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Imaging Correlates of the Epileptogenic Zone and Functional Imaging Correlates of the Epileptogenic Zone and Functional Deficit Zone using Diffusion Tensor Imaging (DTI) By Beate Diehl Thesis submitted for the degree of Doctor of Philosophy Department of Clinical and Experimental Epilepsy Institute of Neurology University College London Beate Diehl - PhD Thesis DECLARATION I, Beate Diehl, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. Beate Diehl London, October 2010 - i - Beate Diehl - PhD Thesis ABSTRACT Focal epilepsy is a common serious neurologic disorder. One out of three patients is medication refractory and epilepsy surgery may be the best treatment option. Neuroimaging and electroencephalography (EEG) techniques are critical tools to localise the ictal onset zone and for performing functional mapping to identify the eloquent cortex in order to minimise functional deficits following resection. Diffusion tensor magnetic resonance imaging (DTI) informs about amplitude (diffusivity) and directionality (anisotropy) of diffusional motion of water molecules in tissue.This allows inferring information of microstructure within the brain and reconstructing major white matter tracts (diffusion tensor tractography, DTT), providing in vivo insights into connectivity. The contribution of DTI to the evaluation of candidates for epilepsy surgery was examined: 1. Structure function relationships were explored particularly correlates of memory and language dysfunction often associated with intractable temporal lobe epilepsy (TLE; chapters 3 and 4). Abnormal diffusion measures were found in both the left and right uncinate fasciculus (UF), correlating in the expected directions in the left UF with auditory memory and in the right UF with delayed visual memory performance. Examining the arcuate fasciculus (AF), bilateral diffusion changes were found with correlations between left AF DTI measures and language scores. 2. The second aim of this thesis was to validate DTT results and test the hypothesis that cortical language areas determined by cortical stimulation serve as anchor points for the tractography defined AF (chapter 5). Subdural grid contacts overlying anterior language cortex co-localised in 84.2% with the AF, and in 55.8% in posterior language areas. This provides some validation that the AF - ii - Beate Diehl - PhD Thesis reconstructed using DTT subserves language function, but further study is needed. 3. Lastly, seizure propagation was investigated in a case series of patients with cortical dysplasia (chapter 6). Reduced connectivity with reduced arborization and thinning of the fibre bundles between subcortical WM and the dysplastic cortex was demonstrated. Fibre tracts reconstructed from regions underlying the ictal onset zone showed abnormal connectivity. - iii - Beate Diehl - PhD Thesis ACKNOWLEDGEMENTS This work was conducted part time, initially as a non-resident PhD candidate. The experimental work, data acquisition and main part of the data analysis were performed at the Epilepsy Center, Cleveland Clinic Foundation, Cleveland, USA, where I worked until March 2008. I completed the analysis, resultant publications and the thesis itself following my relocation to the National Hospital for Neurology and Neurosurgery, London, UK, in April 2008. During the course of the past four and half years, the number of people who have contributed their time, work, advice, knowledge and goodwill is vast. First and foremost I would like to thank my supervisors. Working with Prof. John Duncan has opened my eyes to applying advanced neuroimaging techniques to epilepsies. His vision and incredible organisational skills remain a great inspiration as he spearheads one of the most successful groups in epilepsy and imaging and I am honoured to work with him now in the Department of Clinical and Experimental Epilepsy and at the National Hospital for Neurology and Neurosurgery. Prof. Hans O. Lüders, my mentor and teacher, has influenced and shaped my way of thinking regarding focal epilepsies in an unprecedented manner. He is a dedicated teacher and an inspiration to countless US and international fellows whom he has taught how to analyse EEGs and localise the focus during the pre-surgical evaluation. His academic rigour, enthusiasm and passion for neurophysiology and epilepsy have left an unforgettable impression on me. Devising meaningful, translational research requires a solid understanding of the clinical needs; in this context I fondly recall the many discussions I had with Dr Holly Morris. His vast clinical experience has deeply shaped my clinical practice, and inspired inquisitiveness. In addition, his encouragement played a crucial role - iv - Beate Diehl - PhD Thesis in my successfully