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Cellular Functional Architecture of the Human Cone Photoreceptor Mosaic

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Cellular Functional Architecture of the Human Cone Photoreceptor Mosaic Cellular Functional Architecture of the Human Cone Photoreceptor Mosaic By William Scott Tuten A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Vision Science in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Austin Roorda, Chair Professor Susana Chung Professor Gerald Westheimer Fall 2014 Cellular Functional Architecture of the Human Cone Photoreceptor Mosaic © 2014 by William Scott Tuten Abstract Cellular Functional Architecture of the Human Cone Photoreceptor Mosaic by William Scott Tuten Doctor of Philosophy in Vision Science University of California, Berkeley Professor Austin Roorda, Chair Chromatic and high-acuity aspects of vision are mediated by cone photoreceptors, which sample the image relayed by the eye’s optics and transduce it into the neural signals that give rise to perception. Our understanding of how individual cones function has largely been gleaned from in vitro electrophysiological preparations, which allow the experimenter to stimulate single receptors while simultaneously recording their outputs. Building upon these findings requires investigating how signals arising from single sensory input neurons are handled downstream by the nervous system, up to and including the perceptual stage. With these goals in mind, the tools to approach these questions in vivo must be developed. The challenges associated with studying the perceptions arising from single sensory receptors are not trivial—doing so requires an ability to visualize and repeatedly stimulate the receptor of interest, which can be difficult when it is situated within a densely packed array of similar cells that is itself contained within a sensory organ. The eye, however, represents a unique case because the receptor layer can be visualized directly through the transparent cornea and lens. The fidelity of this view is diluted only by optical imperfections in the refractive components of the eye. Advances in ocular imaging that have taken place over the past 20 years now make it possible to overcome these imperfections and image individual photoreceptors in vivo. The series of experiments described in this document involve the development of methods to overcome these obstacles, the application of this technology to study single-cone-driven perception in healthy subjects, and the translation of these tools to the clinical realm, where cone structure and function were studied with micron-scale resolution in patients with retinal disease. 1 TABLE OF CONTENTS Abstract ........................................................................................................................................... 1 TABLE OF CONTENTS........................................................................................................................ i LIST OF FIGURES ............................................................................................................................... v LIST OF ABBREVIATIONS ................................................................................................................. vi ACKNOWLEDGEMENTS ................................................................................................................. viii CHAPTER 1 – Imaging and Stimulating the Retina with Adaptive Optics Scanning Laser Ophthalmoscopy ............................................................................................................................. 1 1.1 Introduction .......................................................................................................................... 1 1.1.1 Optical Quality of the Eye: a Historical Overview ......................................................... 1 1.1.2 Optical Quality of the Eye: Current Measurement and Correction Techniques .......... 4 1.1.3 The Development of Adaptive Optics Scanning Laser Ophthalmoscopy ..................... 6 1.2 Methods ............................................................................................................................... 7 1.2.1 High-resolution Retinal Imaging with AOSLO ............................................................... 7 1.2.2 Stimulus Calibration ...................................................................................................... 8 1.2.3 Real-time Eye Tracking and Targeted Stimulus Delivery ............................................ 10 1.2.4 Measurement and Correction of Transverse Chromatic Aberration ......................... 11 1.3 Summary ............................................................................................................................. 12 CHAPTER 2 – Revealing a Microscopic Sensitivity Gradient in the Parafoveal Cone Mosaic ....... 13 2.1 Abstract .............................................................................................................................. 13 2.2 Introduction ........................................................................................................................ 13 2.3 Methods ............................................................................................................................. 14 2.3.1 Adaptive Optics Scanning Laser Ophthalmoscope Imaging and Stimulation ............. 14 2.3.2 Chromatic Dispersion Correction in a Multi-wavelength AOSLO ............................... 15 2.3.3 Subjects and Psychophysical Procedures ................................................................... 16 2.3.4 Data Analysis and Cone Modeling .............................................................................. 17 2.4 Results ................................................................................................................................ 19 2.4.1 Cone-sized Microstimulation ...................................................................................... 19 2.4.2 Single-cone Increment Thresholds ............................................................................. 21 i 2.4.5 Positional Effect of Stimulus Placement ..................................................................... 22 2.4.6 Light Capture Model ................................................................................................... 27 2.5 Discussion ........................................................................................................................... 31 2.6 Summary ............................................................................................................................. 33 2.7 Acknowledgements ............................................................................................................ 34 CHAPTER 3 – Functional Mapping of the Parafoveal Trichromatic Cone Mosaic ........................ 35 3.1 Abstract .............................................................................................................................. 35 3.2 Introduction ........................................................................................................................ 35 3.3 Methods ............................................................................................................................. 38 3.3.1 Cone-resolved Retinal Densitometry with AOSLO...................................................... 38 3.3.2 Generating Functional Maps of the Trichromatic Mosaic .......................................... 41 3.3.3 Data Analysis and Modeling ....................................................................................... 41 3.4 Results ................................................................................................................................ 44 3.5 Discussion ........................................................................................................................... 47 3.6 Summary and Future Directions ........................................................................................ 51 3.7 Acknowledgements ............................................................................................................ 52 CHAPTER 4 – Adaptive Optics Microperimetry: Methods and Validation in Normal Eyes and Patients with Retinal Disease ........................................................................................................ 53 4.1 Abstract .............................................................................................................................. 53 4.2 Introduction ........................................................................................................................ 53 4.3 Methods ............................................................................................................................. 55 4.3.1 Participants ................................................................................................................. 55 4.3.2 Measuring Visual Sensitivity Across Eccentricity in Normal Subjects ........................ 55 4.3.3 Choosing a Threshold Algorithm: Bland-Altman Analysis of QUEST vs 4-2 dB ........... 57 4.3.4 Automated Retrieval of Previously-Tested Locations ................................................ 58 4.3.5 Structure-Function Relationships in Normal Subjects: Probing Angioscotomas ........ 60 4.3.6 Structure-Function Relationships in Outer Retinal Disease: Two Case Reports ........ 60 4.4 Results ................................................................................................................................ 60 4.4.1 Measuring Visual Sensitivity Across Eccentricity
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