Front cover 1
Using Eye Movements as an Experimental Probe of Brain Function 4
Copyright page 5
List of contributors 6
Foreword 14
Contents 16
Section 1. Using Novel Techniques to Define the Neural Control of Extraocular Muscles 24
Chapter 1.1. Mapping the oculomotor system 26
Introduction 26
Neuroanatomical methods 27
Premotor cell groups of the oculomotor system 27
Abbreviations 32
Acknowledgements 33
References 33
Chapter 1.2. Neuronal signalling expression profiles of motoneurons supplying multiply or singly innervated extraocular muscle fibres in monkey 36
Introduction 36
Methods and materials 37
Results 37
Conclusions 39
Acknowledgements 39
References 39
Chapter 1.3. Histochemical characterisation of trigeminal neurons that innervate monkey extraocular muscles 40
Introduction 40
Methods 42
Results and discussion 42
References 42
Chapter 1.4. Functional anatomy of the extraocular muscles during vergence 44
Introduction 44
Methods 45
Results 45
Discussion 47
Abbreviations 50
Acknowledgements 50
References 50
Chapter 1.5. Induced extraocular muscle afferent signals: from pigeons to people 52
Introduction 52
Methods 53
Single unit results 53
Behavioural results on the VOR 54
Experiments on human oculomotor control 54
Summary 57
Acknowledgements 57
References 57
Chapter 1.6. Monkey primary somatosensory cortex has a proprioceptive representation of eye position 60
Introduction 60
Methods 61
Results 61
Discussion 64
Acknowledgements 67
References 67
Chapter 1.7. Acute superior oblique palsy in the monkey: effects of viewing conditions on ocular alignment and modelling of the ocular motor plant 70
Introduction 70
Effects of viewing conditions on ocular misalignment 71
Mathematical simulations of ocular motor behaviour 72
References 75
Chapter 1.8. Dynamic aspects of trochlear nerve palsy 76
Introduction 76
Methods 77
Results 78
Discussion 80
Acknowledgements 81
References 81
Chapter 1.9. Ocular motor nerve palsies: implications for diagnosis and mechanisms of repair 82
Introduction 82
Methods 83
Results 83
Discussion 86
Acknowledgement 88
References 88
Chapter 1.10. Extraocular proprioception and new treatments for infantile nystagmus syndrome 90
Introduction 90
Methods 91
Results 92
Discussion 92
Acknowledgements 97
References 97
Section 2. New Insights into Brainstem Generation of Ocular Motor Commands 100
Chapter 2.1. Neural circuits for triggering saccades in the brainstem 102
Introduction 102
Conclusions 107
References 108
Chapter 2.2. Brainstem circuits controlling lid-eye coordination in monkey 110
Introduction 110
Materials and methods 111
Results 111
Discussion 113
Abbreviations 117
Acknowledgement 117
References 117
Chapter 2.3. Defining the pupillary component of the perioculomotor preganglionic population within a unitary primate Edinger-Westphal nucleus 120
Introduction 120
Results 121
Discussion 127
Acknowledgement 128
References 128
Chapter 2.4. Frontal eye field signals that may trigger the brainstem saccade generator 130
Introduction 130
Methods 131
Results 132
Discussion 134
Acknowledgements 137
References 137
Chapter 2.5. The role of omnipause neurons: why glycine? 138
Introduction 138
Methods 140
Results 140
Discussion 142
Acknowledgement 143
References 143
Chapter 2.6. Applying saccade models to account for oscillations 146
Introduction 146
Saccadic oscillations 147
Prior models of saccadic oscillations 147
A new model of saccadic oscillations 147
Experimental results 148
Discussion 151
References 152
Chapter 2.7. Dynamics of saccadic oscillations 154
Introduction 154
Instabilities of fixation 155
Conclusion 158
Acknowledgement 159
References 159
Chapter 2.8. Effects of failure of development of crossing brainstem pathways on ocular motor control 160
Introduction 160
Conclusion 162
Abbreviation 163
Acknowledgement 163
References 163
Chapter 2.9. Neuronal evidence for individual eye control in the primate cMRF 166
