The Hippocampus Book (Oxford Neuroscience Series)

Cover\r......Page 1
The Hippocampus Book......Page 4
Copyright\r......Page 5
Dedication\r......Page 6
Preface\r......Page 8
Acknowledgments......Page 10
Contents......Page 12
Contributors......Page 20
1.1 Overview......Page 24
1.2 Why Study the Hippocampal Formation on its Own?......Page 25
1.3 Defining the Contemporary Era......Page 26
1.4 Organization and Content of the Book......Page 27
2.2.1 A Famous Dispute About the Significance of the Hippocampus......Page 30
2.3.1 The Hippocampal Formation and Olfactory Function......Page 31
2.3.2 The Hippocampal Formation and Emotion......Page 32
2.3.3 The Hippocampal Formation and Attention Control......Page 33
2.3.5 More Direct Evidence for Hippocampal Involvement in Memory......Page 34
2.4 Special Features of Hippocampal Anatomy and Neurobiology......Page 37
2.4.1 Early Neuroanatomical Studies of the Hippocampus......Page 38
2.4.3 New Anatomical Techniques that Revolutionized Connectivity Studies......Page 39
2.4.5 New Tracing Studies Using Axonal Transport......Page 41
2.4.7 Hippocampal Synapses Are Highly Plastic: Early Studies of Sprouting......Page 42
2.4.10 Development of Hippocampal Slices: From Seahorse to Workhorse......Page 43
2.5.2 Gray Type 2 Synapses are Inhibitory and are Located on the Soma of Pyramidal and Granule Cells......Page 44
2.5.4 Long-lasting Alterations of Synaptic Efficiency After Physiological Stimulation......Page 45
2.5.6 Studies of Epileptiform Behavior......Page 46
2.6.2 Pioneers of Intracellular Recording......Page 47
2.6.4 Field Potential Analysis......Page 48
2.6.6 Pharmacological Analysis of Cellular Properties......Page 51
References......Page 52
3.1.2 Similarities and Differences Between the Hippocampal Formation and other Cortical Areas......Page 58
3.1.3 Hippocampal Formation: With A Unique Set of Unidirectional, Excitatory Pathways......Page 59
3.2 Historical Overview of Hippocampal Nomenclature – What’s in a Name?......Page 60
3.2.2 Subdivision of Hippocampal Areas......Page 63
3.3.1 Rat Hippocampal Formation......Page 65
3.3.2 Major Fiber Systems of the Rat Hippocampal Formation......Page 68
3.3.3 Monkey Hippocampal Formation......Page 69
3.3.4 Human Hippocampal Formation......Page 70
3.4 Neuroanatomy of the Rat Hippocampal Formation......Page 72
3.4.1 Dentate Gyrus......Page 76
3.4.2 Hippocampus......Page 88
3.4.3 Subiculum......Page 97
3.4.4 Presubiculum and Parasubiculum......Page 102
3.4.5 Entorhinal Cortex......Page 104
3.5.1 Transmitters and Receptors......Page 115
3.6 Comparative Neuroanatomy of the Rat, Monkey, and Human Hippocampal Formation......Page 116
3.6.2 Comparison of Rat and Monkey Hippocampal Formation......Page 117
3.6.3 Comparison of Monkey and Human Hippocampal Formation......Page 125
3.7.2 Functional Implications of the Septotemporal Topography of Connections......Page 128
3.7.3 Functional Implications of the Transverse Topography of Connections......Page 129
3.8 Conclusions......Page 130
References......Page 131
4.2 Neurogenesis and Cell Migration......Page 136
4.2.2 Granule Cells......Page 137
4.2.3 Local Circuit Neurons and Hilar Neurons......Page 139
4.3 Development of Hippocampal Connections......Page 141
4.3.1 Entorhinal Connections......Page 142
4.3.2 Commissural Connections......Page 144
4.3.3 Septal Connections......Page 146
4.3.4 General Principles Underlying the Formation of Synaptic Connections in the Hippocampus......Page 147
4.4.2 Neuronal Differentiation......Page 148
References......Page 149
5.2 CA1 Pyramidal Neurons......Page 154
5.2.1 Dendritic Morphology......Page 155
5.2.2 Dendritic Spines and Synapses......Page 157
5.2.3 Excitatory and Inhibitory Synaptic Inputs......Page 158
