How animals think and feel an introduction to non human psychology

Preface Chapter 1—Introduction Evolution Scientific Study of Animal Behavior Tinbergen’s Four Whys PART I: ANIMAL COGNITION Chapter 2—Sensory and Perceptual Processes Associative Learnin

How Animals Think and Feel

An Introduction to Non-Human Psychology

Ken Cheng

Copyright © 2016 by ABC-CLIO, LLC

All rights reserved No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, except for the inclusion of brief quotations in a review, without prior permission in writing from the publisher.

Library of Congress Cataloging-in-Publication Data

Names: Cheng, Ken, author.

Title: How animals think and feel : an introduction to non-human psychology / Ken Cheng.

Description: Santa Barbara, California : Greenwood, 2016 | Includes bibliographical references and index.

Identifiers: LCCN 2016034919 (print) | LCCN 2016035224 (ebook) | ISBN 9781440837142 (hardcopy : alk paper) | ISBN

9781440837159 (eBook)

Subjects: LCSH: Animal psychology | Animal behavior.

Classification: LCC QL785 C443 2016 (print) | LCC QL785 (ebook) | DDC 591.5—dc23

LC record available at https://lccn.loc.gov/2016034919

130 Cremona Drive, P.O Box 1911

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This book is printed on acid-free paper

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Dedicated to my family—Danielle, Tia, and Max

Preface

Chapter 1—Introduction

Evolution

Scientific Study of Animal Behavior

Tinbergen’s Four Whys

PART I: ANIMAL COGNITION

Chapter 2—Sensory and Perceptual Processes

Associative Learning: Classical Conditioning

Associative Learning: Operant Conditioning

Interval Timing

Multiple Oscillators for Timing

Conclusion

Chapter 6—Numerical Cognition

Analog Magnitude System: Approximate Counts

Object-Tracking System: One, Two, Three, Too Many

Training Animals to Count

Conclusion

Chapter 7—Emotions

Emotions and Motivation

Emotions in Comparative Perspective

What about Emotions in Invertebrate Animals?

Emotions, Consciousness, and Ethics

Conclusion

Chapter 8—Animal Communication

Signals and Cues

Wide Range of Signals

Signals of Quality: Sexual Selection at Work

Alarm Calls: Warning Signals

Debate: How Important Is the Actual Information Conveyed through Animal Communication?

Cognitive Processes in Communication

Debate: Do Animals Have Metacognition?

Self-Recognition: The Mirror Test

Social Learning

Theory of Mind

Conclusion

PART II: CASE STUDIES OF SELECTED ANIMALS Chapter 10—Honeybees

Eusocial Lifestyle

Honeybee Cognition

Colony Collapse: A Multifaceted Syndrome

Conclusion

Chapter 11—Jumping Spiders

Best Arthropod Eyes

Myrmarachne: Ant-Mimicking Jumping Spiders

Portia: Stalker Playing Mind Games

New Caledonian Crows

Western Scrub Jays

Planning and Prospective Cognition

Cooperation and Altruism

Imitation

Artificial “Language”

Conclusion

Chapter 16—Dogs

WEIRD Human and WHOC Dogs

Domestication of the Dog: Coevolution of Uncertain OriginCanid Play and Wild Justice

Sensitivity to Humans

Word Learning in Two Dogs: A Record for NonprimatesConclusion

Chapter 17—Great Apes

Primates and Great Apes: Some Basic Biology

Manual Skills and Clever Foraging

Brain and Intelligence in Primates

Nim, Kanzi, and Ape Language

What about Humans?

Debate: What Is Special about Humans?

Glossary

References and Other Interesting Materials

About the Author and Contributors

Index

What the nervous systems of animals let them do makes the greatest show on the planet This book isabout the minds of animals Most of it concerns nonhuman animals and what they are capable of, withthe last short chapter reflecting on the rise of humans and what might have made this species come todominate this planet The book is written as an introductory reference source for those with noknowledge of the fields featured: a large chunk of comparative cognition, but also behavioralecology, evolutionary biology, neuroscience, perception, developmental psychology, anthropology,and philosophy While the descriptions have been kept simple, the book has not shied away fromsome key ideas that could be highly complex The reader will come across topics such as theperception of polarized light (Chapters 2 and 4), principal-components analysis (Chapters 12 and17), and embodied cognition (Chapters 12 and 16) And while the book serves as a reference source,the writing style was steered away from the straight-and-narrow, cut-and-dried toward the lively andcolorful, often not shying away from big words

An introductory chapter (1) sets out evolutionary theory, crucial to the consideration of anyaspects of behavior Chapter 1 also lays out a brief history of the relevant fields of scientific study, inorder to set the stage for the show to come The two halves of the book then present a range of topics

of animal thinking (Part I) and highlights on particular groups of animals (Part II) Part I starts off withthe sensory world, the world from which animals get the information for everything that may belabeled “thinking” (Chapter 2) The ubiquitous phenomenon of learning is featured next, includingboth basic and more complex learning (Chapter 3) The next three chapters concern fundamentaldimensions of experience that many animals process: space (Chapter 4), time (Chapter 5), andnumber (Chapter 6) A range of lab studies are described, along with naturalistic observations Allthe knowledge of the world is useless from an evolutionary standpoint unless one does somethingwith it What to do depends on one’s motivations; and emotions fuel motivations Animal emotionsare spotlighted in Chapter 7 in a comparative perspective Chapter 8 describes the intricacies of the

world of animal communication, offering a definition of signal, showcasing the wide range of signals,

and explaining some of the functions of animal signals Part I concludes with a potpourri of complexcognition, including planning, social learning, and cognition about the minds of others

Part II brings on nine chapters on a diverse range of animals with “star” characteristics Althoughthe list is biased toward those animals more closely related to humans, three groups of invertebrateanimals take the stage Honeybees (Chapter 10) are perhaps the world’s economically most importantinsect Worker bees can do an amazing lot of things with tiny brains Jumping spiders ( Chapter 11)have some of the best invertebrate eyes, which they use in active hunting They stalk like miniaturetigers of the undergrowth, and like honeybees, they accomplish much with tiny brains Cephalopods(Chapter 12), on the other hand, have some of the biggest nervous systems among invertebrateanimals These mollusks include squids, cuttlefish, and octopuses Among the fascinating behaviorshighlighted, they display patterns on their skins, controlled by their nervous systems, and they play.Two groups of birds with large brains relative to their body sizes then enter on stage Corvids

(Chapter 13) are a family that includes crows, ravens, and jays Depending on the species, they excel

at different kinds of behaviors—from spatial memory to tool use to planning Parrots (Chapter 14)comprise a large group of birds showing clever behaviors An alpine parrot that raids garbage bins,the kea, and one African grey parrot that has learned some language take starring roles Threedifferent mammals then take the stage Dolphins (Chapter 15) have huge brains relative to their bodysize, and they exhibit a wide range of smart behaviors, although everything they accomplish is alsodone by less brainy animals Dogs (Chapter 16) have coevolved with humans Much of their cognitionhas been forged in this coevolution—including, especially, their sensitivities to humans Great apes(Chapter 17) are our nearest cousins They are like us in many ways, except that all of them areteetering on the verge of being wiped out in the wild The chapter not only highlights some of theirsmart behaviors, but also considers why so few great ape species have survived to this day What is

it about the extant (surviving) lot that has carried them? The last chapter (18) contains a briefdiscussion of the rise of humans It includes four commentaries from distinguished authors who havethought about this issue

The curtain calls (end of the book) include a glossary and a reference list The glossary providesbrief definitions of key technical terms and also describes a few key persons in the history of thefield The reference and materials list contains the few bibliographic sources mentioned in the book,and also other materials, including video clips, that might interest readers

I would like to thank my editor, Maxine Taylor, for her comments and encouragement I wouldalso like to thank colleagues who have provided valuable suggestions on a number of chapters; theseassociates include Sara Shettleworth, Dick Stevenson, Karen Hollis, Jonathon Crystal, Robert Gerlai,Culum Brown, Andy Barron, Ximena Nelson, Jennifer Basil, Rachael Shaw, Eloise Deaux, and DickByrne I am grateful to other colleagues who kindly supplied photographs or other materials; theseassociates include Dominic Tran, Jonathon Crystal, Carolynn Smith, Tom Flower, Matthew Walters,Ximena Nelson, Jennifer Basil, Guy Levy, Nir Nesher, Binyamin Hochner, Chuan-Chin Chiao, RogerHanlon, Gyula Gajdon, Ludwig Huber, Leigh Ann Hartsfield, Eloise Deaux, and John Pilley All ofthese suggestions and materials have helped to improve the book

Ken ChengFebruary 2016

Introduction

Other species of animals (hereafter simply animals) fill our world, and not only as food A number ofthem have become our companions, most of which were domesticated over the course of humancivilization Domestic dogs and cats in the world number in the hundreds of millions Others—such

as rats, mice, and flies of the genus Drosophila—have become mainstays of laboratories, “model”

species for diverse branches of science We have had a hand in shaping their evolutionary history.Animals that we have not directly “engineered,” wild animals, also fill our world, whether in urban,rural, or natural landscapes Birds can be heard singing in most suburbs, and countless insects flit inthe air while others, such as ants, dominate the terrestrial landscape This book serves as a concisereference for one aspect of animal life: their minds What information about their physical world dodifferent animals take in? What do they make of this information, by way of learning and memory?How do they get about from one place to another? Do they have a sense of time? Do they haveemotions and feelings? How do they communicate? And for the social animals, what do they make oftheir social world?

Our ancestors would have been interested in animals and their behavior well before recordedhistory and well before the rise of civilization some 10,000 years ago Modern humans—and by that,

anthropologists mean becoming the species Homo sapiens, some 200,000 years ago—have mostly

been hunter-gatherers, a lifestyle that still characterizes a few peoples today Hunter-gatherersamassed a large variety of food, including many different kinds of animals Food animals consistednot only of big game—perhaps the image that fills popular thinking—but also a variety of smallterrestrial vertebrate animals, marine animals of all kinds for people living near water, and insectsand other invertebrate animals Understanding their behavior would have been part and parcel ofhunter-gatherer life Our ancestors would not have studied animal behavior formally with the aim ofpublishing articles But they would surely have developed informal knowledge in day after day ofobserving, tracking, and hunting and gathering them They might even have shared this knowledgeinformally while relaxing in the evening, in the form of storytelling, thus transmitting knowledge

culturally This sharing of knowledge is probably one of the keys to the spectacular rise of Homo sapiens (Chapter 18).

