Physiology & Behavior, Vol. 15, pp. 225--235. Pergamon Press and Brain Research Publ., 1975. Printed in the U.S.A.

THEORETICAL REVIEW A Model of Hormones and Agonistic Behavior I ALAN I. LESH N ER

Department o f Psychology, Bucknell University, Lewisburg, PA 17837

(Received 16 December 1974) LESHNER, A. I. A model of hormones and agonistic behavior. PHYSIOL. BEHAV. 15(2) 225-235, 1975. - A model of the interaction between endocrine function and agonistic responding was developed that incorporates three specific hypotheses about the relatic,nship between hormones and agonistic behavior: (1) The baseline hormonal state of the organism contributes to the determination of whether, in what way, and how intensely the animal will react when it is exposed to appropriate environmental stimuli. (2) One function of the hormonal responses to environmental stimulation and behavioral experiences is to modify the continuing and future behavior of the individual in the same or similar situations. (3) Another function of these hormonal responses is to modify the individual's stimulus qualities so that other individuals' agonistic reactions to it will be modified. The data on hormones and agonistic behavior were reviewed in the context of this model, and some directions for future research were proposed. Agonistic behavior

Hormones

Model

Aggression

THE complex role of endocrine functioning in agonistic responding has been studied as if it were divided into three parts. Some studies have focused on the effects of hormonal change on agonistic responding, others have focused on the effects of agonistic experiences on endocrine functioning, and others have focused on the relationship of endocrine status to an animal's effectiveness as an agonistic stimulus. Although all of these studies deal with some aspect of the relationship between hormones and behavior in agonistic situations, there have been no real attempts to integrate these three elements into a comprehensive model describing the total relationship of hormones and agonistic behavior. The purpose of this paper is to present such a model. The particular case of hormones and agonistic behavior in mice and rats is used to develop and test the model, although periodic references will be made to the relationship of hormones and agonistic behavior in other species.

Submission

Victory

Defeat

for the control of responses to particular environmental or exciting stimuli. The way in which these stimuli are perceived, which is ultimately under the control of the baseline hormonal state, then determines whether, in what way, and how intensely the animal reacts to those exciting stimuli. Both the experiences of the animal in the situation and the behavior in which it engages produce further hormonal changes through the effects of these experiences on neural activity. These changes in the animal's hormonal characteristics really represent changes in the animal's dynamic baseline hormonal characteristics, which, therefore, will alter its reactions to these stimuli. In the same way that the animal's experiences can modify its continuing or future behavioral responses, these expereinces also can produce changes in the animal's stimulus qualities. Because the exciting stimulus in an agonistic situation usually is another dynamic organism, subject to the same factors as affect the animal under study, when the animal's stimulus qualities change so should the exciting stimulus' reactions to it change. In this way, the animal's behavioral and physiological reactions to stimulation feed back and modify both its continuing and future behavior patterns and the stimuli impinging on it. The model presented in Figure 1 incorporates three specific hypotheses about the relationship between hormones and agonistic behavior.

THE MODEL Figure 1 presents a model describing the relationship between hormones and agonistic behavior. According to the model proposed here, the baseline hormonal state of the organism presets or prepares its sensory receptors and the central neural processing mechanisms which are responsible

1Supported in part by Research Grant MH 23870 from the National Institute of Mental Health and by a grant from the Bucknell University Research Council. The author thanks E. K. Adkins, D. K. Candland, R. M. Tarpy and W. A. Walker for their critical comments on earlier versions of this manuscript. Particular thanks are due the many students and colleagues who have provided stimulating discussion of the issues raised here. 225

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Hypothesis i. The baseline hormonal state of the organism contributes to the determination of whether, in what way, and how intensely the animal will react when exposed to environmental or exciting stimuli. Hypothesis 2. One function of the endocrine responses to environmental stimuli or behavioral reactions is to feed back and modify both the continuing and future behavior of the animal in similar situations. Hypothesis 3. Another function of these endocrine responses is to modify the stimulus qualities of the organism so that other animals' reactions to it will be modified and, thus, the form of the stimuli they emit will be modified. The applicability of this model to the case of agonistic behavior in mice and rats will be tested by examining some of the data collected from studies of hormonal effects on agonistic behavior and of the effects of agonistic experiences on endocrine function. Before proceeding to a brief review of the relevant literature, it may be profitable to digress to a clarification of some of the terms used. A CLARIFICATION OF SOME TERMS The term agonistic behavior refers to a class of behaviors aggressive, submissive, and defensive - that occur in competitive situations. Competition may be for resources, space, mates, or to facilitate the establishment of social hierarchies so that animals can live together peacefully [9,10]. The adaptive significance and the inevitability of agonistic interactions have been described often (e.g., [9, 4 1 , 7 8 , 9 9 , 100]). -

