HANDBOOKof

PSYCHOLOGY

VOLUME 3

BIOLOGICAL PSYCHOLOGY

Michela Gallagher

Randy J. Nelson

Volume Editors

Irving B. Weiner

Editor-in-Chief

John Wiley & Sons, Inc.

HANDBOOKof

PSYCHOLOGY

HANDBOOKof

PSYCHOLOGY

HANDBOOKof

PSYCHOLOGY

VOLUME 3

BIOLOGICAL PSYCHOLOGY

Michela Gallagher

Randy J. Nelson

Volume Editors

Irving B. Weiner

Editor-in-Chief

John Wiley & Sons, Inc.

This book is printed on acid-free paper.

Copyright © 2003 by John Wiley & Sons, Inc., Hoboken, New Jersey. All rights reserved.

Published simultaneously in Canada.

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Library of Congress Cataloging-in-Publication Data:

Handbook of psychology / Irving B. Weiner, editor-in-chief.p. cm.

Includes bibliographical references and indexes.Contents: v. 1. History of psychology / edited by Donald K. Freedheim — v. 2. Research

methods in psychology / edited by John A. Schinka, Wayne F. Velicer — v. 3. Biologicalpsychology / edited by Michela Gallagher, Randy J. Nelson — v. 4. Experimentalpsychology / edited by Alice F. Healy, Robert W. Proctor — v. 5. Personality and socialpsychology / edited by Theodore Millon, Melvin J. Lerner — v. 6. Developmentalpsychology / edited by Richard M. Lerner, M. Ann Easterbrooks, Jayanthi Mistry — v. 7.Educational psychology / edited by William M. Reynolds, Gloria E. Miller — v. 8.Clinical psychology / edited by George Stricker, Thomas A. Widiger — v. 9. Health psychology /edited by Arthur M. Nezu, Christine Maguth Nezu, Pamela A. Geller — v. 10. Assessmentpsychology / edited by John R. Graham, Jack A. Naglieri — v. 11. Forensic psychology /edited by Alan M. Goldstein — v. 12. Industrial and organizational psychology / editedby Walter C. Borman, Daniel R. Ilgen, Richard J. Klimoski.

ISBN 0-471-17669-9 (set) — ISBN 0-471-38320-1 (cloth : alk. paper : v. 1) — ISBN 0-471-38513-1 (cloth : alk. paper : v. 2) — ISBN 0-471-38403-8 (cloth : alk. paper : v. 3) — ISBN 0-471-39262-6 (cloth : alk. paper : v. 4) — ISBN 0-471-38404-6 (cloth : alk. paper : v. 5) — ISBN 0-471-38405-4 (cloth : alk. paper : v. 6) — ISBN 0-471-38406-2 (cloth : alk. paper : v. 7) — ISBN 0-471-39263-4 (cloth : alk. paper : v. 8) — ISBN 0-471-38514-X (cloth : alk. paper : v. 9) — ISBN 0-471-38407-0 (cloth : alk. paper : v. 10) — ISBN 0-471-38321-X (cloth : alk. paper : v. 11) — ISBN 0-471-38408-9 (cloth : alk. paper : v. 12)

1. Psychology. I. Weiner, Irving B.

BF121.H1955 2003150—dc21

2002066380Printed in the United States of America.

10 9 8 7 6 5 4 3 2 1

➇

Editorial Board

Volume 1History of Psychology

Donald K. Freedheim, PhDCase Western Reserve UniversityCleveland, Ohio

Volume 2Research Methods in Psychology

John A. Schinka, PhDUniversity of South FloridaTampa, Florida

Wayne F. Velicer, PhDUniversity of Rhode IslandKingston, Rhode Island

Volume 3Biological Psychology

Michela Gallagher, PhDJohns Hopkins UniversityBaltimore, Maryland

Randy J. Nelson, PhDOhio State UniversityColumbus, Ohio

Volume 4Experimental Psychology

Alice F. Healy, PhDUniversity of ColoradoBoulder, Colorado

Robert W. Proctor, PhD Purdue UniversityWest Lafayette, Indiana

Volume 5Personality and Social Psychology

Theodore Millon, PhDInstitute for Advanced Studies in

Personology and PsychopathologyCoral Gables, Florida

Melvin J. Lerner, PhDFlorida Atlantic UniversityBoca Raton, Florida

Volume 6Developmental Psychology

Richard M. Lerner, PhDM. Ann Easterbrooks, PhDJayanthi Mistry, PhD

Tufts UniversityMedford, Massachusetts

Volume 7Educational Psychology

William M. Reynolds, PhDHumboldt State UniversityArcata, California

Gloria E. Miller, PhDUniversity of DenverDenver, Colorado

Volume 8Clinical Psychology

George Stricker, PhDAdelphi UniversityGarden City, New York

Thomas A. Widiger, PhDUniversity of KentuckyLexington, Kentucky

Volume 9Health Psychology

Arthur M. Nezu, PhDChristine Maguth Nezu, PhDPamela A. Geller, PhD

Drexel UniversityPhiladelphia, Pennsylvania

Volume 10Assessment Psychology

John R. Graham, PhDKent State UniversityKent, Ohio

Jack A. Naglieri, PhDGeorge Mason UniversityFairfax, Virginia

Volume 11Forensic Psychology

Alan M. Goldstein, PhDJohn Jay College of Criminal

Justice–CUNYNew York, New York

Volume 12Industrial and OrganizationalPsychology

Walter C. Borman, PhDUniversity of South FloridaTampa, Florida

Daniel R. Ilgen, PhDMichigan State UniversityEast Lansing, Michigan

Richard J. Klimoski, PhDGeorge Mason UniversityFairfax, Virginia

v

Handbook of Psychology Preface

Psychology at the beginning of the twenty-first century hasbecome a highly diverse field of scientific study and appliedtechnology. Psychologists commonly regard their disciplineas the science of behavior, and the American PsychologicalAssociation has formally designated 2000 to 2010 as the“Decade of Behavior.” The pursuits of behavioral scientistsrange from the natural sciences to the social sciences and em-brace a wide variety of objects of investigation. Some psy-chologists have more in common with biologists than withmost other psychologists, and some have more in commonwith sociologists than with most of their psychological col-leagues. Some psychologists are interested primarily in the be-havior of animals, some in the behavior of people, and othersin the behavior of organizations. These and other dimensionsof difference among psychological scientists are matched byequal if not greater heterogeneity among psychological practi-tioners, who currently apply a vast array of methods in manydifferent settings to achieve highly varied purposes.

Psychology has been rich in comprehensive encyclope-dias and in handbooks devoted to specific topics in the field.However, there has not previously been any single handbookdesigned to cover the broad scope of psychological scienceand practice. The present 12-volume Handbook of Psychol-ogy was conceived to occupy this place in the literature.Leading national and international scholars and practitionershave collaborated to produce 297 authoritative and detailedchapters covering all fundamental facets of the discipline,and the Handbook has been organized to capture the breadthand diversity of psychology and to encompass interests andconcerns shared by psychologists in all branches of the field.

Two unifying threads run through the science of behavior.The first is a common history rooted in conceptual and em-pirical approaches to understanding the nature of behavior.The specific histories of all specialty areas in psychologytrace their origins to the formulations of the classical philoso-phers and the methodology of the early experimentalists, andappreciation for the historical evolution of psychology in allof its variations transcends individual identities as being onekind of psychologist or another. Accordingly, Volume 1 inthe Handbook is devoted to the history of psychology asit emerged in many areas of scientific study and appliedtechnology.

A second unifying thread in psychology is a commitmentto the development and utilization of research methodssuitable for collecting and analyzing behavioral data. Withattention both to specific procedures and their applicationin particular settings, Volume 2 addresses research methodsin psychology.

Volumes 3 through 7 of the Handbook present the sub-stantive content of psychological knowledge in five broadareas of study: biological psychology (Volume 3), experi-mental psychology (Volume 4), personality and social psy-chology (Volume 5), developmental psychology (Volume 6),and educational psychology (Volume 7). Volumes 8 through12 address the application of psychological knowledge infive broad areas of professional practice: clinical psychology(Volume 8), health psychology (Volume 9), assessment psy-chology (Volume 10), forensic psychology (Volume 11), andindustrial and organizational psychology (Volume 12). Eachof these volumes reviews what is currently known in theseareas of study and application and identifies pertinent sourcesof information in the literature. Each discusses unresolved is-sues and unanswered questions and proposes future direc-tions in conceptualization, research, and practice. Each of thevolumes also reflects the investment of scientific psycholo-gists in practical applications of their findings and the atten-tion of applied psychologists to the scientific basis of theirmethods.

The Handbook of Psychology was prepared for the pur-pose of educating and informing readers about the presentstate of psychological knowledge and about anticipated ad-vances in behavioral science research and practice. With thispurpose in mind, the individual Handbook volumes addressthe needs and interests of three groups. First, for graduate stu-dents in behavioral science, the volumes provide advancedinstruction in the basic concepts and methods that define thefields they cover, together with a review of current knowl-edge, core literature, and likely future developments. Second,in addition to serving as graduate textbooks, the volumesoffer professional psychologists an opportunity to read andcontemplate the views of distinguished colleagues concern-ing the central thrusts of research and leading edges of prac-tice in their respective fields. Third, for psychologists seekingto become conversant with fields outside their own specialty

vii

viii Handbook of Psychology Preface

and for persons outside of psychology seeking informa-tion about psychological matters, the Handbook volumesserve as a reference source for expanding their knowledgeand directing them to additional sources in the literature.

