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Understanding the Mechanisms of Motor Learning in the Vestibulo-Ocular Reflex

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Understanding the Mechanisms of Motor Learning in the Vestibulo-Ocular Reflex Understanding the Mechanisms of Motor Learning in the Vestibulo-ocular Reflex by Heather Kathryn Titley A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Physiology University of Toronto © Copyright by Heather Titley 2011 Understanding the Mechanisms of Motor Learning in the Vestibulo-ocular Reflex Heather Kathryn Titley Doctor of Philosophy Department of Physiology University of Toronto 2011 Abstract The vestibulo-ocular reflex (VOR) is a simple reflex that stabilizes gaze by moving the eyes in the opposite direction to the head. The gain of the VOR (ratio of head to eye velocity) can be increased or decreased during motor learning. It is thought that the memory for learned changes in the VOR gain is initially encoded within the cerebellar flocculus. Furthermore, these learned gain changes can be disrupted or consolidated into a long-term memory. In this thesis we describe novel results that show that consolidation of the VOR can take place rapidly, within 1 hour after learning has stopped. Furthermore, we demonstrated that unlike learning, which has been shown to have frequency selectivity, disruption and rapid consolidation generalize across the range of frequencies. We suggest that disruption and rapid consolidation in the VOR are local mechanisms within the cerebellar cortex, and do not require new learning. This thesis also provides additional evidence for the idea that learned gain increases and decreases are the result of separate mechanisms, most likely long-term depression and potentiation respectively, at the parallel fibre-Purkinje cell synapses. We demonstrate that learned gain increases, but not decreases, require the activation of type 1 metabotropic glutamate receptors (mGluR1) and B type γ-aminobutyric acid (GABAB) receptors. Blocking one or both of these receptors with an ii antagonist inverts gain-up learning, while the agonist augments gain-up learning. Furthermore, we provide novel evidence that these receptors are co-activated during gain-up learning. iii Acknowledgments I would first like to thank my supervisor Dr. Dianne Broussard for her patience and guidance throughout the years. Without her help this work would not have been possible. Her support throughout the years has been invaluable, and much appreciated. I am grateful to the members of my advisory committee Dr. Douglas Tweed and Dr. Sheena Josselyn for their many helpful suggestions. I would like to thank my colleague Raquel Heskin-Sweezie for both her help with the many projects and also for her support and friendship over the years. I would also like to thank Tracey Robinson, Shawna Vandenburg, and Dr. Badru Moloo in the Animal Resources Centre who took such excellent care of the cats. I am thankful to Yao-Fang Tan and Dr. Martin Wojtowicz for use of their vibratome, and to Gabriela Reyes and Dr. Jonathan Brotchie for use of their microtome. I am also grateful to Jordan Antflick, Dr. Laura Pacey and Dr. David Hampson for their help with the immunohistochemistry and for allowing me to use their cryostat. This thesis is dedicated to my Mom, Dad, and my brother Travis, for their constant love, support, and faith in me. I would like to thank my family and especially my friends who stood by me and believed in me, especially when I didn’t believe in myself. Thanks guys! iv Table of Contents Acknowledgments.......................................................................................................................... iv Table of Contents .............................................................................................................................v List of Tables ................................................................................................................................. xi List of Figures ............................................................................................................................... xii List of Appendices ....................................................................................................................... xiv List of Abbreviations .....................................................................................................................xv Chapter 1 ..........................................................................................................................................1 1 General Introduction ...................................................................................................................1 1.1 The vestibular system ..........................................................................................................1 1.1.1 The semicircular canals ............................................................................................1 1.1.2 Secondary vestibular nuclei .....................................................................................3 1.1.3 Extraocular motor neurons .......................................................................................4 1.2 The Vestibulo-ocular reflex .................................................................................................4 1.3 The Cerebellum ....................................................................................................................6 1.4 Motor learning .....................................................................................................................9 1.4.1 Smooth pursuit and cancellation ............................................................................11 1.5 Sites of learning .................................................................................................................12 1.5.1 The many theories of learning ...............................................................................13 1.5.2 The flocculus vs. paraflocculus ..............................................................................22 1.5.3 The signals that guide learning ..............................................................................23 1.5.4 Evidence from eye-blink conditioning ...................................................................24 1.5.5 Current theories of VOR motor learning ...............................................................26 1.5.6 An alternative theory..............................................................................................29 1.6 Consolidation of learning ...................................................................................................32 v 1.6.1 Disruption ..............................................................................................................33 1.6.2 Consolidation .........................................................................................................33 1.6.3 Rapid consolidation ...............................................................................................36 1.7 Characteristics of learning .................................................................................................37 1.7.1 Frequency selectivity in VOR learning..................................................................38 1.8 Synaptic plasticity ..............................................................................................................40 1.8.1 Calcium dependency ..............................................................................................41 1.8.2 Mechanisms of post-synaptic LTD at the PF-PC synapses ...................................43 1.8.3 Requirement of LTD for motor learning ...............................................................47 1.8.4 mGluR1 receptors ..................................................................................................50 1.8.4.1 mGluR1 is required for LTD and motor learning ...................................52 1.8.5 GABAB receptors ...................................................................................................55 1.8.5.1 GABAB receptors enhance mGluR1 signalling .......................................56 1.8.6 Long-term potentiation ..........................................................................................61 1.8.7 Other types of cerebellar plasticity ........................................................................63 1.8.8 Brainstem plasticity ...............................................................................................64 1.9 List of hypotheses ..............................................................................................................65 Chapter 2 ........................................................................................................................................66 2 General methods .......................................................................................................................66 2.1 Surgery methods ................................................................................................................66 2.1.1 Anaesthesia ............................................................................................................67 2.1.2 Analgesia and antibiotics .......................................................................................67 2.1.3 Head holder surgery ...............................................................................................67 2.1.4 Eye coil surgery .....................................................................................................68 2.1.5 Cylinder surgery .....................................................................................................68
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