virtually all present theories of development. It is to the credit of Rousseau, however, that he recognized the value of all stages, not just the earliest, in the normal ontogeny of behavior. In this regard, he anticipated contemporary trends. Because of his early and sustained influence on educational theorists, Rousseau’s ideas can be traced in a rather direct line from the 18th century to the present. Although this influence was mediated in large measure via the contributions of Froebel and Pestalozzi, there is another, rather more indirect, line of influence that was also in-

spired, in part, by Rousseau. This involves the French educational tradition as expressed in the work of J.-M. Itard, teacher of the famous “wildboy” of Aveynon and extending through Itard’s disciple, E. A. Sequin, to the Italian educator and developmental theorist M. Montessori (Lane, 1976; Curtiss, 1977; Kramer, 1977). The work of Itard and Sequin was also unique in that it represented the first attempt to devise educational, mental testing, and therapeutic techniques for dealing with children with neurobehavioral pathologies such as mental retardation, blindness, and deafness ( Kanner, 1964; Hallahan and Cruickshank, 1973). Notwithstanding these pioneer efforts, it was not until the turn of the present century, due in large part to the influence of psychiatrists A. Meyer and S. Freud, that psychiatry and related disciplines considered children part of their professional responsibility. Although the English psychiatrist H. Maudsley included a brief chapter on childhood mental disorders in his classic book, The Puthologv of Mind, published in 1882, it was not until 1935 that the psychiatrist L. Kanner, a student of A. Meyer, published the first textbook dealing with childhood psychopathology. Early attempts to evaluate the learning abilities of normal and retarded children and adults by A. Binet, W. Stern, L. Terman, and others, which led to the development of testing scales for children, may also owe a debt to this French tradition (Boring, 1957;Hilgard, 1987). As I discuss below, however, the child testing movement that began early in the present century was also greatly influenced by the Darwinian tradition and was largely conceived independently of Rousseau and the French educators. Finally, it is worth noting that one of the most prominent educators of the 20th century, John Dewey, often expressed his indebtedness to the ideas of Rousseau, Froebel, and Pestalozzi (Curti, 1959). Despite the various encouraging harbingers of a changing view of childhood in the 18th and early 19th centuries, it was not until the last half of the 19th century that the attitudes of a large segment of society in America, England, and Europe began to reflect this new perspective to any significant extent. Dramatic testimony of this change can be found in the appearance of popular novels whose main characters were abused, downtrodden, or poorly educated and neglected children (e.g., Oliver Twist and David Copperfield by Charles Dickens were first published in 1838 and 1849, respectively). It was also about this same time that

Emergence of Developmental Neuroethology

politicians began to express an interest in the welfare and protection of children. In England, Lord Shaftesbury,in particular, devoted much of his professional life to establishing laws for protecting children from widespread abuses by parents, teachers, and employers. Perhaps Shaftesbury best summarized the situation faced by many children in mid- 19th-century England when he stated, “It would often be better if children had no parents at all” (1868, p. 249). Slow but steady progress continued to be made throughout the last half of the 19th century for the legal protection of children. However, as vividly portrayed in the text and photographs of Jacob Riis’ important photo essay, How The Other Half Lives, published in 1890, the problems were by no means entirely eliminated even by the close of the century (Schorsch, 1979). The establishment of the disciplines of behavioral development and child psychology as scientific enterprises worthy of serious study by psychologists and others remained largely for the 20th century. As early as 1909, the title of a book by Ellen Key expressed this ensuing trend by referring to the new century as The Century of the Child. And, in 1895 C. L. Herrick, an important influence in the establishment of neuroscience and psychobiology in America (Windle, 1979), noted that No one can seriously doubt that the golden age of children is approaching, for a thousand tokens bear unmistakable witness that the king is coming to his own and that the father of the man is soon to take that proverbial pre-eminence he has long held only in theory, (Hemck, 1895, p. 34)

Herrick was referring here to the theory of evolution and the theory of recapitulation ( “ontogeny recapitulates phylogeny”), which, as described in the following sections, were major influences in the establishment of the modern, scientific study of neurobehavioral development.

Preformation vs. Epigenesis: Trends in Embryology One of the most enduring and fundamental debates in the history of biology was over the problem of how in each generation a complex, functioning organism could arise from the vastly more simple fertilized egg derived from the parents. This ancient inquiry into the process ofindividual development marked the beginning of an interest in ontogenetic issues. Although philosophers and naturalists as far back as Aristotle were concerned with

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this question, it was not until the 17th and 18th centuries that the problem of development became a matter of sustained and serious interest. Initially, the two major explanations of the process of development, preformation and epigenesis, appeared to be so different as to be virtually irreconcilable. Preformation theory argued that the fertilized egg, although apparently formless and unorganized, contained a full set of adult organs and characters too small to be seen. Thus, what appeared to be the de novo formation of tissues, organs, and other structures was, in fact, considered merely an increase in size. By contrast, proponents of epigenesis, beginning with Aristotle, held that the fertilized egg was, in fact, formless and unorganized and that ontogeny was actually a process whereby organs arose de nova by a gradual differentiation of the unorganized egg into an adult organism. Because virtually all of the pertinent facts of cell biology and embryology were unknown prior to 1700, both camps were forced to take refuge in metaphysics and theology for a “full” explanation of ontogeny. Gradually, however, as more and more information became available increasingly sophisticated theories replaced the older views, although most biologists continued to align themselves with one or the other camp until late in the 19th century. It was only when the understanding of cell biology became sufficient to provide a rationale for experimentation that the problem of development was finally resolved. Thus, by 1900 a sketchy but, nonetheless, valid outline of the developmental process was available that has served as a foundation for all subsequent progress in this field. Not surprisingly, by the opening of the 20th century a number of psychologists and biologists had shown a growing interest in how this new information in embryology and cell biology could aid them in understanding neural and behavioral development. With a few notable exceptions, however, most of them failed to fully comprehend either the facts or significance of the theoretical resolution of the preformation-epigenesis debate. Consequently, new, albeit familiar, debates arose over similar issues, which now were couched in terms of nature vs. nurture, heredity vs. environment, and maturation vs. experience. Ifbiologists and psychologists interested in neurobehavioral development had made a more concerted and sincere effort to understand the details of the earlier preformationepigenesis controversy, as well as the facts supporting its subsequent resolution, then the long and

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often bitter arguments over the nature vs. nurture issue would have been more quickly recognized as anachronistic and counterproductive. Only recently, more than 90 years after the fact, do a majority of workers in this field finally appear prepared to acknowledge what was commonplace to most leading biologists at the turn of the century, namely, that ontogeny is the result of a preorganized code in the genes that in concert with a long series of epigenetic events, involving intra- and extraorganismic stimuli, gradually transforms the fertilized egg into the complex, adult animal. Because I previously reviewed the impact of the preformation-epigenesis debate on studies of neurobehavioral development in considerable detail (Oppenheim, 1982a), what follows is a condensed and highly selective synopsis of that history. As important as experimental advances in embryology were for elucidating the specific issues being debated by the adherents of epigenesis and preformationism, they were perhaps of even greater historic value in signaling an entirely new conceptual approach to embryology and development that transcended the details of the original debates. For the first time, experimental analysis came to be the preferred mode of research upon the embryo, and the role of proximate factors, including cellular interactions and environmental influences, began to be emphasized over the purely normative, descriptive, and comparative approach of previous investigators. This advance was especially pertinent to conceptions about the role of heredity and environment in development, including neural and behavioral development. If a specific date is needed to serve as a watershed for this changing conceptual perspective, my choice would be 1894. It was in that year that W. Roux founded the journal Archive fur Entwicklungsmechanik der Organismen (Archivesfor the Development Mechanics of Organisms),which became the chief exponent for the new embryology and still survives today. Further, 1894 also marked the appearance of H. Driesch’s visionary treatise on experimental embryology, Analytische Theorie der Organischen Entwicklung. Together, these two events signaled a dramatic shift in the thoughts and activities of embryologists, away from the descriptive, phylogenetic emphasis of comparative embryology to the analytic, organismic approach of experimental embryology. In a lengthy introduction to the first issue of his journal, Roux ( 1894) formulated the problems, methods, and scope of this new field. The major task as he saw it was “the reduc-

tion of the formative processes of development to the natural laws which underlie them” (p. 15 1 ). The method, of course, was causal-analytic or experimental: By isolating, transposing, destroying, weakening, stimulating, false union, passive deformation, changing the diet and the functional size of the parts of the eggs, embryos or more developed organisms, by the application of unaccustomed agencies like light, heat, electricity and by the withdrawal of customary influences, we may be able to ascertain a great many formative operations in the parts ofthe organism. (p. 167)

The new field was to encompass all of biology: Just as developmental mechanics utilizes for its own purposes all methods which may be productive of causal understanding and all biological disciplines, so does it embrace as its field of investigation all living things, from the lowest Protists to the highest animal and vegetable organisms. (p. 186)

And, with his characteristic sagacity Roux predicted that . . . developmental mechanics as the science of the causes of these formations will sometime constitute the common basis of all other biological disciplines and, in continued symbiosis with these, play a prominent part in the solutions of the problems of life. (p. 187)

A prophecy that, unfortunately, still remains to be fulfilled. In addition to his acknowledged role as a patron saint of experimental embryology, Roux is also remembered for his early support of preformationism and the notion of self-differentiation. Yet, as Jane Oppenheimer ( 1967) pointed out (and as is often forgotten), Roux was also very much concerned with the role of environmental influences in development. In fact, he discussed this problem in great detail in his first book, published in 1881, the Darwinian-inspired, Der Kampf der Theile im Or-

gunismus ( T h e Struggle ofthe Parts in the Orguni s m ) . This book, an attempt to show that there were parallels between the struggle for existence among organisms (natural selection) and the competition between molecules, cells, and tissues within the organism ( “intraselection” ), had as one of its central themes the role of functional adaptations during development. Here and in subsequent publications (see Russell, 1916, 1930; Oppenheimer, 1967) Roux reported observations and experiments aimed at determining the effects of gravity, light, heat, magnetism, and electricity on various features of developing embryos. In his first

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publication (his thesis), Roux ( 1878) described how the size, pattern, and structure of developing blood vessels are modified by, and adjusted to, the needs and functions of the vascularized tissues. It is especially pertinent to the central theme of this article that Roux had the foresight to recognize that this approach would be particularly relevant to our understanding of the development of the nervous system and behavior. Roux’s interest in the functional development of the nervous system is not surprising. As a student at the University of Jena during 187 1-1878, he attended the lectures of Wilhelm Preyer, the pioneer physiologist, behavioral embryologist, and child psychologist, whose own contributions I discuss below. Roux entered medicine at the urging of Preyer and explicitly recognized Preyer’s influence, often citing his physiological and behavioral studies on embryos. Thus, it is not merely conjecture to ascribe at least some of the impetus for Roux to found an experimental, physiological embryology to his early association with Preyer. Even more specifically, Roux’s argument that the functioning of organs during development may contribute to further functional and structural development (see below) appears to reflect Preyer’s influence. In his book Specielle Physiologie des Embryo, Preyer ( 1885) pointed out that “organ formation is determined by function, rather than function by organ, as it may appear in the mature organism. The most firm proof for organs being determined by function is provided by the influence which a change in function has on morphological development, for example, if one limb is exercised more than another one, the muscle and nerve fibers increase accordingly” ( p. 3 ) . In Der Kampf der Theile im Organismus ( 1881 ) Roux devoted considerable space to a discussion of the possible role of sensory stimulation and spontaneous neural function in the development of the sense organs, central nervous system (CNS) (especially nerve pathways and connectivity), and muscle, joints, and bones. Moreover, he made a clear distinction between the role of function in the actual development of organs vs. its role in the later maintenance against regression and atrophy. With regard to the development of sense organs, he argues that: “The sense organs are. . .stimulated by sensory input and this input can participate formatively in the shaping of their perceiving parts. . . .” ( p. 49). And, similarly, in the case of muscle Roux suggested that “. . . many muscles function in the embryo; consequently the dependent parts of the