The preparation of this Handbook was made possible bythe diligence and scholarly sophistication of the 25 volumeeditors and co-editors who constituted the Editorial Board.As Editor-in-Chief, I want to thank each of them for the plea-sure of their collaboration in this project. I compliment themfor having recruited an outstanding cast of contributors totheir volumes and then working closely with these authors toachieve chapters that will stand each in their own right as

valuable contributions to the literature. I would like finally toexpress my appreciation to the editorial staff of John Wileyand Sons for the opportunity to share in the development ofthis project and its pursuit to fruition, most particularly toJennifer Simon, Senior Editor, and her two assistants, MaryPorterfield and Isabel Pratt. Without Jennifer’s vision of theHandbook and her keen judgment and unflagging support inproducing it, the occasion to write this preface would nothave arrived.

IRVING B. WEINERTampa, Florida

Volume Preface

ix

The topic of this volume represents a perspective that can betraced to the founding of psychology as a scientific disci-pline. Since the late 19th century, biological psychologistshave used the methods of the natural sciences to study rela-tionships between biological and psychological processes.Today, a natural science perspective and the investigation ofbiological processes have increasingly penetrated all areas ofpsychology. For instance, social and personality psycholo-gists have become conversant with evolutionary concepts intheir studies of traits, prejudice, and even physical attraction.Many cognitive psychologists have forsaken black boxes infavor of functional magnetic resonance imaging brain scans,and clinical psychologists, as participants in the mentalhealth care of their clients, have become more familiar withthe basis for the action of pharmacological therapeutics onthe brain. The scientific revolution in molecular biology andgenetics will continue to fuel the biological psychology per-spective. Indeed, it can be anticipated that some of the mostsignificant scientific discoveries of the 21st century willcome from understanding the biological basis of psychologi-cal functions.

The contributors to this volume provide the reader with anaccessible view of the contemporary field of biological psy-chology. The chapters span content areas from basic sensorysystems to memory and language and include a perspectiveon different levels of scientific analysis from molecules tocomputational models of biological systems. We have assem-bled this material with a view toward engaging the field andour readership in an appreciation of the accomplishments andspecial role of biological psychology in the discipline.Notwithstanding the trend for a greater influence of biologi-cal studies in the field of psychology in general, biologicalpsychology represents a distinctive fusion of biology andpsychology in its theory and methods. For example, evolutionas a fundamental tenet in the field of biology has long perme-ated the work of biological psychologists. The rapid growthin publications in the area of evolutionary psychology overthe past two decades suggests a growing acceptance of theimportance of evolutionary ideas in the behavioral sciences.

In addition to this influence, the contribution of biology,rooted in evolutionary and ethological traditions, hassustained a broad base of comparative studies by biological

psychologists, as reflected in the contents of this volume.Research in the field of psychology using different speciesserves a dual purpose. Many studies using nonhuman speciesare motivated by the utility of information that can be gainedthat is relevant to humans, using a range of preparations andtechniques in research that are not otherwise possible. Of equalimportance, comparative research provides insights into vari-ation in biological organisms. Studies of a variety of speciescan show how different solutions have been achieved for bothprocessing input from the environment and elaborating adap-tive behavioral strategies. The organization and content of thisvolume focus squarely on the need to recognize these dual ob-jectives in studies of biological and psychological processes.

The question of how translation is made across species isever more central to the undertaking of biological psychol-ogy. In the not-distant past, most psychologists viewed re-search using nonhuman animals as irrelevant to a broad rangeof psychological functions in humans, including affective andcognitive processes that were considered exclusive capacitiesof the human mind and social lives of humans in relation-ships. Today, animal models are increasingly recognized aspossessing at least some elements of cognitive and affectiveprocesses that are potentially informative for understandingnormal functions and disorders in humans. This progress hascontributed to a number of research areas described in the en-suing chapters, many of which include insights that havecome from using new gene targeting technology. Becausehuman studies do not provide the opportunity for rigorous ex-perimental control and manipulation of genetic, molecular,cellular, and brain and behavioral system processes, the useof genetically manipulated mice has become a powerful toolin research. At the same time, the limitations and pitfalls ofwholesale acceptance of such animal models are clear to bio-logical psychologists. In addition to the fact that mousespecies have faced different evolutionary pressures andadapted to different ecological niches, the use of geneticallyaltered systems presents new challenges because these novelmice are likely to express new constraints and influences be-yond their target characters. The tradition of comparativestudies of different animal species makes the role of biologi-cal psychology central to the effort to use these new andpowerful approaches to advance scientific understanding.

x Volume Preface

A related overriding theme in biological psychology is thesignificance of translating across levels of analysis. Biologi-cal descriptions of psychological processes are viewedby many, particularly outside the field, as a reductionistendeavor. As such, reductionism might represent merely adescent to a level of description in which psychological func-tions are translated into the physical and chemical lexicon ofmolecular events. It is increasingly evident that researchdirected across levels of analysis serves yet another purpose.In addition to determining biological substrates, such investi-gations can work in the other direction, to test between com-peting hypotheses and models of psychological functions. Itis also the case that molecular biologists who study the brainare increasingly seeking contact with investigators who workat the level of systems. More genes are expressed in the brainthan in all other organs of the body combined. Gene expres-sion is controlled by intricate information-processing net-works within a neuron and is inextricably tied to the activityof neurons as elements in larger information-processing sys-tems. Psychological functions (e.g., the conditions that aresufficient to produce long-term memory or the environmentalinputs that are necessary to elicit maternal behavior) will aidin understanding the functional significance of complex mo-lecular systems at the cellular level. Scientific advances arerapidly shifting the biological psychology paradigm from oneof reductionism to an appreciation that vertical integrationacross levels of analysis is essential to understand the proper-ties of biological organisms.

In chapter 1 Russil Durrant and Bruce J. Ellis introducesome of the core ideas and assumptions that comprise thefield of evolutionary psychology. Although they focus on re-productive behaviors, Durrant and Ellis also illustrate howthe ideas of evolutionary psychology can be employed in thedevelopment of specific, testable hypotheses, about humanmind and behavior. Their ideas go far past the usual matingbehaviors, and they even provide an adaptive scenario forself-esteem studies. Durrant and Ellis note that one of themost crucial tasks for evolutionary psychologists in the com-ing decades will be the identification and elucidation of psy-chological adaptations. Although most of the obvious andplausible psychological adaptations have already beencataloged, many more remain undiscovered or inadequatelycharacterized. Because adaptations are the product of naturalselection operating in ancestral environments, and becausepsychological traits such as jealousy, language, and self-esteem are not easily reconstructed from material evidencesuch as fossils and artifacts, direct evidence for behavioraladaptations may be difficult to obtain. One of the challengesfor evolutionary psychology, according to Durrant and Ellis,is to develop increasingly more rigorous and systematic

methods for inferring the evolutionary history of psychologi-cal characteristics, as well as to determine how best to char-acterize psychological adaptations.

As mentioned, within the past 10 years a novel intellectualbridge has been formed between psychology and molecularbiology. Molecular biologists have mapped large segments ofthe mouse genome as part of the ambitious Human GenomeProject. As genes have been identified and sequenced, mo-lecular biologists have begun the difficult task of identifyingthe functions of these genes. An increasingly common ge-netic engineering technique used to discover the function ofgenes is targeted disruption (knockout) of a single gene. Byselectively disrupting the expression of a single gene, molec-ular biologists reason that the function of that targeted genecan be determined. In other cases, a specific gene is added(knockin). In many cases, the phenotypic description ofknockout and knockin mice includes alterations in behavior.In chapter 2 Stephen C. Maxson explores behavior genetics,generally, and describes the implications of molecular genet-ics for psychology, specifically. He describes classic studieson the heritability of behavior (viz., selective breeding) aswell as twin and adoption studies. Maxson adroitly docu-ments gene mapping and genome projects in relation tobehavioral studies. After presenting an introduction to mo-lecular and developmental genetics, he emphasizes the im-portance of population genetics in studies of the evolution ofbehavior. Finally, Maxson explores the ethical and legal man-ifestations of behavioral genetics in the context of academicsand society as a whole.

Using the comparative method has been particularly suc-cessful for understanding the sensory and perceptual machin-ery in animals. In chapter 3 Gerald H. Jacobs describes thegreat success that he and others have had using the compara-tive approach to elucidate the mechanisms and processes un-derlying vision. Most studies of nonhuman vision are likelymotivated to understand human vision. The remaining stud-ies of vision in nonhuman animals are aimed at understand-ing comparative features of vision in their own right, oftenfrom an evolutionary perspective with the intent to discovercommon and different solutions for seeing. Jacobs considersboth approaches in his review of comparative vision. After adescription of the fundamental features of photic environ-ments, he provides basic design features and describes theevolution of eyes. Jacobs then focuses on photosensitivity asa model of the comparative approach. He details photopig-ments, ocular filtering, and the role of the nervous system inphotosensitivity. Three important issues in comparativevision—detection of change, resolution of spatial structure,and use of chromatic cues—are also addressed. Finally,Jacobs includes a section on the difficulty of measuring

Volume Preface xi

animal vision, as well as his perspective of where this field islikely to evolve.

