Auditory and Vestibular Efferents (eBook)

Series Preface 8
Volume Preface 10
Contents 12
Contributors 14
Chapter 1: Introduction to Efferent Systems 18
1.1 Introduction and Overview 18
1.2 Overview of the Volume 22
1.3 Comparison with Other Sensory Systems 27
1.4 Summary 28
References 29
Chapter 2: Anatomy of Olivocochlear Neurons 33
2.1 Introduction 33
2.2 OC Neurons in the Brain Stem 33
2.2.1 Distributions of Lateral vs. Medial Olivocochlear Neurons 33
2.2.2 Numbers of Neurons 36
2.2.3 Axonal Characteristics 37
2.3 Peripheral Projections 37
2.3.1 Separate Terminations of LOC and MOC Neurons 37
2.3.2 Terminations of LOC Fibers 38
2.3.3 Terminations of MOC Fibers 39
2.4 Central Branches to the Cochlear and Vestibular Nuclei 41
2.5 Neurochemistry 43
2.6 Ultrastructure of Synaptic Inputs to OC Neurons 43
2.7 Neural Pathway of the Medial Olivocochlear Reflex 45
2.7.1 Direct Reflex Pathway 45
2.7.2 Modulatory Pathways 48
2.8 Summary 48
References 49
Chapter 3: Physiology of the Medial and Lateral Olivocochlear Systems 54
3.1 Introduction 54
3.2 MOC Effects in the Cochlea: Overview 56
3.2.1 MOC Activation Increases CM 56
3.2.2 MOC Activation Decreases EP and Has Other Related Effects 57
3.3 Classic MOC Fast Effects in a Silent Background 58
3.3.1 Classic MOC Fast Effects on Basilar-Membrane Motion 58
3.3.2 Classic MOC Fast Effects on Otoacoustic Emissions 59
3.3.3 Classic MOC Fast Effects on IHC and AN Responses 62
3.4 Classic MOC Fast Effects in a Noisy Background 63
3.5 Nonclassic MOC Fast Effects in a Silent Background 65
3.5.1 Nonclassic MOC Fast Effects in the Basal Half of the Cochlea 66
3.5.2 Nonclassic MOC Fast Effects in the Apical Half of the Cochlea 67
3.6 MOC Slow Effects 69
3.7 MOC-Fiber Responses to Sound 70
3.8 MOC Acoustic Reflexes 73
3.8.1 Sound-Elicited MOC Effects on AN Fibers 73
3.8.2 Sound-Elicited MOC Effects on Otoacoustic Emissions 75
3.8.2.1 MOC Reflex Tuning 77
3.8.2.2 MOC Reflex Amplitude as a Function of Elicitor Bandwidth 78
3.8.2.3 MOC Reflex Laterality 79
3.8.2.4 MOC Reflex Strength 80
3.8.3 Descending Influences on MOC Acoustic Reflex Properties in Humans 80
3.9 MOC Function in Hearing 82
3.9.1 MOC Activity Changes the Dynamic Range of Hearing and Thereby Increases the Discriminability of Transients in Background Noise 
83 
3.9.2 MOC Activity Helps to Protect Against Acoustic Trauma 84
3.9.3 Possible Roles of MOC Activity in Attention and Learning 84
3.10 LOC Physiology and Function 85
3.10.1 LOC Effects in the Cochlea 86
3.10.2 LOC Response to Sound 86
3.10.3 LOC Function in Hearing 86
3.11 Summary and Future Directions 87
References 88
Chapter 4: Pharmacology and Neurochemistry of Olivocochlear Efferents 97
4.1 Introduction 97
4.1.1 Overview of Biochemical and Biophysical Steps in Efferent Activation 97
4.1.2 Historical Perspective of Issues in the Pharmacology of the Olivocochlear Efferents 98
4.2 Cholinergic Medial Efferent Transmission 100
4.2.1 The Medial Efferent Synapse 100
4.2.2 Events at the Efferent Terminal 101
4.2.3 ACh Metabolism 101
4.2.4 Presynaptic Cholinergic Receptors 102
4.2.5 Synaptic Facilitation of Efferent Effects 103
4.2.6 Postsynaptic Cholinergic Receptor 103
4.2.6.1 Overview 103
4.2.6.2 Pharmacology of Medial Efferent Transmission 104