Agonistic behavior may be observed in many situations and under a variety of circumstances [82, 83, 84]. The emphasis in this paper will be on data collected in studies of intermale or spontaneous agonistic behaviors, although other classes of agonistic behavior will be considered periodically. Intermale aggression and defense refer to the group of agonistic reactions which occur when two unfamiliar conspecifics meet [ 58,82 ]. This particular form of agonistic behavior has been selected because its endocrine characteristics have been studied most extensively. The term aggression has been used to refer to a variety of behaviors, and a number of definitions of this term have been proposed. These have included definitions referring specifically to classes or forms of aggressive behavior (e.g., [82]) or referring to tendencies to act aggressively (e.g., [ 118] ). In this paper, aggression is considered as any action by which one individual either causes or threatens to cause physical injury to another. This definition is designed to include both injurious forms of aggression, such as attacking or fighting, and noninjurious forms of aggression, like ritualized threats or displays (cf., [39]). The terms submissive and defensive behaviors are used here to include the wide range of behavior patterns like flight, passivity, threats, and avoidance exhibited by defeated or subordinate animals in agonistic encounters. The literature on the relationship between hormones and agonistic behavior in mice and rats is extensive. Reviews of this literature have been provided elsewhere (e.g., [5, 42, 54, 83]). In this paper, I shall summarize the state of knowledge in this field to provide a basis for evaluating the proposed model.

HORMONES AND AGONISTIC BEHAVIOR HYPOTHESIS 1: HORMONAL EFFECTS ON AGONISTIC BEHAVIOR

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Sex Differences in Aggressiveness

Although the effects on aggression of manipulating almost all of the endocrine subsystems have been studied [ 103,116], primary focus has been placed on the effects of manipulating the levels of the hormones of the pituitarygonadal and pituitary-adrenocortical axes [42].

In most mammalian species the male is more aggressive than the female [56, 102, 108], and it has been suggested [47] that these sex differences are due to differences in both the perinatal and adult hormonal characteristics of the animals. In most mammalian species the female is the neutral sex: The fetus will develop as a male both morphologically and behaviorally only if the male sex hormones are present perinatally. In the absence o f all sex hormones, as well as in the presence of the female sex hormones, the animal will develop in the female direction [ 1 ]. In the case o f aggressive behavior, treatment of female mice on postnatal Days 0 to 12 or 14 predisposes them to be aggressive if androgen treatment is reapplied in adulthood [28, 29, 4 7 ] . Although this critical period for perinatal sensitization corresponds well with the period of maximal uptake of testosterone by the developing animal's brain [ 115 ], sensitizing effects of large dosages of testosterone have been observed up to 30 days of age [49]. Males castrated on postnatal Day 1 are less responsive to androgen treatment in adulthood than those castrated on Day 10 [48]; and neonatal castration is effective in blocking adult aggressiveness only if males are castrated on Days 0 to 2, but not on Day 6 [90]. That these perinatal androgen manipulations affect central activity, rather than acting via some peripheral effects of the treatment, is emphasized by the finding that perinatal treatment with the anti-androgen cyproterone acetate does not affect the aggressiveness of male mice [21]. Cyproterone acetate seems to exert its anti-androgenic effects predominantly on peripheral rather than on central structures.

