Preface Brain Behav Evol 2014;84:79–80 DOI: 10.1159/000366460
Published online: September 20, 2014
Perspectives on Human Brain Evolution Chet C. Sherwood Department of Anthropology, The George Washington University, Washington, D.C., USA
Human brain evolution is arguably among the most difficult problems in biology, with many unresolved questions. It is still largely a mystery how and why brain size increased over the 6–8 million years since our lineage split from the other great apes. It is also unclear how evolutionary changes in brain morphology and molecular biology relate to the distinctive behaviors that our species exhibits in terms of language, abstract thinking, creativity and insight into mental states. The historical nature of human brain evolution requires data from fragmentary paleontological remains of hominin ancestors, their ecological context, and archaeological evidence of cultural products such as stone tools. These paleoanthropological data offer a window into the selective pressures that might have shaped the brain of ancestors and relatives in our lineage over millions of years. Unraveling the behavioral neuroscience of human brain specializations also poses a significant challenge. While it is relatively straightforward to document differences between humans and other primates in neuroanatomy, connectivity, cell biology and gene expression, it is much more difficult to understand how neural variation yields the cognitive differences that characterize our species. Furthermore, it is complicated to sort through the tens of millions of nucleotide base pair differences in the genome between humans and the great apes, in order to determine which ones have the most significance for our species’ unique brain development, structure and function. © 2014 S. Karger AG, Basel 0006–8977/14/0842–0079$39.50/0 E-Mail [email protected] www.karger.com/bbe
These challenges are being addressed by a community of dedicated investigators studying human evolutionary neuroscience. Over the last several decades, important advances have been fueled by the accumulation of data from a range of sources, including comparative neuroanatomy, evolutionary genomics and paleontological excavations. New opportunities now exist for integrating these diverse datasets using techniques from informatics and systems biology. Further progress in addressing major problems in human brain evolution therefore will be driven by interdisciplinary and collaborative research efforts that take advantage of emerging computational tools. This will demand that scientists from diverse backgrounds are able to communicate with one another regardless of their divergent technical expertise, theoretical history and particular jargon. For example, the differences in cranial endocast morphology among ancient hominin species can only be deciphered in the context of the insights offered by clinical neurology and functional neuroimaging. These lines of inquiry provide a basis for understanding the relationship between structure and function in the brain, which, in turn, can be applied to the interpretation of fossils. Similarly, cataloging differences in the genome between humans and other species reveals little about the evolution of behavior and cognition without an understanding of how specific mutations encode variation in the development of neural circuits and the physiological activity of cells. Chet C. Sherwood Department of Anthropology, The George Washington University 2110 G Street, NW Washington, DC 20052 (USA) E-Mail sherwood @ gwu.edu
This special issue of Brain, Behavior and Evolution represents an effort to bridge various disciplinary approaches to human brain evolution and bring them into conversation with one another. The articles collected in this volume stem from presentations given at the 25th Annual Karger Workshop in Evolutionary Neuroscience, held on November 7, 2013. The goal of the workshop was to gather researchers at the vanguard of human evolutionary neuroscience who approach the problem from diverse methodological and theoretical perspectives. In this issue, Christine Charvet and Barbara Finlay argue that developmental and anatomical gradients in the brain have cascading effects that are reflected in cellular and computational architecture, and which scale with overall brain size. The evidence that they present urges a view of human brain organization as the predictable outcome of highly coordinated developmental processes, rather than a hodgepodge of individual specializations. Jeremy Borjon and Asif Ghazanfar outline a provocative hypothesis that vocal turn taking, which is a characteristic feature of human conversations, does not require a large and convoluted brain. They describe the dynamics of vocal exchange in a small cooperative-breeding New World monkey species, the common marmoset, which exhibits convergent similarities to human conversational turn taking. This challenges the notion that all features of human language are necessarily correlated with brain size evolution, but instead suggests that subtle rewiring of motivational circuitry might also play a critical role. Noriyoshi Usui, Marissa Co and Genevieve Konopka present a valuable overview of molecular evolution underlying human language and cognition by drawing on evidence from neuropsychiatric and neurodevelopmental disorders as well as comparative genomics. They highlight the manner in which analysis of networks of gene expression covariance can be a powerful means of revealing modifications in biological pathways. Simon Neubauer’s contribution discusses the opportunities that fossil endocasts afford to glimpse brain evolution in extinct human ancestors and relatives, with par-