Civilization arose with the dawn of agriculture, when seeds and animals were domesticated

Geographer and biologist Jared Diamond, in his Pulitzer Prize–winning book Guns, Germs, and Steel

(1999), argued that the domestication of large mammals launched a leap in the rise of civilization inEurasia Large mammals supplied not only food, but also work power for both agriculture and,eventually, warfare In domesticating animals, large and small, mammal or not, our ancestors musthave been concerned about their behavior; after all, it requires certain behaviors of the animals tobreed But the knowledge and practice of domestication would have come about informally as well; itwas well before the days of “ag (agricultural) schools.”

Systematic observations of animals and their behavior had begun by the time of recorded history

or shortly thereafter The Greek philosopher Aristotle, for example, documented observations ofanimals Formal studies of animals rose with the dawn of modern science in the Renaissance Modernphilosophers then—and to philosophers, “modern” means the 17th century onward—partook ofscience, much like the Greek philosophers did French philosopher René Descartes was perhaps mostfamous for his dualist philosophy of mind, including the oft-repeated phrase “I think, therefore I am.”But he also contributed to modern mathematics The reader might know about dividing an ideal

(mathematical) plane along two axes (typically the x- and y-axes familiar to scientists), each having

coordinates This is now called the Cartesian plane, with Cartesian coordinates, named afterDescartes This form of reduction allowed geometry to be cast in terms of the algebra of numbers,leading to today’s algebraic geometry Descartes also studied human perception and the behavior ofanimals

He came up with the concept of a reflex, which he thought was mediated in humans by the pinealgland While the pineal gland as a seat for reflexes is now known to be wrong, the reflex has certainly

stayed around A reflex is an unthinking form of behavior, usually stereotyped, in response to specific

stimuli Information from the stimulus—as example, Descartes used the heat from touching a fire—travels up a nerve to the pineal gland The pineal then issues a command, automatic in nature, toremove the limb from the fire For the record, this withdrawal reflex is mediated in our spinal cord,and the limb is removed from the hot stove before we become aware of the pain, a response thatindeed bypasses conscious cogitation Descartes saw much, if not all, of animal behavior—except forhuman conscious thinking—as reflexive in nature, a stance that we now think too extreme

Perhaps the most important concept that Descartes promoted was reduction in science The basicidea is that complex phenomena can be unpacked and explained as the workings of underlyingcomponents Reductive explanations form a major part of science beyond the study of behavior.These underlying components are often at what we would consider a lower, more-detailed level.Thus, many think that at least some behaviors can be explained in terms of cellular events in theorgans of the body, including but not limited to brains and muscles Cellular events, such as thesynthesis of protein, can be explained in terms of the “behavior” of different chemicals, and so on.Reduction characterizes especially the proximate explanations for behavior to be discussed later inthis chapter

Evolution

A major guiding principle of modern biological sciences is the evolution of organisms To quote anoft-repeated saying by evolutionary biologist Theodosius Dobzhansky, “Nothing in biology makessense except in the light of evolution.” The study of behavior is no exception Evolution is mostassociated with the British naturalist Charles Darwin (Box 1.1) Darwin did not come up with theconcept of evolution; it had already been proposed, long ago as well as by some of Darwin’scontemporaries Nor was he the only one to explain the evolution of organisms by natural selection.Another British naturalist, Alfred Russel Wallace, also had the idea But Darwin did write a major

book on the topic, On the Origin of Species (1859), and for that, he deserves much credit.

Not every biologist was an evolutionist in Darwin’s time, but one major influential evolutionarytheory was that of Frenchman Jean Baptiste Lamarck Lamarck thought that evolution was directed—

directed to higher, more complex, more ideal forms Life can be characterized as a ladder, scala

naturae in Latin, with better-adapted species somehow replacing less well-adapted ones that were going extinct It was this scala naturae that Darwin and Wallace’s natural selection offered an

alternative for

The theory of natural selection can be summarized in three principles or “ingredients”:heritability, variation, and selection These principles explain adaptive evolution, or how apopulation can become better suited, over generations, to the conditions in which it is living We mustthink in terms of populations here, and not of adapting an individual to circumstances The firstingredient is heritability Darwin noted that like begets like: offspring have many of thecharacteristics of their parents Much of this comes from his association with breeders Breeding isafter all the process of artificial selection This notion of heritability is common to evolutionarytheory Lamarck had a version of it Lamarck thought that characteristics acquired in the lifetime of aparent may be passed on to offspring A famous example is that a giraffe that practiced stretching itsneck in its life would pass on a longer neck to daughters and sons Darwin was fine with that idea as

one basis of heritability, alluding to it, for example, at the end of On the Origin of Species in the

words “use and disuse,” another formulation for the inheritance of acquired characteristics This waswell before the time of modern genetics Neither Darwin nor Lamarck knew anything about thegenetic basis of inheritance

BOX 1.1 The Life of Charles Darwin

Charles Darwin (1809–1882) gathered many specimens, both geological and biological, on his long trip (1831–1836) aboard the

Beagle On the Galápagos Islands, perhaps the most famous part of the trip, Darwin collected many birds, but often he did not

document them properly (his finches, for example, now popularly called Darwin’s finches).

Darwin did not come up with the idea of natural selection on the Galápagos Islands, or even shortly after his return He had many specimens to sort out, and the world was waiting for the chronicles of his travels He needed help to make sense of his specimens in order to come up with his theory of natural selection Ornithologist and illustrator John Gould helped identify the Galápagos finches for him While Darwin thought that the specimens were a motley assortment of finches, blackbirds, grosbeaks, and wrens, Gould corrected him by pointing out that they were all different species of finches These variants of the finches found

on the mainland, along with specimens of different species of island mockingbirds, furnished key evidence for the idea of common

descent: the birds were descended and transformed from the stock on the mainland Today we call this an adaptive radiation.

Some people think that political scientist Thomas Malthus’s essay on population was the key fuel that lit up the idea of natural selection for Darwin In the essay, Malthus pointed out that populations, of their own accord, would quickly grow to outstrip resources Others think that Alfred Russel Wallace’s paper, sent to Darwin in 1858, provided key ideas Wallace, in Asia making his living by collecting samples for others, had sent Darwin his paper explaining natural selection—to solicit comments from a respected colleague At any rate, shortly after that event, an extraordinary meeting of the Linnean Society was arranged by Darwin’s contemporaries At the meeting, a paper each from Darwin and Wallace was presented, with neither of the authors

present Darwin was sick with grief for a lost child, and Wallace was in Asia Shortly thereafter, Darwin started writing On the Origin of Species, his “species book,” which was published in 1859.

The second ingredient needed for adaptive evolution by natural selection is variation, which isubiquitous in life forms Darwin would have been well aware of variation within any species,between individuals, from his associations with animal breeders as well as his own naturalistobservations Variation furnishes materials for the third ingredient, selection, to work on Selectionmeans differential reproduction: those best suited to the conditions get to reproduce more than thoseless suited

With these ingredients, evolution of better-and-better-adapted populations will take place over

many generations The reach of these Darwinian principles is not restricted to life forms Scientistscan, for example, “evolve” better robots this way, in what is called evolutionary robotics What areevolving are typically the programs running the robots One starts with an assortment of programs(providing the ingredient of variation), and lets the robots loose The roboticist picks the best-performing robots, according to chosen criteria, in each generation Like breeding animals, this isartificial selection The roboticist reproduces that lot, each with some variations, thus providingheritability while generating more variation for selection to continue to work on Over generations,better-and-better-performing robots arise.

A few points about this nutshell summary are worth emphasizing By Darwinian principles ofevolution, the course of evolution is not directed It is not headed toward some ideal form, towardbigger brains, or toward any other goal The cold logic of selection is that whatever is best suited tocircumstances gets to reproduce more The process is ruthless in culling, often called blind, andforms can evolve and have evolved in myriad directions, producing a proliferation of life forms best

characterized as a tree of life, a metaphor that Darwin drew in the only figure in On the Origin of Species While the history of life has seen many complex forms arise, many organisms remain single-

celled organisms, or less; many microbes are simpler than a complex eukaryotic cell, the kind that weanimals possess What has unfolded is a stupendous diversity filling umpteen niches, making thegreatest variety show on the planet

Natural selection does not necessarily produce perfect or optimally adapted forms It is not anengineer starting with best-design principles, but rather a cobbler and a tinkerer, working withmaterials handed to it, constrained by developmental pathways and the need to survive and reproduce

in each generation Imperfect forms provide one kind of evidence, of many, for Darwinian evolution

—refuting the thesis that species were created to be ideally adapted to their circumstances A famousexample is the panda’s “thumb.” The panda has a manipulative digit resembling our thumb in itsfunction But the panda’s “thumb” is not made from the bones similar to those that make up ourfingers Rather, it is actually a modified wrist bone While by engineering principles it would makesense to turn one of the digits (claws) into a thumb, this was not a possible path Natural selection has

to modify what it can Perhaps even poorer engineering is the wiring in our exquisite primate eyes:the bundle of nerves that takes the sensory information to the brain comes in front of the receptivesurface, the retina, instead of going behind it according to sensible design principles These foiblesare sometimes found because once the evolutionary improvement starts down one path, it willcontinue improving along that path, even if the path does not lead to the absolute best possibleoutcome in the end

In terms of cognition in animals, this means that many forms of cognition will not use the bestcomputational principles for solving a task Shortcuts, abbreviations, and approximations will often

be found They will evolve if they work well enough to improve the reproductive fitness of theowner

Natural selection makes organisms better adapted to the world that they live in, but not allevolution is adaptive The copying of genes is a very nearly unerring process, but that qualifier “verynearly” spells a lot of nonadaptive evolution over deep time on Earth In rare instances, genes are notcopied correctly when cells reproduce, producing mutations If these mutations produce detrimentaleffects in organisms, they will soon be weeded out by natural selection But many mutations areneutral when it comes to reproductive fitness, the currency of evolution And these would just stay

around in later generations The process is statistically regular enough that differences in geneticsequence are often used to date how long two different lineages of organisms have been separatesince their last common ancestor.