5.2.4 Axon Morphology and Synaptic Targets......Page 159
5.2.5 Resting Potential and Action Potential Firing Properties......Page 160
5.2.6 Resting Membrane Properties......Page 162
5.2.9 Mechanisms of Compensation for Synaptic Attenuation in CA1 Dendrites......Page 165
5.2.10 Pyramidal Neuron Function: Passive Versus Active Dendrites......Page 166
5.2.11 Dendritic Excitability and Voltage-Gated Channels in CA1 Neurons......Page 167
5.2.12 Sources of CA[Sup(2+)]  Elevation in CA1 Pyramidal Neuron Dendrites......Page 169
5.2.13 Distribution of Voltage-Gated Channels in the Dendrites of CA1 Neurons......Page 170
5.2.15 General Lessons Regarding Pyramidal Neuron Function......Page 173
5.3 CA3 Pyramidal Neurons......Page 174
5.3.1 Dendritic Morphology......Page 175
5.3.3 Excitatory and Inhibitory Synaptic Inputs......Page 176
5.3.5 Resting Potential and Action Potential Firing Properties......Page 177
5.3.7 Active Properties of CA3 Dendrites......Page 179
5.4.2 Dendritic Spines and Synaptic Inputs......Page 180
5.4.4 Resting and Active Properties......Page 181
5.5 Dentate Granule Neurons......Page 183
5.5.2 Excitatory and Inhibitory Synaptic Inputs......Page 184
5.5.4 Resting Potential and Action Potential Firing Properties......Page 185
5.5.5 Resting Membrane Properties......Page 186
5.6 Mossy Cells in the Hilus......Page 187
5.6.5 Other Spiny Neurons in the Hilus......Page 189
5.7 Pyramidal and Nonpyramidal Neurons of Entorhinal Cortex......Page 190
5.7.1 Stellate Cells of Layer II......Page 191
5.7.3 Pyramidal Cells of Layer III......Page 193
5.7.4 Pyramidal Cells of Deep Layers......Page 195
5.9 Local Circuit Inhibitory Interneurons......Page 197
5.9.1 Understanding Interneuron Diversity......Page 200
5.9.2 Dendritic Morphology......Page 202
5.9.3 Dendritic Spines......Page 204
5.9.4 Excitatory and Inhibitory Synapses......Page 205
5.9.5 Axon Morphology and Synaptic Targets......Page 206
5.9.7 Voltage-Gated Channels in Inhibitory Interneurons......Page 207
References......Page 209
6.1 Overview......Page 224
6.2 General Features of Synaptic Transmission: Structure......Page 225
6.2.1 Transmitter Release and Diffusion......Page 226
6.2.2 Receptors and Receptor Activation......Page 228
6.2.3 Quantal Transmission......Page 230
6.2.4 Short-term Plasticity......Page 231
6.3 Glutamatergic Synaptic Transmission......Page 232
6.3.1 AMPA Receptors......Page 234
6.3.3 NMDA Receptors......Page 236
6.3.5 Metabotropic Glutamate Receptors......Page 237
6.4.1 GABA[Sub(A)] Receptors......Page 239
6.5 Other Neurotransmitters......Page 241
6.6 Special Features of Individual Hippocampal Synapses......Page 243
6.6.1 Small Excitatory Spine Synapses......Page 244
6.6.2 Mossy Fiber Synapses......Page 247
6.6.3 Other Glutamatergic Synapses on Interneurons......Page 249
6.6.4 Inhibitory Synapses......Page 250
References......Page 252
7.2.1 Introduction: Proteins Involved in Synaptic Release......Page 264
7.2.3 Synaptic Vesicle Docking and Priming at the Active Zone: Role of the SNARE Complex, Munc18, and Munc13......Page 265
7.2.4 Ca[Sup(2+)] -triggered Synaptic Release: Role of Synaptotagmin......Page 267
7.2.5 Ca[Sup(2+)] -triggered Synaptic Release: Role of Rab3A and RIM1......Page 268
7.2.7 Synaptic Vesicle Endocytosis, Recycling, and Refilling......Page 269
7.3.1 Introduction: Ionotropic and Metabotropic Receptors......Page 270
7.3.2 AMPA Receptors......Page 272
7.3.3 NMDA Receptors......Page 274
7.3.4 Kainate Receptors......Page 275
7.3.5 Metabotropic Glutamate Receptors......Page 278
7.4 Trafficking of Glutamate Receptors and Hippocampal Synaptic Plasticity......Page 279
7.4.1 Synaptic Transport of AMPA Receptors in LTP and LTD......Page 280
