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In the Light of Evolution
Volume VI: Brain and Behavior



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In the Light of Evolution Volume VI: Brain and Behavior

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In the Light of Evolution Volume VI: Brain and Behavior GEORG F. STRIEDTER, JOHN C. AVISE, and FRANCISCO J. AYALA, Editors THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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THE NATIONAL ACADEMIES PRESS   500 Fifth Street, NW  Washington, DC 20001 This volume is based on the Arthur M. Sackler Colloquium of the National Academy of Sci- ences, “In the Light of Evolution VI: Brain and Behavior,” held January 20-21, 2012, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, California. The articles appearing in these pages were contributed by speakers at the colloquium and have been anonymously reviewed. Any opinions, findings, conclusions, or recommendations expressed in this volume are those of the authors and do not necessarily reflect the view of the National Academy of Sciences. In the light of evolution / John C. Avise and Francisco J. Ayala, editors. p. cm. Vol. I based on a colloquium of the National Academy of Sciences, held December 1–2, 2006, in Irvine, California. Includes bibliographical references. ISBN-13: 978-0-309-26175-3 ISBN-10: 0-309-26175-9 1. Evolution (Biology)—Congresses. I. Avise, John C, 1948–. II . Ayala, Francisco José, 1934– III . National Academy of Sciences (U.S.) QH359.I55 2007 576.8—dc22 2007032455 Additional copies of this book are available from the National Academies Press, 500 Fifth St., NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www. nap.edu. Cover image: Pictured is a diffusion MRI image of a human brain, viewed from above, with the back of the head at the bottom of the image. Each line represents thousands of axons, traveling as a group along a particular axis (green: front to back; red: left to right; blue: top to bottom). This technique represents one of numerous methods used to infer the evolutionary processes that shaped the brain and behavior. Articles in this Arthur M. Sackler Colloquium, “In the Light of Evolution VI: Brain and Behavior,” explore research on how and why com- plex nervous systems evolved, showing the progress that has been made since the dawn of evolutionary neuroscience 150 years ago. Image courtesy of Patric Hagmann (Department of Radiology, University Hospital Center, University of Lausanne, Switzerland). Copyright 2013 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the ­ cademy has a mandate that requires it to advise the federal govern- A ment on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its mem- bers, sharing with the National Academy of Sciences the responsibility for advis- ing the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Insti- tute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in pro- viding services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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Arthur M. Sackler, M.D. 1913–1987 Born in Brooklyn, New York, Arthur M. Sackler was edu­cated in the arts, sciences, and humanities at New York University. These interests remained the focus of his life, as he became widely known as a scientist, art collector, and philan­hropist, t endowing institutions of learning and culture through­ ut the world. o He felt that his fundamental role was as a doctor, a vocation he decided upon at the age of four. After completing his internship and service as house physician at Lincoln Hospital in New York City, he became a resident in psychiatry at Creedmoor State Hospital. There, in the 1940s, he started research that resulted in more than 150 papers in neuroendocri- nology, psychiatry, and experimental medicine. He considered his scien- tific research in the metabolic basis of schizophrenia his most significant contribution to science and served as editor of the Journal of Clinical and Experimental Psychobiology from 1950 to 1962. In 1960 he started publica- tion of Medical Tribune, a weekly medical newspaper that reached over one million readers in 20 countries. He established the Laboratories for Therapeutic Research in 1938, a facility in New York for basic research that he directed until 1983. As a generous benefactor to the causes of medicine and basic science, Arthur Sackler built and contributed to a wide range of scientific insti- tutions: the Sackler School of Medicine established in 1972 at Tel Aviv University, Tel Aviv, Israel; the Sackler Institute of Graduate Biomedical Science at New York University, founded in 1980; the Arthur M. Sackler Science Center dedicated in 1985 at Clark University, Worcester, Massachu- setts; and the Sackler School of Graduate Biomedical Sciences, established in 1980, and the Arthur M. Sackler Center for Health Communications, established in 1986, both at Tufts University, Boston, Massachusetts. His pre-eminence in the art world is already legendary. According to his wife Jillian, one of his favorite relaxations was to visit museums and art galleries and pick out great pieces others had overlooked. His interest in art is reflected in his philanthropy; he endowed galleries at the Metropolitan Museum of Art and Princeton University, a museum at vii

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Harvard University, and the Arthur M. Sackler Gallery of Asian Art in Washington, D.C. True to his oft-stated determination to create bridges between peoples, he offered to build a teaching museum in China, which Jillian made possible after his death, and in 1993 opened the Arthur M. Sackler Museum of Art and Archaeology at Peking University in Beijing. In a world that often sees science and art as two separate cultures, Arthur Sackler saw them as inextricably related. In a speech given at the State University of New York at Stony Brook, Some reflections on the arts, sciences and humanities, a year before his death, he observed: ‘‘Communi- cation is, for me, the primum movens of all culture. In the arts . . . I find the emotional component most moving. In science, it is the intellectual content. Both are deeply interlinked in the humanities.’’ The Arthur M. Sackler Colloquia at the National Academy of Sciences pay tribute to this faith in communication as the prime mover of knowledge and culture. viii

