© 2003 by CRC Press LLC

METHODS & NEW FRONTIERS IN NEUROSCIENCE

Series Editors
Sidney A. Simon, Ph.D.
Miguel A.L. Nicolelis, M.D., Ph.D.

Published Titles
Apoptosis in Neurobiology
Yusuf A. Hannun, M.D., Professor of Biomedical Research and Chairman/Department
of Biochemistry and Molecular Biology, Medical University of South Carolina
Rose-Mary Boustany, M.D., tenured Associate Professor of Pediatrics and Neurobiology,
Duke University Medical Center
Methods for Neural Ensemble Recordings
Miguel A.L. Nicolelis, M.D., Ph.D., Professor of Neurobiology and Biomedical Engineering,
Duke University Medical Center
Methods of Behavioral Analysis in Neuroscience
Jerry J. Buccafusco, Ph.D., Alzheimer’s Research Center, Professor of Pharmacology and
Toxicology, Professor of Psychiatry and Health Behavior, Medical College of Georgia
Neural Prostheses for Restoration of Sensory and Motor Function
John K. Chapin, Ph.D., Professor of Physiology and Pharmacology, State University of
New York Health Science Center
Karen A. Moxon, Ph.D., Assistant Professor/School of Biomedical Engineering, Science,
and Health Systems, Drexel University
Computational Neuroscience: Realistic Modeling for Experimentalists
Eric DeSchutter, M.D., Ph.D., Professor/Department of Medicine, University of Antwerp
Methods in Pain Research
Lawrence Kruger, Ph.D., Professor or Neurobiology (Emeritus), UCLA School of Medicine
and Brain Research Institute
Motor Neurobiology of the Spinal Cord
Timothy C. Cope, Ph.D., Professor of Physiology, Emory University School of Medicine
Nicotinic Receptors in the Nervous System
Edward D. Levin, Ph.D., Associate Professor/Department of Psychiatry and Pharmacology
and Molecular Cancer Biology and Department of Psychiatry and Behavioral
Sciences, Duke University School of Medicine
Methods in Genomic Neuroscience
Helmin R. Chin, Ph.D., Genetics Research Branch, NIMH, NIH
Steven O. Moldin, Ph.D, Genetics Research Branch, NIMH, NIH
Methods in Chemosensory Research
Sidney A. Simon, Ph.D., Professor of Neurobiology, Biomedical Engineering, and
Anesthesiology, Duke University
Miguel A.L. Nicolelis, M.D., Ph.D., Professor of Neurobiology and Biomedical Engineering,
Duke University

© 2003 by CRC Press LLC

 The Somatosensory System: Deciphering the Brain’s Own Body Image,
Randall J. Nelson, Ph.D., Professor of Anatomy and Neurobiology,
University of Tennessee Health Sciences Center
New Concepts in Cerebral Ischemia
Rick C. S. Lin, Ph.D., Professor of Anatomy, University of Mississippi Medical Center
DNA Arrays: Technologies and Experimental Strategies
Elena Grigorenko, Ph.D., Technology Development Group, Millennium Pharmaceuticals
Methods for Alcohol-Related Neuroscience Research
Yuan Liu, Ph.D., National Institute of Neurological Disorders and Stroke, National Institutes
of Health
David M. Lovinger, Ph.D., Laboratory of Integrative Neuroscience, NIAAA
In Vivo Optical Imaging of Brain Function
Ron Frostig, Ph.D., Associate Professor/Department of Psychobiology,
University of California, Irvine

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© 2003 by CRC Press LLC
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Cover illustration credits

Photographs: Cotton-top tamarin, Primate Cognitive Neuroscience Lab, Cambridge, MA: Geertrui
Spaepen; rhesus monkey, Cayo Santiago, Puerto Rico: Cory Miller; chacma baboon, Kruger National
Park, South Africa: Spook Skelton.
Vocalizations: Cotton-top tamarin long call and rhesus monkey shrill bark, courtesy of Primate Cognitive
Neuroscience Lab, Cambridge, MA; baboon “wahoo” call, courtesy of Dorothy Cheney and Robert Seyfarth.
Brain outlines are based on photographs from the Comparative Mammalian Brain Collection at the
University of Wisconsin–Madison and Michigan State University.