7.4.2 NMDA Receptor-associated Cytoskeletal and Signaling Proteins......Page 282
7.5.1 Introduction: Building of Hippocampus-speci Genetic Models......Page 284
7.5.2 NMDA Receptor Mutant Mice......Page 285
7.5.3 AMPA Receptor Mutant Mice......Page 290
7.5.4 Kainate Receptor Mutant Mice......Page 293
7.5.6 Synopsis of the Section......Page 294
7.6.2 GABA[Sub(A)] Receptors......Page 295
7.6.3 GABA[Sub(B)] Receptors......Page 301
7.7.2 Role of Dystrophin-associated Protein Complex in GABA[Sub(A)] Receptor Function......Page 303
7.8.1 GABA[Sub(A)] Receptor Mutant Mice......Page 304
7.9.1 Introduction: Muscarinic and Nicotinic Receptors......Page 305
7.9.3 Hippocampal Nicotinic Receptors......Page 306
References......Page 307
8.1.1 Neuronal Classification Issues......Page 318
8.1.2 Input Specificity of Extrinsic Afferents......Page 319
8.1.5 Circuit Specific Receptor Distribution......Page 320
8.2.1 Inputs to the Dentate Gyrus......Page 322
8.2.2 Granule Cell Projection to Area CA3......Page 323
8.2.4 Interneuron – Granule Cell Connections......Page 324
8.3.1 Inputs to CA3 and CA1......Page 326
8.3.2 Pyramidal Cell – Interneuron Connections......Page 327
8.3.3 Interneuron – Pyramidal Cell Connections......Page 328
8.3.5 Interneuron – Interneuron Connections......Page 333
8.3.6 Gap Junction Connections......Page 334
8.4 Summary......Page 335
References......Page 336
9.2.1 Naturally Occurring Structural Plasticity......Page 342
9.2.3 Experience and Dendritic Architecture......Page 343
9.2.4 Structural Plasticity Following Damage......Page 344
9.3 Adult Neurogenesis......Page 345
9.3.2 Hormones and Adult Neurogenesis......Page 347
9.3.3 Experience and Adult Neurogenesis......Page 349
9.3.4 Neurogenesis Following Damage......Page 352
9.4.1 A Possible Role in Learning?......Page 353
9.4.2 A Possible Role in Endocrine Regulations?......Page 355
References......Page 356
10.1 Overview......Page 364
10.1.1 LTP: The First Two Decades......Page 365
10.2.2 Single Stimuli in Hippocampal Pathways Produce Two Transient Aftereffects: Facilitation and Depression......Page 368
10.3.1 Long-term Potentiation: Tetanic Stimulation Induces a Persistent Increase in Synaptic Efficacy......Page 371
10.3.3 Three Distinct Temporal Components of Potentiation: STP, Early LTP, Late LTP......Page 374
10.3.4 Input-Specificity of LTP: Potentiation Occurs Only at Active Synapses......Page 375
10.3.5 Associativity: Induction of LTP Is Influenced by Activity at Other Synapses......Page 376
10.3.6 Requirement for Tight Coincidence of Presynaptic and Postsynaptic Activity Implies a Hebbian Induction Rule......Page 377
10.3.7 Molecular Basis for the Hebbian Induction Rule: Voltage Dependence of the NMDA Receptor Explains Cooperativity, Input Specificity, and Associativity......Page 378
10.3.8 Spike Timing-dependent Plasticity (STDP)......Page 379
10.3.9 Ca[Sup(2+)]  Signaling in LTP......Page 380
10.3.10 Metabotropic Glutamate Receptors Contribute to Induction of NMDA Receptor-dependent LTP......Page 381
10.3.11 Role of GABA Receptors in the Induction of NMDAR-dependent LTP......Page 382
10.3.12 E-S Potentiation: A Component of LTP That Reflects Enhanced Coupling Between Synaptic Drive and Cell Firing......Page 383
10.3.13 Metaplasticity: The Magnitude and Direction of Activity-dependent Changes in Synaptic Weight Are Influenced by Prior Activity......Page 385
10.3.14 Synaptic Scaling and Long-term Changes in Intrinsic Excitability......Page 389
10.4.3 Early LTP Involves Multiple Protein Kinasedependent Mechanisms......Page 390
10.4.4 Site of Expression of Early LTP: Experimental Approaches......Page 395
10.4.5 E-LTP: Presynaptic Mechanisms of Expression......Page 397