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tendons, parts of the skeleton, the joints, ligaments and fasciae are subject to activity and are thereby forced to develop dependent properties” ( p. 5 1 ). Within the developing CNS, he proposed that “. . . possibly nerve tracts in the nervous system have to be made functional through the specific stimulus for them [and that] it seems to me justified to assume that the respective parts lack completion in fine molecular relationships which are only produced through functional stimulation” ( p. 182). Finally, in a more general vein, Roux pointed out that We are not justified in regarding the formations present at birth as purely inherited. We are unable to decide how much is inherited, and how much is acquired through functional adaptation, because we don’t know the extent and speed of embryonic adaptation, and because we are as yet unable to distinguish between primary inherited and secondary (acquired) features. (p. 48)

Although space does not permit a detailed discussion, it is still worth mentioning that with regard to his general views on the role of function in neural and behavioral development Roux was neither entirely original nor unique. During the last half of the 19th century, similar views were often expressed by psychologists, philosophers, anatomists, and physiologists (see Oppenheim, 1982a). Due in part to the prevailing influence of British associationism (Warren, 1921 ) and in part to the neo-Lamarckian emphasis on the role of the environment in development and evolution (i.e., the notion that both ontogeny and phylogeny reflect an “adjustment of the inner to the outer”), biology, in the last half of the 19th century, tended to emphasize the role ofthe environment in the ontogeny of the nervous system and behavior. For all tissues and organs, including the nervous system, structure and function was thought to be an artificial dichotomy of what was actually a single biologic process, in which bidirectional interactions (Gottlieb, 1983) were thought to be commonplace and fundamental. For instance, in an early attempt to provide scientificjustification for the philosophically ancient idea that learning, memory, and experience (“function”) must reflect structural changes the British psychologist, A. Bain ( 1855) suggested that “for every act of memory, every exercise of bodily aptitude, every habit, recollection, train of ideas, there is a specific grouping or co-ordination of sensations and movements by virtue of speciJic growths in the cell junctions” (p. 91; emphasis added). The physiologist W. B. Carpenter ( 1874) later explicitly applied this notion to neural devel-

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opment, for, as he put it, “the nervous system grows to the manner in which it is habitually exercised’ (p. 106). W. James popularized this view in his immensely influential book Principles of PLyychology ( 1890) when, after having restated the long passage from Carpenter that included the above quote, James concluded by noting, “Dr. Carpenter’s phrase that our nervous system grows to modes in which it has been exercised expresses the philosophy of habit in a nutshell” (p. 112). Roux had an enormous influence on embryology and psychology at the turn of the 20th century. In fact, many of his ideas and concepts later became so closely enmeshed into the very fabric of these fields that they often lost all attachment to their originator-the fate of all great innovators. With few exceptions, biologists and psychologists today who study neurobehavioral development appear to be unaware of Roux’s work and influence and thus have failed to recognize that many of their own ideas about development, epigenesis, extrinsic vs. intrinsic stimuli, and structure-function interactions were anticipated by him almost 100 years ago. By the end of the first decade of the 20th century, sufficient information had already been generated by the new conceptual framework in embryology to warrant the publication of a book entitled Experimental Embryology by J. W. Jenkinson ( 1909), almost half of which was devoted to describing experiments aimed at explicating the role of both extrinsic and intrinsic stimuli in normal ontogeny. It is worth noting that a few prominent developmental psychologists were familiar with these exciting new findings and recognized their significance for conceptions of behavioral development (e.g., Baldwin, 1895, 1902). Although the stage was set for a sustained attack on neurobehavioral development in which experimental methods and the theory of epigenesis were the major leitmotifs, the fulfillment of this legacy in the present century (as noted below) was slow in coming. BEGINNING OF THE “MODERN” PERIOD: “DARWINIAN” INFLUENCES

There is a long intellectual history in Western civilization of attempts to draw analogies and suggest causal relationships between the “evolution” or the historic progress of civilization, including the evolution of humans (phylogeny), with the development (ontogeny) of the embryo, fetus, and child

(Lovejoy, 1936; Kessen, 1965; Gould, 1977). For my present purpose to describe the main events leading to modern conceptions of neurobehavioral development, the most important ideas about this relationship were based largely upon Darwin’s theory of evolution by natural selection. In the last half of the 19th century, it was widely believed that the individual development ( ontogeny ) of all animals, including humans, recapitulated or retraced their evolution (phylogeny). For instance, the human embryo, fetus, infant, and child were believed to represent ancestral stages of mankind such that the developing organism was thought to pass through transient stages in which they expressed the Characteristics of adult fish, amphibians, birds, and mammals, as well as various prior stages of primate and human evolution, before finally acquiring the features of a “modern” human being. According to this view, it was thought that by studying an animal’s development one could reconstruct its evolution, even in the absence of paleontological evidence. For physiologists and psychologists, it meant that the functional aspects of an animal’s evolution, including behavior, could also be reconstructed by studying the course of individual development or ontogeny. As one enthusiastic supporter of this view put it Just as the developmental history of the human embryo in his mother’s womb is only an abbreviated repetition of the history extending over millions of years, of the bodily evolution of our animal ancestors, beginning from the worm, so the mental development of the human child is only a still more abbreviated repetition ofthe intellectual development of these same ancestors. . . (Engels, 1876, p. 241)

Thus, the ontogeny of humans and other animals was viewed as one important key for unlocking the hidden mysteries of behavioral evolution. It was this view that made the infant and child legitimate subjects for psychological investigation. (This rationale was clearly expressed in the title of A. F. Chamberlain’s book, The Child: A Study in Evolution, published in 1906.) Even though the avowed goal of this movement, initially, was to establish evolutionary relationships, and not to elucidate the specific ontogenetic antecedents or causal mechanisms of later behavior, it, nonetheless, helped focus attention on ontogeny and thereby hastened the advancement of developmental investigations of all kinds, including the study of neurobehavioral development. For this reason, the Darwinian influence was perhaps the single most important factor I have considered so far in estab-

Emergence of Developmental Neuroethology lishing a sustained interest in neurobehavioral development.

Wilhelm Preyer: Infancy and the Embryology of Behavior One of the first persons influenced by Danvin and evolutionary theory to undertake ontogenetic studies was the physiologist Wilhelm Preyer. Preyer was a colleague of Ernst Haeckel (the father of recapitulation theory) at the University of Jena in Germany, and had earlier studied with the great French physiologist, Claude Bernard ( Carmichael, 1973; Gottlieb, 1973). In his monumental book, The Mind of the Child, first published in Germany in 1882 as Die Seele des Kinde (English translation, 1888), Preyer recorded his systematic, daily observations of the development of motor activity, sensation, perception, language, emotion, and cognition in his son, from birth to 3 years. Because Preyer’s observations were only based upon a single individual, however, their importance lies not so much in the extent to which the details have been substantiated by later, more extensive, investigations but rather in the fact that they demonstrated the potential of systematic child study for elucidating the path of individual development. Preyer’s example inspired innumerable other people to conduct similar “biographies” or diaries of the “mental” development of individual children (Anderson, 1965; Dennis, 1949, 1972). Further, although he only conducted the simplest of experiments and manipulations in studying his own son, Preyer’s association with Claude Bernard, an avid proponent of the experimental method in biology, instilled in him the beliefthat only by experimental means could one hope to unravel the causal factors in behavioral development. In the closing pages of a later book on embryonic development (see below), Preyer expressed this belief when he stated that, “The commanding duty . . . is to tackle experimentally [ emphasis added] the great problem of development . . . (Preyer, 1885, p. 5 1 1 ) . Preyer’s contributions to the study of embryonic and fetal behavior (against his studies of postnatal behavior) have been largely neglected or ignored by developmental psychologists and this aspect of his work is seldom mentioned in historical accounts of psychology (but, see Cairns, 1983). Although it is understandable that psychologists would be more interested in Preyer’s work on human infants and children (and, in contrast to his book on this subject, his embryological work pub-

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lished in German has never been entirely translated into English), it is, nonetheless, regrettable that this oversight has occurred. His embryological book is much richer in conceptual insights that are relevant to all stages of development, including infancy and childhood. Preyer’s major embryological contributions were published in 1885 in a book titled Specielle Physiologie des Embryo ( The Special Physiology ofthe Embryo). The use of the word “special” in the title probably reflects Preyer’s important recognition that the embryo and developing organism are not just incomplete, incipient, or miniature forms of the adult but rather that they have special physiologicaland behavioral ( “ontogenetic”) adaptations peculiar to their own needs and requirements. In his earlier book on the child, Preyer argued that, “The fundamental activities of the mind, which are manifested only after birth, do not originate after birth” (Preyer, 1888, p. xii). It was apparently this belief that led him to carry out the most extensive investigationsof the physiology and behavior of prenatal and larval life up to that time as reported in his 1885 book (portions of this book are available in English; see Coghill and Legner, 1937). Preyer made observations and conducted experiments on embryos of invertebrates, frogs, birds, reptiles, and mammals, many of which have been confirmed and extended by subsequent investigations using more modern techniques. One of his more enduring contributions concerns the role of motor activity in behavioral development. Preyer believed that spontaneous motor activity preceded the onset of responsiveness to sensory stimuli and that motor activity was the foundation for the later development of perceptual, emotional, and cognitive functions. Many subsequent developmental theorists, including S. Freud, G. Coghill, H. Werner, and J. Piaget, expressed similar notions in their own conceptions of behavioral development. The related notion of Preyer that the infant and child are spontaneously active and that this activity is important for development is also now a common theme in many current theories of behavioral development.

Douglas Spalding and ComparativeDevelopmental Behavioral Studies Darwin’s theory of evolution by natural selection not only stimulated an active interest in child development in the late 19th century but also

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opened up a new era of comparative-developmental research. It was reasoned that if the theory of evolution was in general true, then by studying and comparing the similarities and differences among living species, aided by embryological and paleontological evidence, the specific evolutionary relationships between animals could be elucidated. Darwin was keenly aware of the value of using behavioral, as well as morphological, traits, as a means for establishing such relationships; his friend and colleague, G. J. Romanes, assumed the task of forging a comparative psychology based upon Darwinian principles. And, as noted above, W. Preyer wasted no time in using this new Darwinian framework as an impetus and guide for his own comparative studies of the physiology and behavior of many different vertebrate embryos and fetuses, which were done with an eye toward establishing similarities and differences between species at the very onset of development in the egg or in

utero. Another important person in the history of developmental psychobiology influenced by Darwin -and who in turn had an influence on Preyerwas the English naturalist D. A. Spalding. Some historians of psychology (Gray, 1962, 1967) evaluated Spalding’s contributions to be of such import that he be considered the father of developmental psychobiology. Others include Spalding as an important pioneer in the field of ethology (Thorpe, 1979). It is clear that Spalding’s work was influential enough to ensure for him a firm place in the history of both these fields. He was one of the first persons to carry out sensory / perceptual deprivation experiments in an attempt to elucidate the role of the sensory environment in behavioral development. Spalding’s research was primarily with newly hatched chicks and involved attempts to determine the extent to which the chick‘s behavior was instinctual. He studied embryonic and hatching behavior, pecking, and imprinting, as well as early postnatal visual and auditory development. Spalding’s major conceptual contribution was his emphasis on the experimental approach. (It seems likely that it was this emphasis on experimentation that attracted Preyer to Spalding’s work.) In an era when experiments were discouraged and even disparaged-if they were considered at all-Spalding’s work marked an important advance over most previous attempts to deal with the question of instincts. As one contemporary, G. H. Lewes, remarked, “Mr. Spalding has not only proved himself an acute thinker, he has shown a rare ability in devising experiments, and we may . . . expect that

his researches will mark an epoch” (Lewes, 1877, p. 438). Despite Lewes’ prophecy, however, Spalding’s research, all published in the span of a few years in the 187Os, failed to initiate an immediate interest in experimental approaches to behavioral development. It was not until about 20 years later, following the abortive infiltration of Darwinian notions into psychology, that Spalding’s line of research was fully appreciated and revived by scientists interested in animal behavior (James, 1890). Thanks in large measure to the work of subsequent pioneers in developmental psychobiology, such as C. Lloyd Morgan, G. Romanes, W. Mills, F. Breed, and E. L. Thorndike (and later J. B. Watson), Spalding’s contributions were resuscitated and, together with other influences, helped establish the basis for a comparative-developmental psychobiology and developmental ethology in the 20th century. Regrettably, however, even this turn-of-the-century revival of interest in an experimental approach to problems of behavioral development eventually languished. From the 1920s until the 196Os, attempts to study behavioral development experimentally, with an emphasis on evolution, ecology, and natural history-all of which were major concerns of Spalding and his followers-fell victim to the increasing emphasis in psychology on mechanisms of learning and memory in mature organisms and on the attempt to study behavior in carefully contrived laboratory settings. Part of the reason for this later shift of emphasis of behavioral studies stems from the unfortunate attempt by some early 20th-century psychologists and biologists to categorize many behaviors as instinctual and thus-so they argued-independent of learning or experience. This trend was partly motivated and sustained by the nativist views of this period, especially “social Darwinism” and the Eugenics movement (see below). The reactions that developed against this view in psychology (known as the anti-instinct movement) argued instead that most behavior, especially human behavior, was learned and thus was qualitatively different from “animal” behavior. This countermovement, along with other “anti-biological’’ trends in psychology, became sufficiently successful such that by 1930 the mainstream of all branches of psychology had repudiated the usefulness of concepts from embryology, genetics, and evolution. Francis Galton: Heredity vs. Environment Francis Galton, cousin of Charles Darwin and a quintessential Victorian, was a man of such diverse