Introduction 166
Methods 167
Results 167
Discussion 172
Acknowledgements 172
References 172
Section 3. Using Eye Movements as an Index of Transformation of Signals by the Cerebellum and Brainstem 174
Chapter 3.1. Complex spike activity signals the direction and size of dysmetric saccade errors 176
Introduction 176
Methods 177
Results 181
Discussion 182
References 182
Chapter 3.2. Role of the MST-DLPN pathway in smooth pursuit adaptation 184
Introduction 184
Methods 184
Results 185
Discussion 185
Acknowledgement 188
References 188
Chapter 3.3. Lesions of the cerebellar nodulus and uvula in monkeys: effect on otolith-ocular reflexes 190
Introduction 190
Methods 191
Results 191
Conclusion 194
Acknowledgements 194
References 195
Chapter 3.4. Vergence eye movement signals in the cerebellar dorsal vermis 196
Introduction 196
Materials and methods 196
Results 197
Discussion 199
Acknowledgement 199
References 199
Chapter 3.5. Oculomotor anatomy and the motor-error problem: the role of the paramedian tract nuclei 200
Introduction 200
Modelling strategy 202
Modelling results 203
Application to robotics 205
Application to biology 206
Conclusions 208
Abbreviations 208
Acknowledgements 208
References 208
Chapter 3.6. Impulsive testing of semicircular canal function 210
Introduction 210
Recording and analysing the impulsive VOR 211
Impulsive VOR with unilateral and bilateral vestibular loss 215
Mechanism of impulsive VOR asymmetry after unilateral vestibular deafferentation 215
Clinical head impulse testing and catch-up saccades 215
Acknowledgements 216
References 216
Chapter 3.7. Inter-ocular differences of the horizontal vestibulo-ocular reflex during impulsive testing 218
Introduction 218
Methods 218
Results 219
Discussion 219
Acknowledgement 221
References 221
Chapter 3.8. Control of ocular torsion in the rotational vestibulo-ocular reflexes 222
Introduction 222
Acknowledgement 228
References 228
Chapter 3.9. Do humans show velocity-storage in the vertical rVORquest 230
Introduction 230
Materials and methods 230
Results 232
Discussion 232
Acknowledgement 233
References 233
Chapter 3.10. Preserved otolith function in patients with cerebellar atrophy and bilateral vestibulopathy 234
Introduction 234
Case reports 235
Methods 235
Results 235
Discussion 236
Acknowledgements 236
References 237
Chapter 3.11. Three-dimensional kinematics of saccadic eye movements in humans with cerebellar degeneration 238
Introduction 238
Methods 239
Results 240
Discussion 241
Acknowledgment 241
References 241
Chapter 3.12. Inferior olive hypertrophy and cerebellar learning are both needed to explain ocular oscillations in oculopalatal tremor 242
Introduction 242
Methods 244
Results 245
Discussion 247
References 249
Chapter 3.13. Impulsive head rotation resets oculopalatal tremor: examination of a model 250
Introduction 250
Subjects and methods 251
Results 254
Discussion 254
Acknowledgement 256
References 256
Section 4. Using Eye Movements as a Probe of Sensory-Motor Processing and Navigation 258
Chapter 4.1. Human ocular following: evidence that responses to large-field stimuli are limited by local and global inhibitory influences 260
Introduction 261
Methods 261
Results 263
Discussion 264
Acknowledgement 265
References 265
Chapter 4.2. Short-latency disparity vergence eye movements: dependence on the preëxisting vergence angle 268
Introduction 268
Methods 269
Results 270
Discussion 272
Acknowledgements 274
References 274
Chapter 4.3. MSTd neurons during ocular following and smooth pursuit perturbation 276
Introduction 276
Methods 278
Results 279
Discussion 281
Acknowledgement 282
References 282
Chapter 4.4. Neural activity in cortical areas MST and FEF in relation to smooth pursuit gain control 284
Introduction 284
A dual pathway model for smooth pursuit gain control 285
Neural activities in MST and FEF 285