Pituitary-Gonadal Effects on Aggression

Pituitary-Adrenal Effects on Aggression

Interest in this problem area seems to have emerged from the early observations that in most species the male is more aggressive than the female [56, 102, 108], and a number of lines of evidence have stressed the importance of androgenic stimulation for the expression of aggression: (1) Castrating male mice reduces their aggressiveness, and replacement therapy with moderate dosages of testosterone restores the aggressiveness of castrates to normal levels [13,15]. Although moderate dosages of testosterone are effective in restoring the aggressiveness of castrates, higher dosages are ineffective. This finding implies that there is an inverted U-shaped relationship between testosterone levels and aggressiveness: Both reduced and elevated levels lead to decreased aggressiveness [ 14,15 ]. It may be, however, that the effects of high dosages of androgen are pharmacological, and, therefore, that although both reduced and elevated androgen levels lead to decreases in aggressiveness, their mechanisms of action and physiological significances differ. (2) Aggression appears developmentally at the same time that the high level of androgen secretion which characterizes adult males first becomes evident [22,80]. In addition, treatment with testosterone propionate early in life accelerates the development of aggression in mice: Testosterone-treated male mice first show aggression at 18 days of age rather than at 34 days of age [76]. (3) There is a positive correlation between individual differences in aggressiveness and ventral prostate weight, a rough index of androgen levels [23] ; and mice of aggressive strains, like the Turku aggressive strain, have heavier testes than those of nonaggressive strains [64]. (4) Injecting nonaggressive mice with testosterone increases their aggressiveness [7].

Although classically the androgens were considered the most important hormones in the control of aggression, recent studies have implicated the hormones o f the pituitary-adrenocortical axis in determining levels of aggressiveness. It should be noted here that the effects of pituitary-adrenocortical manipulations on aggression are not so dramatic as those of pituitary-gonadal manipulations and that these effects of pituitary-adrenal manipulations are not always consistent across b o t h strains and methods of testing (cf., [25, 30, 36]. Bilateral adrenalectomy reduces aggressiveness [24, 57, 75]. Treatment of adrenalectomized mice with moderate dosages of either corticosterone or dexamethasone restores their aggressiveness, while treatment with high dosages of corticosterone reduces the aggressiveness of intact mice [39,71 ]. Because a change in adrenocortical activity always is accompanied by a change in the pituitary secretion of adrenocorticotrophic hormone (ACTH), and because ACTH has been shown to have extra-adrenal effects on other behaviors, interest developed in the question of whether there is a direct relationship between ACTH levels and aggressiveness. Treatment with ACTH over long time periods reduces aggressiveness [16, 17, 19, 24, 7 5 ] , while short-term treatment with ACTH leads to increases in aggressiveness [20,74]. Interestingly, the long-term suppressive effect of ACTH appears to be due to some extraadrenal, extra-testicular effects of ACTH, although the short-term facilitatory effect of ACTH on aggression seems to be a result of the slight increases in corticosterone levels which this manipulation produces [74,75 ].

Hypothesis 1 suggests that the baseline hormonal state of the organism predisposes it to react in a specific way and to a specific degree to a standard stimulus. F o r agonistic behavior, this hypothesis suggests that the baseline hormonal state predisposes the animal to react more or less aggressively and more or less submissively to novel conspecifics. This hypothesis does not imply necessarily that aggressive and submissive responses represent opposite poles of a continuum. Rather, it suggests that the hormonal state of the animal affects both components of agonistic responding. Much experimental attention has been devoted to the study of hormonal effects on aggressive behavior, but only a few studies have examined the effects on submissive behaviors of manipulating endocrine function. I shall consider the effects of endocrine manipulations on aggressive behavior first and then review the studies concerned with the hormonal basis of submission. Because aggression and submission are incompatible in their extremes, Hypoth esis 1 suggests that those hormonal characteristics which predispose an animal to be highly aggressive should predispose it to be nonsubmissive, and the reverse. HORMONAL EFFECTS ON AGGRESSION

