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Brain Function, Connectivity and Structural Abnormalities

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Brain Function, Connectivity and Structural Abnormalities Department of Psychiatry and Clinical Psychobiology School of Medicine The vegetative and the minimally conscious states: brain function, connectivity and structural abnormalities. Thesis presented by Davinia Fernández-Espejo To obtain the degree of Doctor of Philosophy from the University of Barcelona In accordance with the requirements of the European PhD Diploma Supervised by Dr. Carme Junqué, University of Barcelona, Spain Dr. Adrian Owen, MRC Cognition and Brain Sciences Unit, Cambridge, UK Doctoral Programme in Biomedicine Dr. Carme Junqué i Plaja, Professor at the University of Barcelona, and Dr. Adrian M. Owen, Senior scientist/Assistant director at the MRC Cognition and Brain Sciences Unit (UK), CERTIFY that they have supervised and guided the PhD thesis entitled “The vegetative and the minimally conscious states: brain function, connectivity and structural abnormalities”, presented by Davinia Fernández-Espejo. They hereby assert that this thesis fulfils the requirements to be defended for the Degree of Doctor of Philosophy. Signature, Signature, Dr. Carme Junqué i Plaja Dr. Adrian M. Owen University of Barcelona MRC Cognition and Brain Sciences Unit Barcelona, November 2010 III The work reported in this thesis was carried out at the Neuropsychology Group, Department of Psychiatry and Clinical Psychobiology, School of Medicine, University of Barcelona, and the Impaired Consciousness Research Group, Wolfson Brain Imaging Centre, Addenbrooke´s Hospital, and the MRC Cognition and Brain Sciences Unit. The groups belong respectively to the Institut d‟Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) and the University of Cambridge and Medical Research Council. The present work, as well as the studies that have been included, have been financially supported by the following grants and institutions: pre-doctoral fellowship (Formación de Profesorado Universitario [FPU]) from the Spanish Ministry for Education (AP2006-00862) to Davinia Fernández-Espejo; SAF2007-66077 from the Spanish Ministry of Science and Innovation and 2009SGR0941 from the Generalitat de Catalunya to Carme Junqué; National Institute for Health Research, Biomedical Research Centre at Cambridge, UK Department of Health Technology Platform, in addition to grants from the U.K. Medical Research Council (U.1055.01.002.00007.01) and the James S. McDonnell Foundation to Adrian Owen. IV Agradecimientos Acknowledgements Gracias a todos los que, de manera directa o indirecta y sabiéndolo o no, habéis hecho posible esta tesis. En especial: A mis directores de tesis, la Dra. Junqué y el Dr. Owen: Carme, por darme la oportunidad de formar parte de este grupo, por compartir conmigo tu pasión por la ciencia, guiarme y apoyarme durante estos años y, sobre todo, por haber hecho que me sienta querida y valorada en todo momento y que sepa que la puerta siempre estará abierta. ¡Moltes gràcies! Adrian, thanks for all the doors you´ve opened for me, all your help, support and for that ‘magic’ ability you have for finding always the perfect way out of any problem I´ve had. Also for trusting me to be part of the Canadian adventure! A todos los miembros del Departamento de Psiquiatría y Psicobiología Clínica. En especial al Dr. Pere Vendrell, el Dr. David Bartrés-Faz y Pilar Bouzas. Pere, gracias por hacer que todo esto funcione, estar siempre dispuesto a ayudar, tu capacidad de crítica constructiva y por esas conversaciones en las que intentamos arreglar el mundo de las que tanto he disfrutado. David, por haber tenido siempre palabras de ánimo y porque ha sido un placer colaborar contigo. Pilar, gracias por tu ayuda y por contagiar serenidad en los momentos de ‘crisis de papeleo’. Y, por supuesto, gracias a todos los compañeros del Grupo de Neuropsicología, sin excepción, a los que ya os habéis ido, los que os acabáis de incorporar, los que nos habéis acompañado sólo unos meses y, sobre todo, a aquellos con los que he compartido cada día. Porque, aunque suene a tópico, entre todos habéis convertido este grupo en una gran familia con la que disfrutar de las alegrías y compartir frustraciones y confidencias. Porque gracias a vosotros estos cuatro años han sido una experiencia inolvidable y porque gracias a vuestro apoyo, aún en los momentos más duros siempre me he levantado cada mañana con ganas de venir al labo. En especial a: Giusi, Naro y Sara, mis tres doctoras favoritas, Eva y Leyre, los dos soletes del labo, Benji, mi compi en los primeros pasos, Blanca, Bárbara, Cris Sánchez, Bea, Eider, Roser, Dídac, Joana, Cleo, Silvia, Julia, Nuria Pujol, Dani, Cris Solé, Xavi y Hugo. Pero sobre todo a los que, de vosotros, habéis cruzado las puertas del labo y pasado a formar parte de mi vida como amigos. Mi niña italiana, mis compis del norte y mis catalanas favoritas, espero que sepáis lo importantes que sois para mí. Gracias por TODO! Al Institut de