Principles of Learning and Memory Edited by Rainer H. Kluwe, Gerd Liier and Frank Răsler

Springer Basel AG

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Prof. DT. RaincT II. Kluwc InSlitut fur Kognitionsforschung Uni\'ersilat der Bundcswchr Holstcnhofweg 8S 0 - 22043 lIamburg

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Short List of Contents

Short List of Contents v

Contents vii

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. xiii

A FORMATION OF MEMORIES 1

1 The Principle of Contiguity 3

2 The Principle of Learning Based on Multiple Brain Structures 15

3 The Principles of Brain Plasticity 27

4 The Principle of Emotional Learning 51

B ORGANIZATION OF MEMORIES 69

5 The Principle of Code-Specific Memory Representations 71

6 The Principle of Multiple Memory Systems 93

7 Modules of Working Memory 113

C CONSOLIDATION OF MEMORIES 135

8 The Principle of Memory Consolidation and Its Pharmacological Modulation 137

9 The Principle of Cross-Cortical Consolidation of Declarative Memories 155

10 The Principle of Bottleneck Structures 171

D CONTROL OF MEMORIES 185

11 The Principle of Controlling Neuronal Dynamics in Neocortex: Rapid Reorganization

and Consolidation of Neuronal Assemblies 187

12 The Principle of Inhibition 207

13 Towards Principles of Executive Control: How Mental Sets are Selected 223

E ADAPTIVE SPECIALIZATION OF MEMORIES 241

14 The Principle of Species Independent Learning Phenomena 243

15 The Principle of Adaptive Specialization as It Applies to Learning and Memory 259

References 281

Name Index 337

Subject Index 349

List of Contributors 357

Contents

Short List of Contents vContents viiPreface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. xiii

A FORMATION OFMEMORIES 1

1 The Principle of Contiguity 3Harald Lachnit

Historical Antecedents: Philosophical Roots and Early Psychology 3Empirical Departures from the Omnipotent Law of Contiguity 4Theoretical Attempts to Retain the Law of Contiguity 5Further Empirical Challenges to the Law of Contiguity 6Competition Protects the Principle of Contiguity 7Contiguity of Memory Traces 9Back to the Significance of Contiguity for Learning 10The Behavioral Expression of an Association Needs More Than Contiguity IIRenouncing Contiguity in Favor of Time and Rate? 13

2 The Principle of Learning Based on Multiple Brain Structures 15Thomas Kress and Irene Daum

Classical conditioning as a Model System in the Neurobiology of Learning 15Neuroanatomical Basis of Delay Conditioning 17The Role of the Hippocampus 17The Role of the Cerebellum 18The Role of the Basal Ganglia 21

Brain Substrates of Complex Conditioning 22Cerebellar-Hippocampal Interactions 22Neuropsychological Studies in Patients with Damage to the Hippocampal System 23Cerebellar - Prefrontal Interactions 24

Recent Developments 26Conclusion 26

3 The Principles of Brain Plasticity 27Brigitte Roder & Frank Rosier

Training-Induced Plasticity 27Somatosensory System 28Auditory System 31Visual System 32Motor System 33Effects of enriched environments 34Mechanisms 34

Lesion-Induced Plasticity 35Intramodal Plasticity after Partial Deafferentiation 36

VIII Contents

Intermodal Plasticity after Totally Deafferenting One Sensory System 42Differences between Developmental and Adult Plasticity 48

4 The Principle of Emotional Learning 51Gerhard Roth

Studies on the Interaction between Memory and Emotional States 51The Memory System Inside the Brain 53What are Emotions and Where do they Originate in the Brain? 57The Neuronal Basis of Interaction between Memory and Emotion 61The Role of Stress on Memory 63Cellular Mechanisms of the Interaction between Memory and Emotions 64Conclusion 68

B ORGANIZAnON OF MEMORIES 69

5 The Principle of Code-Specific Memory Representations 71Frank Rtjsler and Martin Reil

Empirical Foundations 71Theoretical Foundations 73Findings from Brain Imaging Studies 76Spatial and Verbal Working Memory 77Spatial and Object Working Memory 83Long-term Memory for Verbal, Spatial, Color, and Motor Associations 84Category-specific Representations 88

