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Peripersonal Space: a Multisensory Interface for Body-Objects Interactions

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Peripersonal Space: a Multisensory Interface for Body-Objects Interactions Peripersonal space : a multisensory interface for body-objects interactions Claudio Brozzoli To cite this version: Claudio Brozzoli. Peripersonal space : a multisensory interface for body-objects interactions. Human health and pathology. Université Claude Bernard - Lyon I, 2009. English. NNT : 2009LYO10233. tel-00675247 HAL Id: tel-00675247 https://tel.archives-ouvertes.fr/tel-00675247 Submitted on 29 Feb 2012 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. N° d’ordre 233-2009 Année 2009 THESE DE L‘UNIVERSITE DE LYON Délivrée par L’UNIVERSITE CLAUDE BERNARD LYON 1 ECOLE DOCTORALE Neurosciences et Cognition DIPLOME DE DOCTORAT (arrêté du 7 août 2006) soutenue publiquement le 20/11/2009 par M. Claudio BROZZOLI PERIPERSONAL SPACE : A MULTISENSORY INTERFACE FOR BODY-OBJECTS INTERACTIONS Directeur de thèse : Dr. FARNÈ Alessandro, Ph.D. JURY: Prof. Y. Rossetti M.D., Ph.D. Dr. A. Farnè Ph.D., D.R. Prof. S. Soto-Faraco Ph.D. Prof. C. Spence Ph.D. Prof. O. Blanke M.D., Ph.D. Prof. F. Pavani, Ph.D. Dr. J.-R. Duhamel Ph.D., D.R. A Fede, perché questo spazio mi ha preso nel tempo che a volte era suo AKNOWLEDGEMENTS It has been amazingly exciting. I started something I didnt know what it could be. Then the trip kept on, impossible to be stopped, terrible sometime, but always exciting. And if during this long ride I loved everything I did, it is also because without doubt Im in debt to many people who have contributed to my work, both directly and indirectly. Or just because they were present. Or they would have liked to be. Thus, in random order, thank you all. Dopo avermi iniziato come laureando al pungente piacere della stimolazione elettrica, allimportanza dei catch trials e alla conoscenza dellestinzione, come se non bastasse, mi ha anche introdotto allo “spazio peripersonale”. Solo per questo direi già: grazie Ale! Poi cè tutto il resto, le neuroscienze che ha continuato a farmi scoprire in questi anni con lo stesso piacere dun gioco, la fiducia che mi ha dato, la libertà che mi ha lasciato di spaziare dove più avevo voglia di giocare. E ancora, i dischi di Luigi Tenco, il prosecco e laffetto. Per tutto quello che in questi anni ho potuto realizzare e per tutto quello che questi anni hanno fatto di me, grazie Ale, il Professore che mi ha insegnato, il Supervisore che mi ha guidato e incoraggiato, lAmico che sei stato fin dallinizio. Mes sincères remerciements vont à Alice, dont les mots directes mes fascinent et mont fait du bien plus de ce que jai pu montrer. Merci pour le support que tu ma donné et qui va au delà des neurosciences et du français; pour le bourguignon qui a pas encore trouvé des égales. Avec Ale et Giulio vous avez été mon repère familiale à Lyon. Per chiudere questa famiglia scientifica, ringrazio di tutto cuore Lucilla, la sorella scientifica, ma soprattutto lamica che ha ascoltato, risposto, considerato, capito, cercato e trovato il mio affetto. Lamica che mi mancherà. La ringrazio fortemente anche per il lavoro che abbiamo realizzato insieme e che senza di lei sarebbe stato niente affatto lo stesso e sicuramente meno divertente. Je remercie vivement tous les chercheurs et les composents de lUnité INSERM U864. Travailler à lunité a été un plaisir et latmosphère toujours tellement agréable que jespère de pouvoir encore avoir loccasion de vous retrouver. Un grand et chaleureux merci à tous les étudiants de lUnité INSERM 864: Laurence, Muriel, Alessia et tous les autres qui mont taquiné et incouragé quand necéssaire. A special thanks goes to Nicholas Holmes and Tamar Makin with whom collaborating has been interesting and not less amazing. They introduced me efficiently to the TMS technique. And lot of TV series. A Alfredo e Pina, che instancabili, mi hanno seguito in tutti i miei tentativi e sostenuto lungo diverse vie, va il mio grazie più constante e longevo. Pour le K factor que ma fait aimé Lyon, les amis qui ont contribué à mon bien être, en trouvant toujours la façon pour remplir mes pauses de la rédaction de thèse, entre le 203 et le Broc, Eva, JB, Virginie et tous les autres: merci! v vi CONTENTS RESUME’ 1 ABSTRACT 3 INTRODUCTION 5 Multisensory perception 8 Multisensory perception in human behaviour 10 Multisensory attention 12 The spatial organization of numbers 14 CROSS-MODAL SHIFT OF ATTENTION 17 Discussion 29 Multisensory integration through anatomical convergence 29 Multisensory interactions through feedback on unisensory areas and