10.4.6 E-LTP: Postsynaptic Mechanisms of Expression......Page 398
10.4.7 Retrograde Signaling System Is Required for Communication Between the Postsynaptic Site of Induction and the Presynaptic Terminal......Page 404
10.4.8 Membrane Spanning Molecules Contribute to Signaling Between Presynaptic and Postsynaptic Sides of the Synapse......Page 405
10.4.9 Late LTP: Persistent Potentiation Requires Gene Transcription and Protein Synthesis......Page 407
10.4.10 Structural Remodeling and Growth of Spines Can Be Stimulated by Induction of LTP......Page 414
10.5.3 Induction Mechanisms of Mossy Fiber LTP......Page 419
10.5.4 Expression of Mossy Fiber LTP Is Presynaptic......Page 422
10.5.5 E-LTP and L-LTP at Mossy Fiber Synapses Can Be Distinguished by the Effects of Protein Synthesis Inhibitors......Page 423
10.6.1 Modulation by Other Neurotransmitters and Neuromodulators......Page 424
10.6.2 Cyclical Influences Modulate Induction of LTP......Page 427
10.7.1 Overview......Page 428
10.7.2 NMDAR-dependent LTD: Properties and Characteristics......Page 429
10.7.3 NMDAR-dependent LTD: Induction Mechanisms......Page 431
10.7.4 NMDAR-dependent LTD: Expression Mechanisms......Page 433
10.7.5 mGluR-dependent LTD......Page 435
10.7.6 Homosynaptic Depotentiation......Page 437
10.7.7 Heterosynaptic LTD and Depotentiation: Activity in One Input Can Induce LTD in Another......Page 438
10.7.8 LTD and Depotentiation at Mossy Fiber – CA3 Pyramidal Cell Synapse......Page 440
10.8.1 LTP and LTD at Glutamatergic Synapses on Interneurons......Page 441
10.9.1 Hippocampal Synaptic Plasticity During Development......Page 443
10.9.2 Synaptic Plasticity and the Aging Hippocampus......Page 444
10.9.3 Animal Models of Cognitive Decline......Page 446
10.10.1 Synaptic Plasticity and Memory Hypothesis......Page 448
10.10.2 Detectability: Is Learning Associated with the Induction of LTP?......Page 450
10.10.3 Anterograde Alteration: Do Manipulations That Block the Induction or Expression of Synaptic Plasticity Impair Learning?......Page 453
10.10.4 Retrograde Alteration: Does Further Induction or Reversal of LTP Cause Forgetting?......Page 462
10.10.6 Synaptic Plasticity, Learning, and Memory: The Story So Far......Page 464
References......Page 465
11.1 Overview......Page 496
11.2.2 Each EEG Pattern Has Distinct Behavioral Correlates......Page 498
11.3.1 Hippocampal Theta Activity: Historical Overview......Page 500
11.3.3 Both Types of Theta Activity Are Dependent on the Medial Septal/DBB but Only t-Theta Is Dependent on the Entorhinal Cortex......Page 501
11.3.7 Theta Activity in Nonhippocampal Areas......Page 502
11.3.9 Functions of Theta......Page 503
11.4.1 Sharp Waves, Ripples, and Single Units During Large Irregular Activity......Page 504
11.4.4 Behavioral Correlates and Functions of LIA......Page 505
11.4.7 Olfactory Stimulation Can Elicit Hippocampal Gamma and Beta Waves......Page 506
11.5 Single-cell Recording in the Hippocampal Formation Reveals Two Major Classes of Units: Principal Cells and Theta Cells......Page 507
11.5.1 Distinctive Spatial Cells – Complex-spike Place Cells, Head-direction Cells, and Grid Cells – Are Found in Various Regions of the Hippocampal Formation......Page 508
11.6.3 Hippocampal Theta Cells Have Behavioral Correlates Similar to Those of the Hippocampal EEG......Page 511
11.7.1 Place Cells Signal the Animal’s Location in an Environment......Page 512
11.7.2 Basic Properties of Place Fields......Page 513
11.7.3 Place Fields are Nondirectional in Unrestricted Open-field Environments but Directional When Behavior is Restricted to Routes......Page 516
11.7.4 What Proportion of Complex-spike Cells Are Place Cells?......Page 518
