Domain of Physiology and Fribourg Cognition Center Department of Medicine University of Fribourg Switzerland Multisensory integration in non-human primates and humans Thesis Presented to the Faculty of Science of the University of Fribourg (Switzerland) in consideration for the award of the academic grade of Doctor rerum naturalium Field : Neuroscience By Florian Lanz From Switzerland Thesis No xxxx Imprimerie Saint-Paul 2013 Accepted by the Faculty of Science of the University of Fribourg (Switzerland) upon the recommendation of Professor Eric Rouiller, Doctor Gérard Loquet, Professor Pierre Lavenex and Professor Micah Murray. Fribourg, Thesis supervisor : Dean : Prof. Eric Rouiller Prof. Fritz Müller 2 “Qu’importe la surdité de l’oreille, quand l’esprit entend? La seule surdité, la vraie surdité, la surdité incurable, c’est celle de l’intelligence” Victor Hugo à Ferdinand Berthier “Ce qui est essentiel à la perception sensorielle n’est pas ce qui sépare les sens les uns des autres, mais ce qui les unit entre eux; à chacune de nos expériences internes (même non sensorielles) et à notre environnement.” Erich von Hornbostel, The Unity of the Senses, 1927. 3 Acknowledgements With this paragraph, I would like to extend my grateful thanks to all the people who have contributed to the outcome of this thesis. I want first to express my appreciation to Professor Eric Rouiller, my thesis supervisor, who welcomed me in his research group and allowed me to do this work in the best conditions. Thank you for your patience, your proofreading, your invaluable piece of advices and for your presence throughout this path. Dr. Gérard Loquet please accepts my sincere thanks for your patience, your availability and your invaluable advices both in professional and private field. Thank you for all the time that you have spared for the elaboration of Matlab and TDT programs and for all these proofreadings so important and beneficial. I sincerely thank Véronique Moret for her advice, for her help and her time dedicated to the analysis and the creation of multimedia supports (figures and videos). Thank you for the shared discussions, not always scientifically related. A big thank you to Joseph Corpataux, Jacques Maillard and Laurent Bossy for taking care of our animals. Thank you for your help, your advice as for the animal detention. And thank you for all these good moments spent outside the institute (e.g. dinners shared together). A thank you to Xavier Lanz and colleagues for their help in the elaboration and the manufacturing of our various devices. Thank you to Professor Micah Murray and to Professor Pierre Lavenex, both experts for my thesis. Thank you for your corrections and for your time. Thanks to Adjia Hamadjida and Simon Badoud for having shared scientific and not scientific moments around a coffee or a meal. Thanks to David Michel and Karine Sciboz for your advice and the dinners shared together. A special thanks to my parents, my family and Julie for their support without defect and who helped me to successfully reach the point where I am today. Finally I must express my appreciation to each collaborator from Professor Eric Rouiller’s laboratory who welcomed me and with whom I have learned by one way or another so much in sciences. Thank you for the good atmosphere, the advice and the support. And thanks to Lionel and Jazz 4 Contents Foreword ................................................................................................................................... 8 Avant-Propos et résumé ......................................................................................................... 10 Glossary ................................................................................................................................... 12 I. Introduction ......................................................................................................................... 17 I.1 Auditory System ............................................................................................................. 17 I.1.1 Theoretical considerations ....................................................................................... 17 I.1.1.1 Anatomy ............................................................................................................ 17 I.1.1.2 Physiology of hearing ....................................................................................... 20 I.1.1.3 Ascending auditory pathway ............................................................................. 23 I.2 Visual system .................................................................................................................. 25 I.2.1 Theoretical considerations ....................................................................................... 25 I.2.1.1 Anatomy ............................................................................................................ 27 I.2.1.2 Physiology of the vision .................................................................................... 28 I.2.1.3 Visual Ascending Pathways .............................................................................. 30 I.3 Somatosensory system .................................................................................................... 32 I.4 Multisensory integration ................................................................................................. 34 I.4.1 Generalities .............................................................................................................. 34 I.4.1.1 Illusions ............................................................................................................. 37 I.4.1.2 Benefits ............................................................................................................. 41 I.4.1.3 Reaction time .................................................................................................... 42 I.4.2 Probabilistic models ................................................................................................. 44 I.4.3 Spatiotemporal perspective ...................................................................................... 45 1.4.4 Types of crossmodal integration ............................................................................. 46 1.4.4.1 Stochastic resonance ........................................................................................ 46 1.4.4.2 Phase coherence ............................................................................................... 47 I.4.5 Neuronal perspective................................................................................................ 48 I.4.5.1 Bayes integration concept ................................................................................. 48 I.4.5.2 Multisensory integration concept ...................................................................... 50 I.4.5.3 Multisensory neurons ........................................................................................ 51 I.4.5.3.1 Superior colliculus ..................................................................................... 51 I.4.5.3.2 Multisensory integration principles ........................................................... 54 5 1.4.5.4 The cortical primary sensory areas ................................................................... 57 I.4.5.4.1 Auditory cortex .......................................................................................... 57 I.4.5.4.2 Visual cortex .............................................................................................. 59 I.4.5.4.3 Somatosensory cortex ................................................................................ 61 I.4.5.4.4 Premotor cortex .......................................................................................... 61 I.4.6 Audio-visual interactions ......................................................................................... 64 I.4.7 Hierarchy of integration of cross modal stimuli ...................................................... 67 I.5 Objective of the Research ............................................................................................... 69 II. General Materials and Methods ...................................................................................... 72 II.1 Subjects .......................................................................................................................... 72 II.1.1 Non-human primates .............................................................................................. 72 II.1.2 Human subjects ....................................................................................................... 73 II.2 Behavioural Protocol ..................................................................................................... 74 II.2.1 Stimuli .................................................................................................................... 74 II.2.2 Sensory-motor task ................................................................................................. 75 II.2.3 Auditory and visual threshold ................................................................................. 76 II.2.4 Multisensory integration ......................................................................................... 77 II.3 Surgery in non-human primates .................................................................................... 78 II.4 Different steps for monkeys behavioural training and CT and MRI