Evolutionary Neuroscience

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 DEDICATION

T hese volumes are dedicated to the memory of Theodore Holmes

Bullock, a remarkable scientist and pioneer in the fields of
comparative neurobiology and brain evolution. In some 60 years
and 400 published titles, Ted truly altered both fields with studies
spanning all major metazoan groups. He was that rare neurobiologist,
perhaps the only one, who could have made significant contributions
to each of the volumes that comprise this work.
Beginning in 1940, Ted’s study of the functional organization of the
nervous system in the enteropneust acorn worms laid the foundation
for his contributions on neural evolution in deuterostomes. This
benchmark publication was followed by studies of the giant nerve
fibers in earthworms and squid, studies that pioneered the use of giant
axons as synaptic models. His interests in the organization and evolu-
tion of invertebrate nervous systems culminated in the 1965 publication of Structure and Function in the
Nervous Systems of Invertebrates, written in collaboration with G. Adrian Horridge. More than 40 years
later, it is a testament to Ted and Adrian that these two volumes are still considered the definitive work in the
field.
Even as Ted continued working on invertebrate nervous systems, he also turned his attention to the
physiology of infrared receptors in pit vipers, the electroreceptors of gymnotid fishes, tectal units in frogs,
and the physiological basis of slothfulness. The 1950s and 1960s thus marked a major expansion in the
focus of Ted’s research, as he began to probe sensory and integrative problems in the nervous systems of so-
called ‘lower vertebrates’ and also began to consider broader topics involving the basic organization of
neurons and how they code and process information. Not surprisingly, he was one of the pioneers and
founders of the new discipline of neuroethology, and such multifarious endeavors continued to command
his attention throughout the 1970s and 1980s.
Given Ted’s remarkable grasp of both cellular and integrative neural mechanisms, one might have
anticipated that he would develop an added interest in slow wave activity and cognition in animals as
diverse as crayfish and humans, and these investigations were the focus of much of his effort during the latter
years of his career.
While most scientists slow down as they approach ‘old age’, Ted’s interests and insights continued to
amaze all who knew him, and his fascination with nature never waned. In spite of a remarkably full and busy
life, Ted always found time to encourage and inspire others. Many of the authors and their chapters in these
volumes clearly reflect not only Ted’s scientific contributions but also the excitement about nervous systems
and their evolution that he brought to personal interactions with anyone who ever sat across his desk or
poked in a tide pool with him.

R. GLENN NORTHCUTT
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CONTENTS

Dedication v
Contents vii
Preface xi
Biography of Editor-in-Chief xiii
Introduction xv
Contributors xvii

PART I: AN INTRODUCTION TO HISTORY, THEORY, METHODS AND CONCEPTS

1 History of Ideas on Brain Evolution 3

G F STRIEDTER, University of California, Irvine, CA,USA

2 Phylogenetic Character Reconstruction 19

J S ALBERT, University of Louisiana, Lafayette, LA, USA

3 Basic Nervous System ‘‘Types’’: One or Many? 33

F HIRTH, Institute of Psychiatry, De Crespigny Park, Denmark Hill, London, UK
H REICHERT, University of Basel, Basel, Switzerland

4 Origin and Evolution of the First Nervous System 51

R LICHTNECKERT and H REICHERT, University of Basel, Basel, Switzerland

5 Neuronal Migration 79
O MARÍN and G LÓPEZ-BENDITO, Consejo Superior de Investigaciones Cientı́ficas y
Universidad Miguel Hernández, Sant Joan d’Alacant, Spain

6 The Role of Transient Connections in Brain Evolution 97

G M INNOCENTI, Karolinska Institutet, Stockholm, Sweden

7 Neural Wiring Optimization 107

C CHERNIAK, Z MOKHTARZADA, and R RODRIGUEZ-ESTEBAN, University
of Maryland, College Park, MD, USA

8 Principles of Brain Scaling 111

C F STEVENS, The Salk Institute, La Jolla, CA, USA
viii CONTENTS

PART II: THE EVOLUTION OF BRAINS IN EARLY VERTEBRATES, FISHES, AMPHIBIANS,

REPTILES AND BIRDS

9 Structure of Brains of Primitive Vertebrates (tunicates, amphioxus, lampreys) and the 123
Basic Features of the Vertebrate Brain
B FRITZSCH, Creighton University, Omaha, NE, USA
J C GLOVER, University of Oslo, Oslo, Norway