Conclusion 287
Acknowledgements 287
References 287
Chapter 4.5. Eye position and cross-sensory learning both contribute to prism adaptation of auditory space 288
Introduction 288
Methods 289
Results 290
Discussion 292
Acknowledgements 292
References 293
Chapter 4.6. Hysteresis effects of the subjective visual vertical during continuous quasi-static whole-body roll rotation 294
Introduction 294
Methods 295
Results 295
Discussion 297
Acknowledgements 297
References 298
Chapter 4.7. Perception of self motion during and after passive rotation of the body around an earth-vertical axis 300
Introduction 300
Methods 301
Results 301
Discussion 304
Acknowledgement 304
References 304
Chapter 4.8. The freezing rotation illusion 306
Introduction 306
Methods 306
Results 307
Discussion 308
References 308
Chapter 4.9. Geometrical considerations on canal-otolith interactions during OVAR and Bayesian modelling 310
Introduction 310
Otolith signals 310
Semicircular canal signals 311
Bayesian modelling 312
Conclusion 312
Acknowledgements 313
Abbreviations 313
References 313
Chapter 4.10. Listing’s plane and the otolith-mediated gravity vector 314
Introduction 314
Methods 314
Results 315
Discussion 316
Acknowledgement 317
References 317
Chapter 4.11. A reinterpretation of the purpose of the translational vestibulo-ocular reflex in human subjects 318
Introduction 318
Methods 319
Results 320
Discussion 322
Acknowledgements 324
References 325
Chapter 4.12. Dynamics of binocular fixation of targets during fore-aft motion 326
Introduction 326
Methods 327
Results 329
Discussion 333
Abbreviations 334
Acknowledgements 334
References 334
Chapter 4.13. Differential coding of head rotation by lateral-vertical canal convergent central vestibular neurons 336
Introduction 336
Methods 337
Results 337
Discussion 340
Abbreviations 340
Acknowledgement 340
References 340
Chapter 4.14. Cyclovergence evoked by up-down acceleration along longitudinal axis in humans 342
Introduction 342
Methods 342
Results 343
Discussion 344
Abbreviation 344
Acknowledgements 344
References 345
Chapter 4.15. Oblique gaze shifts: head movements reveal new aspects of component coupling 346
Introduction 346
Methods 348
Results 348
Discussion 352
Acknowledgements 353
References 353
Chapter 4.16. Head movement control during head-free gaze shifts 354
Head movements during gaze shifts 354
Challenging the head motor control system by increasing head inertia 354
Vestibular feedback guides head movements on-line 355
Cerebellar signals are involved in the on-line control of the head 355
Summary 357
Abbreviations 357
Acknowledgements 357
References 357
Chapter 4.17. Postural changes during eye-head movements 358
Introduction 358
Methods 358
Results 359
Discussion 360
Acknowledgement 361
References 361
Chapter 4.18. Cortical processing in vestibular navigation 362
Introduction 362
Experimental procedures 363
Data analysis 365
Results 366
Discussion 368
References 369
Chapter 4.19. Foot rotation contribution to trunk and gaze stability during whole-body mediated gaze shifts: a principal component analysis study 370
Introduction 370
Materials and methods 371
Results 372
Discussion 373
References 374
Chapter 4.20. Supraspinal locomotor control in quadrupeds and humans 376
Introduction 376
Methods 379
Results 379
Discussion 380
Acknowledgements 384
References 384
Chapter 4.21. Private lines of cortical visual information to the nucleus of the optic tract and dorsolateral pontine nucleus 386
Neuronal substrate of eye movement control 386
Anatomical overlap but cellular specificity of cortical input to NOT-DTN and DLPN 388
Cortical information transmitted to the NOT-DTN and the DLPN 388
Private linesquest 389
References 389
Chapter 4.22. Gravity perception in cerebellar patients 392
Introduction 392
Material and methods 393
Results 393
Discussion 393
Acknowledgements 395
References 395
