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In the Light of Evolution

Volume VII: The Human Mental Machinery



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In the Light of Evolution Volume VII: The Human Mental Machinery

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In the Light of Evolution Volume VII: The Human Mental Machinery CAMILO J. CELA-CONDE, RAÚL GUTIÉRREZ LOMBARDO, 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 Acad- emy of Sciences, “The Human Mental Machinery,” held January 11–12, 2013, 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 col- loquium and have been anonymously reviewed. Any opinions, findings, conclu- sions, 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: 978-0-309-29640-3 ISBN-10: 0-309-29640-4 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., N.W., Lockbox 285, Washington, DC 10055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Cover image: Evoking a sense of beauty and wonder, this limestone carving of Buddha’s head is thought to have been part of a monumental statue from the cave temples of Xiangtangshan in China. Aesthetic values are one of the unique mental traits of humans, along with others such as self-reflection and ethics. Understand- ing the brain processes behind these traits and how they evolved is the topic of the Sackler Colloquium, In the Light of Evolution VII: The Human Mental Machinery. Photograph by John Tsantes (Image used with permission from the Freer Gallery of Art and the Arthur M. Sackler Gallery, Smithsonian Institution, Washington, DC). Copyright 2014 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. C. D. Mote, Jr., 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. C. D. Mote, Jr., 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: The Human Mental Machinery xv PART I CURRENT STUDY OF THE MIND/BRAIN RELATIONSHIPS 1 1 Theory of Mind and Darwin’s Legacy 3 John Searle 2 Affiliation, Empathy, and the Origins of Theory of Mind 19 Robert M. Seyfarth and Dorothy L. Cheney 3 Evolution of Consciousness: Phylogeny, Ontogeny, and Emergence from General Anesthesia 37 George A. Mashour and Michael T. Alkire ix

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x / Contents PART II THE PRIMATE EVOLUTIONARY CONTINUITY 57 4 Similarity in Form and Function of the Hippocampus in Rodents, Monkeys, and Humans 59 Robert E. Clark and Larry R. Squire 5 Evolution of Working Memory 75 Peter Carruthers 6 The Evolution of Episodic Memory 95 Timothy A. Allen and Norbert J. Fortin 7 Neuroethology of Primate Social Behavior 115  Steve W. C. Chang, Lauren J. N. Brent, Geoffrey K. Adams, Jeffrey T. Klein, John M. Pearson, Karli K. Watson, and Michael L. Platt 8 Synaptogenesis and Development of Pyramidal Neuron Dendritic Morphology in the Chimpanzee Neocortex Resembles Humans 135  Serena Bianchi, Cheryl D. Stimpson, Tetyana Duka, Michael D. Larsen, William G. M. Janssen, Zachary Collins, Amy L. Bauernfeind, Steven J. Schapiro, Wallace B. Baze, Mark J. McArthur, William D. Hopkins, Derek E. Wildman, Leonard Lipovich, Christopher W. Kuzawa, Bob Jacobs, Patrick R. Hof, and Chet C. Sherwood PART III THE HUMAN DIFFERENCE: FROM ETHICS TO AESTHETICS 153 9 Making Lasting Memories: Remembering the Significant 157 James L. McGaugh 10  Concepts and Implications of Altruism Bias and Pathological Altruism 169 Barbara A. Oakley 11 Justice- and Fairness-Related Behaviors in Nonhuman Primates 191 Sarah F. Brosnan 12  Powering Up with Indirect Reciprocity in a Large-Scale Field Experiment 211 Erez Yoeli, Moshe Hoffman, David G. Rand, and Martin A. Nowak