10 Evolution of the Nervous System in Fishes 147

M F WULLIMANN and P VERNIER, DEPNS – Institute of Neurobiology A. Fessard,
CNRS, Gif sur Yvette, France

11 Evolution of the Amphibian Nervous System 169

U DICKE and G ROTH, University of Bremen, Bremen, Germany

12 Evolution of the Nervous System in Reptiles 233

L L BRUCE, Creighton University, Omaha, NE, USA

13 Do Birds and Reptiles Possess Homologues of Mammalian Visual, Somatosensory, 265

and Motor Cortices?
L MEDINA, University of Murcia, Murcia, Spain

14 The Evolution of Vocal Learning Systems inBirds and Humans 297

E D JARVIS, Duke University Medical Center, Durham, NC, USA

15 The Evolution of the Amygdala in Vertebrates 313

F MARTÍNEZ-GARCÍA, A NOVEJARQUE, and E LANUZA, Universitat de València,
Burjassot, Spain

16 The Evolution of Vertebrate Eyes 393

R D FERNALD, Stanford University, Stanford, CA, USA

17 Vertebrate Olfactory Subsystems and their Evolution 407

H L EISTHEN and G POLESE, Michigan State University, East Lansing, MI, USA

18 The Evolution of Taste Systems 459

T E FINGER, University of Colorado Medical School, Aurora, CO, USA

19 Shared and Convergent Features of the Auditory System of Vertebrates 479

C E CARR and D SOARES, University of Maryland, College Park, MD, USA

PART III: EVOLUTION OF MAMMALIAN BRAINS

20 How Can Fossils Tell us About the Evolution of the Neocortex? 497
H J JERISON, University of California, Los Angeles, CA, USA

21 The Origin of Neocortex: Lessons from Comparative Embryology 509

Z MOLNÁR, A TAVARE, and A F P CHEUNG, University of Oxford, Oxford, UK

22 Reconstructing the Organization of the Forebrain of the First Mammals 523

J H KAAS, Vanderbilt University, Nashville, TN, USA
 CONTENTS ix

23 Captured in the Net of Space and Time: Understanding Cortical Field Evolution 545
L KRUBITZER and D L HUNT, University of California, Davis, CA, USA

24 The Evolution of the Dorsal Thalamus in Mammals 569

J H KAAS, Vanderbilt University, Nashville, TN, USA

25 The Evolution of the Basal Ganglia in Mammals and Other Vertebrates 587
A REINER, University of Tennessee Health Science Center, Memphis TN, USA
26 The Evolution of the Hippocampus 603
J R MANNS and H EICHENBAUM, Boston University, Boston, MA, USA

27 The Evolution of the Cerebellum 629

M GLICKSTEIN, University College London, London, UK
J OBERDICK, The Ohio State University, Columbus, OH, USA
J VOOGD, Erasmus Medical Center, Rotterdam, The Netherlands

28 Olfactory Cortex: Comparative Anatomy 659

K R ILLIG, University of Virginia, Charlottesville, VA, USA
D A WILSON, University of
Oklahoma, Norman, OK, USA

29 Vestibular System 665

W M GRAF, Howard University College of Medicine, Washington, DC, USA

30 Evolution of Gustation 685

I E DE ARAUJO, M A L NICOLELIS, and S A SIMON, Duke University, Durham, NC, USA

31 The Evolution of the Somatosensory System 697

K C CATANIA, Vanderbilt University, Nashville, TN, USA

32 Somatosensory Specializations of Flying Mammals 715

J M ZOOK, Ohio University, Athens, OH, USA

33 The Evolution of Motor Cortex and Motor Systems 727

R J NUDO and S B FROST, University of Kansas Medical Center, Kansas City, KS, USA

34 The Evolution of Visual Cortex and Visual Systems 757

D C LYON, University of California, Irvine, CA, USA

PART IV: PRIMATE BRAIN EVOLUTION

35 Primate Brain Evolution 793

T M PREUSS, Emory University, Atlanta, GA, USA

36 The Role of Vision in the Origin and Evolution of Primates 827

C F ROSS, University of Chicago, Chicago, IL, USA
R D MARTIN, The Field Museum, Chicago, IL, USA