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interests, having made important contributions to the fields of geography, exploration, meteorology, anthropology, genetics, statistics, and criminology, that it would be misleading to characterize him solely as a psychologist or as having only psychological interests. However, in what must have been an exceedingly busy life he did have some time for psychology and, in fact, one could argue that he made more lasting contributions to this fieldwhich for him was largely an avocation-than many professional psychologists make in a lifetime. Galton’s primary contribution was his belief in the importance of individual variations in behavioral and related biologic characteristics and his attempt to devise quantitative techniques for systematically assessing such differences in both the child and adult (Galton, 1889). Consistent with Darwinian principles, Galton believed that much of the variation between individuals was hereditary and thus potentially subject to natural selection. He attempted to devise measurement techniques and tests by which one could distinguish individuals of different ancestry ( i.e., heredity) in much the same way that zoologists were systematically measuring morphological features of animals as a means of identifying speciesspecific characters. Although it remained for later investigators to fully reap the benefit of Galton’s ideas, there can be little doubt that it was Galton who laid the foundation for a systematic individual or diferential child psychology. Binet, Stern, Spearman, Burt, Cattell, Terman, and other later pioneers in the child testing movement were all influenced to one degree or another by Galton. One of Galton’s important conceptual contributions was his recognition of the usefulness of comparing the behavioral characteristics of individuals with varying degrees of genetic relatedness (i.e., identical and fraternal twins, nontwin siblings, parents and children, etc.) . In this way, Galton thought it would be possible to determine the relative roles of “nature” and “nurture” in behavioral development. By attempting to quantify the similarities and differences in behavioral traits between genetically related and genetically divergent individuals, Galton also deserves to be considered the father of behavioral genetics. G. Stanley Hall and Recapitulation Theory: “The Darwin of the Mind” Because the Darwinian (or evolutionary) influence, which emphasized development (ontogeny ) as an important subject for scientific inquiry, was

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so pervasive around the turn of the present century, it would be unfair, if not misleading, to focus on any one individual as having been especially influenced by this framework. For awhile, at least, virtually everyone studying behavioral development recognized and acknowledged the enormous debt owed to Darwin. There were a few individuals, however, whose contributions were so thoroughly in this tradition, and whose own influence was so important in the later history of this field, that one feels justified in focusing on them to the neglect of other, perhaps only slightly less deserving, individuals. One notable member of the former group was the psychologist G. Stanley Hall. Although there has been a recent revival of interest in Hall (McCullers, 1969; Ross, 1972), for most of this century he has been ignored or forgotten and if remembered at all it is either as a subject of ridicule or for his role in bringing S. Freud to America for Freud’s first and only visit to this country in 1909. The neglect of Hall is regrettable, for, although it is true that he made few lasting empirical contributions to psychology, he nonetheless had a great influence on a number of students and colleagues who later became well known in education, philosophy, and psychology (e.g., L. Terman, E. Thorndike, A. Gesell, and John Dewey) for their studies and views on developmental issues. Moreover, he has an impressive number of historic “firsts” to his credit. He was the first American PhD in psychology in 1878; the first American to work with Wundt and the first American psychologist to study with the great German physiological psychologists H. Helmholtz and E. du Bois Reymond; he founded the first psychology laboratory in 1883 and started the first major psychologyjournal, American Journal ofPsychology, in 1887;and, finally, he was a major organizer and the first president of the American Psychological Association, which began in 1892. (Although seldom remembered, in view of his overriding interest in development, it is also pertinent that Hall was one of the first Americans to study with the pioneer German embryologist, W. His.) Influenced by the 19th-century educational movement in Germany, which was attempting to gather “scientific” information about the educational needs, as well as the thoughts and “mental” activity, of children (a movement Hall witnessed firsthand during visits to Europe), Hall began to proselytize for the initiation ofa similar movement in America. Beginning in the 1880sand continuing for the remainder of his life (Hall died in 1924), he wrote a prodigious number of popular articles and

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delivered innumerable passionate speeches all over the country arguing for the establishment ofa scientifically valid child study movement (Ross, 1972). Not only did Hall’s efforts help bring about a realization of the importance of childhood per se but he also had an important influence in paving the way toward the establishment of a formal discipline concerned with the study of behavioral development, educational problems, and the physical development of children. During the second and third decades of the present century, child development institutions and clinics began to open up all over the country that were devoted to gathering the important normative data on children that was a necessary prelude to experimental studies (Sears, 1975; Senn, 1975). Hall’s efforts earlier in the century were almost certainly an important factor in this trend. Hall’s interest in development was also inspired by biologic theory (he was known as the “Darwin of the mind’), and his own theory of behavioral or mental development was largely an attempt to explain psychological phenomena in evolutionary terms, with a heavy indebtedness to both the biogenetic law of Haeckel (i.e., recapitulation theory) and the neo-Lamarckian belief in the inheritance of acquired characteristics. In agreement with the central tenet of recapitulation theory, Hall believed that an individual’s mental development consisted of a predetermined sequence of stages, in which each stage reflected a distinct and separate step (i.e., an ancestral stage) in the evolution or phylogeny of the mind. Although Hall was one of the most fervent and popular supporters of this view, to one degree or another virtually all psychologists of this period held similar beliefs. In a little-known book published in 1912, a student of Hall’s, G. E. Partridge, presented a coherent account of Hall’s theory that is considerably more balanced than what one typically encounters in textbooks devoted to Hall’s theory of behavioral development. Although the rather pompous title of the book, Genetic Philosophy of Education, An Epitome of the Published Educational Writings of President G. Stanley Hall of Clark University, and the fact that Hall wrote a preface attesting to the accuracy of Partridge’s representation of his beliefs, might raise some doubts concerning Partridge’s objectivity, nevertheless the fact that Hall was willing to accept responsibility for the views expressed in the book is valuable from an historic perspective. Regrettably, space does not permit me to discuss this book in any detail. In lieu of this,

however, I wish to cite a few passages from Partridge’s book that will indicate the richness of Hall’sdevelopmental thoughts and serve to demonstrate the extent to which he anticipated the views of later-even present-day-developmental theorists. With regard to the validity of recapitulation theory: “No one can maintain that the parallel between the individual and the race is as precise and definite as the law of recapitulation would demand. Other laws must be at work according to which the mode ofdevelopment of the individual is modified.” (p. 30)

In recognition of stages and ontogenetic adaptations: “The intellectual life is a growth, a series of stages in which there is always a partial adaptation to the needs of the individual . . .” (p. 63)

On the role of the organism as an active participant in its relation to the environment: “The child moreover does not merely wait for his experience, but seeks it and selects it in ways entirely his own.’’ (P. 6 5 )

Concerning the proper place of education and experience in childrearing: “The problem of education is to discover the stages and manner oftransformations in the child, and learn how to facilitate growth and . . . supply the right culture of nutritive material, suited to each stage. Infancy is a time of growth, and for sensory experience (p. 108) . . . but there should be no forced experience, nor incitement to rapid development of functions.” (p. 206)

Comparing these ideas with his more outlandish and poetic statements, it can be seen that Hall’s theory of behavioral development was a curious blend of vague, romantic, almost mystical, notions of evolutionary determinism on the one hand and a sophisticated, epigenetic conception of ontogenetic stages and developmental transitions on the other. According to Hall, adolescence represented the last major stage influenced by one’s phylogenetic ancestry, and for that reason adolescence took on special importance in his theory. His major publication was a two-volume treatise on this topic published in 1904 and opulently titled Adolescence: Its Psychology and Its Relations to Physiology, Anthropology, Sociology, Sex, Crime, Religion and Education. Hall believed that during adolescence the child ceases to be merely a victim of evolutionary

Emergence of Developmental Neuroethology

trends and instead begins to express the activities and mental characteristics typical of modern man. The transitions between developmental stages leading up to adolescence were thought to represent critical or sensitive periods that were especially vulnerable to the disruptive environmental factors that induced behavioral arrests and later pathology. Hall was in particular interested in the role of the early fixation of archaic (ancestral) traits in the causation of sexual perversions and in the more general problem of human psychosexual development. Sigmund Freud and Psychoanalysis: “Biologist of the Mind”

It is no accident that the ideas of Hall concerning the developmental origins of later-onset behavioral disorders sounds remarkably Freudian. Freud, like Hall, was a strong proponent of Darwinism, neoLamarckianism, and recapitulation theory, and as recent studies have shown, his own theory of personality development was influenced by these as well as by other popular biologic theories of his time (Kern, 1970; Sulloway, 1979). In fact, it is difficult if not impossible to fully appreciate Freud’s theories of psychopathology without understanding the extent to which they were inspired by 19th-century biology. It was likely this shared “psychoevolutionary” approach, as well as their mutual interest in psychosexual development, that inspired Hall to invite Freud to America to present a series of lectures and receive an honorary degree at Clark University on the occasion of that school’s 29th anniversary in 1909. (Hall was President of Clark from 1888-1920.) Freud was familiar with the developmental-evolutionary works of Preyer, Baldwin, Romanes, and others of his period and, although he never directly referred to the work of Romanes in his published writings, it has been noted that Freud’s copy of Romanes’ book on child development, Mental Evolution in Man, published in 1888 (itself a strong exponent of recapitulation and neo-Lamarckianism) ,is one of the most annotated books in Freud’s library (Sulloway, 1979). In view of Freud’s subsequent emphasis on infantile sexual behavior, it is ofparticular interest that in this book Romanes discusses the relationship between mental evaluation and ontogeny and concludes that the onset of sexual behavior in the newborn child occurs at about 7 weeks. According to Romanes, because the evolutionary ancestors of man were sexually reproduc-

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ing organisms it was entirely consistent with recapitulation theory that infants should display rudimentary sexual emotions. If the developing child recapitulates the history of the race, it must recapitulate the sexual history, along with all other aspects. Thus, following Darwin and Romanes, Freud’s psychosexual stages were conceived as specific instances in support of the general validity of the biogenetic law of recapitulation. Each major ontogenetic stage was viewed as the expression of the human legacy of specific phylogenetic-psychosexual influences. One of the most important and pervasive contributions of Freud to developmental theory was his belief in the ovemding importance of early experiences for the development of normal as well as abnormal behavior. Along with the developmental notions of fixation (or arrest) and regression, the potency of early experience was a fundamental aspect of Freud’s general theory of psychopathological development. All three of these developmental tenets-fixation, regression, and early experience-were derived from biology. In Freud’s time, the notion of developmental arrest was a wellknown embryological concept for explaining congenital anatomic abnormalities and Freud previously utilized this information to explain his observations on the effects of childhood cerebral paralysis (Freud, 1897). The application of this notion by Freud to specific behavioral fixations was also influenced by the investigations of D. Spalding (see above)-with which Freud was familiar-showing that young chicks may become “fixated” upon the first object they encounter after hatching, a phenomenon now known as imprinting or early social attachment. Thus, in Freud’s scheme sexual impulses were thought to become fixated (arrested)-owing to abnormal early experiences-at an early developmental-phylogenetic stage, resulting in behavioral pathologies later in life. As noted above, the view that early experiences are of special importance in the development of behavior is an historically old and persistent notion. It would appear that Freud may have been specifically influenced by 19th-century embryology in formulating this aspect of his developmental theory. In support of the role of early experience, Freud often cited the embryological experiments of W. Roux and others, showing that perturbations of the developing embryo at early stages are more disruptive than similar manipulations done later in embryogenesis. The important point to be made