Conclusion 91

6 The Principle of Multiple Memory Systems 93Axel Buchner and Martin Brandt

Distinct Memory Systems 94Levels of Distinction 94

Working Memory 96Modular Working Memory 96Working Memory as Activated Memory 98A Formal Model of Working Memory: The Feature Model 99Sununary ofWorking Memory Models 100

Long-Term Memory 100Declarative versus Non-declarative Memory 100Explicit versus Implicit Memory Measurement 103Episodic versus Semantic Memory 105Global Memory Models 107

Conclusion: Limits of the Principle of Multiple Memory Systems III

7 Modules of Working Memory 113John Jonides, Ching-Yune C. Sylvester, Steven C. Lacey, Tor D. Wager,Thomas E. Nichols, and Edward A wh

Verbal versus Spatial Storage 115Rehearsal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118

Contents IX

Executive Mechanisms 126

Conclusion 133

C CONSOLIDATION OF MEMORIES 135

8 The Principle of Memory Consolidation and Its Pharmacological Modulation 137Rainer K. W. Schwarting

The Consolidation Hypothesis and Its Origins 137Experimental Procedures for Post-Trial Designs 138

Inhibitory Avoidance 139Habituation of Exploration and Other Designs 140Specific Aspects of Post-Trial Designs 141

Pharmacological Manipulations of Consolidation 142An Example for a Pharmacological Post-Trial Approach: Cholinergic Manipulations

in the Nucleus Accumbens of the Laboratory Rat 144Brief Anatomy of the Nucleus Accumbens 144Transmitters in the Nucleus Accumbens 144Cholinergic Activity in the Nucleus Accumbens 146Evidence for a Role of the Nucleus Accumbens in Mnestic Processes 146Post-Trial Manipulations of Cholinergic Function in the NAcc: 147Discussion 149

Conclusion 153

9 The Principle of Cross-Cortical Consolidation of Declarative Memories 155Ken A. Paller

Declarative Memory and Amnesia 156

Defining Declarative Memory 156A Neural Feature of Declarative Memory: Cross-Cortical Consolidation 158Another Neural Feature of Declarative Memory: Coherence Ensembles 159Retrograde Amnesia, Ongoing Hippocampal Contributions, and Sleep 160Beyond Declarative Memory: Questions of Definition 162

Declarative Memory and Conscious Recollection 163Neuroimaging and Declarative Memory 164Conclusion 168

10 The Principle of Bottleneck Structures 171Matthias Brand and Hans J. Markowitsch

Classification of Memory 171Amnesic Syndromes 172Medial Temporal Lobe Amnesia 172Medial diencephalic amnesia 174Basal Forebrain Amnesia 175Amygdala Damage and Memory 175Damage of Non Limbic Structures and Amnesia 176Psychogenic and Functional Amnesia 177

Anatomical Bases of Memory 178Encoding and Consolidation 179

x Contents

Storage of Information 181Retrieval of Information 182

Conclusion 183

D CONTROL OF MEMORIES 185

11 The Principle of Controlling Neuronal Dynamics in Neocortex: Rapid Reorganizationand Consolidation of Neuronal Assemblies 187

Matthias H. J. Munk

Problems in Understanding Cortical Information Processing 188Features of the Cortical Wetware 191Dynamical Organization of Large Neuronal Populations: Synchronisation of Oscillationsin the Ganuna-Frequency Band 194

Mechanisms and Putative Functions of Gamma Oscillations 198Adaptivity versus Consolidation 202Conclusion 204

12 The Principle of Inhibition 207Dale Dagenbach and Aycia K. Kubat-Silman

What Constitutes Inhibition? 208Generalized Inhibitory Theories 209Problems for Generalized Inhibitory Accounts 210

Inhibition and Working Memory 212The Inhibition-Resource Model 213Attention, Inhibition, and Working Memory 213Backward Inhibition in Working Memory 214

Inhibition and Long Term Memory 215Inhibition in Episodic Memory 215Inhibition in Semantic Memory 216

The Neural Correlates of Inhibition 218Conclusion 220

13 Towards Principles of Executive Control: How Mental Sets are Selected 223Ulrich Mayr

Towards Principles of Executive Control: How Mental Sets are Selected 223The Task-Switching Paradigm: Basic Issues and Findings 225Selection of Simple Actions versus Selection of Sets 225Preparation of Mental Set and Residual Switch Costs 226Switch Costs versus Global Selection Costs 228Response Conflict 229Verbal Processing and Selection of Sets 229The Role of Task-Set Inhibition 230