Natural selection shapes animals to function in the world, producing well-oiled factories in theirbodies and brains for surviving in their world But Darwin also realized that many morphological andbehavioral characteristics, especially those found in males, make no sense for survival Acrossdiverse taxa, males often flaunt huge horns, long gaudy tails, and bright plumage, none of which helpsthem survive Contrariwise, such excess baggage hinders their mobility or advertises their presence

to potential predators Add to that the diverse song and dance exhibited in courtship, or the posturingexhibited in territorial disputes, and survival functions seem even less likely In his second great

book, The Descent of Man, and Selection in Relation to Sex, Darwin (1871) proposed sexual

selection to explain such phenomena Some say it is the greatest idea he had

Sexual selection forges characteristics for mating purposes, for reproductive success The oiled factory counts for nought if its products cannot be sold The best-surviving animal has zeroevolutionary currency if it does not reproduce Sexual selection is about winning in the reproductiongame, sometimes at the expense of lowering the odds of survival

best-To this day, scientists follow Darwin in distinguishing two forms of sexual selection Males(typically) may compete with other males for access to females for reproductive purposes This is

known as intrasexual selection, a selective process between same-sex combatants Big horns, in

stags or stag beetles, help in such battles even if they cost nutrients to grow and maintain So doesbody size in general Females, on the other hand, may choose among a “market” of males that displaytheir attractiveness That females are usually the choosier sex among animals stems from the fact thatfor mating it would benefit them to find the male, or males, with the best genetic quality This in turnsstems from the fact that the number of offspring they can produce in their lifetime is often limited

Female choice in sexual selection is called intersexual selection, sexual selection between sexes.

In sum, not only must animals function well to survive at least long enough to reproduce Theyalso must find a suitable mate and actually reproduce Or else their genes will not be represented inthe next generation To continue our economic analogy, not only must animals have a good productiondepartment in their factories, but also they need a great marketing department to sell themselves.Sexual selection selects for marketing

Scientific Study of Animal Behavior

Although Darwin and his contemporaries made many anecdotal observations of animal behavior,formal studies of animal behavior took off in the 20th century This period could be considered thestart of the scientific study of animal behavior Some have spoken of the scientific method, but it ismore an approach to gathering knowledge than a method Scientists do not have recipes that guaranteemeaningful results Broadly, the scientific approach uses systematic observations to test clearlyformulated ideas often called hypotheses The observations might come from natural observations orcontrived situations, usually called experiments Not all science is based on experimentation, as somenatural phenomena cannot be manipulated at all, and other manipulations are unethical We cannotalter events on distant galaxies, and it is unethical to feed students poisons to test toxicity To findsupport for a hypothesis, we must both find support for predictions that the hypothesis makes and rule

out other plausible alternative hypotheses The specter of alternative hypotheses will loom largewhen we consider whether smart behaviors might have less-than-smart killjoy explanations.

The current study of cognition in animals has two scientific roots One is comparative psychology, the study of animal learning and behavior, typically in laboratory conditions with roots

in North America The other is ethology, defined as the biological study of behavior with roots in

Europe Ethological studies in the first half of the 20th century usually took place in natural settings,although they were not limited to natural observations Manipulative studies, field experiments, havebeen and continue to be done Both these traditions have sprouted modern outgrowths

Unsurprisingly, comparative psychology was conducted mostly in departments of psychology.Animal learning was a major focus of this enterprise, indeed a dominating discipline in psychologythen One key pioneer was Edward Lee Thorndike, who presented physical problems to animals andstudied how they solve them In his best-known studies, domestic cats were placed inside puzzleboxes with latches, knobs, and other manipulanda to intrigue them The right combination ofmanipulations let the cats open a door and escape the box to some reward Thorndike found that thecats typically improved gradually, taking on average less time to get out each time they were placed

in the same puzzle box From this came the idea of gradually strengthening connections betweenstimuli and responses

Early 20th-century learning theorists are sometimes lumped as stimulus–response (S–R)psychologists, but this is not an accurate rendition The connection of behavior with consequences

(rewards and punishments) was also important A better characterization is associative learning, the

idea that different kinds of events (stimuli, responses, outcomes) can be linked with one another invarious ways But even the label “associative theory” would not capture the entire scene Aninfluential figure, American B.F Skinner, eschewed theoretical terms such as “association.” Hisbrand of behaviorism recommends sticking to codifying laws and principles of behavior undercontrolled lab conditions, avoiding any sort of mental constructs, associative or otherwise Toengineer controlled conditions, Skinner devised apparatuses: boxes that delivered stimuli andrewards and recorded relevant behaviors without human intervention Such operant chambers,carrying the colloquial name of “Skinner boxes,” are used to this day, now modernized with computercontrols Much of the work to be featured in this book was done in operant chambers Others at thetime were writing papers on reasoning in rats and cognitive maps Cognition in animals had earlyvoices in the United States even in the heyday of associative theories (see Chapter 3)

The studies were systematic, usually quantitative, and they fully deserve the label scientific The

typical laboratory settings for the experiments were quite different from and more impoverished thanwhat wild animals face A limited number of species, such as domesticated rats and pigeons,accounted for most studies And despite the comparative label, most often only a single species wasstudied Implicitly, however, comparisons with humans are implied, an approach called

anthropocentric (centered on humans) by Shettleworth (2010b).

As for ethology, the biological study of behavior, it would not surprise the reader that thediscipline arose in departments of biology The founding of ethology has been pinned on threescientists: Niko Tinbergen of the Netherlands, Konrad Lorenz of Austria, and Karl von Frisch ofAustria The Nobel Prize committee did that by awarding these three the Nobel Prize for Physiology

or Medicine in 1973 Independently, these scientists were observing the behavior of animals innatural settings; all of them also experimented with animals in their natural habitats Von Frisch

pioneered studies on honeybees (Chapter 10); Lorenz was most famous for his studies of imprinting indomestic fowl; and Tinbergen delved into a smorgasbord of wasps, gulls, stickleback fish, andothers He was also famous for formulating Why questions when it comes to behavior, to which wewill return later.

Studying natural behaviors of animals in natural settings differentiated the ethologists from theNorth American learning theorists Another difference was what could be called a nature/nurturedivide The learning psychologists focused on nurture: how behavior can be modified, the crux ofwhat learning is about, and how the environment can shape or select behaviors The ethologistsfocused on nature, paying attention to what they considered innate behaviors, sometimes calledinstincts This divide was of course not absolute Lorenz’s topic of imprinting, for example, wasabout young ducklings and goslings learning to identify mom

But similarities must be pointed out as well Both camps wanted a solid scientific foundation forstudying behavior Both camps held the collection of systematic data in high esteem And both campseschewed mentalistic, folk-psychological talk about what an animal wants or feels These mentalisticconcepts were deemed unobservable and impossible to study, use of such terms only impedingscientific progress

Starting in the 1960s, a cognitive revolution took place in the discipline of psychology Thisstarted in human psychology but soon spread to the study of other species as well Studies of spatialcognition (Chapter 4) and timing (Chapter 5) bloomed in the 1970s, still in laboratories on a limitednumber of species Thus was born the discipline of comparative cognition, often also called animal

cognition Perhaps a watershed is an edited book called Cognitive Processes in Animal Behavior

(Hulse, Fowler, and Honig 1978) Textbooks began appearing in the 1980s, but the 1990s can beconsidered the time of flowering for the discipline In 1999, the Comparative Cognition Society was

founded In 1998, the journal Animal Cognition was launched Also in 1998, Sara Shettleworth (Box 1.2) published her influential overview, Cognition, Evolution, and Behavior, now in its second

edition (Shettleworth 2010b)

Ethology, too, was transforming around the time that Tinbergen, Lorenz, and von Frisch won theirjoint Nobel Prize Lorenz had earlier conceived of behavior as a trait akin to morphologicalcharacteristics such as the shape of limbs As traits, behaviors, especially those with a strong innatebasis, were subject to evolution by the principles of natural selection Scientists rarely callthemselves ethologists anymore They might now call themselves neuroethologists or behavioralecologists Neuroethology is more concerned with the neural basis of natural behaviors such as sex,feeding, escape, or various forms of communication, with cognition now added to the mix Behavioralecology is more concerned with the evolutionary bases of behavior, especially with what adaptivebenefit a behavior might bring to its perpetrator A watershed event for this discipline was the

publication of the book An Introduction to Behavioural Ecology, by John Krebs and Nick Davies (1981) A journal called Behavioral Ecology was launched in 1990.

BOX 1.2 Sara Shettleworth’s Contributions

Sara J Shettleworth is Professor Emerita at the Department of Psychology, University of Toronto, also cross-appointed at the Department of Ecology and Evolutionary Biology She is American-born, and she did her undergraduate studies in the heyday of animal learning based on rigorous analysis of operant behavior in the lab (Chapter 3) As a graduate student at the University of Pennsylvania, she tasted field work when she helped her then-future husband Nicholas Mrosovsky with studies of baby sea turtles

in Costa Rica She wrote that the experience “was more than enough to convince even the most die-hard experimental psychologist of the wonders of species and behaviors outside the laboratory” (Shettleworth 2010c, p R910) She finished her graduate studies at the University of Toronto in Canada, and she has been there ever since.

In the 1970s, Shettleworth was part of a movement trumpeting “constraints on learning,” as it was called Not all behaviors are equally easy to train (Chapter 3) Working with hamsters, Shettleworth found that some behaviors are much easier to train than others: Hamsters learn readily to dig for a bit of food reward, but it was impossible to get them to wash their face to receive

a food reward Face-washing belonged to a different behavior system of grooming, not the foraging behavior system, whereas digging was part of the foraging system Besides a pigeon lab, Shettleworth also studied some wild, food-storing birds, after a

sabbatical at the Department of Zoology at Oxford University She collaborated with John Krebs, one of the authors of An Introduction to Behavioural Ecology.

In the late 1990s, Shettleworth researched and wrote the first edition of Cognition, Evolution, and Behavior In her own

words, she credits her wide acquaintance with both biological and psychological approaches to the study of behavior to “the luck

to be taught by or collaborate with people espousing the whole gamut of approaches to behavior” (Shettleworth 2010c, p R910) The book was revised for a second edition (Shettleworth 2010b) while she was gradually retiring from active professorial duties Shettleworth’s honors include a Guggenheim Fellowship; a Distinguished Scientist Lecturer award from the American Psychological Association; and, in 2008, the Research Award from the Comparative Cognition Society, with a special issue of the

journal Behavioural Processes published in her honor in 2009 Being a role model for budding female scientists, Shettleworth

noted that such models are far more numerous nowadays than when she was a student May her work attract more women to science.

