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Novel Photoreceptor Cells, Pupillometry and Electrodiagnosis in Orbital, Vitreo-Retinal and Refractive Disorders

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Novel Photoreceptor Cells, Pupillometry and Electrodiagnosis in Orbital, Vitreo-Retinal and Refractive Disorders Imperial College London Novel Photoreceptor Cells, Pupillometry and Electrodiagnosis in Orbital, Vitreo-retinal and Refractive Disorders Farhan Husain Zaidi A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy of the University of London and the Diploma of Imperial College Faculty of Medicine Imperial College London, the University of London Course: Clinical Medicine Research Registered Subject Fields: Vision Science, Ophthalmology and Surgery; Specific Areas:- Vision Science: primarily ganglion cells in the eye and orbit (physiology, disease, psychophysics, anatomy); visual pathways; comea/lens Ophthalmology: primarily clinical subspecialties of oculoplastic/orbital surgery and medical/surgical retina; cataract/refractive, glaucoma, general Surgery: primarily orbital, vitreoretinal and facial plastic particularly ocular adnexal surgery; refractive surgery including cataract and cornea Full-time postgraduate student Departments of Ophthalmology, 2002, and Visual Neuroscience, 2002-5, after which full-time research concluded, formal thesis writing commenced, with submission in 2007; examined January 2008 Campuses: St Mary's and the Western Eye Hospitals, Hammersmith Hospitals and South Kensington Supervisors and Examiners Course Supervisors Dr MJ Moseley. Hon. Senior Lecturer in Ophthalmology, Imperial College London; Senior Lecturer in Ophthalmology, City University; formerly Senior Lecturer in Ophthalmology, Imperial College London. Prof AR Fielder. Professor and Head of Dept. of Ophthalmology, City University; Hon. Consultant Ophthalmologist St Mary's and the Western Eye Hospitals; formerly Professor and Head of Dept. of Ophthalmology, Imperial College London. Prof MW Hankins. Professor of Visual Neuroscience, Wellcome Trust Centre for Human Genetics, University of Oxford; Visiting Professor of Visual Neuroscience, Imperial College London; formerly Professor of Visual Neuroscience, Imperial College London. Thesis Examiners The subject fields and the thesis in particular were examined by internal and external examiners for the Doctorate of Philosophy of the University of London and the Diploma of Imperial College by viva voce, 1400 to 1800, at the Western Eye Hospital, Imperial College Healthcare NHS Trust, London, on January 14, 2008. This was successfully passed pending routine minor thesis alterations which are herein complied with as checked and approved by the examiners. Prof PA Bloom (internal examiner). Consultant Ophthalmic Surgeon, St Mary's and the Western Eye Hospitals, London; Service Director, the Western Eye Hospital, Imperial College Healthcare NHS Trust; Hon. Senior Lecturer in Ophthalmology, Imperial College London; Hon. Prof. Middlesex University, London. Relevant special interests: clinical ophthalmology and surgery; doctorate supervision and publications in peer-reviewed journals e.g. electrophysiology and pupillometry in glaucoma and retinal diseases; ganglion cell function; clinical studies in cataract /refractive surgery. Dr LG Ripley (external examiner). Reader in Electronic Engineering, University of Sussex. Relevant special interests: biomedical engineering applied to basic and clinical vision science including pupillometry (invention of the Sussex pupillometer), theory and testing of colour vision (invention of the automated tritan discrimination test); doctorate supervision and publications in peer-reviewed journals e.g. colour vision and contrast sensitivity in orbital surgery (decompression of compressive optic neuropathy in thyroid eye disease) and vitreo-retinal disease (macular hole surgery and screening of diabetic retinopathy). Mid-Course Examiners Prof RG Foster. Professor of Circadian Neuroscience and Head of Departments of Ophthalmology and of Circadian and Visual Neuroscience, Wellcome Trust Centre for Human Genetics, University of Oxford; Visiting Professor of Biology, Imperial College London; formerly Professor of Molecular Neuroscience, Imperial College London. Relevant special interests with doctorate supervision and peer-reviewed publications in circadian biology and non-rod non-cone photoreception, including its discovery in mammals. Dr K Gregory-Evans. Reader in Molecular Ophthalmology, Imperial College London; Hon. Consultant Ophthalmologist, St Mary's and the Western Eye Hospitals. Relevant special interests with doctorate supervision and peer-reviewed publications in genetic and clinical aspects of retinal diseases; retinal electrophysiology; outer photoreceptor dystrophies. 