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EEG-Fmri in Epilepsy and Sleep EEG-fMRI in Epilepsy and Sleep by David T. Rollings A thesis submitted to the University of Birmingham for the degree of DOCTOR OF PHILOSOPHY School of Psychology College of Life and Environmental Sciences University of Birmingham September 2016 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Abstract This thesis used simultaneous electroencephalogram (EEG) and functional magnetic resonance imaging (fMRI) to investigate both epilepsy and sleep. Initially, EEG-fMRI was used in a cohort of patients with complex epilepsy referred from a tertiary epilepsy clinic for both pre- surgical evaluation and diagnostic reasons. The results suggest a limited utility of EEG-fMRI in the epilepsy clinic with a very complex patient group. Following on, investigation of early blood oxygen level dependent (BOLD) signal changes in a group of patients with focal epilepsy demonstrated potentially meaningful BOLD changes occurring six seconds prior to interictal epileptiform discharges, and modelling less than this six seconds can result in overlap of the haemodynamic response function used to model BOLD changes. The same analysis was used to model endogenously occurring sleep paroxysms; K-complexes (KCs), vertex sharp waves (VSWs) and sleep spindles (SSs), finding early BOLD signal changes with SSs in group data. Finally, KCs and VSWs were investigated in more detail in a group of participants under both sleep deprived and non-deprived conditions, demonstrating an increase in overall activation for both KCs and VSWs following sleep deprivation. Overall, we find early BOLD changes are not restricted to pathological events and sleep deprivation can enhance BOLD responses. Dedication This thesis is dedicated to my family. My beautiful wife Sarah, whose unconditional love and unyielding support over these years has brought me here. I am humbled in the presence of her belief in me, her beauty, her patience and strength of character, and my spirit is lifted beyond the firmament simply by that smile. My precious daughter Evie, who at 3 ½ years old has shown a level of patience and understanding that would be a credit to an adult. Her quiet words of support and encouragement, and her very being gave me constant sustenance to see this through. My son Hugo, who, on the day I write this dedication and complete this thesis, took his first steps. That cheeky grin, those cheeks, and gentle eyes make me sure that like his mother and sister, he too has inherited that smile. I could never thank my family enough, but I will spend the rest of my life trying. To my mother and father, Helena and Alec, as well as my brothers John and Paul, I am profoundly thankful for their support and belief in me, not just through my postgraduate studies, but throughout my life. Acknowledgements I would like to sincerely thank Dr Andrew Bagshaw who has not only been my supervisor over the last several years but also a very good friend. Dr Bagshaw embodies the very best qualities of a supervisor; patience, understanding, intellect, and provides constant encouragement and with any other supervisor it is very likely I would not be submitting this thesis. It is my sincere hope that we will continue to work together and carry on as good friends for many years to come. I would also like to thank Dr Pia Rothstein for imparting her SPM expertise and always offering a helping hand when needed. Also Dr Dirk Ostwald, who was a fellow postgraduate student in the early days and went to great lengths in trying to teach me, and many others, about the GLM and the various processes behind the methods commonly used in neuroimaging. Finally, I would like to thank the Neurophysiology department where I have worked for over 12 years. My fellow colleagues, Dr Colin Shirley, and my manager Satinder Bhath who have supported me throughout the years and have always kept an interest in the work I have been doing. Contents CHAPTER 1 - INTRODUCTION ............................................................................................... 1 1.1 Epilepsy ....................................................................................................................... 2 1.1.1 Overview: history and epidemiology of epilepsy ................................................ 2 1.1.2 Definition of epilepsy .......................................................................................... 6 1.1.3 Classification of epilepsy .................................................................................... 8 1.1.4 Mechanisms in epilepsy .................................................................................... 11 1.2 Sleep ........................................................................................................................... 20 1.2.1 Mechanisms of sleep ......................................................................................... 21 1.2.2 Sleep paroxysms ................................................................................................ 28 1.2.3 Epilepsy and sleep: the link ............................................................................... 34 1.3 Electroencephalography ............................................................................................. 36 1.3.1 Technical aspects of EEG .................................................................................. 37 1.3.2 Origin of EEG signals ....................................................................................... 40 1.3.3 EEG in epilepsy ................................................................................................. 46 1.3.4 EEG in sleep ...................................................................................................... 50 1.4 MRI and functional MRI ........................................................................................... 53 1.4.1 Principles of MRI .............................................................................................. 53 1.4.2 Functional MRI ................................................................................................. 56 1.4.3 Pre-processing of fMRI data ............................................................................. 60 1.5 Combined EEG and fMRI ......................................................................................... 62 1.5.1 EEG data acquisition during fMRI .................................................................... 62 1.5.2 EEG-fMRI in epilepsy ....................................................................................... 64 1.5.3 EEG-fMRI in sleep ............................................................................................ 69 1.6 Thesis overview ......................................................................................................... 72 CHAPTER 2 - UTILITY OF EEG-FMRI IN PATIENTS REFERRED FROM THE TERTIARY EPILEPSY CLINIC................................................................................................................... 73 2.1 Abstract ...................................................................................................................... 74 2.2 Introduction ................................................................................................................ 75 2.3 Methods ..................................................................................................................... 77 2.4 Results ........................................................................................................................ 80 2.5 Discussion .................................................................................................................. 90 CHAPTER 3 - EARLY HAEMODYNAMIC CHANGES OBSERVED IN PATIENTS WITH EPILEPSY AND IN A VISUAL EXPERIMENT ......................................................................... 99 3.1 Abstract .................................................................................................................... 100 3.2 Introduction .............................................................................................................. 101 3.3 Methods ................................................................................................................... 103 3.4 Results ...................................................................................................................... 107 3.4.1 Visual dataset .................................................................................................. 107 3.4.2 Epilepsy dataset ............................................................................................... 111 3.5 Discussion ................................................................................................................ 115 3.6 Conclusion ............................................................................................................... 120 CHAPTER 4 - EARLY BOLD SIGNAL CHANGES IN SLEEP PAROXYSMS ..................... 121 4.1 Abstract ...................................................................................................................
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