Section 5. Using Eye Movements as a Probe of Cognition, Memory, and Prediction 396
Chapter 5.1. Brain mechanisms for switching from automatic to controlled eye movements 398
Parallel neural network for controlling behaviour 398
Switching from automatic to controlled behaviour 399
Switch-selective neurons in the pre-SMA 400
Mechanisms of pre-SMA-induced behavioural switching 402
Discussion 403
References 404
Chapter 5.2. The frontal eye field as a prediction map 406
Introduction 406
A prediction map in primate frontal eye field 408
Computational basis of the prediction map 408
Physiological mechanism of the prediction map 408
The sequence of events 410
Site of prediction error calculation 411
Relation to previous FEF studies 411
Other frontal lobe functions 412
References 412
Chapter 5.3. Volition and eye movements 414
Introduction 414
Will, volition, and voluntariness 414
Internally versus externally guided action 415
Executive control 415
Intention 416
A minimalist model 416
Probing volition 418
Conclusion 420
Acknowledgement 420
References 420
Chapter 5.4. Negative motivational control of saccadic eye movement by the lateral habenula 422
What is the lateral habenulaquest 422
Lateral habenula as a source of negative reward signals in dopamine neurons 425
Discussion 425
References 425
Chapter 5.5. Eye movements as a probe of attention 426
Introduction 426
Oculomotor capture, attention, and reward 426
Salience or priority maps in the brain 428
Attended objects and their representations across saccades 430
Conclusions 433
References 433
Chapter 5.6. Using transcranial magnetic stimulation to probe decision-making and memory 436
Introduction 436
TMS to probe the chronometry of cerebral processes 436
Chronometry of antisaccades 437
Chronometry of the organization of spatial working memory 437
Chronometry of prediction 438
References 440
Chapter 5.7. Supplementary eye field contributions to the execution of saccades to remembered target locations 442
Introduction 442
Methods 443
Results 443
Discussion 445
Acknowledgements 446
References 446
Chapter 5.8. Multiple memory-guided saccades: movement memory improves the accuracy of memory-guided saccades 448
Introduction 448
Methods 449
Results 449
Discussion 450
References 450
Chapter 5.9. Visual vector inversion during memory antisaccades - a TMS study 452
Introduction 452
Methods 453
Results 454
Discussion 454
References 455
Chapter 5.10. Predictive signals in the pursuit area of the monkey frontal eye fields 456
Introduction 456
Methods 457
Results 459
Discharge of task-related neurons in the caudal FEF 459
Discussion 462
Acknowledgements 462
References 462
Chapter 5.11. Internally generated smooth eye movement: its dynamic characteristics and role in randomised and predictable pursuit 464
Introduction 464
General methods 466
Experiment 1: extraction of motion from brief target presentation 466
Experiment 2: randomly timed initiation of isolated, internally driven responses 469
Discussion 470
Acknowledgement 471
References 471
Chapter 5.12. Predictive disjunctive pursuit of virtual images perceived to move in depth 474
Introduction 474
Methods 475
Results 476
Discussion 478
Acknowledgement 479
References 479
Chapter 5.13. Tracking in 3-D space under natural viewing condition 482
Introduction 482
Methods 483
Results 483
Discussion 486
References 487
Chapter 5.14. Exploring the pulvinar path to visual cortex 490
Introduction 490
Methods 491
Results 492
Discussion and conclusion 494
References 496
Chapter 5.15. The role of the human pulvinar in visual attention and action: evidence from temporal-order judgment, saccade decision, and antisaccade tasks 498
Introduction 498
Methods 499
Results 502
Discussion 502
Acknowledgements 504
References 505
Section 6. Abnormal Eye Movements: Mechanisms and Treatment Strategies 508