In chapter 4 Cynthia F. Moss and Catherine E. Carr reviewsome of the benefits and problems associated with a compar-ative approach to studies of hearing. Comparative auditionalso has a primary goal of understanding human audition,but a larger proportion of this field is dedicated to under-standing the relationship between the sensory system of theanimal and its biologically relevant stimuli as compared tocomparative vision. The ability to detect and process acousticsignals evolved many times throughout the animal kingdom,from insects and fish to birds and mammals (homoplasies).Even within some animal groups, there is evidence that hear-ing evolved independently several times. Ears appear notonly on opposite sides of the head, but also on a variety ofbody parts. Out of this diversity, many fascinating, specificauditory adaptations have been discovered. A surprisingnumber of general principles of organization and functionhave emerged from studies of diverse solutions to a commonproblem. Comparative studies of audition attempt to bringorder to the variation and to deepen our understanding ofsound processing and perception.

Moss and Carr review many common measures of audi-tory function, anatomy, and physiology in selective species inorder to emphasize general principles and noteworthy spe-cializations. They cover much phylogenetic ground, review-ing insects, fishes, frogs, reptiles, birds, and mammals. Thechapter begins with a brief introduction to acoustic stimuli,followed by a review of ears and auditory systems in a largesample of species, and concludes with a comparative presen-tation of auditory function in behavioral tasks.

Behavioral studies of auditory systems reveal severalcommon patterns across species. For example, hearing oc-curs over a restricted frequency range, often spanning severaloctaves. Absolute hearing sensitivity is best over a limitedfrequency band, typically of high biological importance tothe animal, and this low-threshold region is commonlyflanked by regions of reduced sensitivity at adjacent frequen-cies. Absolute frequency discrimination and frequencyselectivity generally decrease with an increase in sound fre-quency. Some animals, however, display specializations inhearing sensitivity and frequency selectivity for biologicallyrelevant sounds, with two regions of high sensitivity or fre-quency selectivity corresponding with information, for ex-ample, about mates and predators. One important goal ofcomparative audition is to trace adaptations in the auditoryperiphery and merge those adaptations with central adapta-tions and behavior.

The history and state of the art of, as well as future studiesin, comparative motor systems are presented by Karim

Fouad, Hanno Fischer, and Ansgar Büschges in chapter 5.The authors carefully construct an argument for a concept ofcentral control of locomotion and the principles of pattern-generating networks for locomotion. In common with sen-sory systems to understand locomotor activity, the authorsargue that a multilevel approach is needed and present dataranging from the molecular and cellular level (i.e., identifica-tion of the neurons involved, their intrinsic properties, theproperties of their synaptic connections, and the role of spe-cific transmitters and neuromodulators) to the system level(i.e., functional integration of these networks in completemotor programs). They emphasize that both invertebrate andvertebrate locomotor systems have been studied on multiplelevels, ranging from the interactions between identifiableneurons in identified circuits to the analysis of gait. The re-view focuses on (a) the principles of cellular and synapticconstruction of central pattern-generating networks for loco-motion, (b) their location and coordination, (c) the role ofsensory signals in generating a functional network output,(d) the main mechanisms underlying their ability to adaptthrough modifications, and (e) basic features in modulatingthe network function.

Each human sensory system provides an internal neuralrepresentation of the world, transforming energy in the envi-ronment into the cellular coding machinery of vast networksof neurons. In studies of sensory information processing innonhuman primates, particularly in the Old World monkeys,we encounter research that brings us close to understandingfunctions of the human brain. Chapters 6 through 8 provide acurrent guide to sensory modalities in the primate brain thatoccupy extensive cortical systems.

Research on the visual system in primates has outpaced allother modalities. In chapter 6 Tatiana Pasternak, James W.Bisley, and David Calkins provide the reader with an exten-sive background of knowledge on the neuroanatomical orga-nization of visual pathways and functional properties of visu-ally responsive neurons. Their chapter follows the stream ofthe visual system from eye through multiple parallel process-ing and hierarchically organized systems in cortex. It alsocovers one of the most significant topics in vision research inrecent years, viz., the extent to which the properties of visu-ally responsive neurons are psychologically tuned at virtuallyall levels of cortical processing. Rather than passive process-ing of input from the retina, neurons in the visual system arestrongly influenced by the behavioral significance of thestimulus, manifesting effects of current attention and pastexperience.

It can be anticipated that the current pace of research willrapidly expand our understanding of other sensory modalitieswith extensive cortical processing systems in the primate

xii Volume Preface

brain. In chapter 7 Troy A. Hackett and Jon H. Kaas presentan up-to-date account of the anatomy and physiology of in-formation processing in the auditory system. Relative to thevisual and somatosensory systems, the organization of sub-cortical auditory pathways in the primate brain is exceed-ingly complex. At the same time, many findings on the sub-cortical processing of auditory information in primatescomplement findings in other mammalian species. By com-parison with other species, the auditory representation in cor-tex is greatly expanded in the primate brain. Research usingnonhuman primates supports a model of parallel and hierar-chical organization in the auditory cortex that may broadlyshare features with the visual system. The orderly topographyand pattern of cortico-cortical connections define twostreams of auditory processing. The responsiveness of neu-rons in auditory belt and parabelt regions further indicates aspecialization for information about what and where, a dis-tinction made in parallel streams in the visual system. Thechapter provides an interesting discussion of research usingcomplex stimuli, such as species-typical calls, to characterizethe auditory objects or events for which the what pathwaymay be specialized in nonhuman primates.

In dynamic and complex environments, all mammals relyon visual and auditory systems to obtain information. In thebasic tasks of survival—whether evasion of predators, navi-gation of territory, or location of food and water—thesemodalities make it possible to identify and localize objects ata distance. Tactile perception becomes a key modality in pri-mates’ ability to identify and manipulate objects within arm’sreach. In chapter 8 Steven Hsiao, Ken Johnson, and TakashiYoshioka focus on tactile perception, a system that beginswith the transduction of information by four types of cuta-neous mechanoreceptors. The authors review evidence thatinformation from each of these receptor types serves a dis-tinctive role in tactile perception. Among these, the rapidlyadapting class has exquisite sensitivity to minute movementof the skin, as little as 4 �m to 5 �m. By contrast, the slowlyadapting Type 1 class operates over a greater dynamic rangeof stimulation but has extraordinary spatial resolution. Theseand other mechanoreceptors share virtually identical proper-ties in humans and in nonhuman primates. As the pathwaysfor tactile perception are followed into cortical networks, atheme from previous chapters recurs. Tactile responsive neu-rons, similar to neurons in the visual and auditory corticalsystems, are strongly influenced by psychological variablesof attention and experience.

We all learned and accepted that there are five primarysenses—that is, until we stubbed our toes and recalled our“sixth sense.” A critical sensory system that alerts us to realor potential tissue damage is pain. In chapter 9 Terence

Coderre, Catherine Bushnell, and Jeffrey Mogil explore themechanisms of pain. They note that pain has recently come tobe thought of as two separate sensory entities: (a) physiolog-ical pain and (b) pathological pain. Physiological painreflects a typical reaction of the somatosensory system tonoxious stimulation. Physiological pain is adaptive. Rare in-dividuals who cannot process physiological pain informationfrequently injure themselves and are unaware of internaldamage that is normally signaled by pain. Predictably, suchindividuals often become disfigured and have a significantlyshortened life span. Pathological pain reflects the develop-ment of abnormal sensitivity in the somatosensory system,usually precipitated by inflammatory injury or nerve damage.The most common features of pathological pain are pain inthe absence of a noxious stimulus, increased duration of re-sponse to brief-stimulation stimuli, or perception of pain inresponse to normally nonpainful stimulation. The neurologi-cal abnormalities that account for pathological pain remainunspecified and may reside in any of the numerous sitesalong the neuronal pathways that both relay and modulatesomatosensory inputs.

Chapter 9 provides a comprehensive review of the currentknowledge concerning the anatomical, physiological, andneurochemical substrates that underlie both physiologicaland pathological pain. Thus, Coderre and colleagues have de-scribed in detail the pathways that underlie the transmissionof inputs from the periphery to the central nervous system(CNS), the physiological properties of the neurons activatedby painful stimuli, and the neurochemicals that mediate ormodulate synaptic transmission in somatosensory pathways.The review is organized by neuroanatomy into separate sec-tions: (a) the peripheral nervous system and (b) the CNS,which is further divided into (a) the spinal cord dorsalhorn and (b) the brain. The authors made a special effort toidentify critical advances in the field of pain research, espe-cially the processes by which pathological pain develops fol-lowing tissue or nerve injury, as well as how pain is modu-lated by various brain mechanisms. The multidimensionalnature of pain processing in the brain emphasizes the multi-dimensional nature of pain, using anatomical connectivity,physiological function, and brain imaging techniques.Finally, the authors provide some insights into future painsensitivity and expression research, with a focus on molecu-lar biology and behavioral genetics.