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Aggressive and submissive reactions are different classes of behavior which both can be elicited b y the same environmental stimuli [98,99]. Therefore, it is possible that the hormonal state of an animal not only determines the intensity of its reactions but also the form of its responses, whether it will react aggressively or submissively to the stimulus of a novel conspecific (Hypothesis 1). There have been few direct studies of the effects of hormones on submissive behaviors. Therefore, there is little direct evidence to support the view that hormones affect submissiveness generally oppositely from the way they affect aggressiveness. There is some indirect evidence, however, which points toward this conclusion, much of which is correlational and has been collected in species other than mice and rats. (1) As discussed above, there is a positive correlation between individual differences in aggressiveness and certain indices of androgen activity in mice [23,64]. Thus, there is a negative correlation between submissiveness and androgen activity. (2) In Rhesus monkeys, there is a positive correlation between dominance status and circulating testosterone levels, and as dominance status changes, so do testosterone levels: As dominance is achieved, testosterone levels rise, as dominance is lost, testosterone levels fall [93,94]. These data are merely correlational, however, and it is impossible to determine whether a change in status leads to a change in gonadal hormone characteristics, or the reverse. (3) In squirrel monkeys, eventual dominance status can be predicted from baseline urinary 17-hydroxycorticosteroid levels: Eventually subordinate monkeys have lower baseline levels of adrenocortical activity than eventually dominant monkeys [39,72]. This kind of correlation between hormonal states prior to agonistic exposure and eventual status argues better for Hypothesis 1 than those correlations between hormone levels and already-achieved status. (4) Those pituitaryadrenocortical manipulations which reduce aggressiveness are precisely those which also have been shown to increase fearfulness (at least in shock-mediated situations): Increases in ACTH levels reduce aggressiveness and increase fearfulness [18]. Thus, it is possible that ACTH reduces aggressiveness because it increases fear in the presence of the novel, potentially aggressive conspecific [106], and thereby predisposes the animal to be more submissive. Studies by Scott (e.g., [ 9 9 ] ) and Seward (e.g., [ 1 0 2 ] ) and recent studies from this laboratory (Leshner and Nock, unpublished observations) suggest that the motivational state underlying submissive responses is fear-of-beingattacked. Therefore, we [73] have begun to examine the effects o f hormonal manipulations on the acquisition and performance of fear responses in a situation where the motivating stimulus is attack by a trained fighter. In this way we can begin to study more directly the way in which the hormonal state of the animal might predispose it to react more or less submissively (fearfully) to agonistic stimuli. We use a passive avoidance task for this analysis where the aversive stimulus is attack by a trained fighter (see Scott [99] for a description of a similar active avoidance task). Across all manipulations of pituitaryadrenocortical activity those manipulations which reduce aggressiveness also lead to increases in fear-of-beingattacked. Thus, those pituitary-adrenocortical manipulations which predispose an animal to be less aggressive, also

predispose it to be more fearful and, perhaps, more submissive. Interestingly, although manipulations of androgen levels have dramatic effects on aggressive responding, the level of the androgens seems irrelevant to an animal's fearfulness in this agonistic situation (Leshner and Moyer, unpublished observations). Therefore, it appears that although the levels of the pituitary-adrenocortical hormones are critical to both aggressiveness and fearfulness, the levels of the androgens are critical to the amount of aggression displayed but irrelevant to the amount of fear elicited in the situation. SUMMARY: HORMONAL EFFECTS ON AGONISTIC BEHAVIOR This review of selected studies on hormonal effects on agonistic behavior suggests that the baseline hormonal state of the individual can predispose it to react more or less aggressively and more or less fearfully or submissively to the standard stimulus of a potentially aggressive novel conspecific (Hypothesis l). Very low androgen levels seem to predispose the animal to be nonaggressive, while moderate levels predispose it to be more aggressive. No direct evidence has been provided to show that decreases in androgen levels also predispose it to be more submissive, although the correlational studies reviewed seem to show that submissiveness and agressiveness are related to testosterone levels in opposite ways. On the other hand, the fact that the level of the androgens is irrelevant to an animal's fear of being attacked suggests that the .androgens may in fact only affect the aggressive component and not the submissive component of agonistic responding. The case of t h e pituitary-adrenocortical hormones and agonistic behavior is clearer than the case of the pituitary-gonadal hormones: High ACTH levels have been shown both to reduce aggressiveness and to increase fearfulness in the presence of a novel conspecific, while intermediate pituitary-adrenocortical hormone levels seem to predispose the animal to be more aggressive and less fearful. Caution should be exercised in evaluating the importance of endocrine factors in determining agonistic responses. Most of the studies reviewed here examined hormone-behavior relationships in naive subjects, and very few animals in the wild achieve adulthood in the same kind of behaviorally-naive state as these laboratory animals. The influence of early experience on aggressive responding, an effect which may or may not be hormonally mediated, has been investigated to only a limited degree. We do know that prior agonistic experiences have dramatic effects on later aggressive behaviors (e.g., [101]), and that these prior experience effects are not reversed readily by hormonal intervention (e.g., [36]). Thus, although the hormonal state of an animal clearly is important in determining its agonistic responses, it is but one of a number of factors which interact to determine the level of aggressiveness an animal will show when exposed to agonistic stimuli. MEDIATION OF HORMONAL EFFECTS ON AGONISTIC BEHAVIOR How do hormones exert their effects on agonistic behavior? There are a number of ways in which hormones might affect behavior [12], and the model presented here argues that the primary way in which hormones affect agonistic behaviors is through modifying the state of the