4.2.6.3 Pharmacology of KCa Channels 106
4.2.6.4 Medial Efferents: In Vivo vs. In Vitro Findings 106
4.3 Other Efferent Neurotransmitters 106
4.3.1 Overview 106
4.3.2 Lateral Efferent Origins 107
4.3.3 Acetylcholine 107
4.3.4 Opioid Peptides 108
4.3.5 Calcitonin Gene-Related Peptide (CGRP) 108
4.3.6 GABA 108
4.3.7 Serotonin (5-Hydroxytryptamine) 109
4.3.8 Glycine 109
4.3.9 Dopamine 109
4.4 Summary 110
References 111
Chapter 5: Cholinergic Inhibition of Hair Cells 116
5.1 Introduction 116
5.2 Historical Background 117
5.3 Cellular Physiology 119
5.3.1 Intracellular Recordings from Hair Cells of the Fish Lateral Line 119
5.3.2 Details of Inhibitory Postsynaptic Potentials and Effect on Receptor Potentials in Turtle Hair Cells 120
5.3.3 Application of ACh to Isolated OHCs 121
5.3.4 Tight-Seal Recordings in the Mammalian Organ of Corti 124
5.3.4.1 Responses to ACh in IHCs and OHCs 124
5.3.4.2 Spontaneous and Evoked Synaptic Currents in IHCs and OHCs 125
5.3.4.3 Cholinergic Inhibition of IHC Action Potentials 125
5.4 Summary of “Two-Channel Hypothesis vs. Second-Messenger Mechanisms” 129
5.5 Determination of Molecular Components 130
5.5.1 Cloning of a9 131
5.5.2 Cloning of a10 131
5.6 Genetically Modified Mouse Models 132
5.6.1 a9 and a10 Knockouts 132
5.6.2 a9 and a10 Overexpressors 135
5.6.3 SK2 Knockout Mice 136
5.6.4 a9 Knock-in Mice 138
5.7 Summary and Conclusions 140
References 141
Chapter 6: The Efferent Vestibular System 147
6.1 Introduction 147
6.2 Afferents and Hair Cells 148
6.2.1 Afferent Discharge Properties 148
6.2.2 Hair Cells and Their Innervation 149
6.2.3 Afferent Morphology and Physiology 152
6.3 Efferents: A Historical Perspective 154
6.4 Neuroanatomical Organization of the EVS 155
6.4.1 Location of Cell Bodies and Their Dendritic Morphology 155
6.4.2 Axonal Pathways to the Periphery 157
6.4.3 Peripheral Branching Patterns 159
6.4.4 Synaptic Ultrastructure of Efferent Terminals 159
6.5 Efferent Neurotransmitters and Receptors 161
6.5.1 Acetylcholine 161
6.5.2 Adenosine 5'-Triphosphate 
162 
6.5.3 Calcitonin Gene-Related Peptide 163
6.5.4 Opioid Peptides 163
6.5.5 g-Aminobutyric Acid 163
6.5.6 Nitric Oxide 164
6.6 Afferent Responses to Electrical Activation of the EVS 165
6.6.1 Mammals 165
6.6.2 Oyster Toadfish (Opsanus tau) 168
6.6.3 Anurans (Frogs and Toads, Rana and Bufo Species) 168
6.6.4 Red-Eared Turtles (Trachemys scripta elegans) 170
6.7 Sites of Efferent Actions: Hair Cells or Afferents 171
6.8 Pharmacology of Efferent Neurotransmission 173
6.8.1 Hair-Cell Inhibition 174
6.8.2 Hair-Cell Excitation 176
6.8.3 Fast Afferent Excitation 178
6.8.4 Slow Afferent Excitation 179
6.9 Efferent Modulation of Afferent Responses to Natural Stimulation 180
6.10 Functional Studies of the EVS 181
6.10.1 Response of EVS Neurons to Natural Stimulation 181
6.10.2 Efferent-Mediated Modulation of Afferent Discharge 183
6.10.3 Possible Functions of the EVS 186
6.11 Summary 188
References 188
Chapter 7: Development of the Inner Ear Efferent System 199
7.1 Introduction 199
7.2 Central Development 202
7.3 Defects of Efferent Development Revealed Through Targeted Mutations 204
7.4 Neurochemical Development of Auditory Efferents 206
7.4.1 Cholinergic Development 206
7.5 Peripheral Development 209