Nowadays, the boundaries between behavioral ecology and neuroethology are often blurred.Studies in behavioral ecology often consider the information and the sensory processes that underlieanimals’ decisions, decisions that affect its reproductive fitness And studies in neuroethology oftenconsider how sensory or information processing systems might have evolved—the evolutionaryprocesses that might have constrained how brains work to get information

Both editions of Shettleworth’s book summarized a vast range of research on cognition inanimals, not only from the tradition of comparative cognition, but also from behavioral ecology Thestudy of communication (Chapter 8 of this book), for example, stems largely from the behavioralecological tradition The books also featured evolutionary considerations prominently, in whatShettleworth and others have called an ecological approach According to this approach, cognitionhas evolved not so that the animal can do lab tasks that experimenters might throw at it, but rather sothat it can solve important problems that it faces in its life Animal intelligence is not a general scale,

on which we humans sit at the top Rather, intelligence is geared (adapted) for life’s problems ratherthan for experimenters’ problems Spatial cognition offers examples A bird that relies on storingfood in many locations needs good spatial memory to retrieve the caches An ant that forages on abarren salt pan needs a navigation system to get back home without relying on terrestrial landmarks(Chapter 4)

Tinbergen’s Four Whys

This chapter ends by returning to one of the founders of ethology, Niko Tinbergen ( Box 1.3), toaddress the questions that scientists might ask in explaining a behavior In a famous paper in 1963,Tinbergen outlined four different kinds of Why questions that a scientist might ask about an animal

exhibiting a behavior (Table 1.1) These Why questions are divided into proximate and ultimate

explanations

The proximate explanations are found in the lifetime of the organism These may be referred to as

causes or causal explanations of behavior The first of these is mechanism This is a How question

more than a Why question It asks what it is about the impinging stimuli and the inner workings of theanimal that makes the behavior come about Much of learning theory and comparative cognition aims

at this kind of explanation, elucidating the principles concerned with how environmental events shapelearning and, more and more so now, what nervous processes underlie learning or cognition Much of

the branch of neuroscience concerned with behavior, called behavioral neuroscience, also focuses

on mechanistic explanations, as do many neuroethological studies

TABLE 1.1 Tinbergen’s Four Why Questions

Proximate C ause s Brie f Explication

Mechanism Immediate stimuli and underlying mechanisms

Development Genetic make-up, experiences, and life trajectories

Ultimate Explanations Brie f Explication

Function Adaptive benefits: What is the behavior good for?

Evolution Evolutionary history of the behavior: When did it arise in the history of life, and why did it arise?

BOX 1.3 The Life and Career of Niko Tinbergen

Nikolaas (Niko) Tinbergen (1907–1988) grew up in The Hague, Netherlands, then called Holland As a youth, Tinbergen was very interested in nature and the outdoors He was part of the Dutch Youth League for Nature Study He undertook undergraduate studies and then sought a doctoral degree at the University of Leiden, Netherlands In 1932, he took a trip with his newlywed wife to Greenland for a year, for a research-filled honeymoon Kruuk (2003) wrote that the Greenland experience changed Tinbergen, bringing out the hunter in him Tinbergen came to see observing and photographing animals—he was a keen photographer—as a form of hunting, and he came to treat animals from an objective standpoint, as mechanisms to be figured out His career was interrupted for three years by the Second World War, with two of those spent in a German prison camp in Holland He had met the Austrian ethologist Konrad Lorenz before the war, spending some happy time at Lorenz’s residence The War put them on different sides, with Lorenz also imprisoned for a number of years by the Russians Despite the ravages of war, they met again some time later in England.

Tinbergen became a Professor at Leiden, but he left Holland for Oxford University (one of the two top universities in Britain, along with Cambridge) in September 1949 In 1973, along with Konrad Lorenz and Karl von Frisch, Tinbergen was awarded the Nobel Prize in Physiology or Medicine Tinbergen is perhaps best known today for establishing the systematic observation of behavior as a field of study, and for his four Whys, described in this chapter That famous paper on the four Whys (Tinbergen 1963) has been cited well over 2,000 times, according to Google Scholar Besides the Nobel, he received a number of other honors, among them the Fellow of the Royal Society in the U.K and awards from the American Psychological Association More than having just a bibliometric impact, he had many students who went on to establish themselves in science, thus spreading the modern study of animal behavior.

The second kind of proximate explanation is development A developmental explanation seeks toexplain the course of events in an animal’s life that leads the animal to exhibit a particular behavior

An interplay of the genes that it was conceived with and the trajectory of life events usually figuresinto the explanation Nature and nurture make the stuff of developmental explanations, crucial to bothdevelopmental biologists and developmental psychologists That mix now contains life events that

cause chemical changes around the genes without changing the sequence of genes, called epigenetic changes Such epigenetic changes may make the expression of genes more or less likely Thus, genes

that we animals were born with might be silenced by some life events On this “hot” topic, scientistsare working out which epigenetic changes may be passed on to the next generation, a process ofacquired inheritance that is Lamarckian in nature

Turning to ultimate explanations of behavior, these probe beyond the lifetime of an organism topotentially the entire history of life on the planet Functional questions address what adaptive benefitsthe behavior has for the animal currently This Why question can be rephrased as “What is it goodfor?” Or to give it a more evolutionary tack, “Why has this behavior been selected?” Here, bothnatural selection and sexual selection might have played a role, sometimes working in oppositedirections.

Before presenting the fourth, evolutionary explanation, a hypothetical example helps to illustratethe three Why questions discussed so far Suppose that scientists take a normal macaque monkey, thesubject of lots of lab experiments They offer the monkey a choice of little tomatoes: one green unripeone and one red ripe one Over repeated choices, if not right from the start, they find the monkeyreliably choosing the red ripe one They extract from the experiment the fact that the monkey can tellred from green, and ask why

A mechanistic answer would tell of the visual receptors in the eye of the monkey Having threedifferent types of color receptors is crucial, with two of them most sensitive to longer wavelengths,

with maximal sensitivity in the green and yellow (to us) ranges Without this trichromatic color

vision (based on three different kinds of receptors), red and green would be indistinguishable (seeChapter 2) The explanation can drill down to cellular and molecular levels, all of these making upthe mechanistic story

A developmental explanation can tell of the genes that build the proteins making up light-sensitivepigments The two genes for the pigment proteins of the two crucial longer-wavelength receptors arenext to each other, and very (about 98 percent) similar It can also tell the developmental story thatearly experience with color is essential for the proper development of color vision, pointing out arole for nurture

The description of the hypothetical experiment might have conjured up a functional explanationfor readers Monkeys eat fruit, and being able to tell ripe ones apart from unripe ones is beneficial.The evolution of trichromatic vision gives many of us primates, including humans, that advantage Asecond functional explanation has been proposed Shades of red and yellow are importantcomponents of facial expressions in primates (again, including humans) Trichromatic vision allowsthe monkey to better read the expressions of its conspecifics As evidence for this latter hypothesis,scientists have compared many primates to measure how much of their faces is bare, uncovered byhair It turns out that trichromatic vision is most likely to be found in those species with a largeproportion of bare face

The final kind of Why question is evolution This asks when the behavior arose in the history oflife, and if possible, what circumstances might have driven its evolution To answer evolutionaryquestions, scientists usually have to look beyond the study species to compare multiple species One

common strategy is the comparative method This is an attempt to put the behavior, or any trait in

question (e.g., trichromatic vision), onto a map documenting evolutionary relations between a range

of species, called a phylogeny The simplified example in Figure 1.1 illustrates four species of

primates, of which the studied macaque is one of the species Suppose that scientists have determinedwhether each of these species possesses trichromatic vision If the studied macaque species—and theworld contains multiple macaque species—is the only one with trichromatic vision, one wouldconclude that trichromatic vision first evolved in this species That is the simplest or mostparsimonious explanation, one that requires the fewest assumptions It is not the only possibility,

because all these species, or rather the ancestor to all of them, might once have possessedtrichromatic vision, but three of the species have lost it This is less parsimonious, because it requiresexplaining how three species lost this trait in evolutionary history.

If on the other hand, the two macaque species have trichromatic vision, and the other species donot, the most parsimonious story is to suppose that the common ancestor of macaques evolved thetrait What is the real story? All these species have trichromatic vision All Old World monkeys andapes have color vision The origins of trichromatic vision go a deep way back in primate history

Because the genetic basis is well understood in this case, the genetic underpinnings suggest aplausible, even probable evolutionary scenario A common mistake in genetic copying—andremember that this means common among very, very rare events—is that a gene is duplicated, so thattwo copies of it, often right next to each other, are produced By itself, this does not have much byway of fitness consequences It is like having two copies of the same recipe rather than one: you stillget the same dish (protein) at the end But then one of those copies of the genes can undergo somemutations Recall that the genes for two of the light-sensitive pigments are very similar The mutatedgene would then contain instructions to produce a slightly different photosensitive chemical Using thedifferent chemicals from the two genes results in two different kinds of color receptors, giving us ourglorious trichromatic color vision

FIGURE 1.1 A tiny fragment of the clade of primates showing the evolutionary relationships between just four species.

This example is “cherry picked” for illustration The route to evolutionary explanations oftenposes two serious obstacles One is that the needed phylogeny might not be at hand Scientists have by

no means mapped out the entire tree of life, and on many sub-branches of it, the relations of descentamong species or groups of species are unclear Without a map to pin behavioral observations onto,

an evolutionary explanation is impossible The second limitation is that even if the phylogeny isexcellent and well confirmed, scientists might not have data from enough species on the trait ofinterest to piece together a convincing evolutionary explanation

Our world of animals, these actors in The Greatest Show on the Planet, is under threat nowadays.Many species are under the threat of extinction, including the sea turtles that Shettleworth once

studied We are the only member of genus Homo on the planet now, and soon we may be the only

great ape outside of zoo settings, the habitats of all other great apes being under great pressure.Furthermore, populations of many animals have been in decline for a few centuries now Terrestrialvertebrates, not counting the species that have gone extinct, have declined by an average of 25

percent A word has been coined for this decline: defaunation If nothing else, this book hopefully

will make you appreciate our fellow animals more With the basic history and background in tow, it

is time to continue on our journey into the minds of animals

Part I

Animal Cognition

Sensory and Perceptual Processes

Much of cognition is taking information about the world and using it to make decisions and takeactions Getting the information is the first order of business, and sensory and perceptual processes

do that for all animals As a rough divide, the senses convert information from the world into nervoussignals that the brain can understand Perceptual processes make sense of the sensory information Inthis context, the world includes not only the physical and social worlds external to an animal, but alsothe processes within the perceiver’s body These bodily signals convey motivational states such ashunger and thirst, and also what the skeletal muscles are doing Making muscles do the right things iscrucial for escaping predators or capturing prey

This chapter covers three themes on sensory and perceptual processes First, the basic process of

sensory transduction is key to all sensory information Transduction means converting physical

energy from the world into nervous impulses, the signals for brains to process Second, the range ofsensory mechanisms across the animal kingdom is impressive Even in ourselves, we possess farmore than the traditional folk-psychological five senses Scientifically, sensory processes are dividedaccording to the type of physical energy that is being transduced: optical, mechanical, chemical, evenelectrical and magnetic, as well as stimuli associated with temperature and pain Different animalspossess different sensory capacities, with some having senses that we do not have This means that

different animals have different subjective sensory worlds, termed Umwelt Third, getting sensory

data transduced is only the start of the job of making sense of the world Perceptual processes convertsensory data into representations of the world, often called percepts

Transduction

The key process in obtaining sensory information is transduction This is the process of convertingdifferent forms of physical energy into nerve impulses, which are signals that nervous systems workwith and can “understand.” To appreciate how transduction works, see Figure 2.1, which provides a

basic sketch of how nerve cells—neurons—work Neurons pass a signal along by undergoing action potentials, which are rapid changes in voltage across the cell’s membrane Neurons are slightly

charged electrically, a bit negatively charged inside their membranes under resting conditions Whenthe electrical voltage is disturbed enough, with the membrane potential becoming less negative inside,then rapid changes in electric potential take place With the movement of different kinds of ions(charged particles), the membrane potential first becomes positive on the inside, and then goes back

to its resting potential, slightly negative inside—all within about 5 milliseconds

FIGURE 2.1 Author’s schematic drawing of a neuron Typically information from other neurons is received at the dendritic end, and

information is passed on at the end of the axon.