The ability to detect chemicals in the environment likelyrepresents the most primitive sensory faculty and remainscritical for survival and reproductive success in modernprokaryotes, protists, and animals. Chemicals in solution aredetected by the taste sensory system; chemical sensation hasa central role in the detection of what is edible and where it is

Volume Preface xiii

found. It is well known, for example, that the flavor of food(i.e., the combination of its taste and smell) is a major deter-minant of ingestion. Humans are able to detect volatile chem-icals in air with our olfactory sensory system. Individualsmay use chemical senses to protect themselves from ingest-ing or inhaling toxins that can cause harm. The chemicalsenses, olfaction and taste, are reviewed in chapter 10 byPatricia M. Di Lorenzo and Steven L. Youngentob.

Until recently, the study of taste and olfaction has pro-gressed at a relatively slow pace when compared to the studyof the other sensory modalities such as vision or audition.This reflects, in part, the difficulty in defining the physicaldimensions of chemosensory stimuli. We can use humandevices to deliver exactly 0.5-m candles of 484 �m of lightenergy to the eye and then conduct appropriate psy-chophysics studies consistently across laboratories andacross participants. Until recently, however, it has been im-possible to present, for example, 3 units of rose smells to anexperimental participant. In the absence of confidence thatany given array of stimuli would span the limits of chemicalsensibility, investigators have been slow to agree on schemeswith which taste and olfactory stimuli are encoded by thenervous system. As Di Lorenzo and Youngentob reveal,technological advances, particularly in the realm of molecu-lar neuroscience, are providing the tools for unraveling someof the longstanding mysteries of the chemical senses.Some of the surprising findings that have resulted from thisincreasingly molecular approach to chemosensation are thediscovery of a fifth basic taste quality (i.e., umami) and thediscovery that the differential activation of different subsetsof sensory neurons, to various degrees, forms the basis forneural coding and further processing by higher centers inthe olfactory pathway. For both olfaction and taste, the care-ful combination of molecular approaches with precise psy-chophysics promise to yield insights into the processing ofchemical signals. Next, we move from input to output.

To fuel the brain and locomotor activities, we need energy.Because most bacteria and all animals are heterotrophs, theymust eat to obtain energy. What and how much we eatdepends on many factors, including factors related to palat-ability or taste, learning, social and cultural influences, envi-ronmental factors, and physiological controls. The relativecontribution of these many factors to the regulation of feed-ing varies across species and testing situations. In chapter 11Timothy H. Moran and Randall R. Sakai detail the psychobi-ology of food and fluid intake. They focus on three interact-ing systems important in the regulation of feeding: (a) signalsrelated to metabolic state, especially to the degree adiposity;(b) affective signals related to taste and nutritional conse-quences that serve to reinforce aspects of ingestive behavior;

and (c) signals that arise within an individual meal thatproduce satiety. Moran and Sakai also identify the importantinteractions among these systems that permit the overallregulation of energy balance.

Individuals are motivated to maintain an optimal level ofwater, sodium, and other nutrients in the body. ClaudeBernard, the 19th-century French physiologist, was the firstto describe animals’ ability to maintain a relatively constantinternal environment, or milieu intérieur. Animals are waterycreatures. By weight, mammals are approximately two-thirdswater. The cells of animals require water for virtually allmetabolic processes. Additionally, water serves as a solventfor sodium, chloride, and potassium ions, as well as sugars,amino acids, proteins, vitamins, and many other solutes, andis therefore essential for the smooth functioning of the ner-vous system and for other physiological processes. Becausewater participates in so many processes, and because it iscontinuously lost during perspiration, respiration, urination,and defecation, it must be replaced periodically. Unlike min-erals or energy, very little extra water is stored in the body.When water use exceeds water intake, the body conserveswater, mainly by reducing the amount of water excreted fromthe kidneys. Eventually, physiological conservation can nolonger compensate for water use and incidental water loss,and the individual searches for water and drinks.

Regulation of sodium intake and regulation of water intakeare closely linked to one another. According to Moran andSakai, the body relies primarily on osmotic and volumetricsignals to inform the brain of body fluid status and to engagespecific neurohormonal systems (e.g., the renin-angiotensinsystem) to restore fluid balance. As with food intake, signalsthat stimulate drinking, as well as those that terminate drink-ing, interact to ensure that the organism consumes adequateamounts of both water and electrolytes. The signals for satiety,and how satiety changes the taste and motivation for seekingfood and water, remain to be specified.

We continue with a review of motivated behavior in chap-ter 12. Elaine M. Hull and Juan M. Dominguez review the re-cent progress made in understanding sexual differentiation,as well as the hormonal and neural mechanisms that driveand direct male and female sexual behavior. They begin theirchapter by considering the adaptive function of sexual be-havior by asking why sexual reproduction is by far the mostcommon means of propagating multicellular species, eventhough asexual reproduction is theoretically much faster andeasier. The prevailing hypothesis is that sexual behaviorevolved to help elude pathogens that might become soprecisely adaptive to a set of genetically identical clones thatfuture generations of the host species would never rid them-selves of the pathogens. By mixing up the genomic character

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of their offspring, sexually reproducing creatures could pre-vent the pathogens—even with their faster generational timeand hence faster evolution—from too much specialization.Pathogens that preyed on one specific genome would be ex-tinct after the single generation of gene swapping that occurswith each sexual union. Thus, sexual reproduction has se-lected pathogens to be generalists among individuals, al-though sufficiently specific to be limited to a few hostspecies.

Hull and Dominguez next provide a description of the cop-ulatory patterns that are common across mammalian speciesand summarize various laboratory tests of sexual behavior.After a thorough description of sexual behavior, the mecha-nisms underlying sexual behavior are presented. Because hor-mones are important for sex differentiation in all mammalianand avian species and because hormones also activate sexualbehavior in adulthood, the chapter focuses on the endocrinemechanisms underlying sexual behavior and explores themechanisms by which hormones modulate brain and behavior.The authors next describe the hormonal and neural control offemale sexual behavior, followed by a similar treatment of theregulation of male sexual behavior. In each case, they firstsummarize the effects of pharmacological and endocrine treat-ments on sexual behavior. The pharmacological data indicatewhich neurotransmitter systems are involved in the variouscomponents of sexual behavior (e.g., sexual motivation vs.performance). A variety of techniques has been used to deter-mine where in the brain sexual behavior is mediated, includinglesions and stimulation, local application of drugs and hor-mones, and measures of neural activity. Finally, Hull andDominguez observe that the hormonal and neural mechanismsthat control sexual behavior are similar to the mechanisms thatregulate other social behaviors.

The authors close with a series of questions and issues thatremain largely unanswered. For example, they suggest thatmore neuroanatomical work is necessary to track the neuralcircuits underlying sexual behavior in both females andmales. Neurotransmitter signatures of those neurons areimportant pieces of the puzzle, as well as neurotransmitter re-ceptor interactions and intracellular signal transduction acti-vation in response to various neurotransmitter and hormonaleffects. What changes in gene transcription are induced byspecific hormones? How do rapid membrane effects ofsteroids influence sexual behavior? What changes in genetranscription mediate the effects of previous sexual experi-ence? They close with broader questions that include the in-terrelationships among sexual and other social behaviors, andhow species-specific differences in behavior are related totheir ecological niches. All of these issues are critical for afull understanding of sexual behavior.

Life on Earth evolves in the presence of pronounced tem-poral fluctuations. The planet rotates daily on its axis. Lightavailability and temperature vary predictably throughouteach day and across the seasons. The tides rise and subside inpredictable ways. These fluctuations in environmental factorsexert dramatic effects on living creatures. For example, dailybiological adjustments occur in both plants and animals,which perform some processes only at night and others onlyduring the day. Similarly, daily peaks in the metabolic activ-ity of warm-blooded animals tend to coincide with the dailyonset of their physical activity. Increased activity alone doesnot drive metabolic rates; rather, the general pattern of meta-bolic needs is anticipated by reference to an internal biologi-cal clock. The ability to anticipate the onset of the daily lightand dark periods confers sufficient advantages that endoge-nous, self-sustained circadian clocks are virtually ubiquitousamong extant organisms In chapter 13 Federica Latta andEve Van Cauter discuss the importance of biological clocksand sleep on cognition and behavior.

In addition to synchronizing biochemical, physiological,and behavioral activities to the external environment, biolog-ical clocks are important to multicellular organisms for syn-chronizing the internal environment. For instance, if a spe-cific biochemical process is most efficiently conducted in thedark, then individuals that mobilize metabolic precursors, en-zymes, and energy sources just prior to the onset of darkwould presumably have a selective advantage over individu-als that organized their internal processes at random times.Thus, there is a daily temporal pattern, or phase relationship,to which all biochemical, physiological, and behavioralprocesses are linked.

Latta and Van Cauter provide an overview of the circadiansystem, as well as its development. Then, they discuss theregulation of sleep in the context of biological rhythms andshow how sleep-wake homeostasis interacts with alertnessand cognitive function, mood, cardiovascular, metabolic, andendocrine regulation. Their chapter closes with a descriptionof sleep disorders in the context of circadian dysregulation.