Mental Sets, Working Memory and Long-Term Memory 231Working Memory as the Selection Device 231The Role of Long-Term-Memory Retrieval 232The Retrieval-Structure View of Task-Set Selection 233Selection of Sets and Representational Coherence 236

Contents XI

Representational Coherence 237Neurocognitive Implementation of Representational Coherence 237Representational Coherence and the Retrieval-View of Task Switching 238

Conclusion 240

E ADAPTIVE SPECIALIZATION OF MEMORIES 241

14 The Principle of Species Independent Learning Phenomena 243Qnur Giintiirkiin and Daniel Durstewitz

The Power of General Process Learning Theory 245Cellular Basis of Association Learning 246The Evolutionary Diversity of Learning 250Constraints on Learning in Pigeons 252The Neural Basis of Learning Constraints 255

15 The Principle of Adaptive Specialization as It Applies to Learning and Memory 259Charles R. Gallistel

Adaptive Specialization in the Memory Mechanism 259Thermodynarnic Stability 260High Density 261Information is Information 262Coding 263

Adaptive Specialization in Learning Processes 265Learning Current Location 265Learning the Solar Ephemeris 267Learning a Language 269Conditioning 270

Conclusion 278

References 281Name Index 337

Subject Index 349

List of Contributors 357

Preface

"How the brain enables the mind is the question to be answered in the twenty-first century ..."(Gazzaniga, 1998, p. xii). This question is at the core of research on human learning and memory.Whereas previous attempts at addressing Gazzaniga's "grand question" have focused solely onpsychological processes, researchers are now calling for interdisciplinary work that bridges theareas cognitive psychology, cognitive neuroscience, cognitive neuropsychology, neuroanatomy,physiology and biology. This volume reviews the recent research on human learning andmemory. Our goal is to provide an overview of the exciting incites provided by researchinvestigations that meld multiple research methodologies and domains.

Research on learning and memory is performed at different levels of analysis rangingfrom the cell to observable behavior. The breadth of research methodologies raises the challengeof integrating the different approaches. In order to answer questions about the brain structuresand systems that enable human cognitive activity, it is necessary to relate approaches and resultsfrom experimental psychology to those provided by biology, neuroanatomy, or neuroscience. Theformer are concerned with the systems level of behavior, the latter with more elementary levelsof neurons and neuronal networks. It is only through a synthesis of the disciplines that cover thewhole hierarchy of analysis, that researchers can develop a better understanding of the system,its components, its constituting elements, and, last but not least, its interaction with theenvironment

The emphasis of the chapters in this volume is on the interconnections between the levelof behavior and the level of neural activities and structures. The goal is to overcome thetraditional borders separating different fields of research in order to present an integrated patternof results that enables a broader, interdisciplinary view and a deeper understanding of humanlearning and memory. The volume thus presents an interdisciplinary synthesis of current researchconnecting cognitive science and neuroscience.

The large amount of research and the broad range of phenomena require us to focus onselected topics. We selected phenomena that are central to human learning and memory, and thatare studied from different perspectives in cognitive psychology, in neuroscience, and in biology.By analyzing the literature fifteen principles were delineated which seem to be most central forresearch on learning and memory and which are currently being investigated through aninterdisciplinary approach. These principles can be subsumed under five main themes: (A)Formation of memories; (B) Organization of memories during encoding, storage and retrieval;(C) Consolidation of memories; (D) Control of memories during information processing; and (E)Adaptive specialization of memories.

XIV Preface

A. Formation ofmemories: The human cognitive system is able to learn and to change,to improve and to adapt performance based on experience and changes in the environment. Howdoes the brain enable learning and memory? The first four chapters by Lachnit, by Kress andDaum, by Roder and Rosier, and by Roth focus on the mechanisms and underlying brainstructures that participate in the formation of new memories, i.e. on the processes that lead to theacquisition of knowledge. The chapters discuss results from animal and human research thatpoint to four basic principles: spatio-temporal contiguity, multiple brain structures underlyingexperience-related changes, brain plasticity, and emotional learning.