37 The Evolution of Sensory and Motor Systems in Primates 847

J H KAAS, Vanderbilt University, Nashville, TN, USA

38 The Evolution of Parallel Pathways in the Brains of Primates 871

V A CASAGRANDE and I KHAYTIN, Vanderbilt University, Nashville, TN, USA
J BOYD, Medical University of South Carolina, Charleston, SC, USA
x CONTENTS

39 The Evolution of the Primate and Human Auditory System 893

T A HACKETT, Vanderbilt University, Nashville, TN, USA

40 The Evolution of Language Systems in the Human Brain 905

T W DEACON, University of California, Berkeley, CA, USA

41 The Evolution of Hemispheric Specializations of the Human Brain 925

M C CORBALLIS, University of Auckland, Auckland, New Zealand
42 Neurological Specializations for Manual Gesture and Tool Use in Humans 941
S H FREY, University of Oregon, Eugene, OR, USA

43 Frontal Cortex Evolution in Primates 953

E C BUSH, Harvey Mudd College, Claremont, CA, USA
J M ALLMAN, California Institute of Technology, Pasadena, CA, USA

Index 957
 PREFACE

T his volume is for readers who are curious about how complex brains, such as the human brain, evolved
from the much simpler nervous systems of ancient non-vertebrate ancestors. The chapters for this
volume have been carefully selected from those in a larger, more comprehensive four-volume effort, the
Evolution of Nervous Systems, published in 2007. To help fill in gaps, two short essays have been added
from the 2009 Encyclopedia of Neuroscience, online. The chapters reflect the thoughts of the most knowl-
edgeable experts in the field. While this condensation left out many wonderful chapters, both short and long,
it allowed publication of a single volume on brain evolution that preserves much of the intent of the original
four volumes while bringing a collection of exciting essays to a broader readership. The present chapters are
presented in four parts that preserve the broad topics of the original four volumes. The first section of eight
chapters includes historical and current theory on brain evolution, observations on brain development, as
evolution depends on altered development, and current concepts of how the first nervous systems were
organized. The second series of eleven chapters focuses on the nervous systems of primitive vertebrates,
fishes, amphibians, reptiles, and birds, with many comparisons with mammals. The chapters provide an
understanding of how the nervous system of mammals evolved, as well as how other vertebrates evolve
complex, but different nervous systems. The third series of fifteen chapters covers the evolution of mamma-
lian brains. As the use of skull endocasts from fossil mammals offers a direct window into the past, the
sequence starts with a discussion of how fossils can help us understand brain evolution. Other chapters
discuss the origin and evolution of neocortex, as this homolog of the small, thin dorsal cortex of reptiles
became the highly variable, flexible, and often dominant brain structure in mammals. Included chapters also
discuss the evolution of other parts of the brain, such as the basal ganglia, cerebellum, dorsal thalamus, and
sensory and motor systems. The last series of nine chapters provides a broad view of primate evolution,
describes the role of vision in shaping the nervous system of early primates, and outlines the evolution of
sensory and motor systems in primates. Other chapters discuss frontal cortex, and how hemispheric
specializations and systems for language, gesture, and tool use evolved in humans.
While the selection of specific chapters for this collection was my responsibility, I am deeply indebted to
the volume editors of the earlier series, George Striedter, John Rubenstein, Theodore Bullock, Leah
Krubitzer, and Todd Preuss, for their wisdom and efforts in selecting outstanding authors for chapters
and carefully editing the results. I also thank Johannes Menzel, Publisher, and Elsevier for bringing this
present volume and the previous series to life. I hope this volume provokes and guides students of brain
evolution, generates further interest, and results in future publications with new and greater contributions to
our understandings of brain evolution.

JON H. KAAS
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BIOGRAPHY OF EDITOR-IN-CHIEF

J on H. Kaas is currently Distinguished Centennial Professor

of Psychology at Vanderbilt University. He received his PhD
training in comparative studies of forebrain organization in mam-
mals in the laboratory of I. T. Diamond at Duke University, and
postdoctoral training studying cortical organization in the compara-
tive neurophysiology laboratory of C. N. Woolsey at the University
of Wisconsin. His research has focused on determining the organiza-
tions of sensory and motor systems in mammals, especially in
primates, with an effort to understand the evolution of the forebrain
from early mammals to present-day humans. He has published over
275 research papers and 170 reviews. He is an elected member of the
National Academy of Sciences, and of the American Academy of
Arts and Sciences. He is also a member of the La Jolla Group for
Explaining the Origin of Humans.
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 INTRODUCTION