obtaining funding, in order to perform the research which is the basis of this thesis. At the Cleveland Clinic, Jean Tkach, PhD was instrumental in providing the MRI physics framework for data acquisition and implementation of the programmes for DTI analysis and tractography. Her incredible dedication to support imaging research in epilepsy at CCF is fondly remembered. Eric LaPresto had laid the groundwork for much of the image processing and registration at CCF by programming the software. I am most grateful for Jean and Eric’s incredible patience with generations of MDs including myself, who used these tools for clinical research. In the last year, Zhe Piao strengthened the engineering team and worked hand in hand with Eric and his help was most appreciated. Collaboration with Robyn Busch, PhD was crucial for expert advice concerning neuropsychological measures and the neuropsychological data collection and analysis. Her help in maintaining the database and communicating with the Institutional Review Board in order to keep the ethics approvals current and complying with the yearly reporting requirements was essential and much appreciated. Of my colleagues at NHNN, I wish to particularly mention Dr. Shelagh Smith. Her constant encouragement, support and help to master all challenges that came with my recent relocation were crucial to allow me to complete this thesis. Equally, Prof. Martin Koltzenburg’s support as chair of the Department of Clinical Neurophysiology was critical to facilitate my relocation to London and in supporting my research. His advice for professional development was instrumental to encourage my successful application for a HEFCE DoH Clinical Senior Lectureship award, to be taken up from 2011. Finally, the Early Career Clinician Scientist award (Milken Family Foundation) allowed me to conduct many aspects of the research presented in this thesis. I - v - Beate Diehl - PhD Thesis am deeply grateful to their generous support for two consecutive years of funding (2006 and 2007). Lastly I would like to acknowledge my patients, who I had the honour of treating in my first years of independent professional practice. Their unique diseases and the questions they asked, have inspired me to pursue the answers. STATEMENT OF WORK DONE BY MYSELF AND OTHERS I performed the following work in all studies underlying this thesis: Study designs and methods, ethics approvals, grant funding, patient selection, a majority of the informed consent procedures (less than 20% patient informed consent was obtained either via a collaborator (Robyn Bush) or a research nurse), data transfers and image analyses including all coregistration procedures, ROI placement and analyses, tractography, all statistical data analyses (in part in consultation with Robyn Busch,PhD), review and collection of clinical data, generation of the first drafts of manuscripts, manuscript submission, and all revisions. Furthermore, I presented all data as either posters or platform presentations in national and international meetings. Some of the patients I personally followed at the Cleveland Clinic and they were also admitted under my care during their presurgical investigation with intracranial EEG. Finally, I performed the cortical stimulation procedures in some patients as part of their clinical care; in other cases, the stimulation data were reviewed retrospectively as part of the research protocol for the study. As mentioned in the acknowledgements, the following people were instrumental in providing the technical framework and support: Jean Tkach, PhD, Eric LaPresto, MSc, Zhe Piao, MSc. In an advisory function, the Neuroradiologist Dr. Paul Ruggieri participated in study design. Radiographers of the Neuroradiology Department at CCF acquired the clinical MRI scans and the DTI sequence typically as a short additional scan. Robyn Busch, PhD and her team performed the Neuropsychological evaluation of the patients and also advised on statistical - vi - Beate Diehl - PhD Thesis data analysis and the manuscripts concerned with neuropsychological correlations of DTI measures. - vii - Beate Diehl - PhD Thesis DEDICATION I would like to dedicate this work to my family. My parents, Amalie and Werner Diehl, have kept a watchful and ever supportive eye on my moves and relocations between Germany, France, the USA and the UK. They have enabled me to go to Medical School and embark on the long programme of training to gain all the exceptional experiences I have had. Most importantly, I have to thank my husband Neill Dunfee, who has been so incredibly understanding, following me to London and continuing to put up with the endless trials and tribulations of balancing a clinical job with research, meeting deadlines and all the
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