The Neurobiology of Meditation for the Control of Pain

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The Neurobiology of Meditation for the Control of Pain i Université de Montréal The neurobiology of meditation for the control of pain par Joshua A. Grant Département de Physiologie Faculté de médicine Thèse présentée à la Faculté des études supérieures et postdoctorales en vue de l‟obtention du grade de Ph.D. en sciences neurologiques Janvier 2011 © Joshua Grant 2011 ii Université de Montréal Faculté des études supérieures et postdoctorales Cette thèse intitulée: The neurobiology of meditation for the control of pain présentée par: Joshua A. Grant a été évaluée par un jury composé des personnes suivantes: Trevor Drew, président-rapporteur Pierre Rainville, directeur de recherche Adrianna Mendrek, membre du jury Catherine Bushnell, examinateur externe John Kalaska, représentant du doyen de la FES iii Résumé La douleur est une expérience multidimensionnelle comportant des aspects sensoriels, émotionnels et cognitifs. Il a été montré que cette expérience peut être modulée par des facteurs psychologiques ou des interventions cognitives comme l‟attention, la distraction, l‟hypnose ou les attentes. La tradition orientale suggère également que la pratique de la méditation pourrait avoir des effets analgésiques. D‟un point de vue théorique, plusieurs mécanismes pourraient expliquer ces effets. Cependant, très peu d‟études ont testé ces hypothèses. Les études présentées dans cette thèse avaient donc pour objectif d‟examiner les mécanismes analgésiques de la méditation. Dans un premier temps, une étude psychophysique a été réalisée afin de comparer les réponses à la douleur entre des adeptes de la méditation Zen et des sujets contrôles, dans différentes conditions attentionnelles. Durant la condition attentionnelle de type « mindful », les adeptes de la méditation ont présenté une plus faible sensibilité à la douleur, des réponses attentionnelles à la douleur atypiques et une diminution de la perception de la douleur associée à l‟entraînement à la méditation. Une deuxième étude a été réalisée en imagerie par résonance magnétique fonctionnelle (IRMf) avec des groupes de participants similaires. Dans une condition sans méditation, les adeptes de la méditation ont présenté de plus fortes réponses nociceptives dans les régions primaires de la douleur. Les régions cérébrales associées aux processus d‟évaluation, à la mémoire et aux émotions ont quant à elles montré une diminution d‟activité. De plus, cette diminution était plus importante chez les adeptes de la méditation les plus expérimentés et elle était associée à des iv évaluations de douleur plus faibles. Par ailleurs, des changements de connectivité fonctionnelle entre le cortex préfrontal et une région primaires de la douleur étaient associés à la sensibilité à la douleur chez les adeptes de la méditation. Finalement, une étude d‟imagerie cérébrale structurale (publiée comme deux études séparées) a été réalisée pour examiner les différences d‟épaisseur corticale entre les groupes, pour des régions associées à la douleur. Les adeptes de la méditation ont présenté une épaisseur plus importante de matière grise dans plusieurs régions associées à la douleur et l‟attention. De plus, ces différences étaient associées à une mesure expérientielle de l‟attention, à la sensibilité à la douleur et à l‟expérience de méditation. Dans l‟ensemble, ces résultats suggèrent que la méditation pourrait influencer la perception de la douleur par des changements fonctionnels et physiques dans le cerveau. De plus, le patron d‟activation et la modulation de l‟expérience paraissent uniques en comparaison à ceux d‟autres interventions, ce qui suggère qu‟un état de détachement et un focus mental favorisent la dissociation entre les aspects désagréables et sensoriels d‟un stimulus nociceptif. Mots-clés: douleur, nociception, méditation, Zen, mindfulness, modulation de la douleur, IRMf, émotion, auto régulation, attention v Abstract Pain is a multidimensional experience involving sensory, emotional and cognitive components. It is well known that mental factors or interventions such as attention, distraction, hypnosis or expectation can modulate painful experience. Traditional claims from the East suggest meditative practice may also have analgesic effects. Theoretically there are multiple avenues by which such practices could act, however little work has been done in this regard. The works presented in this dissertation were intended to address this paucity of research by contrasting pain perception in practicing meditators and non-meditating control participants. A psychophysical pain study was first conducted with practitioners of Zen meditation contrasting their responses to pain with control subjects during different attention conditions. Meditators were found to have lower baseline pain sensitivity, atypical attention-related pain responses and training-related reductions of pain ratings during mindful attention. A second study, with similar groups of subjects, employed functional magnetic resonance imaging (fMRI) during the perception of pain. In a non-meditative state, meditators were found to have stronger nociceptive- related brain activity in primary pain regions while simultaneously exhibiting reductions of activation in brain areas associated with appraisal, memory and emotion. These later effects were largest in the most advanced practitioners and were associated with the lowest pain ratings. Importantly, changes in functional connectivity between prefrontal cortex and a primary pain region predicted baseline pain sensitivity in the meditation group. Finally, a structural imaging experiment (published as two separate reports) was conducted to examine whether grey matter vi thickness may differ, in pain-relevant ways, between the groups. Meditators were found to have thicker regional grey matter in several pain and attention-related regions which corresponded both with an experiential measure of attention, pain sensitivity and meditation experience. Taken together these results suggest meditation may influence pain perception through functional as well as physical effects on the brain. The pattern of brain activity and experience modulation appears to be unique, when contrasted with previously studied interventions, and suggests that adopting a non-elaborative but focused mental stance may allow one to dissociate the bothersome qualities from the sensory aspects of a noxious stimulus. Key words: pain, nociception, meditation, Zen, mindfulness, pain modulation, fMRI, emotion, self regulation, attention vii Table of Contents Résumé..................................................................................................... iii Abstract.................................................................................................... v Table of Contents..................................................................................... vii List of Tables........................................................................................... ix List of Figures.......................................................................................... x Abbreviations........................................................................................... xi Dedication................................................................................................ xiii Acknowledgements.................................................................................. xiv Forward.................................................................................................... xv GENERAL INTRODUCTION................................................................ 1 The Neurobiology of Pain................................................................ 2 Brain Imaging and Pain Modulation................................................. 5 Introduction to Meditation................................................................ 10 Science and Meditation..................................................................... 14 Meditation and Pain.......................................................................... 17 Hypotheses........................................................................................ 18 References......................................................................................... 20 ARTICLES.............................................................................................. 27 Article #1 - Pain sensitivity and analgesic effects of mindful states in Zen meditators: a cross-sectional study........................................ 28 Article #2 - A non-elaborative mental stance and decoupling of executive and pain-related cortices predicts low pain sensitivity in Zen meditators.................................................................................. 65 Article #3 - Cortical thickness and pain sensitivity in Zen meditators......................................................................................... 103 viii Article #4 - Associations between cortical thickness, attentional absorption and prior mental training: possible implications for disorders of attention........................................................................ 137 GENERAL DISCUSSION...................................................................... 163 Summary of Our Results.................................................................. 164 Attention........................................................................................... 165 Mindfulness...................................................................................... 169 Meditation and Pain.........................................................................
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