11.7.5 Frame of Reference of Place Fields......Page 519
11.7.6 Place Fields Can Be Controlled by Exteroceptive Sensory Cues......Page 520
11.7.7 Idiothetic Cues Can Control Place Fields......Page 523
11.7.8 Are Place Cells Influenced by Goals, Rewards, or Punishments?......Page 525
11.7.9 Temporal Patterns of Place Cell Firing......Page 526
11.7.10 Place Fields in Young and Aged Animals......Page 528
11.7.11 Hippocampal Place Cell Firing Is In.uenced by Other Areas of the Brain......Page 530
11.7.12 Primate Hippocampal Units also Exhibit Spatial Responses......Page 531
11.8 Place Cells Are Memory Cells......Page 532
11.8.2 Place Field Plasticity During Unidirectional Locomotion......Page 533
11.8.3 Cue Control over Hippocampal Place Cells Can Change as a Function of Experience......Page 534
11.8.4 Control of the Angular Orientation of Place Cells in a Symmetrical Environment Can Be Altered by the Animal’s Experience of Cue Instability......Page 535
11.8.6 NMDA Receptor Confers Mnemonic Properties on Place Cell Firing......Page 537
11.9 Head Direction Cells......Page 538
11.9.1 Head Direction Cells are Controlled by Distal Sensory Cues......Page 539
11.9.3 Head Direction Cells Can also Be Controlled by Idiothetic Cues......Page 540
11.9.4 Head Direction Cells Are Found in Different Anatomically Connected Brain Areas......Page 541
11.10 Interactions Between Hippocampal Place Cells and Head Direction Cells......Page 542
11.11.1 Hippocampal Cells Have Been Implicated in the Processing of Nonspatial Sensory Information......Page 544
11.11.3 Hippocampal Unit Activity During Aversive Classical Conditioning......Page 545
11.11.4 Nictitating Membrane Conditioning in the Rabbit: Role of Theta......Page 546
11.11.5 Single-unit Recording in the Hippocampus During Nictitating Membrane Conditioning of Rabbits......Page 547
11.11.6 Hippocampal Unit Recording During Operant Tasks......Page 549
11.11.7 Comparison of Hippocampal Cells During Operant Conditioning and Place Tasks in Rats......Page 553
11.11.9 Hippocampal Units During Nonspatial Learning in Humans......Page 554
11.12 Other Distinctive Cells in the Hippocampal Formation and Related Areas......Page 555
11.12.1 Subicular Region Has Fewer Place Cells than the Hippocampus Proper, and Their Properties Differ......Page 556
11.12.2 Presubiculum Contains Several Classes of Spatial Cell......Page 557
11.12.5 Cells in the Perirhinal Cortex Code for the Familiarity of Stimuli......Page 558
11.13 Overall Conclusions......Page 559
References......Page 561
12.1 Overview......Page 570
12.2 Patient H.M.......Page 571
12.3.1 Behavioral Tasks and Terms......Page 573
12.3.2 Behavioral Measures......Page 574
12.3.3 Anoxia and Bilateral Hippocampal Lesions......Page 575
12.3.4 Depth Electrode Recordings......Page 577
12.3.5 Neuroimaging......Page 578
12.3.6 Technical Challenge: Alignment of MTL Regions Across Participants......Page 580
12.4.1 Explicit Versus Implicit......Page 582
12.4.2 Encoding Versus Retrieval......Page 585
12.4.3 Time-limited Role in Declarative Memory......Page 586
12.4.4 Spatial Memory......Page 588
12.4.5 Associations, Recollections, Episodes, or Sources......Page 590
12.5 Conclusions......Page 594
References......Page 596
13.1 Overview......Page 602
13.2.1 Value of Interventional Studies to Identify Function......Page 603
13.2.2 Lesions, Functional Hypotheses, and Behavioral Tasks......Page 604
13.2.3 Contemporary Lesion Techniques: Pharmacological and Genetic Interventions......Page 606
13.2.4 Biological Continuity of Hippocampal Function......Page 609
13.3.1 Outline of the Theory......Page 612
13.3.2 Development of a Primate Model of Amnesia......Page 617
