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PRINCIPLES OF Cognitive Neuroscience SECOND EDITION Dale Purves Roberto Cabeza Scott A. Huettel Kevin S. LaBar Michael L. Platt Marty G. Woldorff Contributor Elizabeth M. Brannon Center for Cognitive Neuroscience Duke University Sinauer Associates, Inc. Publishers Sunderland, MA U.S.A. © Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher.

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Page 1: PRINCIPLES OF Cognitive Neuroscience ... - Sinauer · PDF filePRINCIPLES OF Cognitive Neuroscience ... ©2012 Sinauer Associates, Inc. ... Principles of Cognitive Neuroscience, Second

PRINCIPLES OF

Cognitive Neuroscience SECOND EDITION

Dale Purves

Roberto Cabeza

Scott A. Huettel

Kevin S. LaBar

Michael L. Platt

Marty G. Woldorff

Contributor Elizabeth M. Brannon

Center for Cognitive Neuroscience Duke University

Sinauer Associates, Inc. PublishersSunderland, MA U.S.A.

CogNeuroFrontmatter.indd iii 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher.

Page 2: PRINCIPLES OF Cognitive Neuroscience ... - Sinauer · PDF filePRINCIPLES OF Cognitive Neuroscience ... ©2012 Sinauer Associates, Inc. ... Principles of Cognitive Neuroscience, Second

Contents in Brief

CHAPTER 1 Cognitive Neuroscience: Definitions, Themes, and Approaches 1

CHAPTER 2 The Methods of Cognitive Neuroscience 17

CHAPTER 3 Sensory Systems and Perception: Vision 55

CHAPTER 4 Sensory Systems and Perception: Auditory, Mechanical, and Chemical Senses 93

CHAPTER 5 Motor Systems: The Organization of Action 131

CHAPTER 6 Attention and Its Effects on Stimulus Processing 167

CHAPTER 7 The Control of Attention 205

CHAPTER 8 Memory: Varieties and Mechanisms 243

CHAPTER 9 Declarative Memory 279

CHAPTER 10 Emotion 319

CHAPTER 11 Social Cognition 359

CHAPTER 12 Language 393

CHAPTER 13 Executive Functions 429

CHAPTER 14 Decision Making 465

CHAPTER 15 Evolution and Development of Brain and Cognition 503

APPENDIX The Human Nervous System 539

CogNeuroFrontmatter.indd v 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

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Page 3: PRINCIPLES OF Cognitive Neuroscience ... - Sinauer · PDF filePRINCIPLES OF Cognitive Neuroscience ... ©2012 Sinauer Associates, Inc. ... Principles of Cognitive Neuroscience, Second

Cognitive Neuroscience: Definitions, Themes, and Approaches 1

Introduction 1

Cognition 2Natural philosophy and early psychology 2Behaviorism 2Cognitive science 3

Neuroscience 5

Cognitive Neuroscience: The Neurobiological Approach to Cognition 9

Methods: Convergence and Complementarity 10

Conclusions 14

■ BOX 1A CONVERGENCE THROUGH META-ANALYSIS 12

Contents

The Methods of Cognitive Neuroscience 17

Introduction 17

Brain Perturbations That Elucidate Cognitive Functions 19Perturbations imposed by stroke, trauma, or disease 19Pharmacological perturbations 21Perturbation by intracranial brain stimulation 26Perturbation by extracranial brain stimulation 26Optogenetics 28

Measuring Neural Activity during Cognitive Processing 29Direct electrophysiological recording from neurons 29Electroencephalography (EEG) 31Event-related potentials (ERPs) 34Magnetoencephalography (MEG) 36Positron emission tomography (PET) imaging 38

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CogNeuroFrontmatter.indd vi 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

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CONTENTS ■ vii

Functional magnetic resonance imaging (functional MRI or fMRI) 39Using fMRI to analyze activation patterns within a brain area 42Using fMRI to examine activity relationships between brain areas 44Optical brain imaging 45

Assembling Evidence and Delineating Mechanisms 46Associations and dissociations 46Multimethodological approaches 48