Library of Congress Cataloging-in-Publication Data

Primate audition : ethology and neurobiology / edited by Asif A. Ghazanfar.

p. cm. -- (Methods and new frontiers in neuroscience)
Includes bibliographical references and index.
ISBN 0-8493-0956-5
1. Auditory cortex. 2. Auditory perception. 3. Comparative neurobiology. 4.
Primates--Physiology. I. Ghazanfar, Asif A. II. Methods & new frontiers in
neuroscience series

QP383.15 .P75 2002

156′.215--dc21 2002067481

This book contains information obtained from authentic and highly regarded sources. Reprinted material
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Printed in the United States of America 1 2 3 4 5 6 7 8 9 0
Printed on acid-free paper

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Methods & New Frontiers

in Neuroscience
Our goal in creating the Methods & New Frontiers in Neuroscience series is to
present the insights of experts on emerging experimental techniques and theoretical
concepts that are or will be at the vanguard of the study of neuroscience. Books in
the series cover topics ranging from methods to investigate apoptosis to modern
techniques for neural ensemble recordings in behaving animals. The series also
covers new and exciting multidisciplinary areas of brain research, such as compu-
tational neuroscience and neuroengineering, and describes breakthroughs in classical
fields such as behavioral neuroscience. We want these to be the books every neuro-
scientist will use in order to get acquainted with new methodologies in brain research.
These books can be given to graduate students and postdoctoral fellows when they
are looking for guidance to start a new line of research.
Each book is edited by an expert and consists of chapters written by the leaders
in a particular field. Books are richly illustrated and contain comprehensive bibli-
ographies. Chapters provide substantial background material relevant to the partic-
ular subject; hence, they are not only “methods” books. They contain detailed tricks
of the trade and information as to where these methods can be safely applied. In
addition, they include information about where to buy equipment and about Web
sites that are helpful in solving both practical and theoretical problems,
We hope that as the volumes become available, the effort put in by us, by the
publisher, by the book editors, and by the individual authors will contribute to the
further development of brain research. The extent to which we achieve this goal will
be determined by the utility of these books.

Sidney A. Simon, Ph.D.

Miguel A.L. Nicolelis, M.D., Ph.D.
Series Editors

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Preface
Neuroethological research has been critical for our understanding of brain function
and how natural selection shapes brain design for complex behaviors. The value
of this approach is evident in the auditory model systems that are currently popular:
echolocation in bats, song learning and prey localization in birds, and mate choice
in frogs. Even in human neurobiological studies, speech perception and production
represent the paradigm example of a specialized system in the cerebral cortex. It
is therefore surprising that few researchers interested in the neural substrate of
non-human primate auditory processing have adopted a similar naturalistic
approach. With the advent of new signal-processing techniques and the exponential
growth in our knowledge of primate behavior, the time has arrived for a neurobi-
ological investigation of the primate auditory system based on principles derived
from ethology.
A neuroethology of primate hearing may also yield insights into human speech
processing. Like speech, the species-specific vocalizations of non-human primates
mediate social interactions, convey important emotional information, and in some
cases refer to objects and events in the caller’s environment. These functional
similarities suggest that the selective pressures that shaped primate vocal commu-
nication are similar to those that influenced the evolution of human speech. As such,
investigating the perception and production of vocalizations in extant non-human
primates provides one avenue for understanding the neural mechanisms of speech
and for illuminating the substrates underlying the evolution of human language.
Primate Audition: Ethology and Neurobiology is the first book whose primary
purpose is to bridge the epistemological gap between primate ethologists and audi-
tory neurobiologists. To do this, the knowledge of leading world experts on different
aspects of primate auditory function has been brought together in a single volume.
The book covers the state-of-the-art work on a variety of issues in primate auditory
perception. Topics include the functional organization and anatomy of the primate
auditory system, spatial localization of sounds and its neural basis, function and
perception of conspecific and heterospecific vocalizations and their ontogeny, neural
encoding of complex sounds, vocal production and its relationship to perception,
and the acoustic cues guiding vocal recognition. This synthesis of ethological and
neurobiological approaches to primate vocal behavior is likely to yield the richest
understanding of the acoustic and neural bases of primate audition.

