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Traditional and Non-Traditional Inputs to the Vestibular System

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Traditional and Non-Traditional Inputs to the Vestibular System Traditional and Non-Traditional Inputs to the Vestibular System By Stephanie Eileen Wiitala A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Biomedical Engineering) in The University of Michigan 2018 Doctoral Committee: Professor William Michael King, Chair Assistant Professor Cynthia A. Chestek Professor Susan E. Shore Assistant Professor Kathleen H. Sienko Stephanie E. Wiitala [email protected] ORCID iD: 0000-0002-7160-0260 © Stephanie E. Wiitala 2018 For two Elizabeths: Mary Elizabeth and Nancy Elizabeth, and two Michaels: Michael Oliver and Michael Banning ii Table of Contents Dedication ....................................................................................................................................... ii List of Figures ................................................................................................................................. v List of Tables ................................................................................................................................. vi List of Acronyms .......................................................................................................................... vii Abstract ........................................................................................................................................ viii Chapter 1: Introduction ................................................................................................................... 1 1.1 The Vestibular Periphery ................................................................................................. 1 1.1.1 The Vestibular Organs .............................................................................................. 1 1.1.2 Hair Cells .................................................................................................................. 3 1.1.3 Afferents ................................................................................................................... 4 1.1.4 Vestibular Nuclei ...................................................................................................... 6 1.2 Traditional Inputs and Pathways ...................................................................................... 7 1.2.1 The Vestibular-Ocular Reflex (VOR) ....................................................................... 7 1.2.2 The Optokinetic Reflex ............................................................................................. 9 1.2.3 The Vestibulocollic Reflex (VCR) ......................................................................... 12 1.3 Non-Traditional Inputs and Pathways ............................................................................ 15 1.3.1 Efference Copy ....................................................................................................... 15 1.3.2 Galvanic Vestibular Stimulation (GVS) ................................................................. 17 1.3.3 Sound ...................................................................................................................... 19 1.4 Summary of Thesis ......................................................................................................... 21 Chapter 2: Interaction of Pre-Programmed Eye Movements with the Vestibular-Ocular Reflex 22 2.1 Abstract .......................................................................................................................... 22 2.2 Introduction .................................................................................................................... 23 2.3 Model ............................................................................................................................. 26 2.4 Experimental Methods ................................................................................................... 31 2.4.1 Surgical Preparation ................................................................................................ 31 2.4.2 Test Procedure ........................................................................................................ 32 2.4.3 Data Analysis .......................................................................................................... 32 iii 2.5 Results ............................................................................................................................ 35 2.6 Discussion ...................................................................................................................... 43 Chapter 3: Effect of a Single Noise Exposure on Ocular and Postural Stability in Guinea Pig ... 51 3.1 Abstract .......................................................................................................................... 51 3.2 Introduction .................................................................................................................... 52 3.3 Methods .......................................................................................................................... 54 3.3.1 Surgical Preparation ................................................................................................ 54 3.3.2 Noise Exposure ....................................................................................................... 55 3.3.3 Data Collection ....................................................................................................... 55 3.3.4 Data Analysis .......................................................................................................... 56 3.3.5 Statistics .................................................................................................................. 57 3.3.6 Histology ................................................................................................................. 58 3.4 Results ............................................................................................................................ 58 3.5 Discussion ...................................................................................................................... 64 Chapter 4: A Shared Neural Integrator for Human Posture Control ............................................. 69 4.1 Abstract .......................................................................................................................... 69 4.2 Introduction .................................................................................................................... 70 4.3 Model ............................................................................................................................. 74 4.4 Experimental Methods ................................................................................................... 80 4.5 Results ........................................................................................................................... 83 4.6 Discussion ...................................................................................................................... 87 Chapter 5: Conclusion and Significance ....................................................................................... 94 5.1 Gaze Shifts in Primates & Gaze Stabilization in Rodents ............................................. 95 5.2 Noise-induced Vestibular Loss ...................................................................................... 96 5.3 Eye Movement Models in Postural Control ................................................................... 97 5.4 Limitations ..................................................................................................................... 98 Chapter 6: Future Directions ....................................................................................................... 100 6.1 Adaptation in Pre-Programmed Eye Movements ......................................................... 100 6.2 Long-Term Effects of Long-Term Noise Exposure ..................................................... 101 6.3 Improving Diagnostics with Optokinetic and Galvanic Vestibular Stimulation .......... 103 Bibliography ............................................................................................................................... 104 iv List of Figures Figure 1.1 – Vestibule with detail of semi-circular canal ampulla ................................................. 2 Figure 1.2 – Hair cell membrane potential and afferent firing in response to cupula deflection ... 4 Figure 1.3 – Firing dynamics of regular and irregular afferents compared to cupula dynamics .... 5 Figure 1.4 – Excitatory vestibular-ocular reflex pathway .............................................................. 8 Figure 1.5 – Eye velocity in response to constant velocity full-field visual flow (top) and whole- body rotation in the dark (bottom). ............................................................................................... 10 Figure 1.6 – Head response to body rotation with the VCR (Closed Loop VCR) and without the VCR (Head Plant) ......................................................................................................................... 13 Figure 2.1 – Proposed Model of Gaze Stabilization ..................................................................... 27 Figure 2.2 - Model Simulations Compared to Dichgans’ Data .................................................... 35 Figure 2.3 – Exemplary data from healthy guinea pigs ................................................................ 37 Figure 2.4 –Aggregate
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