■ INTRODUCTORY BOX EARLY BRAIN MAPPING IN HUMANS 18

■ BOX 2A AN INTRODUCTION TO STRUCTURAL BRAIN IMAGING TECHNIQUES 22

■ BOX 2B IMAGING STRUCTURAL CONNECTIONS IN THE BRAIN 24

■ BOX 2C NEUROIMAGING GENOMICS 51

Sensory Systems and Perception: Vision 55

Introduction 55

Visual Stimuli 55

The Initiation of Vision 56

Subcortical Visual Processing 59

Cortical Visual Processing 61

Other Key Characteristics of the Visual Cortex 64Topography 64Cortical magnification 66Cortical modularity 66Visual receptive fields 67

Visual Perception 69Lightness and brightness 69Color 73Form 76Distance and depth 79Motion 83Object recognition 85Perceiving remembered images 88

■ INTRODUCTORY BOX PROSOPAGNOSIA 56

■ BOX 3A SYNESTHESIA 65

■ BOX 3B MEASURING PERCEPTION 70

■ BOX 3C THE INVERSE PROBLEM 78

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CogNeuroFrontmatter.indd vii 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

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viii ■ CONTENTS

Sensory Systems and Perception: Auditory, Mechanical, and Chemical Senses 93

Introduction 93

The Auditory System 93Sound stimuli 93The peripheral auditory system 96The auditory cortices 100The perception of sound 100Perceiving the location of sound sources 107

The Mechanosensory Systems 110The cutaneous/subcutaneous system 110The pain system 116

The Chemosensory Modalities 119The olfactory system 120The taste system 122Trigeminal chemosensation 124

Some Final Points about Sensory Systems 124Coding and labeled lines 124The malleability of sensory circuitry 124Awareness of sensory stimuli 126The representation of sensory percepts 127

■ INTRODUCTORY BOX THE REMARKABLE SUCCESS OF COCHLEAR IMPLANTS 94

■ BOX 4A MEASURING LOUDNESS 101

■ BOX 4B MUSIC AND ITS EFFECTS 103

■ BOX 4C SOMATOSENSORY ILLUSIONS 112

■ BOX 4D PHANTOM LIMBS 115

Motor Systems: The Organization of Action 1317

Introduction 131

Motor Control Is Hierarchical 132Anatomical organization of motor systems 133

Cortical Pathways for Motor Control 137Organization of the primary motor cortex 139Movement maps in the primary motor cortex 141

Coding Movements by the Activity of Neuronal Populations 143

Planning Movements 144Selecting goals for action 146Motivational control of goal selection 148

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CONTENTS ■ ix

Sequential Movements and the Supplementary Motor Area 149

Sensory-Motor Coordination 151

Initiation of Movement by the Basal Ganglia 152

Basal Ganglia and Cognition 156

Error Correction and Motor Coordination by the Cerebellum 159

Cerebellar Contributions to Cognitive Behavior 161

■ INTRODUCTORY BOX APRAXIA 132

■ BOX 5A REFLEXES, CENTRAL PATTERN GENERATORS, AND RHYTHMIC BEHAVIORS 135

■ BOX 5B MOTOR CONTROL OF FACIAL EXPRESSIONS 138

■ BOX 5C MOTOR SYSTEMS AND INTERVAL TIMING 153

Attention and Its Effects on Stimulus Processing 167

Introduction 167

The Concept of Attention 169Global states, arousal, and attention 169The selective nature of attention 169

Behavioral Studies of Attention Capacity and Selection 170The level at which selection occurs 170Endogenously versus exogenously driven selective attention 172

Neuroscience Approaches to Studying Attention 174Studying the neural effects of attention on stimulus processing 175Studying the control of attention in the brain 175

Neural Effects of Attention on Stimulus Processing: Auditory Spatial Attention 176

Electrophysiological studies of the effects of auditory spatial attention 176Neuroimaging studies of the effects of auditory spatial attention 178Animal studies of the effects of auditory spatial attention 180The effects of auditory spatial attention on auditory feature processing 180