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here is that Freud’s entire developmental theory of behavioral pathology (and, by implication, his views on normal development as well) was greatly indebted to, and indeed was in large measure a direct extension of, the Darwinian and other biologic notions of evolution, embryology, neuroscience, and developmental psychobiology that existed in the closing years of the 19th century (Zilboorg and Henry, 1941; Sulloway, 1979). James Mark Baldwin: Cognition, Social Development, and Evolution

In a letter to his friend and scientific colleague W. Fliess, written in 1897, Freud commented that, It is interesting that writers are now turning so much to child psychology. Today I received another book o n the subject, by James Mark Baldwin. So one still remains a child of one’s own age, even with something one had thought was one’s very own. (Freud, 1954, p. 228)

The person whom Freud refers to here was an American psychologist, J. M. Baldwin, who in 1895 published an important book, Mental Development in the Child and the Race. Baldwin had considerable influence on psychology around the turn of the century but for various reasons (see below) was soon forgotten, Only recently, after over 50 years of relative obscurity, have his contributions as a developmental theorist begun to be clearly recognized by child psychologists (Mueller, 1976; Phillips, 1977 ). Based largely upon observations of his own daughters, Baldwin formulated a theory of cognitive, personality, and social development that bears a striking resemblance to modern ideas on the subject, especially to ideas that are in general thought to have originated with J. Piaget and other modern cognitive theorists. For instance, Baldwin used the terms accommodation, assimilation, and schema in much the same way they are used today to describe cognitive development and, like Piaget, he believed that cognitive development had its roots in early motor behavior. Although Baldwin was in general agreement with the tenets of recapitulation theory, he recognized that only a direct study of behavioral development in the child could determine the extent to which psychological phenomena actually follow the doctrine of recapitulation. He was especially opposed to the facile speculations of G. Stanley Hall on this issue. Baldwin was also one of the few psychologistsof his era familiar with the important new embryologi-

cal work being done at the time. As discussed more fully above (also see Oppenheim, 1982a), biologists of this period who were interested in embryological development were finally turning to experimental techniques (as against normative description ) to determine the extent to which development was “preformed” or predetermined. As a result of this conceptual breakthrough, by the turn of the century embryologists were by and large in general agreement that all adult characteristics arise by an interaction between ”heredity” and environment. Baldwin clearly recognized the value of this view for understanding behavioral development. As he argued All characters are partly congenital and partly acquired. The hereditary impulse is at the start in each case a rudiment (Adage), which is to develop into what the environment, within which its native tendencies must show themselves, may permit it to become. ( 1902, p. 228)

Baldwin made frequent use of this conceptual framework in his theory of social development, and these ideas are spelled out in detail in his 1897 book, Social and Ethical Interpretations in Mental Development: A Study in Social Psychology. In agreement with the earlier proposals of H. George, L. Ward, H. Drummond, and other pioneers in social theory (Hofstadter, 1955), Baldwin stressed the role of social interactions and other environmental circumstances in the development of personality. The later theories of social interactionism proposed by C. H. Cooley and G. H. Mead and the more recent elaboration of these views by R. Sears and others owe a large debt to Baldwin and the other 19th-century pioneers of social psychology (Cairns, 1979). Because of his familiarity with the leading biologic theories of his time, Baldwin was certainly aware of the increasing attacks on neo-Darwinism, in which it was argued that evolution by natural selection, although important, was not sufficient to explain many aspects of phylogeny (neo-Darwinism, by contrast, argued that natural selection was the sole agent in evolution). Opponents of neoDarwinism believed that for many cases of evolution the inheritance of acquired characteristics ( neo-Lamarckianism) was a plausible alternative to natural selection. In an attempt to reconcile the differences between these two camps, Baldwin proposed a theory that he called organic selection (which subsequently came to be known as the “Baldwin effect”), in which he argued that individuals who exhibit nonheritable differences in their

Emergence of Developmental Neuroethology

ability to adapt to environmental contingencies are more likely to survive and reproduce and thus would make a greater contribution to future generations. According to Baldwin, specific differences in behavior that arise originally as adaptations to environmental stimuli would eventually become heritable and appear in later generations even in the absence of the stimuli that originally induced them. In this way, Baldwin believed he could explain examples of apparent Lamarckian inheritance as merely special instances of Darwinian natural selection. Part of the reason that Baldwin’s ideas about ontogeny failed to have a sustained influence on subsequent events in developmental psychology may be due to the fact that he had few students. More importantly, however, was the fact that his academic career was abruptly cut short at a time when he was just reaching the height of his creative abilities. Owing to alleged moral turpitude while at Johns Hopkins University, Baldwin was forced to resign in 1909 at age 48 and quickly became an outcast from American psychology ( Pauley, 1979). At the time of his death in Pans in 1934, at the age of 72, he had been all but forgotten.

THE MODERN PERIOD: PSYCHOLOGY AND EMBRYOLOGY John 6. Watson: The Behaviorist Approach to Development

Had Baldwin remained in academic life, it seems possible that he may have been able to forge a developmental psychology more closely allied with biology. As it happened, however, beginning shortly after the turn of the century the mainstream of American psychology began to concern itself more and more with learning mechanisms, having been influenced by the work and ideas of Sechenov, Pavlov, Sherrington, Loeb, Jennings, and others, which stressed the role of conditioning, reflexes, and related stimulus-response mechanisms in the control of behavior, including behavioral development (Murphy, 1932; Harrell and Harrison, 1938; Pauley, 1987). Although I shall discuss this movement and its influence on the study of behavioral development in later sections, it is worth noting here that one reason for the popularity of this trend was that it encouraged a systematic, experimental (and laboratory) approach to psychology, as opposed to the observational, introspective, and often

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speculative nature of earlier approaches (Boring, 1957; Boakes, 1984; Hilgard, 1987). Although not avowedly anti-biological,this new approach, nonetheless, largely ignored events in biology, a trend that soon resulted in the creation of a developmental psychology that became increasingly unaware of or uninterested in pertinent conceptual advances in biology. Part of the reason for this separation from biology was that after about 19 10 the two biologic theories that had been central to early theories of behavioral development-recapitulation and neo-Lamarckianism-were being repudiated by mainstream biology (Gould, 1977) . Accordingly, psychologists apparently became dubious of any attempt, however meritorious, to interpret behavioral development in terms of evolution or embryology. A related factor was the short-lived, but nonetheless damaging, attempt by a few biologists (and psychologists) to argue that the “newly” established findings of Mendelian genetics supported the belief that most behavior was due to heredity (or nature) and thus was largely instinctual, innate, or predetermined (Chase, 1977). The eventual repudiation of this view also persuaded many psychologists that biology had little to offer to the study of behavior. Although it is perhaps an oversimplification,the views of those who were sympathetic to the emerging environmentalist-learning (behaviorist) trend in psychology were derived in large measure from the earlier associationist philosophers such as J. Hobbes, J. Locke, and James and J. S. Mill (as noted above, however, these philosophical ideas were beginning to receive support from experimental studies on the principles of conditioning, learning, and reflexology). Early behaviorists believed that the developing organism was behaviorally passive and the embryonic nervous system was unorganized. The environment, in the form of experience, learning, use, etc., was considered to provide the major influence in molding and organizing the ontogeny of the nervous system and behavior. While it was sometimes admitted by adherents of this view that the nervous system of the newborn possessed certain anatomic and physiological predispositions, these were considered minimal. It was beliefs such as these that led J. B. Watson, one of the leaders of this movement and an early student of behavioral development in animals and human infants, to argue that all of the capacities, talents, emotions, and temperaments of children arise by conditioning. As he put it, “The behaviorists believe that there is nothing from within to develop”

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(Watson and Watson, 1928, p. 41 ). And, it was Watson who made the famous pronouncement that given complete control over a child‘s development the behaviorist could turn out adults with any specific talent, temperament, or ability the behaviorist desired (Watson, 1924, p. 104). The views of Watson and the behaviorists were exceedingly influential in the period from about 1920-1 940, a time when Watson’s popular books on child rearing practices were considered the Bible by thousands of American mothers. Watson had begun his behavioral studies of infants shortly after World War 1 at Johns Hopkins University, but by 1920 these studies were brought to an abrupt halt following Watson’s resignation from Hopkins (Cohen, 1979; Boakes, 1984). Had Watson continued in academic life, it seems likely that his theoretical views might have had an even deeper and more sustained impact on the field of behavioral developmental than they did. Unfortunately (or fortunately, depending upon one’s views), following a sensationalized divorce precipitated by an extramarital affair with his research assistant (later to become his second wife) Watson was forced to resign his position at Hopkins. He later took a job with an advertising agency in New York, where he remained for the duration of his life (Watson died in 1958). Although many of his popular books and articles on childrearing were written after leaving academia, Watson ceased to have any further direct influence on the study of behavioral development. In addition to his contributions to child psychology, Watson was also a pioneer in comparative psychology, animal behavior, and ethology, as well as in developmental psychobiology. His 1903 PhD dissertation involved the study of brain anatomy and learning ability in the developing rat. Together with his student, K. Lashley, Watson was one of the first psychologists to carry out field studies of animal behavior (Watson, 1908; Watson and Lashley, 19 15) and was an early proponent of the establishment of field stations for conducting behavioral research in natural settings (Watson, 1906). He also wrote an early textbook on animal behavior and development (Watson, 1914). Despite these auspicious beginnings, Watson failed to establish a valid biologic theory of neurobehavioral development that successfully encompassed evolution, genetics, and embryology, as well as associationism and reflexology. This is particularly regrettable for if anyone was prepared to carry on the tradition begun by Hall, Baldwin, and others of this era it was Watson.

One of Watson’s intellectual disciples was the psychologist Z.-Y. Kuo. Kuo had studied with the learning theorist E. Tolman and was an early and especially strong supporter of the anti-instinct movement in American psychology. Beginning in 192 1, Kuo published a series of articles criticizing the use of the concept of instinct in psychology, arguing that only by detailed studies of development could one determine the extent to which instincts were innate vs. being a result of early experience. In general agreement with Watson, Kuo proposed that the specific course, as well as the final product, of behavioral development was in a large measure determined by experience and environment. As he put it, “Behavior is not a manifestation of hereditary factors . . . it is the direct result of environmental stimulation” (Kuo, 1929, p. 196). Kuo went one step further than Watson, however, by arguing that except for the first primitive reflexes all the activities and predispositions of newborn animals were shaped by experience and environmental factors encountered prenatally. The Harvard psychologist and behaviorist E. B. Holt ( 1931 ) further elaborated on this notion by proposing that all behavior, including reflexes, as well as the specific anatomic organization of the nervous system at birth were the result of prenatal learning and conditioning. Lacking any empirical support-and in fact going in the face of considerable contradictory evidence from embryologyHolt’s proposal represented the final, logical, and some might say absurd, extension of the behaviorist’s misguided attempt to establish a field ofbehavioral development based solely upon philosophical associationism, reflexes, and learning and conditioning. Although some might argue that the later ideas of B. F. Skinner concerning the role of environment in the organization of behavior (e.g., Skinner, 1938) were as extreme as those of Holt, in fact Skinner’s views about the ontogeny of behavior were considerably more sophisticated (Skinner, 1966, 1975, 1984; Provine, 1988). It is to the lasting credit of Kuo, however, that, in contrast to the entirely speculative, nonempirical nature of proposals concerning prenatal learning (i.e., Watson, Holt) he felt compelled to tackle the problem of prenatal behavior by direct observation in the laboratory. Answering his own early plea for an embryology of behavior, by the late 1920s Kuo began to study the development of behavior in the chick embryo. Following extensive studies that were published in a series of articles between 1930 and 1940 (see Kuo, 1967), Kuo