While the action potential at a particular point on the membrane is over quickly, the processdisturbs the electric potential of the neighboring area enough to make it undergo an action potential.The action potential thus passes like a wave down the length of the neuron When the action potentialarrives at the end of the neuron, at the tip of its axon, the chemicals stored there, called

neurotransmitters, are released out of the neuron The neurotransmitters can affect the next neuron,

making it more or less likely to undergo an action potential The neurotransmitters are thus crucial forcommunication between neurons The action potential is also called an “impulse” or a “spike,” andthe neuron undergoing an action potential is said to “fire.”

With that briefest sketch of how neurons work, we can now understand how any form of

transduction works The business of transduction is conducted by sensory neurons, often called

“receptors” because they receive information about the world While most neurons “listen” tochemical and sometimes electrical signals from other neurons, sensory neurons are listening to, andsmelling and tasting, and seeing, and even volt-metering the world Different forms of physical energycan get different kinds of sensory neurons to fire, forming the basis for different kinds of senses Yetdespite the subjective differences—think of watching the orchestra play vs hearing its music—theneurophysiological message at the receptor end is the same kind It is a nerve impulse being passed

on (mostly) to the brain for processing Chemicals, electrical signals, light, mechanical pressure(including sound waves), and magnetic signals could all trigger nerve impulses with the right kind ofreceptor (Figure 2.2)

FIGURE 2.2 Author’s drawings of some common forms of sensory transduction A Mechanoreceptor found in the deeper layer of the

skin of vertebrate animals most sensitive to pressure B Another mechanoreceptive system with sensitive hairs that fire when the like statolith sits on them, thus indicating which direction is down C Schematic of a molecule that fits into the surface of a chemoreceptor, triggering the receptor to fire D In photoreception, an opsin molecule could change its shape when light falls on it This change in turn triggers a complex chemical cascade.

stone-Range of Sensory Worlds

Animals, including humans, have more senses than the traditional folk-psychological five of sight,hearing, smell, taste, and touch Biologically, senses are divided according to the kind of physicalenergy that is transduced Photoreception is triggered by light, a small part of the electromagneticspectrum Chemoreception is triggered by dissolved chemicals When the chemicals are dissolved inwater, the sense is taste When the chemicals are dissolved in air, the sense is smell or olfaction.Magnetic information or electrical information may also trigger receptors in some animals that cansense them Tissue damage and extremes of temperatures (heat and cold) can trigger other kinds ofreceptors, often signaling pain to animals Mechanoreception comprises a large class of receptorssensitive to mechanical disturbance, many of which are not well appreciated because they fall outsidethe traditional five

Hearing and touch are the well-known mechanoreceptive systems Hearing is sensitivity toacoustic waves transmitted across a substrate, typically air or water In mammalian ears, the eardrumand canal are not places of transduction; rather, they act as conduits for the sound waves Sensoryhairs deep in the inner ear transduce the auditory information Some insects have ears on their legs,but again it is the sensory hairs rather than the drumlike membranes that transduce auditoryinformation Touch comprises a bunch of different receptor types In mammals, different kinds ofreceptors are sensitive to fine touch and deeper pressure

Far less appreciated is a whole suite of mechanoreceptors that convey information from thebodies of animals Our mammalian inner ears contain a suite of fluid-filled canals and chambers Thesensory hairs in these structures that make up the vestibular system are sensitive to the movement ofthe fluids, which in turn depend on our movements Together the vestibular system provides a reading

of which way the animal is moving its head All kinds of animals receive information about what theirskeletal muscles are doing We (for humans have this suite of receptors as well) can tell, based on

our body senses, where our limbs are, where the limbs are moving to, and how the muscles arecontracting This kind of information is crucial for taking action in the world To use a businessanalogy, senses are like the market research department of a company, seeking information about thebusiness world for the company To be most effective at this enterprise, the market research teammust also know what the company produces and what it is capable of producing.

The suite of senses that an animal possesses gives the animal its own subjective view of the

world This subjective sensory world, called Umwelt by the German biologist Jakob von Uexküll

(1864–1944), differs between different species of animals It is hard to appreciate because we areconstantly immersed in our own Umwelt, making it all too easy to be anthropocentric (human-centered) on this front But this notion must be grasped if we are to appreciate how sensory,perceptual, and cognitive processes might differ among species

Differences in Umwelts can arise in three different ways First, one animal species might possess

a sensory capacity not possessed by another Second, even if two species both possess a sensorycapacity such as audition or vision, they might be sensitive to different physical ranges of that form ofenergy Third, a suite of perceptual and cognitive processes after sensory transduction can make adifference Different senses might dominate an animal’s Umwelt, or one animal might possess somekind of perceptual processing not found in another

Most animals possess the traditional five senses that humans possess, although some have lost asense in evolution from lack of information for that sense Animals that live mostly or completely indarkness, such as moles underground or fish in caves, might lose the sense of sight It is thought thatsuch losses are adaptive, and are not simply the product of nonadaptive changes over the course oftime That is because nervous tissue is expensive, requiring much more energy than other tissues foroperation Sensory neurons, to repeat, are a kind of nervous tissue It is thus expensive to keepsensory systems that have no use Of course, a loss of a sense alters an animal’s Umwelt

Other animals have senses that humans do not possess Many birds and turtles are sensitive to themagnetic field of the Earth, although the mechanistic bases for this sense are still being worked out Asolid demonstration of magnetic sensitivity comes from experiments on baby sea turtles—the adultsbeing too big to handle in lab conditions The sea turtles were in a big round tub surrounded byequipment that can alter local magnetic conditions Experimenters manipulated the magneticconditions to make the turtles “think” that they are to the north or south of their home, and the turtlesobliged by trying to swim south (under simulated north-of-home magnetic conditions) or north (undersimulated south-of-home magnetic conditions) The magnetic sense can give animals directionalinformation, like a magnetic compass, or perhaps, in the case of turtles but perhaps also in migratingbirds, a maplike sense of where they are on Earth It is hard for humans to imagine what these sensesmight be like, because we do not possess anything like them at all The best we can do is to think ofanalogies: looking at a physical magnetic compass or consulting a rough Global Positioning System(GPS) reading

Some fish, such as sharks, rays, and catfishes, can generate or perceive low levels of electriccharges Because nervous processes do their business with fluctuating electric charges, this is a goodway to detect potential prey animals Animals cannot hide by stopping all nervous processes Somesnakes, such as vipers, have sense organs that can detect heat from animals, heat being the infraredend of the electromagnetic spectrum Warm-blooded small prey mammals cannot hide from this kind

of detection system Such predators thus have good functional reasons for possessing these senses An

analogy to our dominant visual system can help us imagine this kind of sensory world: it is as if thesepredators see an electric blob or a heat blob in the same way that we see a visual object.

Even when two animals both possess a particular sensory modality, they may differ in what theyare sensitive to Most nocturnal mammals see in black and white, while most birds, insects, andprimates see in color These latter taxa (groups of animals) in turn are sensitive to different ranges ofthe electromagnetic spectrum Primates possess three (most of us, including humans) or two kinds ofcolor photoreceptors, as do insects But we primates are sensitive to a range from red [about a 700nanometer (nm) wavelength of light] to violet (about a 400 nm wavelength), while insects aresensitive to the range of about 300–600 nm Most birds have four different color photoreceptors,spanning a range of about 300–700 nm Wavelengths beyond our visual capacities are called

ultraviolet (UV) at the short end or infrared at the long end These terms are defined

anthropocentrically in terms of our capacities To birds and insects, nothing is ultra about light at 350nm; it would be a color like other colors

Other than wavelength ranges, birds and insects perceive another aspect of light that we primates

do not: polarized light As light comes through the atmosphere of Earth, it is scattered in systematicways Our primate visual receptors are not sensitive to this systematic scatter, but receptors in otheranimals have evolved to have this sensitivity We can imagine what this sense might be like byimagining a pattern of darker and brighter bands in the sky Importantly, such a pattern acts like avisually based compass, allowing the animal to tell compass direction even if the sun is covered(Chapter 4) Remarkably, some insects can perceive the pattern of polarized light even under dimmoonlit conditions (Box 2.1)

BOX 2.1 Marie Dacke

Marie Dacke is a young neuroethologist, and currently an associate professor in the Vision Group at Lund University in Sweden She has done pioneering work on navigation in African dung beetles Neuroethologists are interested in finding out the neural basis for natural behaviors that are important in animals’ lives These scientists also study behavior a lot, because one has to understand well what one is trying to find a neural basis for.

The night-active dung beetles that Dacke and her colleagues studied gather at night at dung piles After forming small dung balls, the beetles want to roll the balls away quickly, to get away from the competition and any possible usurpers of their efforts.