7.6 Onset of Neurotransmitter-Related Expression Within Cochlea 213
7.7 Acetylcholine Receptors on Hair Cells 216
7.8 Nicotinic Synapse Formation and Maturation of ACh Receptors 217
7.9 Maturation of Efferent Connections and Efferent-Induced Hair Cell Responses 218
7.10 Efferent Connections to Vestibular hair Cells 219
7.11 Conclusion and Outlook 222
References 222
Chapter 8: Evolution of the Octavolateral Efferent System 229
8.1 Introduction 229
8.2 Anatomical Layout and Neurochemistry of the Efferent System 229
8.2.1 The Origin of Octavolateral Efferents 230
8.2.2 The Plesiomorphic Condition as Seen in Fish 231
8.2.2.1 A Small Number of Efferent Neurons Innervates a Large Number of Both Lateral-Line and Inner-Ear Hair Cells 231
8.2.2.2 Are There Any Subpopulations of Efferents? 233
8.2.2.3 Bilateral Distribution of Efferent Somata and Dendrites 234
8.2.2.4 Efferent Transmitters and Neuropeptides 236
8.2.3 The Most Derived Case: Separate Subsystems of Vestibular and Auditory Efferents of High Complexity in Mammals 236
8.2.4 An Intriguing Case with Many Similarities to Mammals: The Archosaurs (Birds and Crocodilians) 237
8.2.4.1 Separation of Auditory and Vestibular Efferents 237
8.2.4.2 Bilateral Distribution in Archosaurs (Crossed and Uncrossed Efferents) 240
8.2.4.3 Evidence for Subpopulations of Auditory Efferents 240
8.2.4.4 Tonotopic Distribution Along the Avian Basilar Papilla 244
8.2.4.5 Efferent Transmitters and Neuropeptides 244
8.2.5 When and Why Did Vestibular and Auditory Efferents Separate? 246
8.2.5.1 Amphibians 246
8.2.5.2 Turtles 247
8.2.5.3 The Lepidosauromorphs (Tuataras, Lizards, Snakes, and Amphisbaenids) 248
8.3 Function of Efferent Innervation to Hair Cells 250
8.3.1 Transferring the Efferents’ Neurochemical Heritage to Hair Cells 250
8.3.1.1 Cholinergic Inhibition 250
8.3.1.2 CGRP 251
8.3.2 Adding New Levels of Sophistication to the Auditory Efferents 253
8.3.2.1 Specializing Together with the Hair Cells: Modulating the Cochlear Amplifier 253
8.3.2.2 Modulating Afferents Instead of Hair Cells: A Mammalian Speciality? 255
8.3.2.3 Branching Out to Nonsensory Cell Types 255
8.3.3 Still an Enigma: Natural Conditions of Efferent Activity 256
8.3.3.1 Protection from Predictable Damage 256
8.3.3.2 Improving Signal Detection 258
8.3.3.3 A Role for Efferents in Auditory Development? 258
8.4 Conclusions and Outlook 259
8.4.1 A Plausible Story of Efferent Evolution 260
8.4.2 Interesting Open Questions 261
References 261
Chapter 9: Central Descending Auditory Pathways 272
9.1 Introduction 273
9.2 Overview of Central Auditory Structures and the Ascending Pathways 274
9.3 Brief Historical View of the Descending System 275
9.4 Divergent Descending Projections from Specific Auditory Regions 277
9.4.1 Projections from the Superior Olivary Complex 277
9.4.2 Projections from the Nuclei of the Lateral Lemniscus 279
9.4.3 Projections from the IC 279
9.4.4 Projections from the Thalamus and Nearby Areas 280
9.4.5 Projections from the Auditory Cortex 282
9.4.5.1 Auditory Cortical Projections to the Thalamus 282
9.4.5.2 Auditory Cortical Projections to the IC 283
9.4.5.3 Auditory Cortical Projections to Nuclei Below the IC 284
9.5 Convergence of Descending Pathways and Targets in Individual Nuclei 285