Preceding chapters in the volume considered specific mo-tivated behaviors, such as feeding and mating. In chapter 14Krista McFarland and Peter W. Kalivas deal with neuralcircuitry in the brain that is relevant to many different goal-directed behaviors. Whether the goal is food or a sexual part-ner, common circuitry is now believed to be required foractivating and guiding behavior to obtain desired outcomes.This brain system, referred to here as the motive circuit, in-volves a network of structures and their interconnectionsin the forebrain that control motor output systems. The au-thors present a scheme, based on much evidence, that the mo-tive circuit is comprised of two separate but interactive

Volume Preface xv

subsystems. One of these provides control over goal-directedbehavior under routine circumstances, where prior experi-ence has established efficient direct control over responsesystems. The other subcortical-limbic circuit serves a com-plementary function to allow new learning about motivation-ally relevant stimuli.

The motive circuit described by McFarland and Kalivasincludes not only anatomically defined pathways but alsodefinition of the neurochemical identity of neurons in the sys-tem. This information has proven vital because the motivecircuit is an important target for drugs of interest for theirpsychological effects. Indeed, the field of psychopharmacol-ogy has converged to a remarkable degree on the brain re-gions described in this chapter. Substances of abuse, acrossmany different classes of agents such as cocaine and heroin,depend on this neural system for their addictive properties.Consequently, the role of subsystems within the motive cir-cuit in drug addiction is a topic of great current interest.Within the scheme described in the chapter, drug-seekingbehavior, including the strong tendency to relapse into addic-tion, may reflect an inherent property of circuit function thatcontrols routine responses or habits. Behavioral and neuralplasticity underlying addiction is becoming an increasinglyimportant topic of study in this area of biological psychologyfor providing an inroad to effective treatment for drug abuse.

Emotion encompasses a wide range of experience and canbe studied through many variables, ranging from verbal de-scriptions to the measurement of covert physiological re-sponses, such as heart rate. In chapter 15 Michael Davis andPeter J. Lang consider this topic, broadly spanning researchin humans and other species. From this comparative perspec-tive, there is no doubt that emotions are fundamentally adap-tive, capturing attention and strongly engaging a dispositionto action. Succinctly put, emotions move us.

Davis and Lang elaborate on a useful framework for orga-nizing the diverse phenomena of emotion, in which emotionsare considered along two dimensions. On one dimension ofvalence, emotional states range from positive (happy, confi-dent) to negative (fear, anger). These different emotionalstates, in turn, are associated with different behavioraltendencies, strongly engaging output systems based on theintegration of current information and past experience. In ad-dition, both positive and negative emotional states can rangefrom relative calm to high degrees of arousal, providing asecond dimension. Finally, the topic of emotion not only en-compasses the regulation of internal emotional states thatmotivate behavior expressive of those states, but also may beimportant for the cognitive evaluation of the emotionalcontent of complex perceptual cues. Davis and Lang areadept guides in covering a range of psychological studies, as

well as research on neural systems involved in emotionalprocesses.

The authors give detailed treatment to one model of emo-tion that has become well studied across species. Perhaps it isnot surprising that the emotion of fear, which is basic to sur-vival, possesses many common features across mammalianspecies. Research over the past decade or so has also revealedthat neural systems engaged in settings that evoke fear showstrong homology in humans and other mammals, includinglaboratory rodents. The study of fear has in turn become oneof best defined models in which to study the neural basis oflearning. Circumstances associated with aversive events pro-vide cues that become potent activators of fear, preparing or-ganisms to deal with threat and danger. Because the circuitryin the brain for this form of learning is delineated, scientistsare making progress in understanding the exact sites andmechanisms where communication between neurons is al-tered to produce this form of emotional learning. In this chap-ter the reader encounters a field where vertical integrationfrom behavior to synaptic plasticity is advancing at a rapidpace.

Life is challenging. The pressure of survival and repro-duction takes its toll on every individual living on the planet;eventually and inevitably the wear and tear of life leads todeath. Mechanisms have evolved to delay death presumablybecause, all other things being equal, conspecific animals thatlive the longest tend to leave the most successful offspring. Inthe Darwinian game of life, individuals who leave the mostsuccessful offspring win. Although some of the variation inlongevity reflects merely good fortune, a significant part ofthe variation in longevity among individuals of the samespecies reflects differences in the ability to cope with the de-mands of living. All living creatures are dynamic vessels ofequilibria, or homeostasis. Any perturbation to homeostasisrequires energy to restore the original steady-state. An indi-vidual’s total energy availability is partitioned among manycompeting needs, such as growth, cellular maintenance, ther-mogenesis, reproduction, and immune function. During envi-ronmental energy shortages, nonessential processes such asgrowth and reproduction are suppressed. If homoeostatic per-turbations require more energy than is readily available afternonessential systems have been inhibited, then survival maybe compromised. All living organisms currently exist be-cause of evolved adaptations that allow individuals to copewith energetically demanding conditions. Surprisingly, thesame neuroendocrine coping mechanisms are engaged in allof these cases, as well as in many other situations.

The goal of chapter 16, written by Angela Liegey Dougalland Andrew Baum, is to present the effects of stress and cop-ing on immune function. Because description should always

xvi Volume Preface

precede formal analyses in science, it is important to agree onwhat is meant by stress. This first descriptive step has provedto be difficult in this field; however, it remains critical inorder to make clear predictions about mechanisms. To evalu-ate the brain regions involved in mediating stress, there mustbe some consensus about what the components of the stressresponse are. The term stress has often been conflated to in-clude the stressor, the stress response, and the physiologicalintermediates between the stressor and stress responses. Theconcept of stress was borrowed from an engineering-physicsterm that had a very specific meaning (i.e., the forces outsidethe system that act against a resisting system). The engineer-ing-physics term for the intrinsic adjustment is strain. For ex-ample, gravity and wind apply stress to a bridge; the bendingof the metal under the pavement in response to the stress isthe strain. Had we retained both terms, we would not be in thecurrent terminological predicament. It is probably too late toreturn to the original engineering-physics definition of theseterms in biological psychology because despite the confusingarray of indefinite uses of the term stress, an impressive sci-entific literature integrating endocrinology, immunology,psychology, and neuroscience has developed around the con-cept of stress. What, then, does it mean to say that an individ-ual is under stress? For the purposes of this chapter, Dougalland Baum use some of the prevailing homeostatic notions ofstress to arrive at a flexible working definition.

The authors next describe coping, which is a way to coun-teract the forces of stress. Next, Dougall and Baum describethe psychological and behavioral responses to stress and em-phasize the effects of stress on immune function. Althoughstress causes many health problems for individuals, all thenews is not bleak. Dougall and Baum review the variousstress management interventions. In some areas researchersare making remarkable progress at identifying the geneticand molecular mechanisms of stress with little regard for theintegrative systems to which these molecular mechanismscontribute. In other areas scientists are still struggling toparse out the interactive effects of behavioral or emotionalfactors such as fear and anxiety on stress responsiveness. Ob-viously, a holistic approach is necessary to understand thebrain stress system—perhaps more importantly than for otherneural systems. Acute stress can actually bolster immunefunction, whereas chronic stress is always immunosuppres-sant. One important goal of future stress research, accordingto Dougall and Baum, is to determine how and when acutestress becomes chronic and how to intervene to prevent thistransition.

As indicated throughout this volume, biological psychologyrepresents a distinctive fusion of biology and psychology. Inchapter 17 Peter C. Holland and Gregory F. Ball provide a syn-thesis of perspectives on learning from these different

disciplines. The study of animal learning, firmly rooted in theorigins of psychology, has traditionally emphasized the role ofexperience in shaping behavior and sought to identify generalprinciples that encompass the phenomena of learning. Giventheir perspective, experimental psychologists have long stud-ied laboratory animals as grist for developing a general processtheory of learning. Their studies have traditionally used tasksin which exposure to environmental events is tightly controlledand discrete responses are monitored. In contrast, the etholog-ical approach based in the field of biology has historicallyemphasized constraints on learning and viewed experience-dependent adaptations in relatively specialized domains, oftenstudied in naturalistic settings. Holland and Ball show howeach of these approaches has contributed to our understandingof the adaptive capacities of organisms. Studies of animallearning have revealed a rich complexity of well-defined asso-ciative processes, which have come to include representationalfunctions in the cognitive domain. At the same time, biologicalpsychology has become more eclectic in its approach with anintegration of the ethological perspective into the field. Thesynthesis provided in this chapter is a particularly good exam-ple of fertilization across disciplines.

The topic of learning is continued in chapter 18 by JosephSteinmetz, Jeansok Kim, and Richard F. Thompson. Here thefocus is on the use of specific models of learning to investigatebiological substrates. The authors present a variety of prepara-tions in which a neural systems analysis has shed light on theneural circuits and mechanisms of learning. Those prepara-tions range from research in relatively simple organisms, suchas invertebrates, to several forms of learning in mammals thathave closely tied research in laboratory animals to an under-standing of the neural basis of learning in humans.