Neural Effects of Attention on Stimulus Processing: Visual Spatial Attention 182

Electrophysiological studies of the effects of visual spatial attention 182Neuroimaging studies of the effects of visual spatial attention 184Combining electrophysiological and neuroimaging studies of visual spatial attention 189Animal studies of the effects of visual spatial attention 189The effects of visual spatial attention on visual feature processing 194

Neural Effects of Attending to Nonspatial Stimulus Attributes 195

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CogNeuroFrontmatter.indd ix 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

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x ■ CONTENTS

The Control of Attention 205

Introduction 205

Clinical Evidence for Brain Regions Involved in Attentional Control 206

Control of Voluntary Attention 210Activation in frontal and parietal cortex during endogenous attentional tasks 210Delineating the role of the frontoparietal network in the control of attention 210Ascertaining the temporal flow of brain activations underlying attentional control 212Single-neuron recordings in frontal and parietal cortex during attentional control 214Preparatory activation of sensory cortices during attentional control 216

Control of Exogenously Induced Changes in Attention 218Attentional shifts triggered by sudden stimulus onsets 218Attentional reorienting activates a ventral frontoparietal system 219

Visual Search 220Behavioral studies of visual search 220Theoretical models of visual search 221Neural processes underlying visual search 223

Attentional Control as a System of Interacting Brain Areas 224

Interactions between Components of the Attentional System 226

Generality of Attentional Control Systems 228

Attention, Levels of Arousal, and Consciousness 231Sleep and wakefulness 232Consciousness 234Neural correlates of consciousness in normal subjects 234Neural correlates of consciousness in pathological conditions 237

■ INTRODUCTORY BOX HEMISPATIAL NEGLECT SYNDROME 206

■ BOX 7A THE DEFAULT-MODE NETWORK 229

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The neural effects of attention to nonspatial auditory features 195The neural effects of attention to nonspatial visual features 196The effects of visual attention to objects 198

Neural Effects of Attention across Sensory Modalities 200

■ INTRODUCTORY BOX THE COCKTAIL PARTY EFFECT 168

■ BOX 6A THE ATTENTIONAL BLINK AND LATE ATTENTIONAL SELECTION 186

■ BOX 6B ATTENTION-RELATED “REENTRANT” ACTIVITY 190

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CONTENTS ■ xi

Memory: Varieties and Mechanisms 243

Introduction 243

Memory Phases, Processes, Systems, and Tasks 245

Dissociating Memory Systems 248Working memory versus declarative memory 248Declarative versus nondeclarative memory 249

Nondeclarative Memory 251

Priming 252Perceptual priming 253Conceptual priming 255Semantic priming 256Repetition enhancement 257

Skill Learning 258Motor skill learning 259Perceptual skill learning 261Cognitive skill learning 263

Conditioning 266

Cellular Mechanisms of Memory 270Habituation and sensitization 272Long-term potentiation and depression 273Linking LTP to memory performance 274Learning-related changes in synaptic morphology 275

■ INTRODUCTORY BOX THE CASE OF H.M. 244

■ BOX 8A INVESTIGATING DECLARATIVE MEMORY IN NON-HUMAN ANIMALS 246

■ BOX 8B MEDIAL TEMPORAL LOBE CONTRIBUTIONS BEYOND DECLARATIVE MEMORY 251

■ BOX 8C CONNECTIONIST MODELS 271

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Declarative Memory 279

Introduction 279

Basic Concepts and Assumptions 281A taxonomy of declarative memory 281A simple neurological model of encoding, storage, and retrieval 283Using the model to explain the effects of brain damage 284

The Nature of Medial Temporal Lobe Representations 285Theories of hippocampal memory function 286Differences between medial temporal lobe subregions 290

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xii ■ CONTENTS

Cortical Regions Storing Semantic and Episodic Memory Representations 293

The organization of semantic knowledge in the cortex 293The reactivation of cortical regions for recent episodic memories 297

Contributions of the Prefrontal Cortex to Encoding and Retrieval 300

Functional neuroimaging of episodic encoding 300Functional neuroimaging of episodic retrieval 303Effects of frontal lobe lesions 306