E volutionary neuroscientists have existed since Darwin’s days, and they are unlikely to go extinct. As
long as neurobiological research is performed on a diversity of species, there will be those who seek to
synthesize the disparate data, and for that synthesis the theory of evolution is indispensable. Still, a full
‘evolutionary synthesis’ in neuroscience is just beginning to take shape. No previous publication surveys the
full spectrum of work in evolutionary neuroscience, ranging as it does from genes to behavior (via anatomy,
physiology, and embryology) and from minute invertebrates to whales, elephants, and Homo sapiens. That
is why this series of four volumes is so invaluable; it attempts to cover all aspects of evolutionary
neuroscience. Volume 1, which lies before you now, is the most far-ranging of all. Its three most integrative
aspects are the following.
First, Volume 1 surveys a vast array of theoretical ideas about nervous system evolution. In the olden days,
evolutionary biology was dominated by the idea of a phylogenetic scale, but we now know that evolution is
nonmonotonic and nonlinear. We have more accurate phylogenetic trees and well-developed methodologies
for reconstructing what evolved from what. We also know how to link evolutionary changes in genes,
anatomy, and physiology to evolutionary changes in behavior by means of both correlative and experi-
mental analyses. As a result, we can construct scenarios of how evolution tinkered with nervous systems to
help adapt species to their environments. In addition to such evolutionary ‘case studies’, we have some fairly
general theories on how nervous systems evolve. For example, we know a great deal about how nervous
systems scale and how conserved sets of genes and processes are used to produce nervous systems that, to
previous generations of evolutionary neuroscientists, seemed completely dissimilar. These advances are
covered in this book.
Second, the present volume includes a broad compilation of data on nervous system development.
Neuroscientists now recognize that evolutionary changes in adult nervous systems are largely caused
by changes in neural development. Meanwhile, developmental neuroscientists have made astonishing
progress in unraveling the molecular mechanisms of neural development in multiple species, leading to
an explosion in evo–devo neuroscience. One major theme emerging from this work is that many
aspects of neural development are highly conserved across vast swaths of phylogeny. A second theme
is that changes in one part of a developing neural system can cause a slew of generally adaptive and
frequently compensatory changes in other parts of the system. Future work must now define how
specific modifications in gene expression and function lead to evolutionary diversity of brain structure,
connectivity, and plasticity.
Third, this volume is unusual in that it covers both invertebrates and vertebrates. Of the three major
textbooks on evolutionary neuroscience that have been published in the last 10 years, none discuss
invertebrates at length. Most of them discuss invertebrate nervous systems merely in the context of tracing
vertebrate brain origins. Indeed, recent advances in comparative molecular biology have seriously altered
how we think about the evolutionary origins of vertebrate brains. However, invertebrate nervous systems
are well worth studying in their own right, for their own rich diversity and enigmatic elegance. Moreover,
when working with invertebrates, it is frequently possible to combine behavioral, molecular, anatomical,
and physiological analyses, and to extend such work across a multitude of species. Such broadly integrative
studies have revealed that invertebrate nervous systems vary dramatically in size, complexity, and function-
ality, but still are built from highly conserved sets of genes. In that respect, they are quite similar to
vertebrate nervous systems, though the diversity is more extreme.
xvi INTRODUCTION

Thus, this first volume shows evolutionary neuroscience to be a vast and vibrant field that holds enormous
possibilities for new discoveries. Every chapter synthesizes an immense amount of data and integrates
experiment and theory, ontogeny and phylogeny, invertebrate and vertebrate neurobiology, genes and
behavior, and/or anatomy and physiology. Given this diversity of synthetic efforts, the chapter sequence
was difficult to optimize. For example, it was impossible to construct separate sections for developmental
and invertebrate neurobiology, because so much of the most interesting developmental work was performed
on invertebrates. This may be frustrating for readers who seek a straightforward connecting thread, but
actually, in this respect, the chapters merely resemble the evolutionary products they discuss: they weave a
tangled web of insights, themes, and approaches that does not form a linear sequence. Still, or perhaps
therefore, they ought to serve as fertile soil for further thoughts and work. That, at least, is our hope.