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Contents Arthur M. Sackler Biography vii Preface to the In the Light of Evolution Series xiii Preface to In the Light of Evolution VI: Brain and Behavior xv PART I EVOLUTIONARY ORIGINS OF NEURONS AND NERVOUS SYSTEMS 1 1 Functionalization of a Protosynaptic Gene Expression Network 3  Cecilia Conaco, Danielle S. Bassett, Hongjun Zhou, Mary Luz Arcila, Sandie M. Degnan, Bernard M. Degnan, and Kenneth S. Kosik 2 Adaptive Evolution of Voltage-Gated Sodium Channels: The First 800 Million Years 21 Harold H. Zakon 3 Evolution of Centralized Nervous Systems: Two Schools of Evolutionary Thought 37 R. Glenn Northcutt ix

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x / Contents PART II DEVELOPMENTAL AND ADULT VARIATION IN NEURAL ORGANIZATION 57 4 Evolving Specialization of the Arthropod Nervous System 61 Erin Jarvis, Heather S. Bruce, and Nipam H. Patel 5 Expansion, Folding, and Abnormal Lamination of the Chick Optic Tectum After Intraventricular Injections of FGF2 75  Luke D. McGowan, Roula A. Alaama, Amanda C. Freise, Johnny C. Huang, Christine J. Charvet, and Georg F. Striedter 6 Cortical Evolution in Mammals: The Bane and Beauty of Phenotypic Variability 91 Leah A. Krubitzer and Adele M. H. Seelke 7 Evolution of Columns, Modules, and Domains in the Neocortex of Primates 113  H. Kaas Jon 8 The Remarkable, Yet Not Extraordinary, Human Brain as a Scaled-Up Primate Brain and Its Associated Cost 127 Suzana Herculano-Houzel PART III FROM NEURAL CIRCUIT EVOLUTION TO ADAPTIVE BEHAVIOR 149 9 Homology and Homoplasy of Swimming Behaviors and Neural Circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia) 153  James M. Newcomb, Akira Sakurai, Joshua L. Lillvis, Charuni A. Gunaratne, and Paul S. Katz 10  Shared Developmental and Evolutionary Origins for Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling 175 Andrew H. Bass and Boris P. Chagnaud 11  Flock or Fight: Neurochemical Signatures of Divergent To Life Histories in Sparrows 193 James L. Goodson, Leah C. Wilson, and Sara E. Schrock

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Contents / xi 12  From Chemotaxis to the Cognitive Map: The Function of Olfaction 211 Lucia F. Jacobs 13  Evolution of Brains and Behavior for Optimal Foraging: A Tale of Two Predators 229 Kenneth C. Catania PART IV PHYLOGENY OF HUMAN BRAINS AND HUMAN MINDS 251 14  Human Brain Evolution: From Gene Discovery to Phenotype Discovery 253 Todd M. Preuss 15  Integration of Faces and Vocalizations in Ventral Prefrontal Cortex: Implications for the Evolution of Audiovisual Speech 273 Lizabeth M. Romanski 16  Math, Monkeys, and the Developing Brain 293 Jessica F. Cantlon 17  Hierarchical Model of the Evolution of Human Brain A Specializations 313 H. Clark Barrett Epilogue 335 References 337 Index 397

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Preface to the In the Light of Evolution Series B iodiversity—the genetic variety of life—is an exuberant product of the evolutionary past, a vast human-supportive resource (aesthetic, intellectual, and material) of the present, and a rich legacy to cher- ish and preserve for the future. Two urgent challenges, and opportunities, for 21st-century science are to gain deeper insights into the evolutionary processes that foster biotic diversity, and to translate that understanding into workable solutions for the regional and global crises that biodiver- sity currently faces. A grasp of evolutionary principles and processes is important in other societal arenas as well, such as education, medicine, sociology, and other applied fields including agriculture, pharmacology, and biotechnology. The ramifications of evolutionary thought also extend into learned realms traditionally reserved for philosophy and religion. In 1973, Theodosius Dobzhansky penned a short commentary entitled “Nothing in biology makes sense except in the light of evolution.” Most scientists agree that evolution provides the unifying framework for inter- preting biological phenomena that otherwise can often seem unrelated and perhaps unintelligible. Given the central position of evolutionary thought in biology, it is sadly ironic that evolutionary perspectives outside the sciences have often been neglected, misunderstood, or purposefully misrepresented. The central goal of the In the Light of Evolution (ILE) series is to pro- mote the evolutionary sciences through state-of-the-art colloquia—in the series of Arthur M. Sackler colloquia sponsored by the National Academy of Sciences—and their published proceedings. Each installment explores xiii

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xiv  /  Preface to the In the Light of Evolution Series evolutionary perspectives on a particular biological topic that is scientifi- cally intriguing but also has special relevance to contemporary societal issues or challenges. Individually and collectively, the ILE series aims to interpret phenomena in various areas of biology through the lens of evolution, address some of the most intellectually engaging as well as pragmatically important societal issues of our times, and foster a greater appreciation of evolutionary biology as a consolidating foundation for the life sciences. The organizers and founding editors of this effort (Avise and Ayala) are the academic grandson and son, respectively, of Theodosius Dobzhansky, to whose fond memory this ILE series is dedicated. May Dobzhansky’s words and insights continue to inspire rational scientific inquiry into nature’s marvelous operations. John C. Avise and Francisco J. Ayala Department of Ecology and Evolutionary Biology, University of California, Irvine (January 2007)