Contributions of the Posterior Parietal Cortex to Encoding and Retrieval 308

The role of posterior parietal cortex during retrieval 308The role of posterior parietal cortex during encoding 311

Memory Consolidation 312Synaptic versus system consolidation 312Theories of system consolidation in declarative memory 313Consolidation, reactivation, and sleep 314

■ INTRODUCTORY BOX DEVELOPMENTAL AMNESIA 280

■ BOX 9A ORGANIZATION OF THE MEDIAL TEMPORAL LOBE MEMORY SYSTEM 286

■ BOX 9B FUNCTIONAL NEUROIMAGING METHODS TO STUDY EPISODIC MEMORY 302

■ BOX 9C ERP STUDIES OF EPISODIC RETRIEVAL 309

Emotion 319

Introduction 319

What Is Emotion? 321

Psychological Classification of Emotions 322Categorical theories 322Dimensional theories 323Component process theories 325

Early Neurobiological Theories of Emotion 325The James-Lange feedback theory 329The Cannon-Bard diencephalic theory 329The Papez circuit and Klüver-Bucy syndrome 331The limbic system theory and its challenges 332

Contemporary Approaches to Studying the Neurobiology of Emotion 334

Hemispheric-asymmetry hypotheses 334Vertical integration models: Fear acquisition 337Vertical integration models: Fear modification 340

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CogNeuroFrontmatter.indd xii 9/14/12 10:46 AM©2012 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

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CONTENTS ■ xiii

Social Cognition 359

Introduction 359

The Self 361Self-reflection 363Embodiment 365

Perception of Social Cues Evident in the Face and Body 367Face perception 367Perception of biological motion 370Interpersonal attention and action direction 372

Social Categorization 374Perception of social category information 374Stereotypes and automatic racial biases 375Monitoring and controlling racial bias 376Impression formation and trust 379

Understanding the Actions and Emotions of Others 380Mirror neurons 381Perspective taking and mental-state attribution 383Theory of mind in children and apes 384Empathy, sympathy, and prosocial behavior 386

Social Competition 388Social rank and stress 388Power motivation and dominance contests 390

■ INTRODUCTORY BOX AUTISM 360

■ BOX 11A MEASURING IMPLICIT AND EXPLICIT RACIAL ATTITUDES 377

■ BOX 11B SOCIAL BONDS AND KINSHIP 389

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Interoception and the somatic marker hypothesis 340In search of categories of emotional experience 343

Interactions with Other Cognitive Functions 345Emotional influences on perception and attention 345Emotional influences on memory consolidation 350

Regulation of Emotion 354

■ INTRODUCTORY BOX THE NEUROSCIENCE AND NEUROETHICS OF POSTTRAU- MATIC STRESS DISORDER 320

■ BOX 10A PSYCHOPHYSIOLOGY AND THE BRAIN-BODY LINK 326

■ BOX 10B STRESS AND THE HYPOTHALAMIC-PITUITARY- ADRENAL AXIS 352

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xiv ■ CONTENTS

Language 393

Introduction 393

Speech 393Producing speech 393Comprehending speech 396Interpreting speech sounds 396Sentences, grammar, and syntax 397The importance of context 398

Acquiring Speech and Language 400Learning a vocabulary 400The shaping of phonemes and phones 400A critical period for language acquisition 401Mechanisms of language learning 402Effects of language deprivation 402

Theories of Language 403Is there a “universal grammar”? 404Connectionist theory 404

The Neural Bases of Language 406Neural bases for producing speech and language 406Neural bases for comprehending language 407Additional evidence from neurosurgery 408Contributions of the right hemisphere to language 413

Noninvasive Studies of Language Organization 414Evidence that the neural basis of language is fundamentally symbolic 418