9.5.1 Projections to the CN 286
9.5.2 Projections to the SOC 288
9.5.3 Projections to the NLL 289
9.5.4 Projections to the IC 290
9.5.5 Projections to the Thalamus from the AC 291
9.6 Loops, Chains, and Branches 293
9.7 Summary and Questions for Future Research 296
References 297
Chapter 10: Central Effects of Efferent Activation 302
10.1 Introduction 302
10.2 Single-Neuron Recordings In Vivo 305
10.2.1 Technical Issues 305
10.2.2 Early Work 308
10.2.3 Recent Studies in CN and IC 310
10.2.3.1 Effects in Quiet 310
10.2.3.2 Effects in Background Noise 313
10.2.4 In Vivo Evidence for MOCS Collateral Involvement in Novel Central Effects 315
10.3 In Vitro Studies 316
10.4 Mechanisms of Nonclassic MOCS Effects in Central Neurons 317
10.5 Behavioral Experiments 319
10.6 Functional Significance 319
10.7 Summary 320
References 321
Chapter 11: Corticofugal Modulation and Beyond for Auditory Signal Processing and Plasticity 324
11.1 Introduction 324
11.2 Necessity of Multiparametric Corticofugal Modulation 325
11.3 Research Performed Before 1995 326
11.4 Experimental Philosophy and Methodology 326
11.4.1 Experimental Philosophy 326
11.4.2 Electric Stimulation of the Primary Auditory Cortex 327
11.4.3 Drug Applications to the Primary Auditory Cortex 327
11.5 Research After 1995 (General) 328
11.6 Corticofugal Modulation in the Frequency Domain 330
11.6.1 Frequency-Dependent Facilitation and Inhibition and Best Frequency Shifts 330
11.6.2 Expanded and Compressed Reorganizations of Tonotopic Maps 333
11.6.3 Role of Excitation and Inhibition in Producing Two Types of Reorganizations 336
11.6.4 Corticofugal Modulation of Cochlear Hair Cells 337
11.6.5 Ipsilateral vs. Contralateral Corticofugal Modulation 339
11.7 Multiparametric Corticofugal Modulation 340
11.7.1 Modulation of Duration Tuning in Eptesicus fuscus 340
11.7.2 Modulation of Delay Tuning in Pteronotus parnellii parnellii 342
11.7.3 Modulation of Response Latencies in Eptesicus fuscus 342
11.7.4 Modulation of the Minimum Threshold in Mus domesticus and Eptesicus fuscus 344
11.7.5 Modulation of Spatial Tuning in Eptesicus fuscus 345
11.7.6 Important Principles of Corticofugal Modulation Emerged in Eptesicus fuscus 345
11.8 Tone-Specific Plasticity (BF shift) Elicited by Auditory Fear Conditioning 345
11.9 Findings Important for the Understanding of the Neural Circuit Eliciting Tone-Specific Plasticity (the BF Shifts) 349
11.9.1 The Corticofugal Auditory System 350
11.9.2 The Primary Auditory Cortex, AI 350
11.9.3 The Thalamic Auditory Nuclei: MGBv vs. MGBm 351
11.9.4 ICc: The Central Nucleus of the Inferior Colliculus 352
11.9.5 The Primary Somatosensory Cortex 352
11.9.6 The Cholinergic Neuromodulator 352
11.9.7 The Amygdala: Inputs from the Sensory Thalamus and Cortex 353
11.9.8 The Prefrontal Cortex 353
11.9.9 The Ascending Reticular Activating System 354
11.10 The Neural Circuit for Tone-Specific Plasticity: Working Mode 354
11.11 Corticofugal Differential Gating for Cortical Plasticity: Nonspecific Plasticity Elicited by Pseudo-Conditioning 356
11.12 Reorganization of the Tonotopic Map Caused by a Cochlear Lesion 357
11.13 Concluding Remarks: Corticofugal Modulation Shared by Different Animal Species and Different Sensory Systems 357
References 358
Index 364