Among the models of learning, the authors discuss in par-ticular depth research on eye-blink conditioning, a simpleform of Pavlovian conditioning that was first demonstrated inhumans about 70 years ago. Since that time, behavioral andneuroscientific research has transformed eye-blink condition-ing into a powerful paradigm for the interdisciplinary studyof brain and behavior. The operational simplicity and mini-mal sensory, motor, and motivational demands of the proce-dure make it applicable with little or no modification across arange of animal species—rodents, rabbits, cats, monkeys, hu-mans—and across the life span, from early infancy to old age.As detailed in the chapter, we now have extensive knowledgeof the neurobiological mechanisms of eye-blink condition-ing. Studies in both animals and humans implicate the cere-bellum and hippocampus in eye-blink conditioning. Simpleassociative learning is mediated by well-characterized brain-stem-cerebellar circuitry, whereas more complex, higherorder conditioning phenomena appear to depend on interac-tions of this circuitry with forebrain structures such as the

Volume Preface xvii

hippocampus. This research arguably provides one of thebest-characterized models of neural systems analysis and ver-tical integration in behavioral neuroscience.

The study of memory is now firmly grounded in the recog-nition that multiple memory systems exist. In chapter 19Howard Eichenbaum traces the historical antecedents of thisunderstanding. As a record of experience, habits and skills de-velop with practice and are enduring forms of memory. Habitsand skills control routine simple activities as well as the ex-quisitely refined performance of the virtuoso. Historically,memory in the form of habits and skills can be seen as thefocus of behaviorism in which effects of experience were stud-ied in terms of stimulus and response topographies. Suchforms of procedural memory that are exhibited in performancehave been distinguished from declarative memory. Declara-tive memory refers to deficits encountered in amnesicsyndromes where habit and skill memory (among other proce-dural types of memory) are entirely preserved but patientshave a profound inability either to recollect episodes of expe-rience consciously from the past or to acquire new knowledge.

The distinction between forms of declarative and proce-dural memory has become well established in studies ofhuman memory. Eichenbaum shows how these distinctionsare addressed in research on neurobiological systems. In par-ticular, the chapter deals with the challenge of translating de-clarative memory into studies with laboratory animals. Theneural circuitry critical for this form of memory is similarlyorganized in the human brain and in the brains of otherspecies including laboratory rodents. Neural structures in themedial temporal lobe, including the hippocampus, are linkedto information-processing systems in cortex. The chapterdeals with research that shows how the organization andfunction of this system allows for distinctive features of cog-nitive memory, involving representational networks that canbe flexibly accessed and used in novel situations. These prop-erties of memory can be tested across human and nonhumansubjects alike. The animal models, in particular, are an im-portant setting for research on the neural mechanisms ofmemory, including the cellular machinery that alters andmaintains changes in synaptic connections.

A central problem in comparative biology and psychologyis to determine the evolutionary mechanisms underlying sim-ilarity between species. As Marc Hauser points out in hischapter on comparative cognition (chapter 20), there aretwo categories of similarity. One category is characterized byhomologies, traits shared by two or more species that arosefrom a common ancestor that expressed the same trait. Thesecond category is characterized by homoplasies, similartraits that evolved independently in different taxonomicgroups usually via convergence. These distinctions are alwaysimportant in comparative approaches, but they are particularly

critical when considering primate cognition, where the bias isto assume that homology underlies similar cognitive func-tions. Few investigators can make this distinction, primarilybecause of a lack of good comparative data. Hauser arguesthat (comparative) primate cognition should make deeperconnections with studies of brain function, generally,and human infant cognitive development, specifically.He uses two examples: (a) the construction of a numbersense and (b) the ability to process speech, to make the casethat the apolygynous marriage between Darwin’s theory ofevolution and the representational-computational theory ofmind that tends to dominate much of current cognitive scienceis a productive endeavor. In the case of number, many ani-mals, primates included, can discriminate small numbers pre-cisely and large numbers approximately. Hauser argues thatover the course of human evolution we acquired a mechanismthat allowed only our species to discriminate large numbersprecisely, and this capacity ultimately led to our unique giftfor complex mathematics. With respect to speech-processingmechanisms, Hauser argues that humans share with otheranimals all of the core perceptual tools for extracting thesalient features of human speech, but that more comparativeneuroanatomical work, tracing circuitry and establishingfunctional connectivity, is necessary to determine the evolu-tionary history of speech processing among primates.

Interest in systems specialized for language in the humanbrain has a long history, dating from the earliest descriptionsof aphasia by neurologists in the 19th century. In chapter 21Eleanor M. Saffran and Myrna F. Schwartz guide the readerthrough this field of study from its historical roots to the con-temporary era, in which new tools and approaches are ad-vancing knowledge in unprecedented ways. The chapterdeals in detail with the kinds of inferences about the funda-mental properties of language that have been gleaned fromthe patterns of language breakdown after brain damage. Thisarea of cognitive neuropsychology has a long tradition in thefield. The authors then describe how recent studies of brainactivation in normal subjects using functional neuroimagingtechnology have confirmed many functions assigned to spe-cific brain regions and circuits based on cases of brain dam-age. They also consider the discrepancies that have emergedfrom comparison of these different approaches. Finally, thechapter includes a discussion of another powerful approachin research in which computational modeling has become animportant adjunct to empirical investigations in the biologi-cal study of language.

A broad perspective on the use of computational models inbiological psychology is the subject of chapter 22. Randall C.O’Reilly and Yuko Munakata discuss a variety of biologicallybased models, ranging from those focused on the propertiesof single neurons as information-processing units to more

xviii Volume Preface

extensive models used to study the properties of neurons innetworks that serve a range of psychological functions.

To provide a background to computational modeling ofboth single neurons and networks, the authors first discussthe biological properties that are central for defining and con-straining models of simulated neurons. Activation functionsfor such models can vary with respect to the real properties ofneurons that they incorporate, yielding an increasing com-plexity in how a neuron is simulated. For example, they de-scribe how variables, such as single-point integration versusmultiple compartments or biological constraints on weight-ing of inputs, can affect the properties of a simulated neuron.

A fundamental question in the study of neuron function isthe nature of the code for information. Firing rate, whichrefers to the frequency of action potentials, has long beenstudied as a coding mechanism. O’Reilly and Munakata ad-dress the debate between models based on rate codes andthose that consider other coding possibilities such as the pre-cise timing of spikes.

For psychological functions, ranging from perception andattention to learning and memory, processing systems involvenetworks of large numbers of neurons. O’Reilly and Munakatadescribe the basic organization and properties of networkmodels for the study of these functions. They then go on to de-scribe specific implementations. For example, they provide anextensive discussion of learning. In particular, they discusstwo influential learning devices incorporated into computa-tional models: a Hebbian mechanism, which rapidly incul-cates change in a network based on correlated activity, anderror-driven mechanisms that can acquire many input-outputmappings for which Hebbian mechanisms are inadequate.

Much of the material in the chapter on computational mod-eling is relevant to empirical research discussed in other chap-ters on sensory information processing and learning. O’Reillyand Munakata’s discussion of modeling relevant to memorymechanisms especially complements material discussedby Eichenbaum in chapter 19. Computational models of theproperties of hippocampus and cortex as a system for declara-tive memory reveal a distinctive information storage processthat can integrate information over many different experi-ences. The interleaving process modeled in this system allowsthe formation of overlapping representations that encodeshared structure across different experiences, while at thesame time minimizing interference between neural representa-tions of different events. In this and other examples discussedin the chapter, computational modeling provides an importantadjunct to the empirical base of research in the field.

A well-worn debate on nature versus nurture has longoccupied the field of psychology. This question is at the heartof research on development. To what extent is development

prearranged by our genetic endowment, and to what extentdoes experience play a role? In chapter 22, on experience anddevelopment, James E. Black shows how biological psychol-ogy has contributed to our understanding of these variables ofnature and nurture, and of their interactions.

Black first emphasizes the degree to which brain structureis predetermined such that early development protects againstvariations in constructing complex neural systems. He nextdescribes how many neural systems have evolved to captureand orchestrate carefully the role of experience in brain devel-opment. In such cases neural systems respond to experienceonly in a relatively narrow developmental window, referred toas a sensitive or critical period. It is interesting that this expe-rience-expectant development is biologically controlled inmany different systems by a sequence in which neural con-nections are overproduced and experience is then allowed toeliminate a large proportion of connections. The process ofoverproduction and selective elimination of synapses at a spe-cific developmental stage allows the brain to be shaped by ex-perience in a specialized domain. Black illustrates this processby drawing on studies of the effects of early experience on thevisual system. The process, however, can be extended to otherdomains involving social behavior and higher cognitive func-tions. Indeed, the scaffolding of experience-expectant devel-opment may be such that sensitive periods are designed tobuild progressively on one another.

Experience-expectant development is distinguished fromexperience-dependent development. In the former case, biol-ogy sets the stage for a modeling of brain development basedon experiences that can be anticipated to occur for all mem-bers of a species within a limited time frame. Experience-dependent development involves the brain’s susceptibility toexperiences that can be unique to the individual member of aspecies. The brain plasticity in this case is not limited to a de-fined critical period but is available throughout life.

Although much of our current understanding of experi-ence and development is based on basic research in labora-tory animals, Black discusses in depth the evidence that theseprinciples also apply to humans. He carefully considers thelimitations of currently available data and the gaps that needto be filled.

In closing this preface, we wish to express our gratitude tothe contributing authors. This volume of the Handbook rep-resents the field of biological psychology with its deep rootsin the history of our discipline and its vital and exciting op-portunities for new discovery in the 21st century.

