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Vergence Eye Movements Redefined: the Neural Control of Fast Versus Slow Vergence

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Vergence Eye Movements Redefined: the Neural Control of Fast Versus Slow Vergence Vergence eye movements redefined: The neural control of fast versus slow vergence Marion R. Van Horn Aerospace Medical Research Unit Department of Physiology McGill University Montreal, Quebec, Canada August 2010 A thesis submitted to the faculty of Graduate Studies and Research in partial fulfilment of the degree of Doctorate in Philosophy Copyright © Marion Van Horn 2010 TABLE OF CONTENTS ABSTRACT…………………………..…………………………..………………... xiii RÉSUMÉ…………………………..…………………………..…………………… xv ACKNOWLEDGEMENTS…………………………..………………………… ..xviii CONTRIBUTIONS OF AUTHORS…………………………..………………….. xx LIST OF ABBREVIATIONS…………………………………..……………….. xxii CHAPTER 1: GENERAL INTRODUCTION & LITERATURE REVIEW 1.1 Overview and conceptual framework………...……………………………… 1 1.2 The extraocular eye muscles and their innervations…………….…………… 4 1.3 Classification of eye movements………………….…………….…………… 8 1.4 The neural control of disconjugate saccades: Hering versus Helmoholtz... 11 1.4.1 Evidence supporting Hering’s Law …………………………….... 11 1.5 The premotor circuitry of conjugate saccades ………………………….... 14 1.5.1 Saccadic burst neurons…………….…………………………….... 15 1.5.2 Omnipause neurons………………..…………………………….... 16 1.5.3 Oculomotor integration ………………………………………….... 17 1.6 The premotor circuitry of saccade-free vergence ……………………….... 19 1.7 Evidence against “Hering’s Law” ……………………………………….... 20 1.8 Research Goals ……………………………….………………………….... 22 CHAPTER 2: DYNAMIC CHARACTERIZATION OF OCULOMOTONEURONS DURING CONJUGATE AND DISCONJUGATE EYE MOVEMENTS 2.1 ABSTRACT ………………………………………………………………. 25 2.2 INTRODUCTION ………………………………………………………... 26 2.3 METHODS .………………………………………………………………. 28 2.3.1 Animal and surgical procedures……………………………………. 28 2.3.2 Behavioral paradigms ………………………………………………. 29 2.3.3 Data acquisition procedures ……………………………………….. 30 i 2.3.4 Data Analysis ………………….…………………………………… 31 2.3.5 Quantification of ocular preference ….…………………………….. 34 2.4 RESULTS ...……..………………………….……………………………... 35 2.4.1 Dynamic analysis during conjugate saccades ………...……………. 35 2.4.2 Dynamic responses estimated during OFF-directed conjugate saccades ……………………………………………….. 38 2.4.3 Example OMN with a preference for the ipsilateral eye ….………. 38 2.4.4 Response of OFF-directed disconjugate saccades …………………. 43 2.4.5 Summary of ocular preferences ……….……………………..…….. 46 2.4.6 Comparison of ocular preference during disconjugate saccades and disconjugate fixation …………………………………………….... 48 2.4.7 Model parameters estimated across oculomotor behaviors: fixation, microsaccades, and saccades …………………………………….... 50 2.5 DISCUSSION ……………………………………………………………... 53 2.5.1 Dynamic discharge of OMNs during conjugate saccades …………. 55 2.5.2 Responses of oculomotoneurons during disconjugate fixation and saccades …………………………………………………………… 56 2.5.3 Comparison of the motor drive of agonist medial and lateral rectus motoneurons during disconjugate saccades…...…………………... 59 2.5.4 Consideration of the antagonist muscle when modeling across oculomotor behaviors ……………………………………………... 60 CHAPTER 3: DYNAMIC CHARACTERIZATION OF SACCADIC BURST NEURONS DURING CONJUGATE AND DISCONJUGATE EYE MOVEMENTS 3.1 ABSTRACT………………………………………………………………... 63 3.2 INTRODUCTION ………………………………………………………… 64 3.3 METHODS ………………………………………………….…….………. 65 3.3.1 Animals and surgical preparations …………………………………. 65 3.3.2 Behavioral paradigms ………………………………………………. 66 3.3.3 Data acquisition procedures…..…………………………………….. 69 ii 3.3.4 Data analysis………………………………………………………….70 3.3.4a Dynamic analysis of BN firing rate …………………………71 3.3.4b Metric analysis of BN discharges …………………………………..72 3.3.5 Quantification of ocular preference……...……………….….………73 3.3.6 Simulation design………………………...……………….….……... 75 3.4 RESULTS………………………………………………………………….....78 3.4.1 SBN discharge timing is appropriate to facilitate vergence movements ………………………...……………………..………. 79 3.4.2 Testing the null hypothesis: SBNs only encode conjugate eye movement dynamics ..………………………………………….…. 79 3.4.3 Rejecting the null hypothesis: The conjugate prediction fails ….…. 84 3.4.4 Comparison across neuron types ….………….………….………… 90 3.4.5 Calculation of the net premotor drive…………………….………… 92 3.4.6 Metric analysis of conjugate and disconjugate saccades .…………. 92 3.4.7 Comparison of dynamic and metric analyses .…………………….. 96 3.4.8 Simulation design…………………………….…………………….. 96 3.4.9 Analysis of simulation weights ……………….…………………… 99 3.5 DISCUSSION…………………………………………………………….. 100 3.5.1 Comparison with previous reports: conjugate saccades …….……. 102 3.5.2 The timing and dynamics of SBN burst activity are appropriate to facilitate vergence during disconjugate saccades ………………… . 102 3.5.3 The role of the saccadic burst generator during saccade-vergence interactions …………………………………………………...