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Brain Behav Evol 2014;84:79–80 DOI: 10.1159/000366460
ticular emphasis on examining differences in the growth and development of endocranial shape. This research draws attention to evolutionary changes of the parietal cortex in the early stages of postnatal development in modern humans. Kari Hanson, Branka Hrvoj-Mihic and Katerina Semendeferi provide a comprehensive overview of the microstructural anatomy of the human cerebral cortex as compared to other great apes. Their review integrates findings concerning human neurodevelopmental disorders, such as William’s syndrome and autism, to shed light on the potential functional significance of variation in pyramidal neuron morphology and inhibitory interneuron distributions. Finally, Richard Passingham and Jeroen Smaers revisit one of the most controversial and enduring questions in human evolutionary neuroscience – is the prefrontal cortex especially enlarged? They marshal new analyses to examine prefrontal cortex size evolution in primates taking into account scaling against sensory and other association cortical systems. They conclude that the prefrontal cortex is disproportionately expanded and therefore might endow humans with enhanced capacities for action planning and generating series of goals. From reading these papers, one thing is for certain – the outlook for human evolutionary neuroscience is exciting. As new tools and different perspectives are integrated into the exploration of human brain evolution, we are gaining a deeper understanding of the dynamic interactions among genes, neurons, circuits, morphology and behavior that have resulted in our species’ extraordinary cognitive capacities. Future breakthroughs will come when evolutionary geneticists feel compelled to be knowledgeable about the latest fossil discoveries, comparative neuroanatomists become ever more aware of the developmental processes that shape phenotypes, and evolutionary psychologists seek out and test the latest findings in behavioral genetics. Ultimately, the most innovative research that will crack the problem of human brain evolution will require collaboration across traditional disciplinary boundaries.
Sherwood
Copyright: S. Karger AG, Basel 2014. Reproduced with the permission of S. Karger AG, Basel. Further reproduction or distribution (electronic or otherwise) is prohibited without permission from the copyright holder.
Published online: September 20, 2014
Perspectives on Human Brain Evolution Chet C. Sherwood Department of Anthropology, The George Washington University, Washington, D.C., USA
Human brain evolution is arguably among the most difficult problems in biology, with many unresolved questions. It is still largely a mystery how and why brain size increased over the 6–8 million years since our lineage split from the other great apes. It is also unclear how evolutionary changes in brain morphology and molecular biology relate to the distinctive behaviors that our species exhibits in terms of language, abstract thinking, creativity and insight into mental states. The historical nature of human brain evolution requires data from fragmentary paleontological remains of hominin ancestors, their ecological context, and archaeological evidence of cultural products such as stone tools. These paleoanthropological data offer a window into the selective pressures that might have shaped the brain of ancestors and relatives in our lineage over millions of years. Unraveling the behavioral neuroscience of human brain specializations also poses a significant challenge. While it is relatively straightforward to document differences between humans and other primates in neuroanatomy, connectivity, cell biology and gene expression, it is much more difficult to understand how neural variation yields the cognitive differences that characterize our species. Furthermore, it is complicated to sort through the tens of millions of nucleotide base pair differences in the genome between humans and the great apes, in order to determine which ones have the most significance for our species’ unique brain development, structure and function. © 2014 S. Karger AG, Basel 0006–8977/14/0842–0079$39.50/0 E-Mail [email protected] www.karger.com/bbe
These challenges are being addressed by a community of dedicated investigators studying human evolutionary neuroscience. Over the last several decades, important advances have been fueled by the accumulation of data from a range of sources, including comparative neuroanatomy, evolutionary genomics and paleontological excavations. New opportunities now exist for integrating these diverse datasets using techniques from informatics and systems biology. Further progress in addressing major problems in human brain evolution therefore will be driven by interdisciplinary and collaborative research efforts that take advantage of emerging computational tools. This will demand that scientists from diverse backgrounds are able to communicate with one another regardless of their divergent technical expertise, theoretical