MICHELA GALLAGHERRANDY J. NELSON

Handbook of Psychology Preface viiIrving B. Weiner

Volume Preface ixMichela Gallagher and Randy J. Nelson

Contributors xxi

1 EVOLUTIONARY PSYCHOLOGY 1Russil Durrant and Bruce J. Ellis

2 BEHAVIORAL GENETICS 35Stephen C. Maxson

3 COMPARATIVE PSYCHOLOGY OF VISION 47Gerald H. Jacobs

4 COMPARATIVE PSYCHOLOGY OF AUDITION 71Cynthia F. Moss and Catherine E. Carr

5 COMPARATIVE PSYCHOLOGY OF MOTOR SYSTEMS 109Karim Fouad, Hanno Fischer, and Ansgar Büschges

6 VISUAL PROCESSING IN THE PRIMATE BRAIN 139Tatiana Pasternak, James W. Bisley, and David Calkins

7 AUDITORY PROCESSING IN THE PRIMATE BRAIN 187Troy A. Hackett and Jon H. Kaas

8 PROCESSING OF TACTILE INFORMATION IN THE PRIMATE BRAIN 211Steven Hsiao, Ken Johnson, and Takashi Yoshioka

9 THE BIOLOGICAL PSYCHOLOGY OF PAIN 237Terence J. Coderre, Jeffrey S. Mogil, and M. Catherine Bushnell

10 OLFACTION AND TASTE 269Patricia M. Di Lorenzo and Steven L. Youngentob

11 FOOD AND FLUID INTAKE 299Timothy H. Moran and Randall R. Sakai

Contents

xix

xx Contents

12 SEX BEHAVIOR 321Elaine M. Hull and Juan M. Dominguez

13 SLEEP AND BIOLOGICAL CLOCKS 355Federica Latta and Eve Van Cauter

14 MOTIVATIONAL SYSTEMS 379Krista McFarland and Peter W. Kalivas

15 EMOTION 405Michael Davis and Peter J. Lang

16 STRESS, COPING, AND IMMUNE FUNCTION 441Angela Liegey Dougall and Andrew Baum

17 THE PSYCHOLOGY AND ETHOLOGY OF LEARNING 457Peter C. Holland and Gregory F. Ball

18 BIOLOGICAL MODELS OF ASSOCIATIVE LEARNING 499Joseph E. Steinmetz, Jeansok Kim, and Richard F. Thompson

19 MEMORY SYSTEMS 543Howard Eichenbaum

20 PRIMATE COGNITION 561Marc D. Hauser

21 LANGUAGE 595Eleanor M. Saffran and Myrna F. Schwartz

22 PSYCHOLOGICAL FUNCTION IN COMPUTATIONAL MODELS OF NEURAL NETWORKS 637Randall C. O’Reilly and Yuko Munakata

23 ENVIRONMENT AND DEVELOPMENT OF THE NERVOUS SYSTEM 655James E. Black

Author Index 669

Subject Index 709

Michael Davis, PhDEmory University School of MedicineDepartment of PsychiatryAtlanta, Georgia

Patricia M. Di Lorenzo, PhDState University of New YorkPsychology DepartmentBinghamton, New York

Juan M. Dominguez, MADepartment of PsychologySUNY BuffaloBuffalo, New York

Angela Liegey Dougall, PhDDepartment of PsychiatryUniversity of Pittsburgh Medical CenterPittsburgh, Pennsylvania

Russil Durrant, PhDDepartment of PsychologyUniversity of CanterburyChristchurch, New Zealand

Howard Eichenbaum, PhDDepartment of PsychologyBoston UniversityBoston, Massachusetts

Bruce J. Ellis, PhDDepartment of PsychologyUniversity of CanterburyChristchurch, New Zealand

Hanno FischerSchool of BiologyUniversity of St. AndrewsSt. Andrews, Scotland

Karim FouadBrain Research InstituteUniversity of ZurichZurich, Switzerland

Gregory F. Ball, PhDDepartment of PsychologyJohns Hopkins UniversityBaltimore, Maryland

Andrew Baum, PhDDepartment of PsychiatryUniversity of Pittsburgh Medical CenterPittsburgh, Pennsylvania

James W. Bisley, PhDLaboratory 1 Sensorimotor ResearchNational Eye InstituteBethesda, Maryland

James E. Black, MD, PhDUniversity of IllinoisBeckman Institute, NPAUrbana, Illinois

Ansgar BüschgesZoologisches InstitutUniversität zu KölnKöln, Germany

M. Catherine Bushnell, PhDPain Mechanisms LaboratoryClinical Research Institute of MontrealMontreal, Quebec, Canada

David Calkins, PhDDepartment of Opthamology and Center for Visual ScienceUniversity of Rochester Medical CenterRochester, New York

Catherine E. Carr, PhDZoology DepartmentUniversity of MarylandCollege Park, Maryland

Terence J. Coderre, PhDPain Mechanisms LaboratoryClinical Research Institute of MontrealMontreal, Quebec, Canada

xxi

Contributors

xxii Contributors

Troy A. Hackett, PhDDepartment of Hearing and

Speech SciencesVanderbilt UniversityNashville, Tennessee

Marc D. Hauser, PhDDepartment of PsychologyHarvard UniversityCambridge, Massachusetts

Peter C. Holland, PhDDepartment of PsychologyJohns Hopkins UniversityBaltimore, Maryland

Steven Hsiao, PhDKrieger Mind/Brain InstituteDepartment of NeuroscienceJohns Hopkins UniversityBaltimore, Maryland

Elaine M. Hull, PhDDepartment of PsychologySUNY BuffaloBuffalo, New York

Gerald H. Jacobs, PhDDepartment of Psychology and Neuroscience

Research InstituteUniversity of California, Santa BarbaraSanta Barbara, California

Ken Johnson, PhDKrieger Mind/Brain InstituteDepartment of NeuroscienceJohns Hopkins UniversityBaltimore, Maryland

Jon H. Kaas, PhDDepartment of PsychologyVanderbilt UniversityNashville, Tennessee

Peter W. Kalivas, PhDDepartment of PhysiologyUniversity of South CarolinaCharleston, South Carolina

Jeansok KimDepartment of PsychologyYale UniversityNew Haven, Connecticut

Peter J. Lang, PhDNational Institute of Mental Health CSEAUniversity of FloridaGainesville, Florida

Federica Latta, PhDDepartment of MedicineUniversity of ChicagoChicago, Illinois

Stephen C. Maxson, PhDDepartment of PsychologyUniversity of ConnecticutStorrs, Connecticut

Krista McFarland, PhDPhysiology and NeuroscienceMedical University of South CarolinaCharleston, South Carolina

Jeffrey S. Mogil, PhDDepartment of PsychologyMcGill UniversityMontreal, Quebec, Canada

Timothy H. Moran, PhDDepartment of PsychiatryJohns Hopkins UniversityBaltimore, Maryland

Cynthia F. Moss, PhDDepartment of PsychologyCollege of Behavioral and Social SciencesUniversity of MarylandCollege Park, Maryland

Yuko MunakataDepartment of PsychologyUniversity of Colorado, BoulderBoulder, Colorado

Randall C. O’ReillyDepartment of PsychologyUniversity of Colorado at BoulderBoulder, Colorado

Tatiana Pasternak, PhDDepartment of Neurobiology and AnatomyUniversity of Rochester Medical CenterRochester, New York

Eleanor M. SaffranDepartment of Communication SciencesDepartment of NeurologyUniversity of California, BerkeleyBerkeley, California

Contributors xxiii

Randall R. Sakai, PhDDepartment of PsychiatryUniversity of CincinnatiCincinnati, Ohio

Myrna F. SchwartzMoss Rehabilitation CenterPhiladelphia, Pennsylvania

Joseph E. Steinmetz, PhDDepartment of PsychologyIndiana UniversityBloomington, Indiana

Richard F. Thompson, PhDNeuroscience ProgramUniversity of Southern CaliforniaLos Angeles, California

Eve Van Cauter, PhDDepartment of MedicineUniversity of ChicagoChicago, Illinois

Takashi YoshiokaJohns Hopkins UniversityKrieger Mind Brain InstituteBaltimore, Maryland

Steven L. Youngentob, PhDPhysiology DepartmentSUNY Health Sciences CenterSyracuse, New York

CHAPTER 1

Evolutionary Psychology

RUSSIL DURRANT AND BRUCE J. ELLIS

1

LEVELS OF EXPLANATION IN EVOLUTIONARY PSYCHOLOGY 2

THE METATHEORY LEVEL OF ANALYSIS 3METATHEORETICAL ASSUMPTIONS THAT

ARE CONSENSUALLY HELD BYEVOLUTIONARY SCIENTISTS 3Natural Selection 4Adaptation 4Sexual Selection 6Inclusive Fitness Theory 7

SPECIAL METATHEORETICAL ASSUMPTIONS OFEVOLUTIONARY PSYCHOLOGY 7Psychological Mechanisms as the Main

Unit of Analysis 8

Domain Specificity of Psychological Mechanisms 9The Environment of Evolutionary Adaptedness 10

THE MIDDLE-LEVEL THEORY LEVEL OF ANALYSIS 11Parental Investment Theory 12Good Genes Sexual Selection Theory 14

THE HYPOTHESES LEVEL OF ANALYSIS 17Good Genes Sexual Selection Theory: Hypotheses 17

THE PREDICTION LEVEL OF ANALYSIS 19Good Genes Sexual Selection Theory: Predictions 20

THE FUTURE OF EVOLUTIONARY PSYCHOLOGY 22The Impact of Evolutionary Psychology 24Future Directions 26

REFERENCES 28

Evolutionary psychology is the application of the principlesand knowledge of evolutionary biology to psychologicaltheory and research. Its central assumption is that thehuman brain is comprised of a large number of specializedmechanisms that were shaped by natural selection over vastperiods of time to solve the recurrent information-processingproblems faced by our ancestors (Symons, 1995). These prob-lems include such things as choosing which foods to eat,negotiating social hierarchies, dividing investment amongoffspring, and selecting mates. The field of evolutionary psy-chology focuses on identifying these information-processingproblems, developing models of the brain-mind mechanismsthat may have evolved to solve them, and testing these modelsin research (Buss, 1995; Tooby & Cosmides, 1992).