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came to the conclusion that the prenatal sensory environment is of crucial importance in the development of the nervous system and behavior. As he was to later put it It is essential, therefore, that we understand first the nature and operation of the stimuli initiating the ontogenesis of behavior and follow up the extremely complicated processes of S-R relationships ( i.e., stimulus-response) throughout both prenatal and postnatal development. This is the keynote to thegenuine understandingofbehavior. (emphasis added; 1967, p. 16 1 )

In retrospect, Kuo is to be commended for his pioneering attempt to study the behavior of embryos, as well as for his more general appeal for developmental studies of behavior (Gottlieb, 1972). Although now commonplace, at the time the plea for a developmental approach in comparative psychology was novel. However, because of his rather dogmatic emphasis on environmental factors and owing to his failure to appreciate the conceptual insights of biology, embryology, and genetics regarding the “heredity-environment” issue (and, indeed, their importance for the study of developmental issues, in general) his contributions failed to provide a conceptual nexus for the establishment of a modern developmental psychobiology (Oppenheim, 1982a). Kuo’s failure in this regard, however was by no means unique. Other developmental psychobiologists of this era, such as Leonard Carmichael ( 1925), who appeared to be somewhat better informed of the contributions of biology and thus seemingly were in a more advantageous position to establish a sound, biologically based theory of behavioral development, also failed in this respect. The behaviorist and antibiologic Zeitgeist in psychology at this time was apparently too dominant to allow a person such as Carmichael, trained in psychology and with only a second-hand familiarity with the facts of embryology, genetics, and evolution, to establish a theory of behavioral development in which biology was used more advantageously than to merely acknowledge that there were anatomic and physiological correlates to behavior. George E. Coghill: Early Neuroembryological Approaches to Behavior Development G. E. Coghill, pioneer neuroembryologist and developmental psychobiologist, studied with C. L. Herrick (brother of the better-known comparative

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neuroanatomist C. J. Herrick) around the turn of the present century and is perhaps best known for his detailed observations on the correlated neural and behavioral changes in developing salamander embryos and larvae (Coghill, 1929). This work of Coghill’s, begun in 1906, represented the first scientific demonstration that behavioral ontogeny was an nonrandom, growth process to equally orderly changes in the development ofthe nervous system. AS an embryologist and anatomist with an abiding interest in behavior and evolution, Coghill was in an especially unique position to synthesize the findings from these various disciplines into a biologically valid theory of neurobehavioral development. Regrettably, Coghill did not live long enough to publish a detailed account of his “psycho-organismal” approach to ontogeny (Hemck, 1949; Oppenheim, 1978). Even in the absence of an explicit formulation of his theory, however, Coghill’s published empirical and conceptual articles provide a wealth of information from which one can discern many of his major views on neurobehavioral ontogeny. The approach Coghill championed was comparative, and thus evolutionary, in the sense that it supported attempts to establish major phylogenetic trends in the development of behavior. Coghill’s approach was also based upon the assumption that ontogenetic changes in behavior were mediated by orderly, predictable changes in the anatomy and physiology of the nervous system and related organ systems, However, because of his embryological background Coghill’s use of the term environment included early embryonic inductions and cellular interactions, as well as function, use, experience, and learning. Coghill believed that the environment made important contributions to both neural and behavioral development and that adaptive modifications in the nervous system and behavior during development were often mediated by function. The developing animal was viewed from an organismic perspective in which behavior was thought to be partly regulated by intrinsic constraints that served to coordinate, organize, and guide development along specific pathways. Coghill rejected the prevailing trends in physiology and behavior (i.e., reflexology and behaviorism) that held that complex, integrated behavior patterns developed out of earlier reflexes or from simple stimulus-response relations. He argued, instead, that from the earliest stages behavior was integrated or patterned, that this integration was guided by intrinsic ( self-regulatory) mechanisms, and that at

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each stage environmental influences had to be accommodated to these self-regulatory processes to be adaptively useful. One of the central tenets of Coghill’s theory was that behavior develops from a relatively undifferentiated state to a state of increasing differentiation, that is, from a state of generalized, global activity to one of increasing refinement and detail. It is important to note, however, that in agreement with the beliefs of organismic biology and Gestalt psychology Coghill maintained that behavior was integrated, patterned, and organized at all developmental stages. Although Coghill’s views were derived in a large measure from his own observations on the behavior and anatomy of the salamander embryo, these ideas were almost immediately recognized as having potential value as a basis for the formulation of a more general theory of vertebrate behavioral development. Beginning in the 1920s and 1930s, Coghill’s work and ideas served as a source of inspiration for child psychologists such as A. Gesell, 0. Irwin, K. Pratt, H. Werner, and M. McGraw. In an apparent reference to Coghill’s embryologically based theory of behavioral development, M. McGraw once remarked It is the experimental embryologists and not the psychologists who deserve credit for formulating the most adequate theory of behavioral development . . . it is they who are bringing the most convincing experimental evidence to bear upon an evaluation of intrinsic and extrinsic factors in the process of growth. (McGraw, 1935, P. 10)

As I discuss more fully below, Coghill’s work on the salamander embryo stimulated a great deal of research during the 1920s and 1930s on the prenatal development of behavior, a trend that languished in the 1940s and was not revived until the 1960s (Hamburger, 1963; Gottlieb, 1973, 1983; Oppenheim, 1982b). Although Coghill’s theoretical approach recognized the role of the environment in development (and in this regard was entirely consistent with our current views of behavioral and biologic development), in the prevailing Zeitgeist of behaviorism and environmental determinism (see below) his argument that endogenous regulatory mechanisms were also important made it almost inevitable that his views would be mistakenly conceived as those of a nativist and predeterminist. Accordingly, it is no surprise that child psychologists who supported Coghill’s theoretical position were also considered nativists. Perhaps no one suffered more from this misguided view than the pioneer child psychologist

and pediatrician A. Gesell, discussed in the following section. The work and ideas of Coghill represent a culmination of several earlier trends in biology, embryology, and psychology. In this regard, his experimental approach and conceptual ideas about neurobehavioral development provided a beginning framework and foundation for both developmental psychobiology and developmental neuroethology. Thus, to the extent that it is ever possible to attribute the establishment of a new field to a single individual Coghill deserves major credit as the father of both these closely related developmental disciplines.

Arnold Gesell: The Embryology of Infant Development

Gesell was criticized and often ridiculed in his lifetime as a blatant nativist. Since his death in 1960, Gesell’s reputation has continued to be adversely affected by the mistaken belief that he was an extreme advocate of genetic predetermination, when, in fact, as I argue below, Gesell’s theory of behavioral development represented an important forerunner of the modern epigenetic approach to neurobehavioral ontogeny. As a student of G. Stanley Hall, Gesell had an early and enduring interest in children and their behavior. After receiving his PhD in 1906, Gesell worked for several years as a child psychologist before deciding that to fully understand child development required a better foundation in biology, embryology, physiology, and anatomy. To meet this goal, Gesell entered Yale Medical School, where he received an MD degree in 19 15. It was at Yale in 19 1 1 that Gesell founded a clinic for the study of child development, the first of its kind in America. Gesell’s major goal in beginning this program of child study was to develop normative criteria that could be used in the diagnostic evaluation of normal, deviant, and defective infants. In this respect, he was motivated by goals similar to those of A. Binet, who slightly earlier developed intelligence tests to be used to detect mentally defective children (Wolf, 1973). In contrast to Binet and most others in the child testing movement, however, Gesell was interested in studying infants (and even premature babies) from the time of birth. Further, Gesell was not primarily interested in intelligence or cognition, per se, but rather in the total developmental status of infants and children as expressed

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in their motor, adaptive, language, and personality-social behavior (Gesell, 1952; Miles, 1964). The broadness of Gesell’s approach is reflected in the wide variety of developmental issues his work touched upon (Miles, 1964; Thelen and Adolph, 1992). There were, for instance, comprehensive studies of twins from infancy to adolescence, including a number of experimental studies in which one twin received specifictraining or experiences that were withheld from the other one; research on cretinism, mongolism, and infantile cerebral palsy; observations on mirror-image behavior ; work on the ontogeny of handedness and oral behavior, including feeding; a study of childhood fears and conditioning; detailed descriptions of perceptual and motor development; a comprehensive study of visual development; the first comprehensive description of behavioral development in premature infants; and naturalistic (ethological) studies of human behavioral development. In addition, he developed the widely used “Gesell” scales of normative behavioral development, wrote a number of enormously popular books and guides on childrearing and development, published several important theoretical articles on the ontogeny of behavior, and developed a number of systematic and innovative techniques for quantifying the infant behavior. Gesell was the first person to use one-way vision screens for unobtrusive observations and one of the first, if not the first, to use cinematography for providing permanent, easily quantifiable records of behavioral development. As L. Kanner, himself one of the pioneers in child development research stated, “His (Gesell’s) work has assured for him a lasting and uncontested place in the history of developmental psychology and psychiatry as one of the outstanding pioneers . . . and leaders in the field” (Kanner, 1960, p. 9 ) . Kanner’s tribute notwithstanding, as noted above Gesells’ theoretical views of behavioral development were vigorously disputed in his lifetime and continue to be the source of misunderstanding and disparagement (see Thelen and Adolph, 1992). Gesell believed that stabilizing mechanisms, intrinsic to the organism, provide the major source of regulation and organization for behavioral development. Gesell used the term maturation to describe these intrinsic controls. To developmental psychologists of this period, still greatly influenced by the views of behaviorism, maturation implied that all behavior was largely predetermined or innate. This, however, was neither Gesell’s meaning nor intention. In a passage from one of his early arti-

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cles, Gesell explained his position on this issue and in doing so provided one of the best summaries available of his general views on development: “They (the Behaviorists) suggest that the individual is fabricated out of the conditioning patterns. They do not give due recognition to the inner checks which set metes and bounds to the area of conditioning and which happily prevent abnormal and grotesque consequences which the theories themselves would make too easily possible. Although it is artificial to press unduly a distinction between intrinsic and extrinsic factors, it must after all, be granted that growth is a function of the organism rather than of the environment as such. The environment furnishes the soil and milieu for the manifestations of development but these manifestations come from inner compulsion and are primarily organized by inherent inner mechanics and by an intrinsic physiology of development. The very plasticity of growth requires that there be limiting and regulatory mechanisms. Growth is a process so intricate and so sensitive that there must be powerful stabilizing factors, intrinsic rather than extrinsic, which preserve the balance of the total pattern and the direction of the growth trend. Maturation is, in a sense, a name for this regulatory mechanism. Just because we do not grant complete dichotomy of internal and external factors, it is necessary to explain what keeps the almost infinite fortuities of the physical and social environment from dominating the organism of the developingindividual.” (1929, p. 319)

Gesell had few students or intellectual disciples and, consequently, although his developmental scales for infants as well as his technical innovations continued to be widely used following his death in 1960, he failed-even in his own lifetime -to initiate a large or sustained following among developmental psychobiologists. Part of the reason for this stems from his apparent reluctance to share his specific technical expertise or knowledge with students and colleagues, especially with nonphysicians. He isolated his clinic and its activities from most outsiders, apparently in the belief that only he and his trusted assistants were competent to carry out the appropriate studies and administer ‘‘his’’ developmental scales (Senn, 1975). In the final analysis, however, misconceptions about his theoretical views were an overriding factor in the rejection of Gesell’s proposals for an “embryology of behavior.” Because his theoretical approach gave endogenous self-regulatory processes and biologic maturation an equal status with learning and experience at a time in our history when most psychologists believed that “environmental” factors, especially learning and conditioning, were the major if not the sole organizing processes in the ontogeny of

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behavior, Gesell was misunderstood and thus failed to serve as the doyen of developmental psychobiology. Nonetheless, modern theories of behavioral development owe an enormous debt to Gesell. There are few issues or questions about development that were not studied or at least recognized and discussed by him, and many of our present conceptions about the development of behavior, including the simplest reflexes to language and cognition, rely in part upon ideas and principles that constituted fundamental aspects of his theory of behavioral development. As happens so often in intellectual and scientific history, we have had to rediscover many important ideas about development that Gesell (and Coghill) knew about almost 50 years ago. Had developmental psychobiologists paid more attention to what these men were saying and less to what others were saying about them, it seems likely that the field would be considerably advanced over what it is today. Only now are we gradually becoming aware that “The infant. . . comes by his mind in the same way that he comes by his body, namely through the mechanisms ofdevelopment. . . It cannot, therefore, be doubted that the general physiology of mental development will find its deeper roots in the same scientific soil which is now intensively cultivated in laboratories ofexperimental embryology.” (Gesell, 1954, pp. 335 and 337)

It would be an exaggeration-but not a great one -to argue that much of the conceptual history of developmental psychobiology from the 1940s to the present has been little more than an elaboration of, and a lengthy footnote to, the ideas of Gesell, Coghill, and a few other pioneer embryologists and developmental psychobiologists of that early era.