Chapter 6.1. How disturbed visual processing early in life leads to disorders of gaze-holding and smooth pursuit 510
Introduction 510
Methods 511
Results 511
Discussion 517
Acknowledgements 518
References 518
Chapter 6.2. Manifest latent nystagmus: a case of sensori-motor switching 520
Introduction 520
Manifest latent nystagmus 520
Binocular vision and perceptual multistability 521
Experiment 1: perceptual reversals with MLN 521
Experiment 2: visual attention and sensori-motor switching 522
Modelling sensori-motor switching in MLN 524
Conclusions 525
References 525
Chapter 6.3. Eye hyperdeviation in mouse cerebellar mutants is comparable to the gravity-dependent component of human downbeat nystagmus 526
Introduction 526
Methods 527
Results 528
Discussion 528
Abbreviations 530
Acknowledgements 530
References 530
Chapter 6.4. New insights into the upward vestibulo-oculomotor pathways in the human brainstem 532
Introduction 532
The MLF tracts 532
The extra-MLF tracts 533
Why two brainstem excitatory pathways for upward vestibular eye movementsquest 535
Conclusions 540
Abbreviations 540
References 540
Chapter 6.5. Mechanisms of vestibulo-ocular reflex (VOR) cancellation in spinocerebellar ataxia type 3 (SCA-3) and episodic ataxia type 2 (EA-2) 542
Introduction 542
Methods 543
Results 544
Discussion 545
Abbreviations 548
Acknowledgement 548
References 548
Chapter 6.6. Modelling drug modulation of nystagmus 550
Introduction 550
Methods 551
Results 553
Discussion 554
Abbreviations 555
Acknowledgements 555
Appendix 555
References 556
Chapter 6.7. Aminopyridines for the treatment of cerebellar and ocular motor disorders 558
Introduction 558
Downbeat nystagmus 559
Upbeat nystagmus 560
Episodic ataxia type 2 563
Acknowledgement 563
References 563
Chapter 6.8. Baclofen, motion sickness susceptibility and the neural basis for velocity storage 566
Introduction 566
Methods 568
Results 568
Discussion 574
Abbreviations 575
Acknowledgements 575
References 575
Chapter 6.9. Oculomotor deficits indicate the progression of Huntington’s Disease 578
Introduction 578
Method 579
Results 579
Discussion 580
Acknowledgements 581
References 581
Chapter 6.10. Eye movements in visual search indicate impaired saliency processing in Parkinson’s disease 582
Introduction 582
Methods 583
Results 583
Discussion 584
Acknowledgements 584
References 585
Chapter 6.11. Ocular motor anatomy in a case of interrupted saccades 586
Introduction 586
Methods 587
Results 587
Discussion 589
Acknowledgements 589
References 589
Chapter 6.12. Mechanism of interrupted saccades in patients with late-onset Tay-Sachs disease 590
Introduction 590
Methods 590
Results 591
Discussion 593
Acknowledgements 593
References 593
Chapter 6.13. Conjugacy of horizontal saccades: application of binocular phase planes 594
Introduction 594
Subjects and methods 595
Results 596
Discussion 596
Acknowledgements 597
References 597
Chapter 6.14. The neuroanatomical basis of slow saccades in spinocerebellar ataxia type 2 (Wadia-subtype) 598
Introduction 598
Case history and methods 599
Results 599
Discussion 603
Acknowledgements 603
References 603
Chapter 6.15. Selective, circuit-wide sparing of floccular connections in hereditary olivopontine cerebellar atrophy with slow saccades 606
Introduction 606
Patient and methods 607
Results 607
Discussion 608
Acknowledgements 608
References 608
Chapter 6.16. A quick look at slow saccades after cardiac surgery: where is the lesionquest 610
Introduction 610
Acknowledgement 612
References 612
Chapter 6.17. Eye and head torsion is affected in patients with midbrain lesions 614
Introduction 614
Case reports and methods 614
Results 615
Discussion 617
Acknowledgement 617
References 618
Chapter 6.18. Horizontal saccadic palsy associated with gliosis of the brainstem midline 620
Introduction 620
Case history and methods 621
Results 621
Discussion 624
Acknowledgements 625
References 625
Subject Index 628