The field of evolutionary psychology has emerged dra-matically over the last 15 years, as indicated by exponentialgrowth in the number of empirical and theoretical articles inthe area (Table 1.1). These articles extend into all branchesof psychology—from cognitive psychology (e.g., Cosmides,1989; Shepard, 1992) to developmental psychology (e.g.,Ellis, McFadyen-Ketchum, Dodge, Pettit, & Bates, 1999;Weisfeld, 1999), abnormal psychology (e.g., Mealey, 1995;

Price, Sloman, Gardner, Gilbert, & Rhode, 1994), socialpsychology (e.g., Daly & Wilson, 1988; Simpson & Kenrick,1997), personality psychology (e.g., Buss, 1991; Sulloway,1996), motivation-emotion (e.g., Nesse & Berridge, 1997;Johnston, 1999), and industrial-organizational psychology(e.g., Colarelli, 1998; Studd, 1996). The first undergraduatetextbook on evolutionary psychology was published in 1999(Buss, 1999), and since then at least three other undergradu-ate textbooks have been published in the area (Barrett,Dunbar, & Lycett, 2002; Cartwright, 2000; Gaulin &McBurney, 2000).

In this chapter we provide an introduction to the field ofevolutionary psychology. We describe the methodology thatevolutionary psychologists use to explain human cognitionand behavior. This description begins at the broadest levelwith a review of the basic, guiding assumptions that are em-ployed by evolutionary psychologists. We then show howevolutionary psychologists apply these assumptions to de-velop more specific theoretical models that are tested in re-search. We use examples of sex and mating to demonstratehow evolutionary psychological theories are developed andtested.

2 Evolutionary Psychology

LEVELS OF EXPLANATION IN EVOLUTIONARY PSYCHOLOGY

Why do siblings fight with each other for parental atten-tion? Why are men more likely than women to kill sexualrivals? Why are women most likely to have extramarital sexwhen they are ovulating? To address such questions, evolu-tionary psychologists employ multiple levels of explanationranging from broad metatheoretical assumptions, to morespecific middle-level theories, to actual hypotheses and

predictions that are tested in research (Buss, 1995; Ketelaar &Ellis, 2000). These levels of explanation are ordered in ahierarchy (see Figure 1.1) and constitute the methodology thatevolutionary psychologists use to address questions abouthuman nature.

At the top of the hierarchy are the basic metatheoreticalassumptions of modern evolutionary theory. This set of guid-ing assumptions, which together are referred to as evolution-ary metatheory, provide the foundation that evolutionaryscientists use to build more specific theoretical models. Webegin by describing (a) the primary set of metatheoreticalassumptions that are consensually held by evolutionary sci-entists and (b) the special set of metatheoretical assumptionsthat distinguish evolutionary psychology. We use the termevolutionary psychological metatheory to refer inclusively tothis primary and special set of assumptions together.

As shown in Figure 1.1, at the next level down in the hier-archy, just below evolutionary psychological metatheory, aremiddle-level evolutionary theories. These theories elaboratethe basic metatheoretical assumptions into a particular psy-chological domain such as mating or cooperation. In thischapter we consider two related middle-level evolutionarytheories—parental investment theory and good genes sexual

TABLE 1.1 Growth of Publications in the Area of EvolutionaryPsychology, as Indexed by the PsycINFO Database

Years of Publication Number of Publicationsa

1985–1988 41989–1992 251993–1996 1001997–2000 231

aNumber of articles, books, and dissertations in the PsycINFO database thatinclude either the phrase evolutionary psychology or evolutionary psycho-logical in the title, in the abstract, or as a keyword. All articles from theJournal of Evolutionary Psychology, which is a psychoanalytic journal, wereexcluded.

Evolutionary Psychological Metatheory

Middle-Level Theories

Hypotheses

Specific Predictions

Basic metatheoretical assumptions of modern evolutionary theory.Special metatheoretical assumptions of evolutionary psychology.

Attachment theory(Bowlby, 1969)

Parental investment theory(Trivers, 1972)

Good genes sexual selectiontheory

Individuals who more fullydisplay traits indicative of high

genetic quality should behealthier and in better conditionthan should conspecifics whodisplay these traits less fully.

The frequency and timing offemale orgasm should varyin a manner that selectivelyfavors the sperm of maleswho display indicators of

high genetic quality.

Males who display indicators ofhigh genetic quality shouldhave more sexual partners

and more offspring.

More symmetrical individualsshould have better mental andphysical health, better immunesystem functioning, and lowerparasite loads than should less

symmetrical individuals.

The timing and frequency oforgasms by women should bepatterned to selectively retain

the sperm of moresymmetrical men.

More symmetrical men shouldhave more lifetime sexual

partners and more extrapairsexual partners than should

less symmetrical men.

Figure 1.1 The hierarchical structure of evolutionary psychological explanations (adapted from Buss, 1995).

Metatheoretical Assumptions That Are Consensually Held by Evolutionary Scientists 3

selection theory—each of which applies the assumptions ofevolutionary psychological metatheory to the question ofreproductive strategies. In different ways these middle-leveltheories attempt to explain differences between the sexes aswell as variation within each sex in physical and psychologi-cal adaptations for mating and parenting.

At the next level down are the actual hypotheses and pre-dictions that are drawn from middle-level evolutionary theo-ries (Figure 1.1). A hypothesis is a general statement aboutthe state of the world that one would expect to observe if thetheory from which it was generated were in fact true. Predic-tions are explicit, testable instantiations of hypotheses. Weconclude this chapter with an evaluation of hypotheses andspecific predictions about sexual behavior that have been de-rived from good genes sexual selection theory. Special atten-tion is paid to comparison of human and nonhuman animalliteratures.

THE METATHEORY LEVEL OF ANALYSIS

Scientists typically rely on basic (although usually implicit)metatheoretical assumptions when they construct and evalu-ate theories. Evolutionary psychologists have often called onbehavioral scientists to make explicit their basic assumptionsabout the origins and structure of the mind (see Gigerenzer,1998). Metatheoretical assumptions shape how scientistsgenerate, develop, and test middle-level theories and their de-rivative hypotheses and predictions (Ketelaar & Ellis, 2000).These basic assumptions are often not directly tested afterthey have been empirically established. Instead they are usedas a starting point for further theory and research. Newton’slaws of motion form the metatheory for classical mechanics,the principles of gradualism and plate tectonics provide ametatheory for geology, and the principles of adaptationthrough natural selection provide a metatheory for biology.Several scholars (e.g., Bjorklund, 1997; Richters, 1997) haveargued that the greatest impediment to psychology’s develop-ment as a science is the absence of a coherent, agreed-uponmetatheory.

A metatheory operates like a map of a challenging con-ceptual terrain. It specifies both the landmarks and the bound-aries of that terrain, suggesting which features are consistentand which are inconsistent with the core logic of the meta-theory. In this way a metatheory provides a set of powerfulmethodological heuristics: “Some tell us what paths to avoid(negative heuristic), and others what paths to pursue (positiveheuristic)” (Lakatos, 1970, p. 47). In the hands of a skilled re-searcher, a metatheory “provides a guide and prevents certainkinds of errors, raises suspicions of certain explanations or

observations, suggests lines of research to be followed, andprovides a sound criterion for recognizing significant ob-servations on natural phenomena” (Lloyd, 1979, p. 18). Theultimate contribution of a metatheory is that it synthesizesmiddle-level theories, allowing the empirical results of avariety of different theory-driven research programs to beexplicated within a broader metatheoretical framework. Thisfacilitates systematic cumulation of knowledge and progres-sion toward a coherent big picture, so to speak, of the subjectmatter (Ketelaar & Ellis, 2000).

METATHEORETICAL ASSUMPTIONS THATARE CONSENSUALLY HELD BYEVOLUTIONARY SCIENTISTS

When asked what his study of the natural world had revealedabout the nature of God, biologist J. B. S. Haldane is reportedto have made this reply: “That he has an inordinate fondnessfor beetles.” Haldane’s retort refers to the extraordinary di-versity of beetle species found throughout the world—some290,000 species have so far been discovered (E. O. Wilson,1992). Beetles, moreover, come in a bewildering variety ofshapes a