2 Acknowledgements I acknowledge the award of a Lindo Wing Fellowship from St Mary's and the Western Eye Hospitals to help support presentation of part of this work at international conferences. I am grateful for the support given during my research at Imperial College London by the Department of Ophthalmology (Head, Prof AR Fielder), later merging to become the Department of Visual Neuroscience (Head, Prof C Kennard), and especially by my supervisors — above all to Dr Merrick Moseley as my principle supervisor for the entire duration of this work, to Professor Alistair Fielder of City University (at the time of Imperial College London) who sponsored my work while he was at Imperial College London and continued to support it thereafter, and to Professor Mark Hankins of the University of Oxford (at the time of Imperial College London) who chaired my mid-course examination and later joined in the administrative supervision of this work. Professor Russell Foster of the University of Oxford (at the time of Imperial College London) and Dr Kevin Gregory-Evans of Imperial College London kindly provided valued suggestions as the mid-course examiners and access to additional facilities in their laboratories. Certain analyses of data were performed using specific computer software in conjunction with Dr. Stuart Peirson and Dr. Katharina Wulff of the University of Oxford, both previously of Imperial College London, and who are specially acknowledged in the relevant chapters. Clinical collaborators at St Mary's and the Western Eye Hospitals very kindly allowed access to their patients. There is no conflict of interest declared by the author The work presented in this thesis is my own Farhan Husain Zaidi 3 Dedication I am grateful to my family fo7 their support over a period of full-time research as a clinician, especially to my late father for his encouragement during this time. For their patience and encouragement I dedicate this thesis to them and to the light that guides. 4 Abstract This thesis presents work that quantifies visual potential and associated visual functions in diseased retina and intra-orbital optic nerve. The aim of the first half of this thesis is to employ pupillometry to differentiate topographic regions of diseased eyes and optic nerves in patients with model diseases which offer potential for clinical application. These disease processes are compressive and traumatic orbital lesions affecting the optic nerve, those of the vitreo-retina, and, to a lesser degree, those affecting the refractive interfaces of the eye. Many of these findings are explained by putative non- rod non-cone photoreception in humans. The second half of this thesis investigates the possible existence of this novel receptor in healthy humans and in subjects with disease using a variety of techniques. The final strand to this thesis explores the hitherto unknown visual potential of the receptor. The principal experimental methods are pupillometry, selectively complemented by electrophysiology. In studying the putative photoreceptor, additionally, behavioural experiments are also employed — actigraphy to study circadian rhythms and psychophysical tests to study visual potential. Imaging and other clinical tests are also used. The general format to test most hypotheses comprises the measurement of pupil waveform parameters such as amplitude and re-constriction in assays based on stimulus paradigms designed to elicit spatial and temporal photoreceptor responses. Non-pupillometric tests utilise standard protocols (electroretinogram, 2-alternative forced choice test, visual acuity, visual field, wrist actigraphy, validated sleep questionnaires, optical coherence tomography, computerised tomography (CT), magnetic resonance imaging (MRI), and fundus fluorescein angiography). This thesis finds that full-field pupil luminance and colour responses are useful in determining macula status in subretinal neovascular membranes (SRNs), retinal detachments, and in diagnosing compressive and traumatic optic neuropathies considered for orbital decompression/surgical exploration. Inter-eye comparison (intra-subject) of pupil responses between healthy and diseased eyes is useful in diagnosing disease using the pupil waveform. The effects of stimulus duration, intensity and photopigment bleaching (adapting light, photostress) are also considered. Cataract is found to cause a variety of changes in pupil perimetric sensitivity, attributed to index myopia, chromatic aberration, and scatter. Study of achromatic and chromatic pupil gratings responses in orbital diseases, proliferative vitreoretinopathy, and amblyopia, parallel the visual responses expected in these conditions and are shown to be cortically-influenced. In this thesis a new index of pupil escape-type events is described, the pupil evasion ratio. Its spectral profile suggests rod, cone, and non-rod non-cone activity from a novel fifth photoreceptor. An assay for the putative photoreceptor is developed and incorporates sustained blue light which
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