A straight line is the fastest getaway, and Dacke and company discovered that the beetles use the pattern of polarized light in moonlit conditions to keep moving straight Paths became meandering when this source was removed; the researchers could alter the preferred paths of dung beetles by altering the direction of polarized light with filters In recent studies, Dacke and her team found that in moonless conditions the beetles also use the Milky Way in the night sky as a directional source for keeping straight The research included testing the beetles, with dung and all, in a planetarium The beetles would not be consulting a star map in this environment, so probably they would perceive the Milky Way as only some dull streak in the sky Even such a poor cue, however, is good enough for moving straight, and natural selection is all in favor of “just good enough.” This discovery won Dacke’s crew an Ig Nobel Prize, which honors research that both makes you laugh and makes you think Winning the prize meant that the science was disseminated all over the world in the media The discovery even made it onto an episode of the

popular TV program The Big Bang Theory Dacke was proud to receive the prize, and she continues to work on promoting

science to the younger generations.

Rats have head-direction cells in their brains that fire the most when the rat’s head is facing a particular direction (Chapter 4) Dacke’s group has discovered similar polarization-direction cells in the dung beetle’s brain Using a polarizing filter to control the direction of polarized light, such cells fire the most when the filter is oriented in particular directions Insects make fine models for examining the neurobiology of natural behaviors.

In audition as well, different animals are sensitive to different ranges of frequency of sound,

measured as cycles per second, or Hertz (Hz) See Figure 2.3 Among vertebrates, many animals canhear infrasounds (too low for us) or ultrasounds (too high for us), both these terms being, again,anthropocentrically defined Thus, bats, dolphins, and mice can hear high sounds out of our range,while elephants can hear low rumbles below our range of hearing Infrasounds are thought to helpelephants communicate over long ranges, perhaps helping them locate one another Bats and dolphinsnot only hear ultrasounds, but also use them in a way that few of us can use sound: in echolocation.They generate high sounds to bounce them off the surround, including objects of interest such aspotential prey From the returning echoes, their brains can deduce where these objects are, the layout

of space, and even something of the texture of the barriers and objects This remarkable capacity ismore like our spatial vision than our audition; most of us are not that good at localization usingaudition Sensory abilities are plastic in most animals, and it should be noted that some humans,mostly among the blind, have developed remarkable echolocating abilities

FIGURE 2.3 Approximate auditory frequency ranges of sensitivities for different vertebrate animals, measured in cycles per second

(Hertz) on a log scale.

Animals living in different ecologies and lifestyles may have different dominant senses Rats,mice, and many insects, for example, have excellent chemical senses, while we primates are notknown for olfactory achievements, but have instead evolved acute vision for arboreal (tree-dwelling)fruit-picking The chemical world looms huge in some animals’ lives Salmon are born in freshwaterrivers and later migrate to spend much of their lives out to sea They return to their natal stream tospawn by recognizing its chemical signature Social insects live in nests of veritable chemical soups.Chemicals emanating from the inhabitants, various pheromones, help in nest cohesion Added to thatmix are chemicals in the food that foragers bring back Bees and ants recognize their nestmates bytheir smell Beekeepers can fool a hive into accepting a foreign queen via this chemical route Thenew queen is placed in a wrapping that takes the worker bees some days to chew through By thattime, the strange queen has taken on the smell of the hive and becomes accepted Olfactory processing

in the honeybee (Chapter 10) has been studied intensively at behavioral and neurobiological levels,and this knowledge has added richly to our understanding of how brains process sensory information.Chemoreceptively gifted animals might have specializations Some male silk moths possess giant

antennae on their heads (their version of noses), packed especially with receptor sites for detecting asingle chemical at very low concentrations Which chemical? The pheromone that females of thespecies send out to attract males for mating.

Perceptual Organization

Within any single modality, perceptual organization and perceptual processes might also differbetween species Vision and touch provide examples Primates possess lens eyes—as do molluskssuch as squid and octopuses, and jumping spiders These lenses focus light on to receptors at the back

of the eye, called the retina Insects do not have lens eyes; instead they have compound eyes

composed of thousands of individual eyes, each one looking, unfocused, at one bit of the world Theresult is a low-resolution “grainy” picture of the world Beyond spatial resolution, receptors for anysense are usually not distributed equally Much like modern human settlement, the population isconcentrated in certain areas akin to cities In primate visual systems, most receptors are packed in

one dense city-like area called the fovea Most of our color photoreceptors are there, giving us acute

color vision in just a narrow wedge of about one degree of vision That is enough range for grabbingtree branches and picking fruits Our periphery has much lower visual resolution, but that hasadvantages in a trade-off: it is more sensitive, and it works better in dim conditions In this trade-off,higher sensitivity (ability to detect low levels of light) comes with less resolution (less acute vision)

Animals living in other ecological conditions pack their visual receptors differently Consider amale fiddler crab living on an open mudflat The crab has panoramic eyes perched on stalks stickingabove its head, while we primates have sacrificed panoramic vision for front-facing eyes with betterdepth perception, important for clambering in trees On the mudflat, the horizon level is where most

of the action is Lots of other crabs are moving about, some of which (other males) might try to stealhis valuable burrow and some of which (females) he hopes to attract for mating It is no wonder thenthat the fiddler crab’s visual system has an acute band packed with visual receptors looking athorizon level, the equivalent of our foveae

Many birds that are potential prey have eyes on the sides of their heads, with wide visual range.Some of these birds also need to focus on the ground to pick up bits of food, such as grain Pigeons,for example, have two foveae in each eye One of the foveae in each eye looks out the side, the twoeyes looking at opposite sides The other two foveae are binocular in nature, with the two bothfocusing just a small myopic distance in front; these binocular foveae are used for picking up grains.These organizational differences make different visual Umwelts for these animals beyond sensoryranges

Visuals Unlimited, Inc./Ken Catania

A star-nosed mole, viewed from the front, showing its large claws and the star-shaped appendage that looks like a branched nose The star-nose is actually not a nose at all, but a touch-sensitive mechanoreceptor with a large representation in the star-nosed mole's cerebral cortex.

multi-In our primate tactile sense, receptors are also concentrated in “cities.” Representation in thetouch area in our forebrain, the somatosensory cortex, is dominated by the hand and face areas Such a

map of sensory representation is called a sensory homunculus, and the reader can check out

introductory psychology texts or Google images for pictorial depictions The somatosensory world ofthe star-nosed mole is quite different The animal is named after the fleshy structure on its face thatlooks like a star-shaped nose, but the star is not a nose at all: it has no chemoreceptors The star is amechanoreceptive organ, a touch sensor par excellence It is like the human hand in being full of touchreceptors But it is unlike our hand in having no muscles and bones, so it cannot be used to pick upbits of food That particular task the mole does with its mouth, after the star has detected a suitableitem Like our hands, the star dominates in cortical representation; it takes up fully one half of themole’s somatosensory cortex, sometimes whimsically called the “molunculus.”

The star-nosed mole uses its star to detect potential food items, such as little bugs The structurebuys it foraging efficiency, as it does this job much better than its “star-nose-less” sister species Anapt metaphor is that the star-nosed mole sees food in its underground world with its star Such ananalogy actually goes deeper Recall that we primates have a small area in each of our eyes, thefovea, that is especially packed with visual receptors If we detect something visually interesting inour periphery, our way of shedding more light on the object is to move our eyes so that our foveae arefocusing on the object The star-nosed mole similarly has tactile foveae: just two of those radiatingrays of the star are especially packed with touch receptors, and are especially well represented in thesomatosensory cortex When the mole detects something interesting with one of the nonfoveal rays ofits star, it moves the appendage to touch the item with its tactile foveae The Umwelt of the star-nosedmole contains a huge dose of touch information

Perceptual Processes

Perceptual processes taking place after transduction of sensory information can help to shape ananimal’s Umwelt as well A full cataloguing of perceptual processes would require a sizeable book,but some examples regarding the visual sense are handy for illustrating the link between perceptualprocesses and Umwelt.

Vision is used not only to make out static objects and scenes in the world, but also to track theworld dynamically as an animal moves It can be used as well to track how the self is moving through

the world Consider optic flow This is the change in the visual scene as we animals move through the

world If we look out the window of a moving train and see the world whiz by, that is optic flow Theoptic flow can, in principle, give us a gauge for how much we have moved forward It turns out thatflying bees use this cue primarily to measure how far they have flown in a certain direction, a process

called odometry (Chapter 4) (This term is named after the odometer, the device in a vehicle such as

a car that tells us how far we have traveled on a trip.) Thus, to bees, optic flow during flight is notjust the scene flashing by, but a crucial navigational component

To ants, cousin species to bees, optic flow is not nearly as important to the sense of distancetraveled (odometry) Ants rely much more on a form of step counting This process has been wellexamined in only one ant species and one bee species, so at the moment we are lacking comparativedata, but this contrast in odometry makes some functional sense For ground-walking insects withstereotypical walks, step counting provides a good measure of distance traveled Not so for flyinginsects Air is a turbulent medium, and the effect of a single wingbeat in terms of distance traveleddepends on how the wind is blowing Number of wingbeats does not provide a reliable estimate ofdistance traveled Optic flow provides a better proxy for estimating distance traveled

Visual object perception is something that humans are good at Taking such a feat for granted,however, can mislead us about what other animals perceive visually What is obvious to us may not

be obvious at all to others To be overly simplistic, what any visual system does is to pull apart thepattern of stimulation in the receptors to extract various features Thus, an important set of features isedge contours oriented at some angle Discovery of neurons in the visual part of the brains of catsresponsive especially to oriented edges won the Nobel Prize in Physiology or Medicine forneurobiologists David Hubel and Torsten Wiesel The earlier stages of visual analysis churn out apalette of features In primates, these would include, among other things, motion information, edgeorientation, color, and disparities between what the two eyes are seeing Other animals, such asinsects, would have a different palette

For animals to perceive an object from a palette of features, the features have to be put togetheragain in the brain Primates possess a dedicated stream of visual processing in the brain, whose job it

is to make out the properties of objects and give us conscious visual perception Seeing objects such

as fruits and tree branches is costing us a lot of expensive brain tissue This is a primate specialty,and we should not imagine that all other seeing animals possess our sophisticated object perception

It is likely that many animals, especially those with small brains, would just perceive a palette offeatures, and leave it at that As an illustration, navigating Australian desert ants are more attuned tothe entire visual panorama than to “obvious” (to humans) objects within that panorama, even when theobvious object is a black cloth 3 meters by 2 meters standing upright just behind their nest, theirdestination in homing

Perception is not solely a one-way route from stimulus to receptor to percept in the brain—stimulus-driven processes that are called “bottom-up processing.” Prior experiences and

expectancies also affect perception, called “top-down processing.” For example, task experiencescan make humans more likely to notice certain stimuli A huge literature in cognitive psychologyaddresses such processes under the theme of priming Consider the case of words primingsemantically related words If we are presented with the word “CAT” in a lexical decision task andare asked to answer whether it is a word or not, we are then better at the task when presented with arelated word Our reaction time to decide “yes” would be faster with words such as “mouse,” “purr,”

or “claw,” compared with the reaction time when we had not yet seen “CAT.” The following twoexamples in other animals illustrate priming-like processes in perception and learning