history and particular jargon. For example, the differences in cranial endocast morphology among ancient hominin species can only be deciphered in the context of the insights offered by clinical neurology and functional neuroimaging. These lines of inquiry provide a basis for understanding the relationship between structure and function in the brain, which, in turn, can be applied to the interpretation of fossils. Similarly, cataloging differences in the genome between humans and other species reveals little about the evolution of behavior and cognition without an understanding of how specific mutations encode variation in the development of neural circuits and the physiological activity of cells. Chet C. Sherwood Department of Anthropology, The George Washington University 2110 G Street, NW Washington, DC 20052 (USA) E-Mail sherwood @ gwu.edu
This special issue of Brain, Behavior and Evolution represents an effort to bridge various disciplinary approaches to human brain evolution and bring them into conversation with one another. The articles collected in this volume stem from presentations given at the 25th Annual Karger Workshop in Evolutionary Neuroscience, held on November 7, 2013. The goal of the workshop was to gather researchers at the vanguard of human evolutionary neuroscience who approach the problem from diverse methodological and theoretical perspectives. In this issue, Christine Charvet and Barbara Finlay argue that developmental and anatomical gradients in the brain have cascading effects that are reflected in cellular and computational architecture, and which scale with overall brain size. The evidence that they present urges a view of human brain organization as the predictable outcome of highly coordinated developmental processes, rather than a hodgepodge of individual specializations. Jeremy Borjon and Asif Ghazanfar outline a provocative hypothesis that vocal turn taking, which is a characteristic feature of human conversations, does not require a large and convoluted brain. They describe the dynamics of vocal exchange in a small cooperative-breeding New World monkey species, the common marmoset, which exhibits convergent similarities to human conversational turn taking. This challenges the notion that all features of human language are necessarily correlated with brain size evolution, but instead suggests that subtle rewiring of motivational circuitry might also play a critical role. Noriyoshi Usui, Marissa Co and Genevieve Konopka present a valuable overview of molecular evolution underlying human language and cognition by drawing on evidence from neuropsychiatric and neurodevelopmental disorders as well as comparative genomics. They highlight the manner in which analysis of networks of gene expression covariance can be a powerful means of revealing modifications in biological pathways. Simon Neubauer’s contribution discusses the opportunities that fossil endocasts afford to glimpse brain evolution in extinct human ancestors and relatives, with par-
80
Brain Behav Evol 2014;84:79–80 DOI: 10.1159/000366460
ticular emphasis on examining differences in the growth and development of endocranial shape. This research draws attention to evolutionary changes of the parietal cortex in the early stages of postnatal development in modern humans. Kari Hanson, Branka Hrvoj-Mihic and Katerina Semendeferi provide a comprehensive overview of the microstructural anatomy of the human cerebral cortex as compared to other great apes. Their review integrates findings concerning human neurodevelopmental disorders, such as William’s syndrome and autism, to shed light on the potential functional significance of variation in pyramidal neuron morphology and inhibitory interneuron distributions. Finally, Richard Passingham and Jeroen Smaers revisit one of the most controversial and enduring questions in human evolutionary neuroscience – is the prefrontal cortex especially enlarged? They marshal new analyses to examine prefrontal cortex size evolution in primates taking into account scaling against sensory and other association cortical systems. They conclude that the prefrontal cortex is disproportionately expanded and therefore might endow humans with enhanced capacities for action planning and generating series of goals. From reading these papers, one thing is for certain – the outlook for human evolutionary neuroscience is exciting. As new tools and different perspectives are integrated into the exploration of human brain evolution, we are gaining a deeper understanding of the dynamic interactions among genes, neurons, circuits, morphology and behavior that have resulted in our species’ extraordinary cognitive capacities. Future breakthroughs will come when evolutionary geneticists feel compelled to be knowledgeable about the latest fossil discoveries, comparative neuroanatomists become ever more aware of the developmental processes that shape phenotypes, and evolutionary psychologists seek out and test the latest findings in behavioral genetics. Ultimately, the most innovative research that will crack the problem of human brain evolution will require collaboration across traditional disciplinary boundaries.
Sherwood
Copyright: S. Karger AG, Basel 2014. Reproduced with the permission of S. Karger AG, Basel. Further reproduction or distribution (electronic or otherwise) is prohibited without permission from the copyright holder.