B. Organization of memories: How are processes of encoding, storage and retrievalrelated to brain structures and neural processes? Probably one of the most important insightsgained through recent research is that these processes are based on highly organized andspecialized structures of the brain (e.g., Damasio, 1989; Squire, Knowlton, & Musen, 1993).Functional modularity of the brain is now one of the key concepts of neuroscience. Dataobtained from experimental analyses of human cognitive performance as well as a theoreticalanalysis of memory phenomena suggest that specialized subsystems perform specific tasks likeencoding, storage, retrieval, and modification of information. These systems are defined bystructural and functional criteria, in particular by the type of information representation that isavailable to them. The goal of research is to identify such specialized subsystems and tounderstand their functional intricacies. This is the central issue addressed by Rosier and Heil, byBuchner and Brandt, and by Jonides, Sylvester, Lacey, Wager, Nichols and Awh. These chapterscover the principles of coding specific storage and retrieval, of multiple memory systems, andof separate systems of working memory.

C. Consolidation ofmemories: The flexible acquisition of new information is essentialfor systems that have to interact with a changing world. Equally important is the ability of thesystem to transform this new information into stable memories that can reliably guide behaviorlater. Chapters by Schwarting, by Paller, and by Brand and Markowitsch focus on themechanisms and processes that support the consolidation of newly acquired knowledge andprovide for enduring memories. These authors cover the principle of memory consolidation andits pharmacological modulation, the principle of cross-cortical consolidation of episodicmemories, and the principle of bottleneck structures necessary for consolidation and retrieval.

D. Control ofmemories: The chapters in this section all deal with the basic mechanismsof how information is represented and how information transfer is controlled in the nervoussystem. The chapter of Munk discusses the principle of transient binding in the CNS, which isa powerful, empirically based hypothesis that explains how the brain can find its equilibriumbetween two seemingly antagonistic processing modes: cortical adaptivity versus consolidation,or rapid reorganization versus the generation of stabilized representations. The principle ofinhibition is another basic mechanism, which regulates activation processes on both the neuronaland behavioral levels of memory representations. Dagenbach & Kubat-Silman review severalinhibitory mechanisms, derived from cognitive psychology, that are relevant to working memoryand long-term memory control. They relate these mechanisms to possible neural correlates.Mayr's chapter draws on recent evidence from behavioral, brain imaging, and single-cellrecording work to sketch out an integrated view of the neurocognitive basis of executive control.

Preface xv

E. Adaptive specialization ofmemories: Pinker (1997), referring to Darwin's claim thatfuture psychological research will be performed on new foundations, stated that the process ofrelating psychological and biological research has been slow except for the importantdevelopment of evolutionary psychology, as initiated by Cosmides and colleagues (e.g. Barkow,Cosmides, & Tooby, 1992). Evolutionary psychology has engendered an unusually strongcombination of approaches that includes cognitive psychology's analysis of informationprocessing and evolutionary biology's analysis of complex, adaptive behavior of species.Giintiirkiin and Durstewitz and ofGal/istel continue this fruitful collaboration in their chapters,which cover the principle of species independent learning phenomena and the principle ofadaptive specialization.

The fifteen chapters ofthis volume are based on the International Symposium on HumanLearning and Memory held in March 7-10, 2001. Speakers from the USA and Germanycontributed to the conference and agreed also to write chapters for this textbook. These scientists,leaders in their fields, were asked to discuss principles from an interdisciplinary point of view.Due to the scope of the chapters, the volume is intended as an advanced textbook for students ofthe disciplines of neuroscience and cognitive science.

The editors acknowledge the financial support provided by the German Research Society(DFG, Bonn) and the State of Lower Saxony (Hannover), which supported the internationalconference held at the Hanse Institute for Advanced Study (Delmenhorst). The hospitality of theHanse Institute is gratefully acknowledged. We are especially grateful for the generous supportof the Academy of Sciences, Gottingen, who made this volume possible. We thank the speakersand the other participating young and senior scientists for joining the conference and for shapingthe project by their lively discussions, and we thank the authors for their readiness to contributeto the volume. Special thanks go to Gale Pearce (Eugene, Oregon, USA) for examining chapterswritten by German authors as a native speaker, and finally to Adjuta Bertsch and Renate Kalk(Marburg, Germany) for accomplishing most of the work that was necessary to prepare a cameraready manuscript.

Hamburg, Gottingen, Marburg, September 2002 Rainer H. Kluwe

Gerd Li.ier

Frank RosIer