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Towards a Chromatic Pupillometry Protocol for Assessing Melanopsin-Driven Post-Illumination Pupil Response in Basic Science and Clinical Investigations

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Towards a Chromatic Pupillometry Protocol for Assessing Melanopsin-Driven Post-Illumination Pupil Response in Basic Science and Clinical Investigations TOWARDS A CHROMATIC PUPILLOMETRY PROTOCOL FOR ASSESSING MELANOPSIN-DRIVEN POST-ILLUMINATION PUPIL RESPONSE IN BASIC SCIENCE AND CLINICAL INVESTIGATIONS by Shaobo Lei A thesis submitted in conformity with the requirements for the degree of Master of Science Institute of Medical Science University of Toronto © Copyright by Shaobo Lei 2016 Towards a Chromatic Pupillometry Protocol for Assessing Melanopsin-Driven Post-Illumination Pupil Response in Basic Science and Clinical Investigations Shaobo Lei Master of Science Institute of Medical Science University of Toronto 2016 Abstract The pupillary light reflex (PLR) is mediated by intrinsically photosensitive retinal ganglions cells (ipRGCs), a sub-group of retinal ganglion cells that contain photopigment melanopsin. Melanopsin activation drives a sustained pupil constriction after the offset of light stimulus, this so-called post-illumination pupil response (PIPR) is an in vivo index of melanopsin-driven ipRGC photoactivity. PIPR can be assessed by chromatic pupillometry, but consensus on a standardized PIPR testing protocol has not been reached yet. The purpose of this thesis is to develop an optimized PIPR testing methodology, and to use it to investigate clinical and basic science questions related to melanopsin and ipRGCs. Based on previous pilot work on full-field chromatic pupillometry, a new and repeatable method was developed to measure PIPR induced by hemifield, central-field and full-field light stimulation. This chromatic pupillometry system was then used to investigate a series of basic science and clinical questions related to melanopsin and ipRGCs. ii Acknowledgments I would like to take this opportunity to express my gratitude to a number of people who have helped me to see through this thesis project. Without their contributions, support, advice and encouragement, this thesis would not be possible. First of all, my deepest gratitude is extended to my supervisor, Dr. Agnes Wong, for offering me this amazing opportunity to study in Canada. This research project has greatly expanded my academic horizon, and opened up many opportunities for my future career. My sincere appreciation is also extended to my co-supervisor, Dr. Herbert Goltz. Thank you for your guidance throughout the process. If it was not for your contributions, support and advice, this thesis would not be what it is today. Next, I would like to express my gratitude to members of my program advisory committee, Dr. Graham Trope and Dr. John Flanagan, for their invaluable input and support in this project. Special thanks to Manokaraananthan Chandrakumar, Jaime Sklar, Alan Blakeman, Luke Gane and Arham Raashid for their technical support. Last, but certainly not least, I would like to thank all of my family for supporting me over the years. Of course, a special mention has to go to my lovely wife Jingwen, and our daughter Sophia. Thank you for being with me and giving me unconditional love and unwavering support. This is for all of you who have made this thesis a reality. Thank you again. iii Contributions Author and degree candidate, Dr. Shaobo Lei, made primary contributions to the conception and design of the study, acquisition, analysis and interpretation of data, drafting the thesis and revising it. Program supervisors, Dr. Agnes Wong and Dr. Herbert Goltz made contributions in this thesis by providing experimental apparatus, participating study designing and thesis editing. Ms. Jaime Sklar and Mr. Manokaraananthan Chandrakumar participated in data acquisition and analysis. Mr. Alan Blakeman and Mr. Luke Gane provided technical support in the setup of the experimental apparatus; Mr. Gane also wrote the computer script that was used to analyze data. Mr. Arham Raashid provided support for statistical analysis iv Table of Contents Acknowledgments .......................................................................................................................... iii Table of Contents ............................................................................................................................ v List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................. x Chapter 1 ......................................................................................................................................... 1 1 Literature Review ....................................................................................................................... 1 1.1 General introduction ........................................................................................................... 1 1.2 Discovery and history of melanopsin-containing intrinsically photosensitive retinal ganglion cells ...................................................................................................................... 3 1.2.1 Early behavioral observations in non-rod, non-cone animals ................................. 3 1.2.2 The discovery of a non-visual photopigment: melanopsin ..................................... 4 1.2.3 The discovery of intrinsically photosensitive retinal ganglion cells ....................... 5 1.2.4 Summary ................................................................................................................. 6 1.3 Anatomical and morphological features of ipRGCs ........................................................... 7 1.3.1 ipRGCs population and distribution ....................................................................... 7 1.3.2 Morphological features of typical ipRGCs: M1 cells ............................................. 7 1.3.3 Morphological features of atypical ipRGCs: M2-M5 ............................................. 8 1.3.4 Central projections of ipRGCs ................................................................................ 9 1.3.5 Summary ............................................................................................................... 10 1.4 Physiological properties of ipRGCs .................................................................................. 11 1.4.1 Light absorption of melanopsin ............................................................................ 11 1.4.2 Menalopsin-driven phototransduction .................................................................. 12 1.4.3 Electrophysiology of ipRGCs ............................................................................... 15 1.5 Functions of melanopsin and the ipRGC system .............................................................. 21 1.5.1 Melanopsin and ipRGC function in non-image-forming photosensation ............. 21 v 1.5.2 Melanopsin and ipRGC functions in image-forming vision ................................. 26 1.6 Chromatic Pupillometry: in vivo assessment of melanopsin-driven ipRGC photoactivity ..................................................................................................................... 28 1.7 Preparation technical development: full-field chromatic pupillometry assessment of the melanopsin-driven post-illumination pupil response .................................................. 32 1.7.1 Rationale for developing full-field chromatic pupillometry ................................. 32 1.7.2 Apparatus and experiment protocols .................................................................... 33 1.7.3 Results: full-field vs central field PIPR in intensity and duration trials ............... 34 1.7.4 Discussions ........................................................................................................... 40 Chapter 2 ....................................................................................................................................... 45 2 Aims and Hypothesis ............................................................................................................... 45 2.1 Introduction ....................................................................................................................... 45 2.2 Hemifield, Central-Field and Full-Field Chromatic Pupillometry for Assessing the Melanopsin-driven Post-illumination Pupil Response: A Methodological Study ............ 46 2.3 The effect of red light exposure on pre-existing PIPR: Implementing PIPR as an in- vivo index of melanopsin photoactivity in basic science research ................................... 47 Chapter 3 ....................................................................................................................................... 49 3 Hemifield, Central-Field and Full-Field Chromatic Pupillometry for Assessing the Melanopsin-driven Post-illumination Pupil Response ............................................................. 49 3.1 Introduction ....................................................................................................................... 49 3.2 Methods ............................................................................................................................. 51 3.2.1 Participants ............................................................................................................ 51 3.2.2 Apparatus .............................................................................................................. 51 3.2.3 Experimental Conditions and Procedure .............................................................. 55 3.2.4 Data
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