Genetic Determination of Language Functions 420

Is Human Language Unique? 420

The Origins of Human Language 424

■ INTRODUCTORY BOX DYSLEXIA 394

■ BOX 12A REPRESENTING SPEECH SOUNDS IN WRITTEN FORM 398

■ BOX 12B LANGUAGE, HANDEDNESS, AND CEREBRAL DOMINANCE 411

■ BOX 12C REPRESENTING NUMBER 421

■ BOX 12D LEARNED VOCAL COMMUNICATION IN NON- HUMAN SPECIES 422

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CONTENTS ■ xv

Executive Functions 429

Introduction 429

A Taxonomy of Executive Function 429

Prefrontal Cortex: A Key Contributor to Executive Function 432

Organization and connectivity of the prefrontal cortex 434Consequences of damage to the prefrontal cortex 436

Establishing and Modifying Behavioral Rules 437Initiating rules for behavior 438Inhibiting rules for behavior 441Inhibiting socially inappropriate behaviors 443Shifting among rules for behavior 444Relating rules to create higher-order models of the world 445Hierarchical models for executive function 449

Control: Matching Behavior to Context 452Conflict monitoring 453Challenges to the conflict-monitoring model 454Functional organization of dorsomedial prefrontal cortex 456

Working Memory: Maintaining Information and Rules over Time 458

Neural substrates of working memory 460

■ INTRODUCTORY BOX ENVIRONMENTAL DEPENDENCY SYNDROME 430

■ BOX 13A COMPARATIVE ANATOMY OF THE PREFRONTAL CORTEX 432

■ BOX 13B THE NEUROBIOLOGY OF INTELLIGENCE 446

■ BOX 13C REASONING 450

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Decision Making 465

Introduction 465

Decision Making: From Rational Choice to Behavioral Economics 467

Reward and Utility 470Dopamine: Pleasure or motivation? 470Reward prediction error 473Responses to negative outcomes 476

Uncertainty: Risk, Ambiguity, and Delay 479Risk and ambiguity 479Delay: Discounting future rewards 481

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xvi ■ CONTENTS

Social Context 483Social rewards 484Social cooperation 485Social punishment 488

Integration: Combining and Comparing Information to Reach a Decision 489

Perceptual decision making 489Value-based decision making 491

Heuristics in Decision Making 495

Future Directions 497

■ INTRODUCTORY BOX ADDICTION TO GAMBLING 466

■ BOX 14A LEARNING VALUES AND FORMING HABITS 476

■ BOX 14B MODELING SIMPLE DECISIONS 492

■ BOX 14C NEUROMARKETING 498

Evolution and Development of Brain and Cognition 503

Introduction 503

Early Thinking about the Evolution and Development of Cognition 505

Early Brain Development 508Neuronal differentiation and myelination 508The development of neural connections 510

Linking Brain and Cognitive Development 511Brain size and the evolution of cognition 514Relative brain size and cerebral complexity 516

Evolution of Brain Development 520

Evolutionary Specializations of Brain and Behavior 522Evolution and development of learning and memory 523Evolution and development of quantitative cognition 526Evolution and development of social cognition 529Evolution and development of language 535

■ INTRODUCTORY BOX SAVANT SYNDROME 504

■ BOX 15A DARWIN AND THE BRAIN 507

■ BOX 15B BRAIN DIFFERENCES IN MODERN HUMANS: IMPLICATIONS FOR COGNITION 516

■ BOX 15C EVOLUTION OF HUMAN BRAIN AND COGNITION EVIDENT IN THE FOSSIL RECORD 518

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CONTENTS ■ xvii

APPENDIXThe Human Nervous System 539

Cellular Components of the Nervous System 539

Nerve Cells and Their Signaling Functions 540

Functional Organization of the Human Nervous System 543Neural circuits 543Neural systems 545

Structural Organization of the Human Nervous System 547

Major Subdivisions of the Central Nervous System 549The brainstem 550The spinal cord 550Surface features of the brain 552Internal features of the brain 557The ventricular system 561

The Brain’s Blood Supply 561

■ BOX A1 INTRACELLULAR RECORDING FROM NERVE CELLS 546

■ BOX A2 ORGANIZATION OF THE CEREBRAL CORTEX 553

■ BOX A3 ANATOMICAL TERMINOLOGY 558

Glossary 565

Illustration Credits 583

Index 591

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