Neurorehabilitació Guttmann, en especial a la Dra. Montse Bernabeu y la Dra. Teresa Roig por vuestro trabajo en el proyecto, vuestra colaboración, disponibilidad y amabilidad. A Rocío, la Dra. Sánchez- V Carrión, con la que compartí mis inicios en la neuroimagen. También a Marilina y a Gisela, las siempre agradables voces al otro lado. Y por supuesto a todas las familias de los pacientes. A la Dra. Neus Fábregas y a Eva Rivas del Servicio de Anestesiología y Reanimación del Hospital Clínic. A la Dra. Maria Antònia Poca y a Eli, del Servicio de Neurocirugía del Hospital Vall d´Hebron. A todos los profesionales del Centre de Diagnostic per la Imatge, en especial la Dra. Núria Bargalló, César, Santi, Manel y Alicia. Y por supuesto al Dr. Carles Falcón. To the Impaired Consciousness Research Group, the people at the HSB and the people at the CBU. In particular thanks to Prof. Pickard and Dr. Coleman, for giving me the opportunity of joining the team and for looking after me in Addenbrooke’s, and to Guy Williams, for all your help. Especial thanks to Damian Cruse, Tristán Bekinschtein, Martin Monti, Beth Parkin, Srivas Chennu, Moos Peeters, Louise Goupil, Jess Grahn and Cristina Nombela: you made the months I spent in Cambridge one of the happiest times of my life, both professional and personally. Thank you, gracias, grazie, dhanyavaad, merci, dankzij! I hope our paths will meet again.... in any Continent ;) Tris, gracias por toda tu ayuda, tu apoyo y tu generosidad. Tampoco me olvido de las chicas Bek: Ali y Luna. Los tres tenéis en mí una amiga para siempre. Marie, thanks for being the perfect housemate and friend! Also to Anne, Richard, Pedro, Paula, Anna.… and all the wonderful people I´ve meet during my months in Cambridge. Damian, thanks for all your help with this thesis but, especially thanks for being always there, for your patience and understanding, for knowing how to listen and for the amazing times we always have together. A mi gente asturiana, mis amigos de siempre. En especial a Lusi, Maru, Pepe, Nuria y Nano. Gracias por aguantar las ausencias, por cuidar de mí y por hacerme saber que, aunque os tenga lejos, siempre estáis ahí para lo que necesite. A Óscar, porque contigo comencé el camino y me has acompañado una gran parte de él. Gracias por todo lo compartido. Y el mayor agradecimiento de todos a mi familia, porque vosotros, más que nadie, habéis hecho esto posible. En especial: a mis padres, ejemplo de superación y de lucha. Sin vuestra generosidad, vuestro cariño y apoyo incondicional y vuestra capacidad de sacrificio nunca habría llegado hasta aquí. Gracias por estar ahí y por hacerme sentir cada día orgullosa del lugar del que provengo. A Yoli, mi mejor amiga, mi mayor apoyo y la única persona del mundo capaz de hacerme entrar en razón. A Jaime, el mejor cuñado que nadie podría desear. A la abuela y a Yayina, allá donde esté, por el coraje y por la dulzura infinita. Y a Vera, la sonrisa que hace que cualquier problema, por grande que sea, se desvanezca en un segundo. ¡GRACIAS! Davinia VI A mi familia, CONTENTS Page Foreword XI Glossary of abbreviations XIII List of figures XV List of tables XVI INTRODUCTION 1 1. Consciousness, awareness and wakefulness 3 1.1. Theoretical framework 3 1.2. Anatomy: structures of wakefulness and awareness 4 2. Disorders of consciousness: definition and clinical aspects 8 2.1. Coma, vegetative state and minimally conscious state 8 2.2. Aetiology 9 2.3. Epidemiology: prevalence and incidence 10 2.4. Prognosis 12 3. Neuropathology: post-mortem findings in DOC patients 15 4. Diagnostic challenges: differential diagnosis, behavioural assessment and misdiagnosis 20 5. Neuroimaging the disorders of consciousness 25 5.1. Functional neuroimaging 25 5.1.1. Activation studies: detecting covert cognitive function 25 5.1.2. Brain function at rest 32 5.2 Structural MRI studies in DOC patients 33 5.3. Electrophysiological studies 35 5.4. Contributions to diagnosis and prognosis 36 APPROACH, OBJECTIVES AND HYPOTHESES 39 1. Approach and general objectives 41 2. Specific objectives and hypotheses 43 METHODS 47 1. Participants 49 IX 2. Clinical and behavioural assessment 51 2.1. Clinical assessment 51 2.2. Behavioural assessment 51 3. Magnetic Resonance Imaging acquisition 52 3.1. Functional MRI 52 3.2. T1-weighted structural MRI 52 3.3. Diffusion tensor imaging 53 4. Neuroimaging techniques 54 4.1. fMRI analysis 54 4.2. DTI analysis 54 4.3. Volume and shape analysis 55 5. Statistical analysis 56 6. Methodological pitfalls 57 RESULTS 59 1. Study I: Cerebral response to speech in the vegetative and minimally conscious states after traumatic brain injury 61 2. Study II: Combination of diffusion tensor and functional magnetic resonance imaging during recovery from the vegetative state 71 3. Study III: Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state 81 4 Study IV: Reductions of thalamic volume and regional shape changes in the vegetative and the minimally conscious states 91 GENERAL DISCUSSION 99 CONCLUSIONS 111 SUMMARY OF THE THESIS 115 1.
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