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Acknowledgments
I am grateful to all the authors who have contributed to this book, for without them
it would not exist. Thanks are also due to Roian Egnor, Tecumseh Fitch, Don Katz,
Merri Rosen, and Laurie Santos for generously helping me edit a good number of
the chapters. I would also like to express my gratitude to my former mentors (in the
temporal order of their initial impact), Professors Mark Desantis, Matthew Grober,
Miguel Nicolelis, and Marc Hauser. The ideas behind putting together this book are
the result of their continuing and converging positive influence on me. Finally, I
would like to thank the series editors, Miguel and Sid, and Barbara Norwitz, Pat
Roberson, and their colleagues at CRC Press for pushing, sympathizing, and sup-
porting when necessary and expertly guiding the book to its completion.

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The Editor
Asif A. Ghazanfar, Ph.D., is a research scientist at the Max Planck Institute for
Biological Cybernetics in Tübingen, Germany. Born in Pullman, WA, and raised in
nearby Moscow, ID, he received his Bachelor of Science degree in philosophy at
the University of Idaho. While earning his degree, he studied the neural and hormonal
bases for sex reversal in a coral reef fish, the saddleback wrasse. In 1998, he earned
his doctoral degree in neurobiology from Duke University in Durham, NC. His
dissertation research uncovered some of the dynamic properties of single neurons
and neural ensembles in the somatosensory corticothalamic pathway. Since then, he
has combined his dual interests in ethology and neurophysiology by studying the
natural vocal behavior of primates and its neural basis. As a postdoctoral fellow at
Harvard University, he studied the acoustic bases for vocal recognition in three
species of non-human primates. Using this ethological work as a foundation, he is
currently investigating how behaviorally relevant acoustic features of species-spe-
cific vocalizations are processed in the auditory cortex of rhesus monkeys.

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Contributors
James A. Agamaite Troy A. Hackett
Laboratory of Auditory Department of Psychology
Neurophysiology Vanderbilt University
Department of Biomedical Engineering Nashville, Tennessee
Johns Hopkins University School of
Medicine Marc D. Hauser
Baltimore, Maryland Primate Cognitive Neuroscience Lab
Department of Psychology
Michael Brosch Harvard University
Leibniz-Institut für Neurobiologie Cambridge, Massachusetts
Magdeburg, Germany
Siddhartha C. Kadia
Charles H. Brown Laboratory of Auditory
Department of Psychology Neurophysiology
University of South Alabama Department of Biomedical Engineering
Mobile, Alabama Johns Hopkins University School of
Medicine
Julia Fischer Baltimore, Maryland
Max Planck Institute for Evolutionary
Anthropology Kristin A. Kelly
Leipzig, Germany Department of Psychological and Brain
Sciences
W. Tecumseh S. Fitch Center for Cognitive Neuroscience
Department of Psychology Dartmouth College
Harvard University Hanover, New Hampshire
Cambridge, Massachusetts
Colleen G. Le Prell
Asif A. Ghazanfar Kresge Hearing Research Institute
Max Planck Institute for Biological University of Michigan
Cybernetics Ann Arbor, Michigan
Tübingen, Germany
Li Liang
Jennifer M. Groh Laboratory of Auditory
Department of Psychological and Brain Neurophysiology
Sciences Department of Biomedical Engineering
Center for Cognitive Neuroscience Johns Hopkins University School of
Dartmouth College Medicine
Hanover, New Hampshire Baltimore, Maryland

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Thomas Lu Gregg H. Recanzone

