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.

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Contents in Brief
CHAPTER 1

Cognitive Neuroscience: Definitions, Themes, and Approaches

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

CHAPTER 6

Attention and Its Effects on Stimulus Processing

CHAPTER 7

The Control of Attention

CHAPTER 8

Memory: Varieties and Mechanisms

CHAPTER 9

Declarative

M
emory

131
167

205
243

279

CHAPTER 10

Emotion

319

CHAPTER 11

Social

CHAPTER 12

Language

CHAPTER 13

Executive unctions
F

CHAPTER 14

Decision

CHAPTER 15

Evolution and Development of Brain and Cognition

Co
gnition

359

393

M
aking

429

465

APPENDIX The Human Nervous System

503

539

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Contents

Cognitive Neuroscience:
Definitions, Themes, and Approaches 1

Introduction
Cognition

Natural philosophy and early psychology

Behaviorism 2
Cognitive science 3

Neuroscience

Cognitive Neuroscience:
The Neurobiological Approach to Cognition

Methods: Convergence and Complementarity

Conclusions

10

14

BOX 1A CONVERGENCE THROUGH META-ANALYSIS 12

The Methods of Cognitive

Neuroscience 17

Introduction

17

Brain Perturbations That Elucidate Cognitive Functions

Perturbations imposed by stroke, trauma, or disease
Pharmacological perturbations 21
Perturbation by intracranial brain stimulation 26
Perturbation by extracranial brain stimulation 26
Optogenetics 28

Measuring Neural Activity during Cognitive Processing

Direct electrophysiological recording from neurons
Electroencephalography (EEG) 31
Event-related potentials (ERPs) 34
Magnetoencephalography (MEG) 36
Positron emission tomography (PET) imaging 38

19

19

29

29

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CONTENTS

vii

Functional magnetic resonance imaging (functional MRI or fMRI) 39

Using fMRI to analyze activation patterns within a brain area 42
Using fMRI to examine activity relationships between brain areas 44
Optical brain imaging 45

Assembling Evidence and Delineating Mechanisms

46

Associations and dissociations 46

Multimethodological 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
Visual Stimuli

55
55

The Initiation of Vision

56

Subcortical Visual Processing

Cortical Visual Processing

59

61

Other Key Characteristics of the Visual Cortex

64

Topography 64
Cortical magnification 66
Cortical modularity 66
Visual receptive fields 67

Visual Perception

69

Lightness and brightness 69

Color 73
Form 76
Distance and depth 79
Motion 83
Object recognition 85
Perceiving 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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viii CONTENTS

Sensory Systems and Perception: Auditory,

Mechanical, and Chemical Senses 93

Introduction

93

The Auditory System

93

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

The Mechanosensory Systems

110

The cutaneous/subcutaneous system

The pain system 116

The Chemosensory Modalities

The olfactory system 120
The taste system 122
Trigeminal chemosensation

107

110

119

124

Some Final Points about Sensory Systems

124

Coding and labeled lines 124

The malleability of sensory circuitry 124
Awareness of sensory stimuli 126
The 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

132

Anatomical organization of motor systems

Cortical Pathways for Motor Control

133

137

Organization of the primary motor cortex 139

Movement maps in the primary motor cortex 141

Coding Movements by the Activity of Neuronal Populations 143

Planning Movements

144

Selecting goals for action 146

Motivational 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

Basal Ganglia and Cognition

152

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

169

Global states, arousal, and attention 169

The selective nature of attention 169

Behavioral Studies of Attention Capacity and Selection

The level at which selection occurs 170
Endogenously versus exogenously driven selective attention

Neuroscience Approaches to Studying Attention

170
172

174

Studying the neural effects of attention on stimulus processing

Studying the control of attention in the brain 175

175

Neural Effects of Attention on Stimulus Processing:

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

178

Neural Effects of Attention on Stimulus Processing:

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

Neural Effects of Attending to Nonspatial Stimulus

Attributes 195

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x CONTENTS

The neural effects of attention to nonspatial auditory features 195

The neural effects of attention to nonspatial visual features 196
The 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

The Control of Attention 205

Introduction 205
Clinical Evidence for Brain Regions Involved in Attentional
Control 206
Control of Voluntary Attention

210

Activation in frontal and parietal cortex during endogenous attentional

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

Control of Exogenously Induced Changes in Attention

218

Attentional shifts triggered by sudden stimulus onsets 218

Attentional reorienting activates a ventral frontoparietal system

Visual Search

219

220

Behavioral studies of visual search 220

Theoretical models of visual search 221
Neural 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

231

Sleep and wakefulness 232

Consciousness 234
Neural correlates of consciousness in normal subjects 234
Neural correlates of consciousness in pathological conditions

237

INTRODUCTORY BOX HEMISPATIAL NEGLECT

SYNDROME 206

BOX 7A THE DEFAULT-MODE NETWORK 229

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CONTENTS

xi

Memory:
Varieties and Mechanisms 243

Introduction 243
Memory Phases, Processes, Systems, and Tasks 245
Dissociating Memory Systems 248
Working memory versus declarative memory 248
Declarative versus nondeclarative memory 249

Nondeclarative Memory 251

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

Skill Learning 258

Motor skill learning 259
Perceptual skill learning 261
Cognitive skill learning 263

Conditioning 266
Cellular Mechanisms of Memory 270
Habituation and sensitization 272
Long-term potentiation and depression 273
Linking LTP to memory performance 274
Learning-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

Declarative Memory

Introduction

279

279

Basic Concepts and Assumptions 281

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

The Nature of Medial Temporal Lobe Representations

Theories of hippocampal memory function 286
Differences between medial temporal lobe subregions

283

285

290

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xii CONTENTS

Cortical Regions Storing Semantic and Episodic Memory

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

297

Contributions of the Prefrontal Cortex to Encoding and

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

Contributions of the Posterior Parietal Cortex to Encoding and

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

Memory Consolidation

312

Synaptic versus system consolidation 312

Theories of system consolidation in declarative memory
Consolidation, reactivation, and sleep 314

313

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

10

Emotion 319

Introduction

319

What Is Emotion?