Honeybees can learn many things (Chapter 10), often in few trials But some tasks are easier andothers are harder Bees take longer to learn harder tasks, and they may not reach as high a level ofachievement as on easy tasks Some hard tasks of shape discrimination, such as discriminating shapesagainst a confusing mottled background, become much easier to learn when the bees have had someexperience with an easy version of the task

Another example of a priming-like phenomenon in animals is the search image This refers to theidea that a predator might be primed to see, and pick off, the most frequently encountered prey type.Niko Tinbergen’s younger brother, Luuk Tinbergen, first proposed this idea, based on somenaturalistic observations now considered less than fully convincing The term suggests that a predatormight keep something akin to a visual image in mind of a prey as it hunts, although this should betaken only metaphorically, as scientists are still unclear about the nature of a search image

Systematic studies with different species of birds have now provided good evidence for thisattentional phenomenon As an example, pigeons might have the task of detecting different types ofgrains against a substrate of pebbles of different shapes and colors that makes grain detection a bithard In a session, different types of grains would be presented in different proportions, and scientistsexamined whether the birds are especially good at picking out the most frequently encountered graintype If offered 80 percent grain A and 20 percent grain B, a bird that is equally good at detectinggrains regardless of their frequency in the population should pick off about 80 percent grain A and 20percent grain B In fact, what is typically found is that more than 80 percent of the birds’ successesare with grain A; in other words, the most frequently encountered type seems to be detected mosteasily Blue jays searching for computer-generated moths shown against a camouflaging backgroundshow a similar phenomenon Birds often seem to be primed to notice the most frequently encounteredprey type

Such top-down effects in perception should not be seen as quirks or mistakes in the system.Current thinking is that they are mostly adaptive Prior experiences furnish statistical informationabout the world—indicating, for instance, that some kinds of stimuli are more likely than other kinds

a priori, before any incoming “data.” Such prior statistical information, when combined with the

outcomes of bottom-up processing, leads the animal to make better perceptual “decisions,” basicallyusing more information to derive the output

Similarly, while we have been discussing sensory modalities separately, animals typicallycombine information from multiple modalities If humans hear a sound and see a blob, broadcastsimultaneously from slightly different locations, we perceive one multimodal event originating from alocation somewhere between the actual broadcast locations of the sound and the blob A similarprinciple applies in multimodal perception: Multiple modes mean more information, which in turnmeans better decisions This is a functional reason why many animal communicative signals come in

multiple modalities (Chapter 8).

Conclusion

In sum, information about the world, including the world of the animal’s own body, comes from thesenses All sensory receptors transduce some form of physical energy into nerve impulses Allsensations and perceptions consist of nervous activities, usually highly processed after thetransduction event Different species of animals differ in their subjective sensory world, or Umwelt.Differences come about because animals might possess different senses Perception of polarizedlight, magnetism, and electric fields are capabilities that humans do not have but that some animals

do Umwelts also differ across animals—because sensory ranges in a particular modality might differacross species, and because different kinds of perception might be the most important for an animal.Differences in perceptual organization and perceptual processes can also create different Umwelts

Human activities are now affecting many sensory processes of other animals Anthropogenic(human-generated) noise provides a case in point The low rumble of traffic noise can make somesounds more difficult to perceive Female crickets orient to the chirps of males for mating They will

do this in lab conditions in which one side of the chamber broadcasts male calls from a speaker:females will move preferentially toward the broadcasting side This sound-based orientation breaksdown, however, if the male calls are played on top of recordings of traffic noise made some 10meters from a highway Physical analysis of the male calls and traffic noise shows that the calls stoodout clearly above the noise; they should have been, in principle, discriminable Scientists attribute thefailure to the distracting effect of the noise How animals cope with environments that are seriouslyaffected by humans, from noise to light pollution to climate change, is currently a hot topic ofresearch, one with important consequences for the conservation of animals

Basic Learning

Sensory and perceptual processes help an animal acquire representations of the present world,including the world of its own body To make the best use of perceptual information, however, it isnecessary to take into account how the world was in the past That is the job of learning Defining

learning is a slippery business that learning theorists have not totally succeeded at Textbooks on

animal learning generally define learning as the change of behavior as a function of experience, withsome proviso that the experience should affect the behavior in the relevant way An ugly qualification

is necessary, because it is easy to come up with experiences that affect behavior, but that scientistswould not call “learning.” If you take an illegal stimulant, you can run faster But the drug taking is notconsidered a form of learning to run faster If you watch a video of Olympic gold-medal sprinterUsain Bolt running and imitate his stride, you might also run faster Scientists would consider that to

be learning, a form of observational learning Defining the relevance clearly and simply is difficult,but it can be left vague on that front A vague definition is enough for the purposes of presenting basiclearning mechanisms

The major point of this chapter is to present basic learning mechanisms, especially associativelearning mechanisms, as a backdrop against which to evaluate more complex forms of cognition.Later chapters will often provide assessments as to whether some seemingly complex behavior can

be explained as a form of associative learning This is necessary because basic associative learning

is ubiquitous in animals with nervous systems Most scientists would invoke intuitively complexcognitive notions such as insight and reasoning only after ruling out associative learning as a basis for

a behavior

This chapter will first discuss briefly the why of learning: Why have so many animals evolved theability to learn? Next, the chapter will look at the nonassociative forms of learning: habituation andsensitization These are forms of learning in which the animal is not connecting different kinds ofevents Either the repetition of the same kind of event leads to changes in the animal’s behavior, orsome unrelated event changes how an animal reacts to a particular stimulus Finally, the chapterexamines two forms of associative learning: classical conditioning and operant conditioning

Why Learn?

A recent review found research papers on learning in every taxonomic group of animals except thosewithout a nervous system, such as the sponges The reader might find the advantages of learningobvious, and ask, Why not learn as much as possible? Two kinds of answers have been offered Amore traditional view is that learning has costs This in turn implies that animals would learn onlywhen the benefits of learning exceed the costs A more modern view takes the ubiquity of associativelearning into consideration, and suggests that associative learning emerges out of the functioning ofnervous systems, with little by way of costs This view asks, indeed, Why not learn?—stipulating

some conditions under which a more inflexible program of behavior would replace learning.

In the traditional view, various costs of learning have been proposed An animal that learnsrequires more nervous tissue than one that does not learn, and neurons are costly in consuming energy

A bigger brain also has other costs It takes longer to grow, delaying time to reproductive maturityand requiring more parental effort Maintaining the products of learning, memory, is thought to havecosts as well Information tends to degrade unless efforts are expended to maintain the information

Efforts translate to costs One palpable cost has been demonstrated in Drosophila fruit flies, geneticists’ favorite model animal Drosophila that learned a task lived a shorter life than their

nonlearning counterparts

The traditional view stipulates that learning should evolve in conditions of intermediatepredictability At one extreme on the predictability continuum, nothing that happens in one momentpredicts what happens next Trying to learn is futile in such conditions Given that the world followsprinciples of physics and biology, such a totally unpredictable world does not exist At thepredictable extreme, whenever “events of type A” occurs, it means “B” (and this does exist) If B isimportant enough, it may pay to program the behavior to A innately, and bypass the process oflearning For example, frogs come wired to treat little moving dots as food to be snapped at, havingwhat are colloquially called “bug detectors” in their visual system In the frog’s Umwelt outside of alab, small moving dots are inevitably food items At intermediate levels of predictability, learningmakes functional sense, to help the animal predict events Lack of total predictability means thatbehavioral reactions cannot be wired in Nevertheless, learning mechanisms typically take advantage

of expected constancies in the world Examples are given later Learning does not startequipotentially from a blank slate, often it works hand-in-hand with innate predispositions

The modern view suggests that if a system of neurons takes in sensory information and the neuronscommunicate with one another, associative learning simply emerges Basic learning is a beneficialemergent property of nervous systems with little cost Under special conditions, however, learningmay be suppressed in favor of a more inflexible program, such as the aforementioned “bug detector”system in frogs Costs of learning might be associated with more complex forms of learning ratherthan with basic learning Such complex learning might include observational learning and other kinds

of complex cognition featured in Chapter 9

nonassociative is that animals are not linking (associating) two types of events In sensitization, the

sensitizing event is not predictive of any stimulus, and it serves to “prime” the animal in some way toreact to other, unrelated stimuli

If you walk into a meeting room in which a fan is whirring, you would notice the sounds of thefan After a while, however, you might hardly notice the whirr This example illustrates short-termhabituation If you exit the room for a while and then re-enter, you would notice the fan again Afterliving near a major road for some time, humans might report subjectively that they get used to the

noise of the traffic From day to day, they seem to notice the noise less Such subjective reactionswould constitute long-term habituation.

Interestingly, in contrast to subjective judgments, several controlled studies have shown thatchanges in heart rate as a response to traffic noise show no sign of habituation This lack ofhabituation is thought to contribute to poorer quality of sleep under the bombardment of traffic noise.Humans, and animals in general, do not habituate to all stimuli Learning is not equipotential; stimuliare not equally learnable

Not all stimuli are equal for habituation when it comes to male shore-living fiddler crabs Theseanimals dig burrows in the sand, and they defend their valuable burrow The burrow provides refugefrom predators and a place to mate with females If another crab heads toward his burrow, the ownerwill dash home pronto, ready to defend his asset If experimenters move an object up and down, malecrabs quickly stop reacting to it, showing habituation In contrast, no matter how many times scientistspulled a dummy plastic model toward a subject crab’s burrow, the crab dashed home, showing nosign of habituation over 50 trials

Other examples of habituation abound When presented with a pure tone for the first time, lab ratsdisplay an orienting response The rats would “perk up,” lifting their heads and turning their eyes andears to inspect their surroundings When presented with the urine of a conspecific, pigs would sniffthe urine Over repeated presentations, rats diminish their orienting response, and pigs sniff less,showing short-term habituation

Habituation comes in short-term and long-term varieties, and these are thought to depend ondifferent neural mechanisms Repeated presentation of a stimulus in a session typically leads to short-term habituation, lasting minutes to hours If we wait, say, three hours after playing a tone 10 times tothe rat, the 11th presentation would elicit an orientation response again Repeated sessions of thesame tone over multiple days, however, can lead to long-term habituation In this case, the response

to a stimulus is diminished even if it is the first one presented in an experimental session

Behaviorally opposite to habituation is sensitization In sensitization, a response to a stimulus

increases as a function of some intervening event that is not related to the stimulus Fear, for example,

is one state that sensitizes reactions to stimuli that are not related to what caused the fear If a loudpopping sound were to go off while you are reading this passage, you would “scrunch” a bitreflexively in a startle reaction That reflex, however, is—hopefully—less than your startle reaction

if the same pop went off at a dramatic point in a horror movie that you were watching Among otherthings, fear sensitizes startle reactions

In laboratory rats, a reliable way to generate fear is to give the rat a mild electric shock Thisevent would be like us getting zapped by static electricity from a door knob In a rat, it causes only abit of pain, but many animals take the shock to mean that they are under attack and in danger, and thusthey show fearful responses A loud noise causes a rat to jump literally: its startle response A rat infear jumps higher in response to a loud sound compared with unfearful rats A shock, an eventunrelated to noises, sensitizes a rat’s startle response, a phenomenon called “fear potentiated startle.”