Jean Piaget: An Embryology of Cognition Because Piaget’s specific proposals and findings concerning the details of human cognitive development are so well known and readily available in virtually any of the multitude of textbooks in child psychology written in the last two decades, I feel no particular need to repeat this material again. By contrast, the general developmental assumptions and beliefs that underlie Piaget’s theory are perhaps less widely known, including the extent to which those beliefs were based upon earlier biologic theories of neurobehavioral ontogeny. Piaget was born in Switzerland in 1896 and received a PhD in zoology at age 22. As a student,

Piaget’s research dealt with the physiological and morphological (phenotypic) adaptations of mollusks in response to different aquatic environments. From this early zoological work, to his work in Paris in the 1920s on verbal reasoning in children, and continuing in his better-known and more recent work on cognitive development from infancy to adolescence, Piaget always focused on the problem of functional adaptations of the organism to environmental events. In an early autobiographic sketch, Piaget expressed this general influence when he commented that . . . my aim of discovering a sort of embryology of intelligence fit in with my biological training from the start of my theoretical thinking I was certain that the problem of the biological relation between the organism and environment extended also into the realm of knowledge (i.e., cognition). (emphasis added, Piaget, 1952, p. 245)

Piaget’s reference here to an “embryology of intelligence” is a reflection of his general belief that to understand cognitive development one must begin to study the period prior to birth. As was the case with Preyer, Coghill, Gesell, McGraw, and others before him, Piaget always contended that child psychology is best viewed as a branch of embryology, in which the physiological, morphological, and mental aspects of neural ontogeny from embryonic stages to the adult are all given consideration. As he once commented, “. . . future theories will be acceptable only if they succeed in integrating interpretations of embryogenesis, organic growth and mental development (Piaget and Inhelder, 1969, pp. 153- 154). In the final sentence of his autobiography, he was even more explicit when he commented that, “I hope to be able some day to demonstrate relationships between mental structures and stages of nervous development and thus to arrive at that general theory of structures which my earlier studies constitute merely an introduction” (Piaget, 1952, p. 256). Piaget’s theory is considered organismic in that, similar to other organismic theorists (e.g., Gesell, Coghill, and Freud), learning and experience, as well as endogenous or autoregulatory mechanisms, are all considered fundamentally involved in the ontogeny of behavior. In apparent agreement with Gesell, Piaget stated that Maturation plays a role throughout mental growth . . . it consists essentially of opening up new possibilities and thus constitutes a necessary but not in itself a sufficient condition for the appearance of certain behavior patterns. . . for this to occur, the maturation must be rein-

Emergence of Developmental Neuroethology forced by functional exercise and a minimum of experience. (Piaget and Inhelder, 1969, p. 154)

Piaget’s specific views on the issue of nature vs. nurture or heredity vs. environment were greatly influenced-as were Gesell’s-by embryology. As Piaget and his long-time colleague B. Inhelder pointed out, “the phenotype is considered to be the product of an indissociable interaction between heredity or endogenous factors and environmental influences, so that it is virtually impossible to draw a clear line between the innate and the acquired” (Piaget and Inhelder, 1976, p. 27). In thinking about how behavioral development involves specific interactions between endogenous and environmental factors, Piaget developed the concepts of schema, assimilation, and accommodation. Schema refers to an organized set of movements or intellectual operations (action patterns). At the simplest level, a schema may involve no more than the ability of infants to grasp, push, pull, or suck objects. Assimilation consists of integrating a new object or new situation into a preexisting schema. For instance, the prehensile or grasping schema is gradually applied to a wider and wider variety of objects (i.e., the new objects are assimilated into the grasping schema as a result of experience). Accommodation elaborates an action schema, making it more flexible and universal (e.g., the grasping schema gradually accommodates itself to large, small, round, angular, light, and heavy objects). Piaget’s theory is a paradigmatic stage theory in that he identified a series of qualitatively distinct steps in the development of cognition. Piaget recognized three major stages in the emergence of adult cognition: ( 1 ) the stage of sensorimotor development, from birth to 2 years; ( 2 ) the stage of concrete operations, from 2-1 1 or 12 years; ( 3 ) the stage of formal operations, beginning at 11 or 12 years. According to Piaget, the sequence or order in which the stages are traversed is fixed, although experience may accelerate or retard the specific timing of a stage (i.e., not all individuals reach a certain stage at the same time). Further, each stage is defined by a set of global structures, behaviors, or operations peculiar to that stage. Despite the qualitative distinctness of each stage, however, there is a continuity between stages. According to Piaget, the integration of successive stages leads to the emergence of the subsequent one. Each period of development partly explains the periods that follow. An important feature of Piaget’s view on stages-and

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one that can be traced back to Rousseau-is that developmental stages are qualitatively distinct from one another and distinct from the adult condition (see Oppenheim, 1981, 1984). Thus, the cognitive stages of infancy and childhood are considered unique and not merely incomplete versions of adult cognitive abilities. Further, and in contrast to the prevailing views of many developmental psychologists, who believe that developmental capacity is determined by learning and conditioning, Piaget has always argued that the learning capacities of the child are determined by stage-specific endogenous properties of the organism. Despite the fact that Piaget began publishing studies on child development in the 192Os, his work had little influence, especially in America, until the 1960s. In the 1960s and 1970s, however, his theories became increasingly popular, influencing the thoughts of psychologists, educators, pediatricians, philosophers, and psychobiologists. Part of the reason for this long period of neglect stems from the mistaken belief that Piaget’s theory of cognitive development represented an extreme form of maturationism or predetermination. Similar to the fate of Gesell, Piaget’s steadfast espousal of a view that placed an equal emphasis on endogenous and environmental factors led to his views being ignored or rejected by the majority of Amencan psychologists of the time, who-as we have seen-were more inclined to support views that rely heavily upon environmental determinants. By contrast, as a result of trends over the past 20 years or so in developmental psychobiology, in which endogenous factors are once again recognized as being important in the ontogeny of behavior, Piaget’s views have gradually begun to be seen as providing a reconciliation between ideas once considered irreconcilable or at least incompatible ( i.e., maturation or endogenous factors vs. environmental factors). By embracing and fostering ideas from biology in explaining the most complex features of human behavioral ontogeny, and by doing so at a time in our history when similar trends in other fields (e.g., ethology) have helped to establish evolutionary and embryological approaches, Piaget seems to have succeeded where Gesell and others failed. That Piaget’s views became so popular, whereas similar proposals of Coghill or Gesell, for instance, were previously rejected, is a strong argument for the influence of the Zeitgeist in intellectual history. Without a receptive audience, potentially great ideas (and great men) are often ignored,

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rejected, or misunderstood. When that happens, only time and retrospective analyses (i.e., historic studies) can act as potential remedial aids for their revival and recognition.

1940-1 960: NEOBEHAVIORISM, PSYCHOANALYSIS, AND EARLY EXPERIENCE Neobehaviorism and Psychoanalysis

During much of this period, developmental psychology, child psychology, and development psychobiology were all outside of the mainstream of academic psychology, which was still mainly concerned with establishinggeneral learning principles in adult animals (Hilgard, 1987). Accordingly, it is not surprising that initially the major new trends in the study of behavioral development were attempts to apply the principles of learning theory to children and related efforts to integrate the insights of psychoanalytic theory, regarding the role of early experience, with principles of learning. Following Watson’s contention that learning and conditioning constitute the major mechanisms of developmental organization beginning in the earliest stages of infancy-and perhaps even beginning in utero-there were a number of attempts to establish that the behavior of the fetus and infant could, in fact, be altered by classical conditioning. Although there were a few positive reports on this issue, these were subsequently challenged for serious methodological shortcomings (Dennis, 1943). Moreover, it was argued that even if fetal or infant conditioning could be demonstrated such processes were unlikely to be a major factor in the normal development of behavior. As one early critic noted “We need to ask whether or not experiments on neonatal conditioning have any bearing upon the question of. . . behavioral development. We think they do not. The possibility of early post-natal training should not be confused with the question as to whether or not conditional responses are formed under . . . normal conditions. (Dennis, 1943, p. 3 3 2 )

Despite such criticisms, many psychologists still tacitly assumed that conditioning and learning were plausible mechanisms for explaining the development of behavior. Notwithstanding the epigenetic, embryologically based theories of Coghill, Gesell, McGraw, and others during this period, for most psychologiststhe only apparent alternative to learn-

ing and conditioning was that behavioral development was due to maturation (ie., heredity or nature). However, because, for them, maturation implied predeterminism and nativism this was not a popular option at the time. In addition to the attempts to demonstrate conditioning in young infants, a substantial amount of effort during this period was also devoted to comparisons between children at different ages, and between children and adults, with regard to differences in their memory, retention, speed of learning, discrimination, and stimulus generalization abilities. Developmental psychology was striving to apply the learning principles of C. Hull, K. Spence, and others, originally derived from adults, to infants and children in the belief that the major, if not the sole, difference between the two resides in the fact that adults have had more time to profit from learning and experience. Although much of this work was methodologically sophisticated, its major shortcoming was that it was not motivated by a genuine interest in development (i.e., why and how developing organisms change). Rather, the major goal seems to have been to demonstrate that general principles of learning derived from studies of adults were applicable to children. Consequently, although much new data were generated, this body of literature belongs more to the history of experimental psychology than to developmental psychology or psychobiology. The more recent attempts to apply operant and other learning techniques to children, and the related attempts to demonstrate operant conditioning and learning in neonates and young infants (see below), suffers from the same drawbacks. Although traditional mechanisms of learning, including operant conditioning, are certainly involved in developmental changes and adaptations, they are only one of many equally important developmental processes. Consequently, to attribute a central place to traditional learning mechanisms in a theory of behavioral development places unnecessary and artificial constraints on the conceptualization of ontogenetic processes. By contrast, when these approaches are used mainly as probes or assays to unravel the natural mechanisms of developmental change such tools can help reveal important features of development. Perhaps the most innovative and influential movement that grew out of the early learning tradition involved the so-called social-learning theories. The origins of this movement can be traced most directly to the attempt in the late 1930s to explain

Emergence of Developmental Neuroethology

various specific aspects of personality development by a combination of learning and psychoanalytic principles. The initial impetus for this recent synthesis came from the prominent learning theorist and Yale psychologist C. Hull (see Cairns and Ornstein, 1979). Although the specific terminology such as primary and secondary drives and so forth was Hullian, the developmental phenomena these concepts were meant to explain were known and widely accepted by most developmentalists of this (and earlier) periods. For instance, concerning the formation of social attachments Freud earlier argued that the reason why an infant needs to perceive the presence of its mother is because it already knows by experience that she satisfies all of its primary needs (Sulloway, 1979). What Hull and his colleagues provided was a conceptual framework that aided in the experimental investigation of these well-known phenomena. Beginning in about 1960 and continuing up to the present, social-learning theories have evolved in two rather different directions. One of these relies heavily upon the operant learning principles of B. F. Skinner in attempting to explain child development as a series of environmentally determined reinforcement contingencies (e.g., Bijou and Baer, 1966). The other trend, developed primarily by A. Bandura ( 1977), places primary emphasis upon social modeling or imitation as mechanisms for initiating new behaviors and developmental change. Both versions, and indeed social-learning theories in general, with few exceptions rely upon learning principles (especially reinforcement) and thus are generally environmentalistic in conception. Development is seen not so much as a process dependent upon intrinsic growth and regulation but rather as a process determined and organized in large measure by learning, conditioning, exposure to social models, and explicit social training. To this extent, these theories represent a continuation of the environmentalist-learning ( Behaviorist) tradition that began with Watson and thus stand in rather sharp contrast to the views of Coghill and Gesell, as well as to the more recent and conceptually related developmental-stage (and organismic) theories of Werner, Piaget, Erickson, Kohlberg, and others (but, see Skinner, 1984). Early Experience: The Influence of Sigmund Freud and Donald Hebb