321

Psychological Classification of Emotions

Categorical theories 322
Dimensional theories 323
Component process theories

322

325

Early Neurobiological Theories of Emotion

325

The James-Lange feedback theory 329

The Cannon-Bard diencephalic theory 329
The Papez circuit and Klver-Bucy syndrome 331
The limbic system theory and its challenges 332

Contemporary Approaches to Studying the Neurobiology of

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

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CONTENTS

xiii

Interoception and the somatic marker hypothesis 340

In search of categories of emotional experience 343

Interactions with Other Cognitive Functions

345

Emotional influences on perception and attention 345

Emotional influences on memory consolidation 350

Regulation of Emotion

354

INTRODUCTORY BOX THE NEUROSCIENCE AND

NEUROETHICS OF POSTTRAUMATIC STRESS DISORDER 320

BOX 10A PSYCHOPHYSIOLOGY AND THE BRAIN-BODY

LINK 326

BOX 10B STRESS AND THE HYPOTHALAMIC-PITUITARYADRENAL AXIS 352

11

Social Cognition 359

Introduction
The Self

359

361

Self-reflection 363
Embodiment 365

Perception of Social Cues Evident in the Face and Body

Face perception 367
Perception of biological motion 370
Interpersonal attention and action direction

Social Categorization

367

372

374

Perception of social category information 374

Stereotypes and automatic racial biases 375
Monitoring and controlling racial bias 376
Impression formation and trust 379

Understanding the Actions and Emotions of Others

380

Mirror neurons 381

Perspective taking and mental-state attribution 383
Theory of mind in children and apes 384
Empathy, sympathy, and prosocial behavior 386

Social Competition

388

Social rank and stress 388

Power 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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xiv CONTENTS

12

Language 393

Introduction
Speech

393

393

Producing speech 393

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

Acquiring Speech and Language

400

Learning a vocabulary 400

The shaping of phonemes and phones 400
A critical period for language acquisition 401
Mechanisms of language learning 402
Effects of language deprivation 402

Theories of Language

403

Is there a universal grammar?

Connectionist theory 404

404

The Neural Bases of Language

406

Neural bases for producing speech and language 406

Neural bases for comprehending language 407
Additional evidence from neurosurgery 408
Contributions of the right hemisphere to language 413

Noninvasive Studies of Language Organization 414

Evidence that the neural basis of language is fundamentally
symbolic 418

Genetic Determination of Language Functions

Is Human Language Unique?

420

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 NONHUMAN SPECIES 422

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CONTENTS

13

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 434
Consequences of damage to the prefrontal cortex 436

Establishing and Modifying Behavioral Rules

437

Initiating rules for behavior 438

Inhibiting rules for behavior 441
Inhibiting socially inappropriate behaviors 443
Shifting among rules for behavior 444
Relating rules to create higher-order models of the world
Hierarchical models for executive function 449

Control: Matching Behavior to Context

445

452

Conflict monitoring 453

Challenges to the conflict-monitoring model 454
Functional 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

14

Decision Making 465

Introduction

465

Decision Making: From Rational Choice to Behavioral

Economics 467
Reward and Utility

470

Dopamine: Pleasure or motivation? 470

Reward prediction error 473
Responses to negative outcomes 476

Uncertainty: Risk, Ambiguity, and Delay

Risk and ambiguity 479
Delay: Discounting future rewards

479

481

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xvi CONTENTS

Social Context

483

Social rewards 484

Social cooperation 485
Social punishment 488

Integration: Combining and Comparing Information to Reach

a Decision 489
Perceptual decision making 489
Value-based decision making 491

Heuristics in Decision Making

Future Directions

495

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

15

Evolution and Development of Brain

and Cognition 503

Introduction 503
Early Thinking about the Evolution and Development of
Cognition 505
Early Brain Development

508

Neuronal differentiation and myelination 508

The development of neural connections 510

Linking Brain and Cognitive Development

511

Brain size and the evolution of cognition 514

Relative brain size and cerebral complexity 516

Evolution of Brain Development

520

Evolutionary Specializations of Brain and Behavior

522

Evolution and development of learning and memory 523

Evolution and development of quantitative cognition 526
Evolution and development of social cognition 529
Evolution 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

APPENDIX
The Human Nervous System

xvii

539

Cellular Components of the Nervous System

Nerve Cells and Their Signaling Functions

539

540

Functional Organization of the Human Nervous System

543

Neural circuits 543

Neural systems 545

Structural Organization of the Human Nervous System 547

Major Subdivisions of the Central Nervous System

549

The brainstem 550

The spinal cord 550
Surface features of the brain 552
Internal features of the brain 557
The ventricular system 561

The Brains 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
Index

583

591

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