HORMONES AND AGONISTIC BEHAVIOR central nervous system circuits which control the interpretation of agonistic stimuli and the integration of agonistic responses. Hormones have dramatic effects on the general metabolic state of the organism and on the state of the musculature [ 105], and could affect behavior b y affecting the general physiological state of the organism [70]. However, hormones cannot direct muscle movements, and the general metabolic effects of some behaviorally-active hormones, like the male sex hormones are minimal. Therefore, it seems more likely that hormonal effects on agonistic behavior are mediated through the nervous system, the final common path for behavioral action (cf., [114]). Hormones may affect behavior through modifying nervous system activity at the level of the peripheral sensory receptors. Adjustment or modification of the state of the sense organs alters the probability of a stimulus eliciting a perceptual response [59], and many hormones affect the state of the peripheral receptors [62,63]. Although a number of sense modalitites are important in agonistic behavior [ 10, 38, 6 5 ] , olfaction appears to be the most important sense [2, 8, 10, 40, 9 5 ] , and changes in both adrenal and gonadal hormone levels have been reported to affect olfactory sensitivity [68, 69, 111]. Whether this effect on olfactory sensitivity is due to a direct action of hormones on the peripheral sense organs, or whether hormones affect olfactory sensitivity b y altering the state of the neural circuits which control the perception of olfactory stimuli is unknown. Thus, the model presented in Figure 1 includes a mechanism through which hormones might modify behavior through affecting the state of the receptors. It is most likely that hormones affect behavior through modifying directly the state of the brain systems, like the limbic system, which c o n t r o l the interpretation of stimuli and the integration of responses. Applying this proposition to the case of agonistic behavior, it is suggested that under one set of hormonal conditions, the responsiveness of the fear circuits or the det0nse circuits is increased, that of the aggression circuits is decreased, and the animal perceives the novel conspecific as fear-provoking and reacts more submissively or defensively, and less aggressively. Under another set of hormonal conditions, the aggression circuits are sensitized, the fear circuits are desensitized, the animal perceives the novel conspecific as aggression-provoking and reacts more aggressively. There have been few studies of this neural mediation proposition, although some indirect evidence supports this view: (1) There are relatively discrete neural circuits responsible for the control of aggressive and submissive or fearful responses, and these circuits differ from each other [35, 53, 55, 60]. (2) Implants of testosterone propionate directly into the septal area restore the aggressiveness of castrated mice [ 8 9 ] , and implants of testosterone into the preoptic area restore the aggressiveness of castrated ring doves [6]. Both of these neural areas have been shown to be important in the control of aggression [55,60], and hormone injections into other, irrelevant areas do not affect aggressiveness [891. (3) Although there have been no direct tests of whether hormone implants into the brain can affect submissive responses, it is clear that hormones can affect other kinds of fear responses through directly modifying the state of specific neural circuits (see reviews in [26, 46, 91,97]).