13.3.3 Domains of Preserved Learning Following Medial Temporal Lobe Lesions in Primates......Page 622
13.3.4 Selective Lesions of Distinct Components of the Medial-temporal Lobe Reveal Heterogeneity of Function......Page 623
13.3.5 Remote Memory, Retrograde Amnesia, and the Time Course of Memory Consolidation in Primates......Page 627
13.3.6 Critique......Page 629
13.4 Hippocampus and Space: Cognitive Map Theory of Hippocampal Function......Page 638
13.4.1 Outline of the Theory......Page 639
13.4.2 Representing Spatial Information, Locale Processing, and the Hippocampal Formation......Page 644
13.4.3 Using Spatial Information: Spatial Navigation and the Hippocampal Formation......Page 648
13.4.4 Comparative Studies of Spatial Memory and the Distinction Between Spatial and Associative Learning......Page 661
13.4.5 Storage and Consolidation of Spatial Memory......Page 671
13.4.6 Critique......Page 675
13.5 Predictable Ambiguity: Con.gural, Relational, and Contextual Theories of Hippocampal Function......Page 677
13.5.1 Configural Association Theory......Page 679
13.5.2 Relational Processing Theory: Refinement of the Declarative Memory Theory......Page 683
13.5.3 Contextual Encoding and Retrieval......Page 689
13.5.4. Critique......Page 697
13.6.1 Concept of Episodic Memory......Page 698
13.6.2 Scene Memory as a Basis for Episodic Memory and Top-down Control by the Prefrontal Cortex......Page 700
13.6.3 What, Where, and When: Studies of Food-caching and Sequence Learning......Page 703
13.6.4 Problem of Awareness......Page 707
13.6.5 Elements of a Neurobiological Theory of the Role of the Hippocampus in Episodic-like Memory......Page 708
References......Page 715
14.2 Introduction......Page 736
14.3.1 Representing Spatial Location and Orientation: Data......Page 737
14.3.2 Representing Spatial Location: Feedforward Models......Page 740
14.3.3 Representing Spatial Location and Orientation: Feedback Models......Page 742
14.3.4 Modeling Phase Coding in Place Cells......Page 748
14.4.2 Spatial Navigation: Feedforward Models......Page 750
14.4.3 Spatial Navigation: Feedback Models......Page 753
14.5.1 Hippocampus and Memory: Data......Page 754
14.5.3 Associative Memory and the Hippocampus......Page 755
14.5.4 Hippocampal Representation, Context, and Novelty......Page 758
14.5.5 Consolidation and Cross-modal Binding of Events in Memory......Page 759
14.5.6 Hippocampal Contributions to Various Types of Memory and Retrieval......Page 760
14.6 Reconciling the Hippocampal Roles in Memory and Space......Page 761
References......Page 765
15.1 Overview......Page 772
15.2.1 Glucocorticoid Receptors Are Present in the Animal and Human Hippocampus......Page 774
15.2.2 There is an Inverted U-Shape Function Between Level of Stress and Memory......Page 775
15.2.3 Stress Modulates Intrinsic Hippocampal Excitability and Activity-dependent Synaptic Plasticity Associated with Learning and Memory......Page 777
15.3.2 Stress or Stress Hormones Can Impair Neurogenesis in the Hippocampus......Page 780
15.3.3 Fetal Programming of GC Regulation......Page 781
15.4 Other Higher Brain Structures Implicated in Stress and Their Interaction with the Hippocampus......Page 782
15.5 How the Hippocampus Orchestrates Behavioral Responses to Arousing Aversive Experiences......Page 783
References......Page 785
16.1 Overview......Page 790
16.2.1 Introduction......Page 791
16.2.2 Clinical Features......Page 792
16.2.3 Etiology......Page 795
16.2.4 Pathophysiology......Page 798
16.3.2 Clinical Features......Page 810
16.3.3 Genetics......Page 816
16.3.4 Pathophysiology......Page 817
16.3.5 Treatment Options......Page 822
References......Page 824
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