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Vision Anomalies in Migraine Vision Anomalies in Migraine Bao Ngoc Nguyen Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy September 2013 Department of Optometry and Vision Sciences The University of Melbourne ii Abstract The aim of this thesis was to investigate visual responses of people with migraine in between attacks, in order to infer possible mechanism/s underlying migraine pathophysiology. The proposed neural abnormality in migraine is cortical hyperexcitability. To measure neural activity in the visual cortex, previous studies have measured the cortical evoked response to patterned visual stimulation; however, these have yielded inconsistent results. This raises the possibility that mechanisms other than cortical hyperexcitability might contribute to vision anomalies in migraine. In this thesis, people with migraine (with and without aura) were compared to non- headache control participants. By measuring the cortical and retinal evoked responses simultaneously, Experiment 1 aimed to determine whether abnormalities in the cortical evoked response could be explained by dysfunction occurring earlier in the visual pathway. People with migraine showed reduced cortical responses but normal retinal function, indicating that the cortical deficits were unlikely to be a result of retinal dysfunction. The purpose of Experiment 2 was to consider whether loss of visual field sensitivity in people with migraine was related to abnormal cortical and/or retinal function. Performance was compared between two visits: less than and more than seven days after a migraine. Migraine sufferers showed repeatable deficits in the cortical evoked response that were not worse in the days immediately after migraine, implying stability of the cortical deficit. In contrast, Experiment 2 found further reductions in sensitivity in the days immediately after a migraine attack, confirming previous reports. Some individuals showed monocular and/or localised visual field defects that were worse after an attack, suggesting that these might be retinal effects of migraine. iii The final experiment explored the balance between inhibition and excitation, one of the competing theories underlying cortical hyperexcitability in migraine. Using a perceptual centre-surround task to assess inhibition and excitation simultaneously, Experiment 3 found increased suppression in people with migraine, indicating increased inhibition, for stimuli of lower centre contrast. The contrast-dependent changes in perception were associated with abnormal contrast gain, as demonstrated by increased cortical evoked responses at low contrast and decreased responses at high contrast. Thus, Experiment 3 provided further evidence for cortical hyperexcitability leading to abnormal visual perception in between migraine attacks. However, cortical hyperexcitability cannot account for all vision anomalies in migraine. Rather, there is also the potential for adverse sequelae of migraine, possibly outside of the brain, in otherwise healthy and asymptomatic individuals (Experiments 1 and 2). This thesis has implications for the use of non-invasive, clinical tests of visual function in clinical and research settings. People with migraine, on average, showed abnormal visual responses, even when asymptomatic and tested more than a few days after a migraine. This result reinforces previous suggestions that regular migraine sufferers should be excluded from normative databases. Additionally, there was considerable inter-individual variability in the visual responses, demonstrating that only a subset of individuals with migraine fall outside the range of normal visual performance. Further investigation of these particular individuals is potentially more informative regarding the pathophysiological processes of this debilitating condition. iv Declaration This is to certify that: i. the thesis comprises only my original work towards the PhD except where indicated in the Preface, ii. due acknowledgement has been made in the text to all other material used, iii. the thesis is fewer than 100 000 words in length, exclusive of tables, maps, bibliographies and appendices. Bao Ngoc Nguyen v vi Preface Part of the work presented in Chapter 2 has been published in the following journal article: Nguyen, B.N., McKendrick, A.M. and Vingrys, A.J. (2012). “Simultaneous retinal and cortical visually evoked electrophysiological responses in between migraine attacks.” Cephalalgia 32: 896-907. and has been published in abstract form in the following conference proceedings: Nguyen, B.N., McKendrick, A.M. and Vingrys, A.J. (2011). “Simultaneous pattern electroretinogram and visual evoked response in migraine.” Investigative Ophthalmology and Visual Science 52: E-Abstract 3521. Part of the work presented in Chapter 3 has been published in the following journal article: Nguyen, B.N., Vingrys, A.J. and McKendrick, A.M. (2013). “The effect of duration post-migraine on visual electrophysiology and visual field performance in people with migraine.” Cephalalgia. Aug 22. [Epub ahead of print]. Part of the work presented in Chapter 4 has been published in abstract form in the following conference proceedings: vii Nguyen, B.N., Vingrys, A.J. and McKendrick, A.M. (2012). “Increased perceptual surround suppression of moving stimuli in migraine with aura.” Clinical and Experimental Ophthalmology 40: 133. As primary author of the aforementioned publications, I was primarily responsible for the planning, execution, and preparation of work for publication in collaboration with my two supervisors, Associate Professor Allison McKendrick and Professor Algis Vingrys who provided assistance in the experimental design, data analysis, and editing of manuscripts. The programming of the perceptual task in Chapter 4 was conducted by Associate Professor Allison McKendrick. Ms Jia Jia Lek assisted in the optometric screening and electrophysiological testing of control participants in Chapter 4. viii Acknowledgements To my supervisors, Associate Professor Allison McKendrick and Professor Algis Vingrys – thank you for everything. To the Faculty of Science at the University of Melbourne – thank you for providing financial support through the Elizabeth and Vernon Puzey Postgraduate Scholarship. To the Department of Optometry and Vision Sciences – thank you for providing me with a home for many years. To Associate Professor Andrew Metha, Dr Michael Pianta, and Dr Larry Abel – thank you for being part of my PhD Advisory Panel. To Dr Bang Bui, Dr Anne Weymouth, Dr Josephine Battista, Dr Zheng He, Dr Phillip Bedggood – thank you for helping with the initial setup and sanity checking of equipment and test protocols. To the members, past and present, of my two research laboratories, the Clinical Psychophysics Unit and the Visual Functions Laboratory – thank you for keeping me fit and fed. To all the research students and participants who volunteered for the experiments – thank you for the many hours you sat through. To my family – thank you for understanding my selfish needs. And to my dearest Jonathan – thank you for the love and life away from work. ix x Table of Contents Abstract................................................................................................................................iii Declaration...........................................................................................................................v Preface ............................................................................................................................... vii Acknowledgements............................................................................................................ix Table of Contents ..............................................................................................................xi List of Figures................................................................................................................... xv List of Tables .................................................................................................................. xvii 1 | A Review of the Literature...........................................................................................1 1.1 Introduction ...............................................................................................................1 1.2 Migraine ......................................................................................................................1 1.2.1 Classification and symptoms ...........................................................................2 1.2.2 Pathophysiology of the migraine attack.........................................................4 1.2.3 Genetics of migraine...................................................................................... 10 1.3 Cortical hyperexcitability....................................................................................... 11 1.3.1 Evidence for hyperexcitability from the visual cortex.............................. 11 1.3.2 Changes in cortical hyperexcitability ........................................................... 25 1.3.3 Investigations of mechanisms of hyperexcitability.................................... 27 1.4 Potential for pre-cortical dysfunction ................................................................. 38 1.4.1 Parallel pathways............................................................................................. 39 1.4.2 Concurrent pre-cortical and cortical dysfunction...................................... 45 1.5 Potential
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