229 HYPOTHESES 2 AND 3: EFFECTS O F AGONISTIC EXPERIENCES ON ENDOCRINE FUNCTION Hypotheses 2 and 3 are concerned with the functions of the hormonal responses to agonistic stimuli and agonistic experiences. Hypothesis 2 suggests that one function of these responses is as part of a feedback mechanism to modify continuing and future responses in agonistic situations. Hypothesis 3 suggests that another function of these hormonal responses is to alter the individual's stimulus qualities so that the way in which the environmental stimuli, particularly those of other individuals, impinge on it will be altered. In order to assess the validity of these hypotheses, it is necessary to review briefly the effects of agonistic experiences on endocrine function. THE DATA Experiences in agonistic situations have marked effects on both pituitary-adrenocortical and pituitary-gonadal function. Following competition, defeated animals show increased levels of adrenocortical activity, while victorious animals seem unaffected [4, 31, 32]. In fact, the mere threat of defeat is suffident to elicit increases in adrenocortical activity in previously defeated mice [33]. A similar relationship has been observed between dominance status and adrenocortical activity in rodents. Subordinate rodents, living under the constant threat of defeat or subjected to repeated defeats, have higher levels of pituitary-adrenocortical activity than dominant rodents [45, 79, 104]. The effects of competition on pituitary-gonadal function are less clear than those on adrenocortical activity. Although Vale and his colleagues [109,110] found no direct effects of fighting or defeat on testicular function, Bronson and Desjardins [30] found that defeat, but not victory, depresses gonadal activity. Competition also affects gonadotrophin activity, and the nature of the animal's agonistic experiences determines the form and duration of its gonadotrophin responses to competition. Fighting leads to decreased serum levels of both luteinizing hormone (LH) and follicle stimulating hormone (FSH), and the magnitude of this depression of gonadotrophin levels is greater in defeated than in victorious mice [34]. The temporal characteristics of the gonadotrophin responses to competition also are different for defeated and victorious mice: FSH levels remain depressed longer following fighting in defeated mice than in victorious mice. However, LH levels remain depressed for long post-experience time periods, and the outcome of the fight does not influence the rate of return of LH levels toward normal levels [27]. HOW DO AGONISTIC EXPERIENCES LEAD TO CHANGES IN ENDOCRINE FUNCTION? The peripheral receptors which receive information about the outcome of an agonistic encounter are not directly connected to the endocrine glands. Therefore, it is likely that the effects of agonistic experiences on endocrine function are mediated through the central nervous system, which b o t h is sensitive to the state of the peripheral receptors and integrates the functioning of the endocrine system (cf., [ 114] ). Agonistic experiences produce dramatic changes in the state of the central nervous system circuits which control endocrine function. Defeat has a significant effect on

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protein synthesis in the brain [50] and alters the state of the brain neurotransmitter systems. Daily fighting experiences lead to increases in central catecholamine and serotonin levels [81,113], and these increases are more pronounced in some brain areas than in others [51, 52, 112]. This altered neurotransmitter activity in particular brain circuits, like the limbic circuits, should be reflected in altered activity levels of both the pituitary-adrenocortical and pituitary-gonadal axes, since these endocrine subsystems are ultimately under the control of precisely these neural areas [3, 96, 97, 107]. SOME FUNCTIONS OF THE HORMONAL RESPONSES TO AGONISTIC EXPERIENCES

Feedback: Effects on Continuing and Fugure Agonistic Behaviors (Hypothesis 2) It is striking that the effects of defeat on endocrine function are similar in form to those experimental manipulations which are most effective in reducing aggressiveness: Animals exposed to defeat have high levels of pituitaryadrenocortical activity and low levels of androgen activity [30,32], and naive subjects with these characteristics are less aggressive than normal animals [75]. Agonistic experiences are not merely instantaneous, and it is probable that the animal's hormonal characteristics change as a result of its initial experiences in the situation. Thus, if an animal's initial experience is defeat, its hormonal characteristics will change in the direction of nonaggressive animals, and, therefore, its behavior should become less and less aggressive and more and more submissive. According to this view (Hypothesis 2), initial experiences in agonistic situations feed back through the endocrine system to alter the animal's perception of the agonistic stimuli and, therefore, its behavior. It also is possible that these initial responses to defeat produce long-term modifications in the animal's hormonal state so that future agonistic reactions will be modified as a function of prior experiences. Early exposure to defeat predisposes an animal to be nonaggressive in adulthood [61], and prior experiences of defeat in adulthood condition an animal to be more subordinate the next time it encounters an agonistic situation [101 ]. It is possible that the hormonal responses to defeat are sufficiently longlasting that a previously-defeated animal enters future agonistic situations in a different baseline hormonal state from inexperienced animals. Thus, the previously-defeated animal would perceive the agonistic stimuli as more fear-provoking, and its behavior would be more submissive and less aggressive (Hypothesis 2). There have been no direct tests of Hypothesis 2, and, therefore, this hypothesis is based solely on the similarity in the forms of the hormonal responses to agonistic experiences like defeat and those states produced by the experimental manipulations which seem to be most effective in modifying aggressiveness. It may be, of course, that this similarity is merely coincidental, and that changes in endocrine characteristics resulting from agonistic experiences do not feed back into the system as proposed here. An evaluation of the validity of Hypothesis 2, therefore, will have to await further investigation (see suggestions below).