An important conceptual trend that began to be increasingly influential in the 1950swas the notion

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that early experiences, as opposed to experiences occurring at later stages in development, are more persistent, enduring, and thus more important for determining both the direction and ultimate end products of behavioral development (i.e., adult behavior patterns). The psychoanalytic theory of Freud played an especially important role in this trend (Beach and Jaynes, 1954). I noted early in this section that the belief that early experiences have a special significance is exceedingly old and has been one of the most persistent and pervasive notions in the entire history of this field. Although Freud’s views, as expressed in his theory of psychosexual development, were in some ways novel, the emphasis on early experience has been a central focus of most theories of development and education since Plato. As early as 1899, Freud noted that, “no one calls in question the fact that the experiences of the earliest years of our childhood leave ineradicable traces in the depths of the mind” (Freud, 1953, p. 303). Despite the fact that such views were commonplace, however, there had been little systematic effort to determine experimentally (or even to conceptualize) precisely how or why (or even if) early experiences were, in fact, as significant as widely believed. The early studies of Spalding on the formation of early social attachments in chicks (see above) and the various lines of evidence from embryology and teratology concerning development arrests and early embryonic vulnerability provided some clues to these questions, but it was Freud and his biologically inspired theory of psychopathology that made the first specific proposals about how childhood experiences can affect adult behavior. Notwithstanding his important lectures given at Clark University in 1909, it is still true that in the early decades of this century Freud’s theories, including his specific views on early experience, remained largely outside the mainstream of child psychology and developmental psychobiology. Although psychoanalytic principles were exceedingly popular among the general population (e.g., by the 1920s there were over 200 popular books in English on Freud and psychoanalysis), this was not so much due to the influence of Freud’s ideas on scientific investigation as it was to the popularization of Freudian ideas through the activities and interests of novelists, poets, philosophers, and other intellectuals. It was not until the 1940sthat psychoanalytic principles concerning early development first began to influence psychologists and psychiatrists interested in the study of developmental processes. I

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already discussed the work of Hull and his colleagues at Yale, who were inspired by Freudian theory to attempt a synthesis of psychoanalytic and learning principles for explaining certain aspects of behavioral (social) development. In addition, there were a small but growing number of studies in psychology that attempted to directly test Freudian theory using animal subjects (e.g., Levy, 1934, 1938; Hunt, 1941 ), as well as an increasing number of studies especially concerned with the effects of early childcare practices on later development and adult personality (e.g., Ribble, 1944). Perhaps one of the most influential contributions from this latter genre was a 1951 article by the neo-Freudian J. Bowlby that reviewed data on the mental health of homeless children (see Bowlby, 1969). Although this report dealt primarily with the effects of maternal deprivation on later psychopathology, it served to draw attention to the general problem of early experience and thus led to considerable discussion and controversy; most importantly, however, it helped stimulate a significant amount of research on this issue in both humans and nonhuman animals, a trend that has persisted right up to the present. The important work of Harlow and others on the role of early social experience in the development of behavior in primates was an especially notable contribution stemming from this tradition (Harlow, Dodswort, and Harlow, 1965). Perhaps the most important influence during this period (other than Freud) regarding ideas about early experience was the work of D. 0. Hebb. In 1949, Hebb, a comparative neuropsychologist, published a book entitled Organization ofBehavior, a Neuropsychological Theory, in which he argued that . . . “the characteristics of learning undergo an important change as the animal grows, particularly in the higher mammals; all learning tends to utilize and build on any early learning. . . ; and, finally, that the learning ofthe mature animal owes its efficacy to the slow and inefficient learning that has gone before, but may also be limited and canalized by it.” (Hebb, 1949, p. 109)

Hebb’s proposals provided a framework that was not only palatable to psychologists in general but that also made specific and testable predictions concerning the expected effects of early experience on later behavior, as well as on neural development and the neural basis of learning and memory. Although in some respects Hebb’s theory was an elaboration of the earlier environmentalist proposals of the behaviorists (e.g., his belief that certain aspects of brain development and postnatal behavior are

dependent upon prenatal “learning”), his views were actually considerably more sophisticated in that he also recognized the roles of spontaneous neural activity, intrinsic regulatory mechanisms, and hereditary or maturational constraints. Hebb’s theory was apparently inspired, in part, by a perceived need to better understand the details of behavioral development to ensure that each child develops to its maximum capacity. In the closing words of his book, Hebb noted that, “The country may be full of potential geniuses for all we know, and it would be a pressing concern for psychology to discover the conditions that will develop whatever potentialities a child may have” ( 1949, p. 303). It would be difficult to exaggerate the enormous impact of Hebb on this field (Beach & Jaynes, 1954). With the possible exception of Freud, Hebb’s ideas initiated and sustained several lines of research that continue in one form or another to the present time. Experimental studies on the role of early sensory and perceptual experience (Gottlieb, 1978), studies on the role of environmental enrichment and deprivation (Riesen, 1975), and studies on the effects of early handling (Denenberg, 1972) were all inspired by the work and ideas of Hebb and his students. Further, attempts to demonstrate the role of early experience in both neural and physiological development (Hubel, 1982; Purves and Lichtman, 1984) were also greatly influenced by Hebb; indeed, beginning in the early 1950s the whole field of physiological psychology was resuscitated by Hebb’s influence (Hilgard, 1987). Admittedly, the general notion that early experience is of major importance in the development of behavior and the nervous system has a long and venerable history that predates Hebb (see above). Nonetheless, the enormous literature that has accumulated over the last four decades verifying this old idea by experimental means owes a great debt to his pioneering efforts. However, his influence does not end there. An important technical advance that occurred in the late 1950sthat has subsequently revolutionized our conceptions of early behavioral development was also inspired partly by Hebb and partly by ethological influences. This was the demonstration by R. Fantz that by the use of relatively simple laboratory procedures one could elicit selective visual responses from human infants as early as a few hours after birth (Fantz, 1961). As a student of the pioneer American ethologist E. Hess, Fantz had earlier carried out extensive studies on the visual pecking preferences of newly hatched chicks and shown

Emergence of Developmental Nruroethology

that visually naive chicks have “innate” perceptual preferences for certain complex shapes, objects, and colors. Fantz’s later work with human infants was an attempt to determine whether similar innate preferences existed in primates and, if so, whether they were adaptive (e.g., do human infants prefer to look at faces or face-like models to aid in the formation of social attachments?). By measuring the amount of time infants gaze at various visual patterns, Fantz demonstrated that one could begin to infer something about the sensory, perceptual, and even cognitive capacities of infancy and childhood and how these might change with age. Armed with these new techniques, and sustained by the belief that the results obtained with them reflected important aspects of neural and psychological development, beginning in the early 1960s and continuing up to the present (Hall and Oppenheim, 1987) psychobiologists have been uncovering a wealth of new data about the sensory, perceptual, learning, and cognitive capacities of neonates, infants, and young children, information that had previously been considered both unobtainable (for technical reasons) and conceptually implausible (see the above discussion of Behaviorism).

NEUROEMBRYOLOGY, BEHAVIORAL EMBRYOLOGY, AND NEUROETHOLOGY Neuroembryology Although today the field of neuroembryology (or developmental neurobiology) is considered a branch of the larger discipline of neurobiology, historically this field has stronger ties to experimental embryology than to neurology or neuroscience. Accordingly, my focus in the present account is on the rise of neuroembryology as a branch of embryology rather than as an historic derivative of neuroscience. This is not to deny, however, that influences from neurology and neuroscience have been without significant impact on modern developmental neurobiology (Young, 1970; Clark and Jacyna, 1987; Brazier, 1988). Indeed, in recent years, as students with divergent backgrounds have begun to turn their attention to developmental problems, it seems likely that at least certain trends in the history of neurology, neurophysiology, neuropharmacology, and neurochemistry will ultimately need to be examined for their impact on the study of neuronal development. However, to the extent

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that neuroembryology has had an influence on the study of neurobehavioral development, including developmental neuroethology, that influence has been derived primarily from the close connection between neuroembryology and experimental embryology. Most of the concepts and principles that have guided and continue to guide investigations in this field were conceived by experimental embryologists who turned their attention to the nervous system. A notable exception is the line of neuroembryological work that reached its culmination in the studies of S. Ramon y Cajal but that was more an outcome of events stemming from early histologic and anatomic studies (Hamburger, 1988; Shepherd, 1991; Lowey, 1971). In the section on preformation vs. epigenesis above, I discussed some of the events in the centuries-old debate over preformation and epigenesis and ended with a description of two related crowning accomplishments of that debate that were achieved at the end of the 19th century, namely, the triumph of experimental analysis over the descriptive approach in embryologyand the reconciliation between preformation and epigenesis that resulted from the deeper understanding of cell biology and genetics. During this same period, workers studying anatomy and histogenesis were making great strides in understanding cell structure (Hughes, 1960; Swazey, 1970). By 1 870, neurohistologists had already worked out a clear view of the neuron and its processes. However, uncertainty remained over the source of nerve fibers ( Billings, 1971 ) . According to one view, known as the network or reticular theory, supported by Schwann, Golgi, Hensen, and others, nerve fibers were believed to be formed from a preneural protoplasmic network that arose independently from nonneural cells. The opposing view, known as the neuron theory, was supported by W. His, S. Ramon y Cajal, and others and argued that the neuron and all its processes were components of a single primordial cell, the neuroblast. In the course of investigations aimed at resolving this controversy, both His and Cajal (and others) made many important discoveries about the development of the nervous system that went far beyond the original issues of the debate. Because these discoveries and their impact on the emergence of neuroembryology have been dealt with in recent articles and books (e.g., Hamburger, 1988; Shepherd, 1991 ), I will not repeat that material here. It is worth noting, however, that although the methods used by the histogeneticists were descriptive

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and anatomic it is to their lasting credit (especially Cajal) that they were nonetheless able to correctly infer many dynamic principles of neuronal development. Impulse transmission, nerve connections, pathway formation, growth cones and axonal guidance, neurotropism, cell migration, regeneration, and the role of experience in neurogenesis were just a few of the topics touched on by these pioneers. However, no matter how brilliant and ingenious the individual, anatomic descriptions of normal embryos can only reveal a limited amount about mechanisms of development. It was precisely this limitation that was remedied by the emergence of experimental embryology. As discussed in the section on preformation vs. epigenesis, experimental embryology was conceived and initiated by the combined efforts of H. Dreisch and W. Roux in the 1880sand 1890s. Subsequently, leadership in the field was assumed by H. Spemann and R. Harrison. Although the classic organizer experiment of Spemann and H. Mangold in 1924 is often considered the beginning of experimental neuroembryology, it is Harrison, not Spemann, who deserves to be called the founder of this field. As Hamburger stated, “He put the stamp of his personality and of his profound insight into basic problems of development on the analysis of neurogenesis” (personal communication). After 1910, however, Harrison turned from neuroembryology to other problems of development, leaving the field to his most prominent student, S. Detwiler, who was later joined by a handful of others, including most notably V. Hamburger, G. Coghill, R. Sperry, and P. Weiss. Although Hamburger began his studies on the nervous system as a student with Spemann in the 1920s, he was also influenced considerably by Harrison, who often visited Spemann’s lab in Freiburg (Hamburger, 1988, 1989). Weiss also worked with Harrison at Yale and carried on Harrison’s pioneering in vitro studies of neuronal development. Despite the impetus provided by Harrison, and notwithstanding the important work of Detwiler, Coghill, Hamburger, Weiss, and Sperry in the 1920s, 1930s, and 1940s, experimental neuroembryology remained as a modest side branch of embryology until the 1960s. Since 1960, this field, now renamed developmental neurobiology, has burgeoned to the extent that it is a dominating influence in both neurobiology and developmental biology. As a result of its newfound popularity, developmental neurobiology has begun to lose some of its uniqueness. Neuroembryology emerged from the convergence of two tra-

ditions, which had roots in separate lines of inquiry and with different conceptual and methodological frames of reference, the histogenetic, anatomic tradition and the experimental embryology tradition. Today, however, the modern offshoot, developmental neurobiology, has begun to incorporate ideas and concepts from other traditions as well. Nonetheless, it is clear to anyone with an eye to the past that it was primarily these two earlier traditions that defined the problems and established the framework that continues to guide much of the field even today (Purves and Lichtman, 1984). Behavioral Embryology