inter- connections among unisensory areas 31 Back-projections from multisensory higher-level to unisensory lower-level areas 32 Early interactions between unisensory areas 34 Conclusion 35 vii Multisensory and motor representations of peripersonal space 36 Multisensory features of peripersonal space: Visuo-tactile interaction around the body 37 Parietal Visuo-tactile interactions 37 Premotor visuo-tactile interactions 42 Subcortical visuo-tactile interactions 46 Dynamic feature of peripersonal space representation 46 A visuo-tactile network 50 Motor features of peripersonal space: Visuo-tactile interactions around the acting body 51 Inferior premotor cortex 52 Mirror neurons: a particular class of visuo-motor neuron 54 Parietal areas 55 Lesion studies 57 Conclusion: A multisensory-motor network for peripersonal space 58 Multisensory based peripersonal space in humans 60 Modularity of space through cross-modal extinction 61 EXTINCTION 63 Peripersonal space in humans: neuropsychological evidence 81 Peripersonal space in humans: evidence from healthy behaviour 84 viii Cross-modal congruency effect: a perceptual paradigm for the investigation of the peripersonal space representation in healthy humans 86 Spatial modulation of CCE 88 Body-part-centred reference frame for the CCE 88 Tool-use dependent modulations of CCE 89 Peripersonal space in humans: neuroimaging studies 91 Conclusions 91 Peripersonal space: a multisensory interface for body-object interactions? 93 What kind of body-object interactions can the body-centered PpS representation subserve? 95 CCE in action 96 The multisensori-motor task 97 The kinematic recording of movements: a real-time method for linking multisensory perception and action 99 The kinematics of grasping 100 Neural network for grasping 102 Conclusion: kinematic-perceptual co-recording 104 RESULTS 105 STUDY 1 110 STUDY 2 143 ix STUDY 3 153 DISCUSSION 185 Main results 187 Peripersonal space: an interface for avoidance reactions 189 A comparison with non-human primates studies 190 Peripersonal space: an interface for voluntary actions 192 A comparison with non-human primates studies 193 CONCLUSIONS AND PERSPECTIVES 197 REFERENCES 203 x RESUME’ L’ESPACE PERIPERSONNEL: UNE INTERFACE MULTISENSORIELLE POUR LES INTERACTIONS ENTRE LE CORPS ET LES OBJETS Notre habilité à interagir avec les objets du monde nécessite l’intégration d’informations provenant de différents canaux sensoriels, dans le cadre de la construction d’une représentation de l’espace en particulier des informations visuelles et tactiles. L’espace péripersonnel et l’intégration visuo-tactile ont été l’objet d’importantes recherche récemment. Des études neurophysiologiques chez le primate non-humain ont montré l’existence de neurones bimodaux activés à la fois par des stimulations tactiles et par des stimulations visuelles si ces dernières étaient présentées près d’une partie du corps (par exemple la main). Il a été proposé que ces neurones bi-modaux constituent le substrat neuronal de la représentation de l’espace péripersonnel. Les études neuropsychologiques menées chez des patients présentant une extinction cross-modale consécutive à une lésion pariétale droite ont permis de suggérer l’existence du même type de représentation de l’espace péripersonnel chez l’homme. Les données issues des études en neuroimagerie fonctionnelle sont venues par la suite conforter cette idée. Plus récemment, à travers l’utilisation d’outils, des données acquises chez le primate humain et non humain ont révélé les propriétés dynamiques de cette représentation spatiale. Selon notre hypothèse la représentation de l’espace péripersonnel est une interface présidant aux interactions du corps avec les objets du monde externe. Nous avons donc évalué le rôle et l’état de l’espace péripersonnel lors de l’exécution de mouvements volontaires vers des objets (comme une simple saisie) et lors de mouvements involontaires d’évitement. Lors d’une première série d’expériences nous avons étudié les coordonnées spatiales du codage des objets qui soudainement se rapprochent du corps grâce à la mesure des potentiels évoqués moteurs. Cette étude a révélé que l’espace péripersonnel joue un rôle dans la représentation des objets approchant le corps et dans la sélection des mouvements appropriés en réponse. Lors d’une seconde série d’expériences nous avons utilisé un paradigme d’interférence visuo-tactile couplé à l’enregistrement cinématique des mouvements de saisie afin d’examiner la représentation de l’espace péripersonnel lors de 1 l’exécution d’actions volontaires. Cette approche novatrice nous a permis de mettre en évidence que l’action
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