Effects on A ttackability (Hypothesis 3) In addition to suppressing continuing aggressive re-

sponses and facilitating the expression of subordinate behaviors, the endocrine responses to defeat may also alter the animal's attackability, and thereby reduce the amount of aggression to which it is subjected. The stimulus qualities of the opponent are critical to the amount of aggression displayed [37], and the behavioral responses and hormonal state of an animal have dramatic effects on its ability to elicit aggression. Changes in both pituitary-adrenocortical and pituitary-gonadal activity levels seem to modify the attackability of an animal, probably through modifying the characteristics of the pheromones which it releases. The effects of endocrine changes on attackability are importnat to Hypothesis 3 because the hormonal responses to defeat are of the same form as those experimental manipulations which have been shown to be effective in reducing the tendency of an animal to elicit aggression. Defeat leads to increases in ACTH levels, and increases in ACTH levels lead to reduce attackability [25,92]. Defeat also seems to lead to reduced androgen levels [30], and the aggression-promoting pheromone released by male mice seems to be androgen-dependent (e.g., [66, 86, 87, 88]. Thus, as androgen levels fall following defeat, so should the animal's tendencies to elicit aggression. As in the case of Hypothesis 2, Hypothesis 3 is based on the similarity in form of the hormonal responses to different agonistic experiences and those hormonal states produced by the experimental manipulations which are effective in modifying an animal's stimulus qualities. Because there have been no direct tests of the continuity in the relationship of endocrine changes following agonistic experience and alterations in the animal's stimulus qualities, an evaluation of the validity of Hypothesis 3, like that of Hypothesis 2, demands further investigation. If Hypotheses 2 and 3 are accurate, the function of the endocrine responses to agonistic experiences are more broadly adaptive than originally suspected. Early investigations into endocrine responses to agonistic contact suggested that the primary function of these hormonal responses was to provide physical adaptation to the stresses inherent in competition, partic~arly defeat [32,33]. Hypotheses 2 and 3 suggest additional, behavioral adaptations as a consequence of the endocrine responses to competition. Hypothesis 2 suggests a mechanism whereby a defeated animal's behavior becomes less aggressive and more submissive, thereby decreasing the amount of aggression to which it is subjected and reducing the amount of stress to which it is exposed. Hypothesis 3 suggests another mechanism by which a defeated animal reduces the amount of aggression or stress to which it is exposed: changes in its aggression-eliciting properties. As the animal's aggressioneliciting potential decreases, so should the amount of aggression to which it is subjected. Thus, it is likely that the endocrine responses to competition provide at least three mechanisms for adapting to the stresses of competition, particularly defeat: a physical mechanism of adaptation to stress, and a behavioral change and a stimulus quality change which serve to reduce the amount of stress to which the animal is exposed. SUMMARY AND CONCLUSIONS The model presented in Figure 1 and the three hypotheses which it incorporates were tested by applying them to the case of the interaction between endocrine function and agonistic behaviors. The data reviewed suggest

HORMONES AND AGONISTIC BEHAVIOR

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FIG. 2. A two-animal version of the model. that changes in endocrine function do modify the form and intensity of agonistic responses to standard exciting stimuli (Hypothesis 1). Under some hormonal states, the animal appears to react more aggressively. Under other hormonal states, the animal appears to react more submissively. Hypotheses 2 and 3 are concerned with some of the functions of the hormonal responses to exciting stimuli and behavioral experiences. Hypothesis 2 suggests that one function of the hormonal responses to agonistic experiences is to feed back and modify both continuing and future agonistic response patterns. This hypothesis has not been tested directly, but the similarity between the hormonal responses to defeat and those experimental manipulations which seem most effective in reducing aggressiveness suggests that these responses could modify either continuing or future agonistic behaviors. Hypothesis 3 suggests that another function of the hormonal responses to agonistic experiences is to alter the animal's stimulus qualities so that the opponent's reactions to it change, and,