Laboratory of Auditory Center for Neuroscience
Neurophysiology Section of Neurobiology, Physiology,
Department of Biomedical Engineering and Behavior
Johns Hopkins University School of University of California
Medicine Davis, California
Baltimore, Maryland
Lizabeth M. Romanski
Ryan Metzger Department of Anatomy and
Department of Psychological and Brain Neurobiology
Sciences University of Rochester
Center for Cognitive Neuroscience Rochester, New York
Dartmouth College
Hanover, New Hampshire Laurie R. Santos
Department of Psychology
Cory T. Miller Yale University
Primate Cognitive Neuroscience Lab New Haven, Connecticut
Department of Psychology
Harvard University Henning Scheich
Cambridge, Massachusetts Leibniz-Institut für Neurobiologie
Magdeburg, Germany
O’Dhaniel A. Mullette-Gillman
Department of Psychological and Brain Mitchell L. Sutter
Sciences Center for Neuroscience
Center for Cognitive Neuroscience Section of Neurobiology, Physiology,
Dartmouth College and Behavior
Hanover, New Hampshire University of California
Davis, California
David B. Moody
Kresge Hearing Research Institute Xiaoqin Wang
University of Michigan Laboratory of Auditory
Ann Arbor, Michigan Neurophysiology
Department of Biomedical Engineering
John D. Newman Johns Hopkins University School of
Laboratory of Comparative Ethology Medicine
National Institute of Child Health and Baltimore, Maryland
Human Development
National Institutes of Health Daniel J. Weiss
Poolesville, Maryland Department of Brain and Cognitive
Sciences
Kevin N. O’Connor University of Rochester
Center for Neuroscience Rochester, New York
Section of Neurobiology, Physiology,
and Behavior
University of California
Davis, California

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Uri Werner-Reiss Klaus Zuberbühler

Department of Psychological and Brain Department of Psychology
Sciences University of St. Andrews
Center for Cognitive Neuroscience Fife, Scotland
Dartmouth College
Hanover, New Hampshire

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Contents
Chapter 1
Primates as Auditory Specialists
Asif A. Ghazanfar and Laurie R. Santos

Chapter 2
Causal Knowledge in Free-Ranging Diana Monkeys
Klaus Zuberbühler

Chapter 3
Auditory Temporal Integration in Primates: A Comparative Analysis
Kevin N. O’Connor and Mitchell L. Sutter

Chapter 4
Mechanisms of Acoustic Perception in the Cotton-Top Tamarin
Cory T. Miller, Daniel J. Weiss, and Marc D. Hauser

Chapter 5
Psychophysical and Perceptual Studies of Primate Communication Calls
Colleen G. Le Prell and David B. Moody

Chapter 6
Primate Vocal Production and Its Implications for Auditory Research
W. Tecumseh S. Fitch

Chapter 7
Developmental Modifications in the Vocal Behavior of Non-Human Primates
Julia Fischer

Chapter 8
Ecological and Physiological Constraints for Primate Vocal Communication
Charles H. Brown

Chapter 9
Neural Representation of Sound Patterns in the Auditory Cortex of Monkeys
Michael Brosch and Henning Scheich

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Chapter 10
Representation of Sound Location in the Primate Brain
Kristin A. Kelly, Ryan Metzger, O’Dhaniel A. Mullette-Gillman, Uri Werner-Reiss,
and Jennifer M. Groh

Chapter 11
The Comparative Anatomy of the Primate Auditory Cortex
Troy A. Hackett

Chapter 12
Auditory Communication and Central Auditory Mechanisms in the Squirrel
Monkey: Past and Present
John D. Newman

Chapter 13
Cortical Mechanisms of Sound Localization and Plasticity in Primates
Gregg H. Recanzone

Chapter 14
Anatomy and Physiology of Auditory–Prefrontal Interactions in Non-Human
Primates
Lizabeth M. Romanski

Chapter 15
Cortical Processing of Complex Sounds and Species-Specific Vocalizations
in the Marmoset Monkey (Callithrix jacchus)
Xiaoqin Wang, Siddhartha C. Kadia, Thomas Lu, Li Liang, and James A. Agamaite

© 2003 by CRC Press LLC