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Preface to In the Light of Evolution, Volume VI: Brain and Behavior T his book is the outgrowth of the Arthur M. Sackler Colloquium “Brain and Behavior,” which was sponsored by the National Acad- emy of Sciences on January 20–21, 2012, at the Academy’s Arnold and Mabel Beckman Center in Irvine, CA. It is the sixth in a series of Colloquia under the general title “In the Light of Evolution.” The first five books in this series were titled Adaptation and Complex Design (Avise and Ayala, 2007), Biodiversity and Extinction (Avise et al., 2008), Two Centuries of Darwin (Avise and Ayala, 2009), The Human Condition (Avise and Ayala, 2010), and Cooperation and Conflict (Strassmann et al., 2011). In On the Origin of Species by Means of Natural Selection, Darwin (1859) barely mentioned the brain. Only in The Descent of Man, and Selection in Relation to Sex, published in 1871, did Darwin emphasize that the human nervous system, like any other organ system, must have evolved. Even so, Darwin himself wrote little on the brain. Instead, Darwin asked his good friend T. H. Huxley to write a chapter for the second edition of The Descent of Man, and Selection in Relation to Sex that dealt specifically with human brain evolution. In this chapter, Huxley laid to rest Richard Owen’s ear- lier argument that human brains are outliers among mammalian brains. Instead, Huxley argued that our brains resemble the brains of other apes in all fundamental respects. He even downplayed the greater size of human brains, noting that brain size is quite variable among humans. Importantly, Huxley did not deny that our brains must somehow differ from the brains of other apes, for he could see no other way to explain our unique cognitive capacities, most notably language. However, Huxley xv

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xvi / Preface to In the Light of Evolution, Volume VI (1863b) postulated that the differences that set our brains apart are not apparent in gross dissections (Cosans, 1994; Desmond, 1994; Gross, 1998; Striedter, 2005). Of course, in the days of Darwin and Huxley, the only methods avail- able for studying large brains were gross dissections or, for functional analyses, gross brain lesions. It was only in the late 1880s that Ramón y Cajal focused neuroanatomy onto structural details by applying Golgi’s famous staining method to the nervous systems of various species (De Carlos and Borrell, 2007). Similarly, techniques for electrical recording of neural activity and brain stimulation were just starting to be developed in the 1870s by Richard Canton, Eduard Hitzig, and many other pioneers (Ferrier, 1886; Young, 1970; Niedermeyer, 2005). Aside from these techni- cal constraints, neurobiological knowledge was limited in Darwin’s day to relatively few species. In particular, ape brains were rare in England at the time, because they could only be obtained through research expedi- tions to Africa. Gorillas, for example, were not even discovered by Western scientists until Richard Owen (1859) described them and their brains in the late 1850s. Since that dawn of evolutionary neuroscience, the arsenal of meth- ods and panoply of data relevant to brain evolution have expanded tre- mendously. Intracellular and extracellular chronic recording techniques, immunohistochemistry, axon tracing, and excitotoxic brain lesions are just a few of the many methods that revolutionized our understanding of brain structure and function. Obviously, neuroscience has also been trans- formed by molecular methods that Darwin could not have envisioned. Researchers can now compare gene sequences and gene expression pat- terns across species. They can also test causal hypotheses about how genes control neural development, brain function, and, ultimately, behavior. Collectively, these methods make it possible to compare across species not just individual structures, such as genes or brain regions, but molecular interactions, developmental processes, and intriguing behaviors. Finally, the range of species studied by comparative neurobiologists now includes not just a few model species but a broad assemblage of vertebrates and, increasingly, invertebrates (Strausfeld, 2012). These methodological advances have unleashed a flood of data rel- evant to brain evolution. Fortunately, conceptual advances in data analysis kept pace. Particularly important have been breakthroughs in phyloge- netic systematics, which have yielded more elaborate and detailed phy- logenetic trees, or cladograms, and sophisticated statistical methods for evaluating phylogenetic correlations between various traits (Nunn, 2011). Cladists have also developed a rigorous methodology for distinguishing similarities caused by homology from those similarities that resulted from independent evolution (Northcutt, 1984; Nieuwenhuys, 1994a; Pritz,

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Preface to In the Light of Evolution, Volume VI / xvii 2005). With these methodologies, comparative biologists can begin to infer the evolutionary processes that created the complex tapestry of neurologi- cal systems in extant species. Because the field of evolutionary neuroscience now includes a vast array of different approaches, data types, and species, how can one select from this diversity a set of 17 chapters that represent the field adequately? The task seems Herculean, if not Sisyphean. Confronted with this chal- lenge, we opted for an eclectic approach. Thus, we here gather 17 chapters that represent a broad assortment of contemporary research in evolution- ary neurobiology.

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