therefore, the amount of aggression to which the animal is exposed decreases. Again, we must rely on indirect evidence to evaluate this hypothesis: The form of the hormonal responses to defeat are such that if they had been produced experimentally they would reduce the animal's attackability and, thus, the amount of aggression to which it is subjected. SOME COMMENTS ON THE MODEL The model presented in Figure 1 emphasizes the relationship between hormones and agonistic behavior in only one animal. However, the proposed effects on the exciting stimulus of hormone-induced changes in the animal's stimulus qualities and the fact that agonistic encounters involve at least two individuals argue that a complete description of hormones and behavior in agonistic situations should include the relationship between hormones and behavior for both antagonists. Therefore, a

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two-animal version of the model is presented in Figure 2, which includes mirror images of the model presented in Figure 1. This version of the model emphasizes the interaction between the behavioral and hormonal states of both animals in affecting each other's behavioral and physiological responses. The model proposed here emphasizes the fact that agonistic interactions are not instantaneous but are relatively long-listing. Therefore, any description of hormonebehavior interactions should include the roles of changes in behavior patterns and hormonal states which are a consequence of prior or initial experiences. This focus on the dynamic and continuing interaction between the individual and its environment is similar to the descriptions of the relationship of hormones and reproductive behaviors suggested by other theorists (e.g., [11,43, 67, 114] ). Most recent conceptions of hormone-behavior interactions (e.g., [11, 12, 85]) have included the proposition that if an animal is in the appropriate hormonal state, it is sensitized to environmental releasing stimuli. This proposition is developed somewhat further here in Hypothesis 1 which suggests that rather than merely sensitizing or desensitizing the organism to environmental stimuli, the hormonal state of an animal predisposes it to react in a specific way to those stimuli. Under one set of hormonal conditions the animal will react in one way; under another set of hormonal conditions the animal will react in another way to the same stimuli. DIRECTIONS FOR RESEARCH It is difficult to assess completely the validity of the model proposed here in the absence of a body of data covering many of the issues this model raises. Therefore, the model's immediate utility may lie as much in its ability to suggest directions for research as in its ability to describe what we know. First, this model reemphasizes the need to study the degree of specificity in hormone-behavior interactions [1 17]. Although it is clear that no single hormone affects only a single type of behavior, and the reverse, Hypothesis 1 and the data on which it is based suggest that the

hormonal state of an animal can predispose it to react in specific alternative ways to a standard agonistic stimulus. It is clear from our review that much additional information is needed to .understand this relationship between hormones and agonistic behavior more completely. Second, although in a gross way we have learned much about the neural mediation of hormonal effects on behavior (cf., [77] ), it may be profitable to begin to specify which particular aspects of neural control of behavior are dependent on the animal's baseline hormonal state: Do hormones affect reactions to environmental or exciting stimuli at the level of sensory coding, at the level of response coordination, or at some intermediate level, like motivation? Third, although some investigators (e.g., [ 1 1 , 6 7 ] ) h a v e focused on the ways in which hormonal responses to environmental stimuli or behavioral experiences can modify dynamic behavior patterns, like reproductive behaviors, this approach has not been applied to other examples of hormone-behavior interactions, like agonistic behavior. Therefore, it might be profitable to begin to study in depth the ways in which the hormonal responses to environmental or experiential stimuli can feed back and modify both an animal's continuing and its future behavioral response patterns (Hypothesis 2). Finally, the view expressed by the model proposed in Figures 1 and 2 and articulated particularly in Hypotheses 2 and 3 emphasizes the need to study the long-chain interactions between dynamic organisms and their dynamic environments. I believe that we have studied the relationship between hormones and agonistic behavior too much as if our subjects were static organisms, interacting once and only instantaneously with a static environment. Some investigators [67] have begun work on these long-chain interactions for the case of reproductive behaviors, and the model proposed here suggests that we begin to apply this approach to the case of agonistic behavior. The form of the model provided in Figure 2 may provide specific clues as to the kinds of manipulations which would be most effective in studying this dynamic interaction among organisms and their environments.

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