Because the present article is concerned with the emergence of developmental psychobiology and developmental neuroethology, two related fields whose focus is to understand the neural basis of behavioral development, it is important to discuss the extent to which neuroembryology has influenced the emergence of these disciplines. In a large measure, this influence has been channeled through the study of behavioral embryology (Gottlieb, 1973b). Asdiscussed above, the field ofbehavioral embryologywas founded by the German physiologist W. Preyer in the last century and resuscitated and sustained by the neuroembryologist G. Coghill in the early part of this century. Coghill undertook his neurobehavioral studies on the salamander embryo with a clear recognition of psychological problems and a firm commitment to behavioral development. In his Presidential address to the American Association of Anatomists in 1933, Coghill defined the “neuro-embryologic study of behavior” as the attempt to understand behavioral development and its neural correlates. Although no other neuroembryologist devoted as much effort to behavioral development as did Coghill, many ofthe leading neuroembryologists ofthis century, such as R. Harrison, S. Detwiler, P. Weiss, W. Windle, R. Levi-Montalcini, A. Hughes, J. Piatt, R. Sperry, and V. Hamburger, also studied the behavioral development of the embryo, fetus, and larva. As Weiss stated, “No account of neurogenesis can be complete without relating itself to the problem of behavior” (1955, p. 390). Coghill’s studies of neurobehavioral development in the salamander began in the first decade of this century and continued until his death in 1940. As discussed in the section on Coghill and elsewhere (Herrick, 1949; Oppenheim, 1978), Coghill’s work had an enormous impact on investiga-

Emergence of Developmentul Neuroethology

tors in embryology, neurology, psychology, pediatrics, and psychiatry earlier in this century. Owing in large measure to his influence, the period between 1920 and 1940 is now considered to have been a halcyon era for the neuroembryological study of behavior. Because of theoretical debates that had began to dominate the field, howeverdebates that could not be resolved with the techniques available at the time-the field eventually languished and was largely moribund by 1960 (Hamburger, 1963; Gottlieb, 1973b). Beginning in the early 1960s,the neuroembryologist V. Hamburger turned his attention to neurobehavioral studies of the chick embryo and in doing so initiated a renewed interest in this field that continues to the present time (Bekoff, 1981; Oppenheim, 1982b; Smothennan and Robinson, 1988). Whereas Coghill’s early work and the work of many others in this field during the period between 1920- 1960 was largely descriptive in nature, this new line of investigation begun by Hamburger and colleagueswas carried out in the tradition of experimental embryology. In his Silliman lectures on experimental embryology given at Yale University in 1948, R. Hamson had made a plea for just such an approach. As he commented: “By ablation and transplantation of parts of the embryo it is possible to fashion almost any kind of nervous system desired and subsequently to study its function without the disturbing effect of trauma. This is one of the most promising lines of investigation leading off from the field covered in the present lecture” (1969, p. 163). Using the simple yet powerful and elegant techniques of experimental embryology, supplemented by behavioral, anatomic, and electrophysiological methods, Hamburger and associates were able to reveal many new aspects of embryonic behavior (Hamburger, 1973, 1976). Notable among these was the demonstration that the movements of the embryo and fetus are mediated by the endogenous activity of neurons in the CNS and thus are not the result of sensory stimulation. The apparent “spontaneous” nature of embryonic, fetal, and larval movements caught the attention of most earlier investigators in this field, including Preyer, Coghill, Harrison, Weiss, and Sperry, but here for the first time was unassailable experimental evidence in support of this notion. One of the central tenets of neuroembryology regarding neurobehavioral function is that the early differentiation of the nervous system establishes the framework and determines the potential-

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ities for behavioral performance. As P. Weiss put it: “The nervous system emerges from its embryonic phase well patterned and nothing could be more misleading than the impression that embryonic neurogenesis merely fabricates blank sheets on which experimental input from the outer world is then to inscribe operative patterns” ( 1970, p. 60). Thus, the work of Hamburger together with earlier studies by Coghill ( 1929), Weiss ( 1941), Sperry ( 1951 ), and a few others provided a strong basis for the notion that organized neuronal structure is present prior to the onset of function and this organization is a major factor in determining the functional and behavioral capacities of the developing nervous system. This notion, together with the belief that early behavior is generated endogenously, were also significant influences on the field of neuroethology. The neuroembryologicalinfluence on neuroethology was mainly channeled through the work of P. Weiss, whose studies on vertebrate locomotion were closely related to the work of the pioneer German neuroethologist E. von Holst and to that of later neuroethologists studying motor patterns in invertebrate species (Hoyle, 1984). However, Coghill’s studies, as well as the more recent work initiated by Hamburger on development of behavior in the chick embryo, also made important contributions to the neuroethological approach to the ontogeny of behavior and for that reason should be considered important milestones in the emergence of developmental neuroethology. Ethology and Neuroethology

The field of ethology began primarily as a European enterprise in which zoologists, biologists, and naturalists attempted to develop a discipline of behavior inspired in large measure by Darwinian principles (Thorpe, 1979). The primary focus of ethology was not the development of behavior. Ethologists, by tradition, were mainly concerned with survival value, physiological mechanisms, and the evolution of behavior in adult organisms. However, one aspect of the ethological approach required investigations (albeit limited in scope) into the role of learning or early experience in the ontogeny of behavior. The so-called deprivation experiment, by which young animals were deprived of specific experiences, was one of the operational procedures by which behaviors were classified as learned or innate by ethologists. Ethologists regarded the major criteria of innateness as: ( 1 ) A

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behavior is stereotyped in its form or pattern; ( 2 ) it is characteristic of the species; ( 3 )it appears in animals reared in isolation; and (4) it develops normally in animals that have never practiced it. One of the major weaknesses of the ethological definition of innate behavior was that anything not due to prior experience-and experience was in general conceived as involving traditional mechanisms of learning and conditioning-was considered innate. As pointed out most forcibly by D. Lehrman in his influential article, “A critique of Konrad Lorenz’s theory of instinctive behavior” (1953), such a view was much too narrow in its conceptualization of what constituted experience. As Lehrman argued It must be realized that an animal raised in isolation from fellow-members of his species is not necessarily isolated from the effects of processes and events which contribute to the development of any particular behavior pattern . . . the isolation experiment by its very nature does not give a positive indication that behavior is innate or indeed any information at all about what the process of development of the behavior really consisted of. (1953, p. 343)

In making this point, Lehrman was echoing the concerns of his mentor, the comparative psychologist T. C. Schneirla (and of Z. Y. Kuo), who had also argued that the ethological conception of innate behavior ignored the enormously complex pathway between genes and behavior that, as experimental embryology was demonstrating, involves a variety of gene-environment and organism-environment interactions and not merely traditional learning mechanisms (Schneirla, 1965) . Further, American psychology (and Schneirla certainly was an American psychologist) strongly believed in the overriding importance of learning and experience (and just as strongly discounted instincts and innate behavior). Accordingly, to many psychologists interested in development the challenge of ethology appeared to be an attempt to undermine what was considered the central pillar of their field, namely, the role of experience and learning in shaping the development of behavior-small wonder, then, that their reaction was often one of barely restrained outrage. Lerhman’s critique of the ethological concept of instinct was a thoughtful, scholarly, and exceedingly well-reasoned discourse that, despite the later appearance of a voluminous literature on the issues involved, has not been surpassed as one of the most influential statements to appear in the last 35 years on the topic of nature vs. nurture. The resulting

controversy between ethologists and their opponents over the role of early experience, although marked by extreme rhetoric on both sides, was in the final analysis a positive influence in that it forced both camps to think more deeply about the issues involved (Lorenz, 1965; Tinbergen, 1968). By doing so, it led to an enormous number of experiments into the developmental antecedents of behavior. Regrettably, most of this work was canied out by investigators outside the ethological tradition. The ethological challenge to the environmentalist-learning tradition that dominated psychology at the time was important for helping foster an interest in developmental issues in general and in the role of experience in particular. The ethological influence was also especially important for emphasizing the value of naturalistic studies of behavior and for bringing evolutionary and other biologic concepts back into prominence in psychobiology (e.g., see Provine, 1984). Within this new framework, learning processes and other means of environmental influence came to be viewed as adaptations that can only be properly understood within the natural ecologic habitat in which the behavior evolved ( Lorenz, 1965). Thus, ethology (together with neuroembryology) helped bring the study of behavioral development back into biology, so to speak. The reawakening of an interest in evolution and genetics and in naturalistic approaches to the study of behavior will almost certainly prove to be the most influential (albeit indirect) and lasting legacies of ethology, far outweighing any negative or retrogressive influences stemming from the innatelearned controversy. Even if the rise of the fields of ethology and psychoanalytic theory had not occurred, both behaviorism and Hebb’s ideas would very likely have served to sustain an interest in the role of experience in neurobehavioral development. By contrast, however, there were no clear signs during this period that psychobiologists were any closer to recognizing the value of viewing neural and behavioral development in an evolutionary and naturalistic (ecologic) context than they had been 40 years earlier. This insight, glimpsed briefly at the turn of this century but then forgotten, is almost entirely due to the influence of ethology. Evolutionary considerations are playing an increasingly important role in modern conceptions of neurobehavioral development, inchding studies in neuroethology. For this, developmental psychobiology will always be indebted to ethology. As implied by its name, neuroethology has

Emergence of Developmental Neuroethology

strong historic ties to both neuroscience and ethology. However, the extent to which neuroethology has been influenced by neuroembryology has seldom, if ever, been discussed. As noted above, this influence was mainly via the work and ideas of P. Weiss, who in a long series of articles on locomotion in salamander embryos (see Weiss, 194 1 ) argued for the role of endogenously active pattern generators that mediate locomotion and other stereotyped motor behaviors. At the same time, E. von Holst and associates in Germany were reaching similar conclusions from their studies of swimming in fish (von Holst, 1939). Because of his early studies on “behavioral physiology” and partly because of his close ties to the early founders of ethology (N. Tingergen and K. Lorenz), von Holst is considered the father of neuroethology. Later, the work of D. Wilson, D. Kennedy, D. Maynard, K. Roeder, H. Mittlestadt, G. Hoyle, F. Huber, C. R. G. Wiersma, and others helped gradually establish and define a unified field of neuroethology (see Hoyle, 1984). However, it was not until 1963 that the term neuroethology was first used (Brown and Hunssperger, 1963), and it took almost two more decades before textbooks appeared and international meetings took place whose focus was on neuroethology. Accordingly, although one can trace the origins of a distinct field of “behavioral physiology,” “ethophysiology,” or neuroethology to the work and ideas of von Holst in the 1930s, and notwithstanding the many subsequent studies done in this tradition in the 1940s, 1950s, and 1960s, a clearly defined field of neuroethology is mainly a recent effort having only emerged in the last 15-20 years (Hoyle, 1984; Ingle and Crews, 1985). Despite the early influence of neuroembryology on this field, developmental studies in neuroethology have been in general neglected. Part of the reason for this is that most neuroethologists have been trained outside the traditions of developmental psychobiology and neuroembryology. Another reason was the rather rigid and dogmatic views of many early ethologists concerning the role (or lack thereof) of experience in behavioral ontogeny. As the articles in the present issue bear witness, this situation is changing rapidly, and therefore I remain hopeful and optimistic that a “new” field of developmental neuroethology is now emerging. The author is indebted to his long-time friend and colleague Bob Provine for his many helpful suggestions on an earlier draft of this article. More generally, it is

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unlikely that the author would ever have had the interest or courage to undertake the present historical analysis without the constant encouragement and influence of his teacher and friend Viktor Hamburger over the past 30 years. Dr. Hamburger’s personal knowledge of many of the events and personalities discussed here was an invaluable source of insight and inspiration. Finally, because the author’s work on this article began over 15 years ago, the ideas expressed here have gone through innumerable changes influenced in part by the comments and suggestions of many colleagues and friends too numerous to cite. The author is profoundly grateful to all of them for their help and advice.

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