GEORG F. STRIEDTER AND JOHN L. R. RUBENSTEIN

 CONTRIBUTORS

J S Albert H Eichenbaum
University of Louisiana, Lafayette, LA, USA Boston University, Boston, MA, USA

J M Allman H L Eisthen
California Institute of Technology, Pasadena, CA, USA Michigan State University, East Lansing, MI, USA

J Boyd R D Fernald
Medical University of South Carolina, Charleston, SC, Stanford University, Stanford, CA, USA
USA
T E Finger
L L Bruce University of Colorado Medical School, Aurora, CO, USA
Creighton University, Omaha, NE, USA
S H Frey
E C Bush University of Oregon, Eugene, OR, USA
Harvey Mudd College, Claremont, CA, USA
B Fritzsch
Creighton University, Omaha, NE, USA
C E Carr
University of Maryland, College Park, MD, USA
S B Frost
University of Kansas Medical Center, Kansas City, KS,
V A Casagrande
USA
Vanderbilt University, Nashville, TN, USA

M Glickstein
K C Catania
University College London, London, UK
Vanderbilt University, Nashville, TN, USA
J C Glover
C Cherniak University of Oslo, Oslo, Norway
University of Maryland, College Park, MD, USA
W M Graf
A F P Cheung Howard University College of Medicine, Washington,
University of Oxford, Oxford, UK DC, USA

M C Corballis T A Hackett
University of Auckland, Auckland, New Zealand Vanderbilt University, Nashville, TN, USA

F Hirth
I E de Araujo
Institute of Psychiatry, De Crespigny Park, Denmark Hill,
Duke University, Durham, NC, USA
London, UK

T W Deacon D L Hunt
University of California, Berkeley, CA, USA University of California, Davis, CA, USA

U Dicke K R Illig
University of Bremen, Bremen, Germany University of Virginia, Charlottesville, VA, USA
xviii CONTRIBUTORS

G M Innocenti Z Molnár
Karolinska Institutet, Stockholm, Sweden University of Oxford, Oxford, UK

E D Jarvis M A L Nicolelis
Duke University Medical Center, Durham, NC, USA Duke University, Durham, NC, USA

H J Jerison A Novejarque
University of California, Los Angeles, CA, USA Universitat de València, Burjassot, Spain

J H Kaas
R J Nudo
Vanderbilt University, Nashville, TN, USA
University of Kansas Medical Center, Kansas City, KS,
USA
I Khaytin
Vanderbilt University, Nashville, TN, USA
J Oberdick
The Ohio State University, Columbus, OH, USA
L Krubitzer
University of California, Davis, CA, USA
G Polese
E Lanuza Michigan State University, East Lansing, MI, USA
Universitat de València, Burjassot, Spain
T M Preuss
R Lichtneckert Emory University, Atlanta, GA, USA
University of Basel, Basel, Switzerland
H Reichert
D C Lyon University of Basel, Basel, Switzerland
University of California, Irvine, CA, USA
A Reiner
G López-Bendito University of Tennessee Health Science Center,
Consejo Superior de Investigaciones Cientı́ficas y Memphis TN, USA
Universidad Miguel Hernández, Sant Joan d’Alacant,
Spain
R Rodriguez-Esteban
University of Maryland, College Park, MD, USA
J R Manns
Boston University, Boston, MA, USA
C F Ross
O Marı́n University of Chicago, Chicago, IL, USA
Consejo Superior de Investigaciones Cientı́ficas y
Universidad Miguel Hernández, Sant Joan d’Alacant, G Roth
Spain University of Bremen, Bremen, Germany

R D Martin S A Simon
The Field Museum, Chicago, IL, USA Duke University, Durham, NC, USA

F Martı́nez-Garcı́a D Soares
Universitat de València, Burjassot, Spain University of Maryland, College Park, MD, USA

L Medina C F Stevens
University of Murcia, Murcia, Spain The Salk Institute, La Jolla, CA, USA

Z Mokhtarzada G F Striedter
University of Maryland, College Park, MD, USA University of California, Irvine, CA, USA
 CONTRIBUTORS xix

A Tavare D A Wilson
University of Oxford, Oxford, UK University of Oklahoma, Norman, OK, USA

P Vernier M F Wullimann
DEPNS – Institute of Neurobiology A. Fessard, CNRS, DEPNS – Institute of Neurobiology A. Fessard, CNRS,
Gif sur Yvette, France Gif sur Yvette, France

J Voogd J M Zook
Erasmus Medical Center, Rotterdam, The Netherlands Ohio University, Athens, OH, USA
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