…... 104 3.5.4 Source of vergence-related signals ………………………………… 108 CHAPTER 4: VERTICAL FACILITATED VERGENCE BY PREMOTOR SACCADIC BURST NEURONS 4.1 ABSTRACT……………………………………………………………….. 114 4.2 INTRODUCTION .………………….…………………………………… 115 4.3 METHODS ……………………………………………………………….. 118 4.3.1 Animals and surgical preparations…………………………………. 118 iii 4.3.2 Behavioral paradigms………………………………………………. 118 4.3.3 Data acquisition …………………………………………………….. 121 4.3.4 Definitions and conventions ……..………………………………… 122 4.3.5 Data analysis ……………………………………………………….. 123 4.3.6 Quantification of ocular preference………………………………… 125 4.3.5 Statistical analysis………….……………………………………….. 125 4.4 RESULTS…………………………………………………………………... 126 4.4.1 Characterization of vergence facilitated by vertical saccades .……. 126 4.4.2 Temporal alignment of peak vertical and vergence velocities …….. 128 4.4.3 Test of the hypothesis: vergence is facilitated by the classical saccadic pathway during disconjugate saccades …………………….……... 131 4.4.4 Estimation of the vergence-related signal encoded by horizontal saccadic burst neurons during vertical disconjugate saccades……. 139 4.4.5 Ocular sensitivities across of the population of SBNs……………... 142 4.4.6 Comparison of ocular preference during horizontal and vertical disconjugate saccades…………………………………………….. 144 4.5 DISCUSSION……………………………………………………………… 148 4.5.1 Vergence velocity is facilitated during vertical disconjugate saccades ……………………………...……………………………. 149 4.5.2 Vergence and vertical velocities are temporally aligned during vertical saccades in monkeys …………………...…………………. 150 4.5.3 The dynamics of SBNs during horizontal and vertical conjugate saccades ……………………………………...................................... 151 4.5.4 SBNs contribute to increasing vergence velocities during disconjugate saccades ……………………………..……………………………… 152 4.5.5 Premotor circuits for the control of changes in vergence angle….… 154 4.6 Supplemental Material ……………………………………………….….. 155 CHAPTER 5: IDENTIFICATION AND DYNAMIC CHARACTERIZATION OF VERGENCE NEURONS IN THE ROSTRAL SUPERIOR COLLICULUS iv 5.1 ABSTRACT……………………………………………………………...... 165 5.2 INTRODUCTION.………………………………………………………... 166 5.3 METHODS…………………………………………………………………. 167 5.3.1 Surgical procedures ………………………………………………... 167 5.3.2 Behavioral paradigms………………………………………………. 168 5.3.2.1 Conjugate paradigms ……………………………………… 168 5.3.2.2 Vergence paradigms……………………………………….. 169 5.3.3 Data acquisition procedures.............………………………………… 169 5.3.3.1 Extracellulular single unit recordings………….………… 170 5.3.3.2 Microstimulation……………………………….………… 171 5.3.4 Data Analysis……………….………………………………………. 171 5.3.4.1 Definitions and Conventions………..………….………… 171 5.3.4.2 Metric analysis………………………...……….………… 172 5.3.4.3 Dynamic analysis……………………………….………… 172 5.3.5 Histology………………..….………………………………………. 173 5.3.6 Statistical analysis…….…….………………………………………. 173 5.4 RESULTS………………………………………………………………….. 173 5.4.1 Neurons in rostral SC dynamically encode vergence during vergence tracking………………………………………………….. ………. 179 5.4.2 Convergence and divergence neurons in the rostral SC encode Slow but not fast vergence…………………………..……………. 182 5.5 DISCUSSION………………………………………………………..……... 184 5.5.1 Microstimulation of the rostral SC…………………………………. 187 5.5.2 The neural control of fast versus slow vergence..……..…………… 190 CHAPTER 6: GENERAL DISCUSSION 6.1 Signals encoded by extraocular motoneurons……………..……………….. 198 6.2 Premotor coding in 3D……………………...……………..……………….. 200 6.3 Superior colliculus ensures binocular realignment of gaze..……………….. 202 6.4 Clinical applications……………..…………………………………………. 205 6.5 Conclusions and future directions…………..……………..……………….. 205 v 6.5.1 Are small motoneurons more specialized in encoding vergence movements?........................................................................................206 6.5.2 What are the upstream sources of vergence?.......................................206 APPENDIX A: LOCAL NEURAL PROCESSING AND THE GENERATION OF DYNAMIC MOTOR COMMANDS WITHIN THE PREMOTOR NETWORK A.1 Abstract ……………………………………………………………………. 210 A.2 Introduction ……………………………………………………………….. 211 A.3 Methods ……………………………………………………………………. 212 A.3.1 Surgical procedures ……………………………………………….. 212 A.3.2 Experimental paradigms and data acquisition…...………………… 214 A.3.3 Data analysis……… ……..………………………………………... 215 A.3.3.1 Metric analysis……………………………………………. 216 A.3.3.2 Dynamic analysis…………………………………………. 216 A.3.3.3 Eye velocity reconstruction……………………………….. 218 A.3.3.4 Spike triggered average and spike field coherence……… 220 A.3.3.5 Spectrogram analysis.……………………………………... 221 A.3.3.5 LFP and spike tuning curves.……………………………… 221 A.4 Results …………………………………………………….…………….. 222 A.4.1 LFPS: a reflection of intracellular activity……... ………………… 222 A.4.2 LFP response timing is consistent with sequential processing within saccadic network …………………………….…………………… 224
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