One of the best-studied cases of sensitization is in a mollusk, the sea slug of the genus Aplysia.

The work won a Nobel Prize (Physiology or Medicine) for the scientist Eric Kandel (whoimmigrated from Austria to the United States, escaping the Nazi regime) This slug has sensitivestructures around its respiratory organ, the gill If anything brushes against any of these structures, theslug withdraws its gill to some extent in a gill withdrawal reflex This happens frequently in its

natural life because the slug lives in coastal waters strewn with debris such as bits of seaweed.Consider for illustrative purposes a structure called the mantle.

If a mild shock is applied to the mantle, resembling a gentle poke, the gill is withdrawn Overrepeated presentations, the extent of gill withdrawal diminishes; the slug habituates A strong shock tothe tail, however, sensitizes the slug The next gentle stimulus to the mantle results in a bigger gillwithdrawal Kandel won the Nobel Prize for elucidating the short-term and long-term forms of

habituation and sensitization in Aplysia.

The reader can probably figure out the functional reasons for habituation and sensitization.Habituation saves the animal from responding to irrelevant or unimportant stimuli, saving energy,effort, and attentional “bandwidth.” Note that habituation is not expressed when the stimulus inquestion is really important, such as when an object moves toward a fiddler crab’s burrow.Sensitization facilitates responses that might be useful under the sensitized conditions A rat in fearmight well be in danger of being attacked by a predator A sudden noise might herald a predatorattack A fear-potentiated jump might launch the rat away from the grasp of the predator; the rat thatshows fear-potentiated startle might run away and live to show fear-potentiated startle another day

Associative Learning: Classical Conditioning

Associative learning is so called because in this type of learning, the animal connects (associates)two types of events The prevailing view is that one event predicts another event for the animal Inclassical conditioning, the animal connects two events in the world, using one event to predict anotherevent In operant conditioning, the animal learns to connect its own behavior to consequences Inaddition, it needs to learn the circumstances under which a behavior brings a consequence That is, abehavior will “work” only in particular conditions

The discovery of classical conditioning is attributed to the Russian physiologist Ivan Pavlov(1849–1936) In his honor, this form of learning is also called Pavlovian conditioning Pavlov hadalready won a Nobel Prize in Physiology or Medicine in 1904 for his work on digestive physiology,but history shows that he became much more famous for his work elucidating the conditioning ofdigestive reflexes

One of the digestive responses that Pavlov’s lab studied was salivation in dogs If a scientist puts

a bit of meat powder in a hungry dog’s mouth, the salivary glands secrete some saliva into the mouth.This salivary reflex proved easy to measure, because a simple operation allowed the collection ofsaliva in a tube The conditioning of this reflex was discovered serendipitously: The dogs were

“ruining” the experiments because they started salivating when the lab assistant entered the lab,

before they had received the meat powder The lab assistant’s entry had become a conditioned stimulus A good scientist, however, recognizes that “ruined” results may be nature’s way of telling

us something far more important The rest, as they say, is history, but let us draw out the essentialbasics from that history

Four key terms characterize classical or Pavlovian conditioning: the unconditioned stimulus, the unconditioned response, the conditioned stimulus, and the conditioned response To start with, the

animal comes wired to exhibit the unconditioned response to an unconditioned stimulus Anunconditioned response is a reflex or reflex-like behavior that an animal shows when presented with

a stimulus In Pavlov’s dogs, meat powder presented in the mouth (unconditioned stimulus) results in

salivation (unconditioned response) For an unconditioned response to be produced reliably, theunconditioned stimulus needs to be biologically significant, such as food to a hungry animal, apotential mate to an animal in the mating season, or the sighting of a predator We have alreadylearned what happens to responses to innocuous neutral stimuli, such as a pure tone: The orientingresponse habituates over repeated presentations While scientists often measure a single behavior orphysiological response, the unconditioned response is much more than a single response Meatpowder would trigger digestive responses in the gut as well as in the salivary glands An electricshock to the feet of rats (unconditioned stimulus) produces fear (unconditioned response), a state thatmobilizes the rat in multiple ways As already mentioned, fear increases the startle response: the ratwould jump higher to a loud noise It also makes the rat freeze more, a behavior in which it staysstock still, avoiding any movement that might trigger the motion-detection systems of a predator’svisual systems It makes rats defecate more, bowel control being a low priority in the face of danger.The colloquial phrase for something truly fear provoking as “scaring the [feces] out of us”—thereader can substitute a more colorful synonym—has some physiological basis Fear also prepares therat’s nerves and muscles for action, to fight or to flee, and it dilates the pupils, dangerous conditionsbeing those in which one might want to take in more visual information.

The conditioned stimulus is an event that serves as a reliable predictor of some biologicallysignificant unconditioned stimulus For example, the arrival of the lab assistant signals the imminentarrival of meat powder for Pavlov’s dogs Over repeated pairings of arrival of lab assistant(conditioned stimulus) followed by meat powder in mouth (unconditioned stimulus), the dogs learn toexhibit a conditioned response to the conditioned stimulus, which is also salivation (and no doubtother digestive responses as well) The conditioned response is exhibited even before the arrival ofthe meat powder A formerly neutral stimulus has come to elicit a response (the conditionedresponse) after conditioning that it did not elicit at the start of training Pavlov’s lab went on todemonstrate classical conditioning systematically using other kinds of conditioned stimuli, such as theticking of a metronome

In the example of fear in rats elicited by electric shock, a systematic predictor event can be linked

to the arrival of shock in fear conditioning A commonly used conditioned stimulus is some tone thatsounds a few seconds before shock arrives Rats learn fear conditioning quickly After a few tone–shock pairings, just the sound of the tone alone elicits fear in rats (a conditioned response exhibitedbefore the arrival of shock), as multiple measures indicate, including the duration of freezing, theamount of feces excreted, and the height of the startle response to loud noise

As might be expected, the great themes of life, food, sex, and (fear of) death form unconditionedstimuli that have been studied Rats and pigeons, traditional lab animals, can be conditioned topredict the arrival of food at the sound of a tone (typical for rats) or the lighting of a key (typical forpigeons) In anticipation of food, a rat would poke its head into the hopper repeatedly A pigeonwould peck at the lit key Food conditioning has also been studied extensively in honeybees Inresponse to a smell (the conditioned stimulus) predicting the arrival of sugar water (the unconditionedstimulus), a worker bee sticks out its long, tonguelike structure, called the proboscis, used to suck upthe sugar water The experimental paradigm is thus called the proboscis extension reflex (PER).Many of the neurobiological details of odor processing and the proboscis extension reflex are known.Turning to sex, some male quail, a small bird sometimes used for food, have been lucky enough toparticipate in experiments on sexual conditioning The conditioned stimulus is a light that goes on

Some seconds later, a receptive female (unconditioned stimulus) is presented when the door thatseparates the two birds opens The male approaches the female and copulates The conditionedstimulus soon comes to elicit approach from the male anticipating a receptive female, a behaviorcalled sign tracking Curiously, the male approaches the conditioned stimulus, and not the door atwhich the female is expected to appear, the latter behavior known as goal tracking.

An acquired conditioned response will diminish if the conditioned stimulus is subsequentlypresented without the unconditioned stimulus This process is called extinction Over repeatedpresentations of a conditioned stimulus without the unconditioned stimulus, the conditioned responsemight diminish and eventually not appear at all to the conditioned stimulus Thus, if an odor that hadpredicted sugar water is presented to a bee without the appearance of sugar water, the bee will stopextending its proboscis after a few such solo presentations of the odor Extinction is not a process ofwiping out the association between the conditioned stimulus and the unconditioned stimulus.Scientists think of it as learning a new association that overrides the older connection betweenconditioned stimulus and unconditioned stimulus That is because the conditioned response mightappear again with a host of “reminder” manipulations Thus, just waiting some time after an extinctionsession, without any further training, might bring back the conditioned response to the conditionedstimulus This is called spontaneous recovery, spontaneous because no training has taken placebetween the extinction procedure and the retest Sometimes, presenting the unconditioned stimulusbriefly again might also act as a reminder, and bring back a conditioned response to a conditionedstimulus

Associative Learning: Operant Conditioning

In operant conditioning, often called instrumental conditioning, the animal learns to do things for theirconsequences Edward Lee Thorndike (1874–1949) is credited as a pioneer in operant conditioning

He placed cats into puzzle-boxes with contraptions such as latches and pulleys, and he timed howlong it took the cats to find the way to open the door to obtain a bit of reward He found that the catsdid not show any signs of insight or of figuring out what to do; rather, they tried a variety ofbehaviors, eventually stumbling on the solution The latency to escape diminished gradually overrepeated tests He thought that successful behaviors were strengthened in the setting of the puzzle-box,

a stimulus–response (S–R) connection, while ineffective behaviors were weakened Thorndike calledthis the law of effect: Behaviors followed by good outcomes are strengthened and are more likely to

be exhibited in the future

It was B F Skinner ( Box 3.1) who perhaps did the most to launch the study of operantconditioning He supplied the field with both methodological tools and a large pile of empiricalresults His designs of operant chambers, also known colloquially as Skinner boxes, meant thatstimuli can be presented automatically and behaviors recorded automatically This facilitated thecollection of data for Skinner and for the many scientists who studied operant conditioning insubsequent years In the beginning, the operant chambers were mechanical contraptions, but they haveevolved to computer-controlled boxes that scientists can program to run experiments (see photo)

Operant conditioning has three key terms: the discriminative stimulus (S), the operant or response (R), and the consequence or outcome (O) In brief, the animal learns that under a particular

condition (the discriminative stimulus), a response results in a particular outcome The R component