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Contents / xi 13 From Perception to Pleasure: Music and Its Neural Substrates 225 Robert J. Zatorre and Valorie N. Salimpoor 14 Learning Where to Look for a Hidden Target 243  Leanne Chukoskie, Joseph Snider, Michael C. Mozer, Richard J. Krauzlis, and Terrence J. Sejnowski 15  Impact of Contour on Aesthetic Judgments and Approach- Avoidance Decisions in Architecture 263  Oshin Vartanian, Gorka Navarrete, Anjan Chatterjee, Lars Brorson Fich, Helmut Leder, Cristián Modroño, Marcos Nadal, Nicolai Rostrup, and Martin Skov 16 Dynamics of Brain Networks in the Aesthetic Appreciation 283  Camilo J. Cela-Conde, Juan García-Prieto, José J. Ramasco, Claudio R. Mirasso, Ricardo Bajo, Enric Munar, Albert Flexas, Francisco del-Pozo, and Fernando Maestú References 305 Index 363

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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 VII: The Human Mental Machinery T his book is the outgrowth of the Arthur M. Sackler Colloquium “The Human Mental Machinery,” which was sponsored by the National Academy of Sciences on January 11–12, 2013, at the Academy’s Arnold and Mabel Beckman Center in Irvine, CA. It is the seventh in a series of colloquia under the general title “In the Light of Evolution.” The first six 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), Cooperation and Conflict (Strassmann et al., 2011), and Brain and Behavior (Striedter et al., 2013). In his Notebook C, Darwin gave us one of his first insights into human nature. There, referring to the human being, Darwin wrote: He is Mammalian—his origin has not been indefinite—he is not a deity, his end under present form will come, (or how dreadfully we are deceived) then he is no exception.—he possesses some of the same general instincts, & moral feelings as animals.—they on the other hand cannot reason—but Man has reasoning powers in excess. Instead of definite instincts—this is a replacement in mental machinery—so analogous to what we see in bodily, that it does not stagger me. (Darwin, 1836–1844) As Darwin noted, our mental machinery makes us different. For instance, it allows us to ask about ourselves, about what a human is. It enables us to question what we are and the ways in which we reached our current nature. One thing we have discovered is that humans possess xv

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xvi / Preface to In the Light of Evolution, Volume VII certain unique mental traits. Self-reflection, as well as ethic and aesthetic values, is among them, constituting an essential part of what we call the human condition. The human mental machinery led our species to have a self-awareness but, at the same time, a sense of justice, willing to punish unfair actions even if the consequences of such outrages harm our own interests. Also, we appreciate searching for novelties, listening to music, viewing beautiful pictures, or living in well-designed houses. But why is this so? What is the meaning of our tendency, among other particularities, to defend and share values, to evaluate the rectitude of our actions and the beauty of our surroundings? The human mental machinery obviously refers to the brain, so the answer to the preceding questions must come from neural considerations. What brain mechanisms correlate with the human capacity to maintain inner speech, or to carry out judgments of value? To what extent are they different from other primates’ equivalent behaviors? This collection of colloquium papers aims to survey what has been learned about the human “mental machinery” since Darwin’s insights. The colloquium brought together leading scientists who have worked on brain and mental traits. Their 16 contributions focus the objective of better understanding human brain processes, their evolution, and their eventual shared mechanisms with other animals. The articles are grouped into three primary sections: current study of the mind–brain relationships; the primate evolutionary continuity; and the human difference: from eth- ics to aesthetics. The explicit objective of this colloquium—improving our knowledge of the content of Darwin’s mental machinery—constitutes an endless task. However, this book offers fresh perspectives coming from interdisciplinary approaches that open new research fields and constitute the state of the art in some important aspects of the mind–brain relationships. An intriguing contradiction seems sketched from the contributions to the colloquium. On the one hand, continuity at least exists between the mental machinery of humans and nonhuman primates. On the other hand, humans manifest conspicuous evolutionarily derived (i.e., exclusive) mental/neural traits. Darwin himself solved this apparent paradox. In chapters III, IV, and V of the Descent of Man, Darwin (1871) holds that human moral and mental faculties differ from those of animals, but not in an essential form. Com- ing back again to the Notebook C annotation (Darwin, 1836–1844), “[Man] possesses some of the same general instincts, & moral feelings as animals . . . but Man has reasoning powers in excess . . . this is a replacement in mental machinery.”