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Thesis Reference Thesis The Voice of Primates: Neuro-evolutionary Aspects of Emotions DEBRACQUE, Coralie Abstract Rightly emphasized by Pascal Belin “Voices are everywhere”. From music to social conversation, the human voice has indeed the extraordinary power to communicate our everyday emotions. Shaped by millions of years of evolution, the vocal recognition of emotions guides individuals in the best decision to take. The capacity to vocally express and then identify an emotion is not a distinctive characteristic of Homo sapiens. In fact, most species in the animal kingdom have such abilities that maximize their chances of survival and reproductive success. Despite homologous traits between humans and other animals, rare are the studies using a comparative approach to better understand emotional processing in voices. To fill this gap, the present thesis aims to investigate perceptual decision-making mechanisms through emotional vocalizations expressed by humans and non-human primates (NHP), our closest relatives. According to this goal, six complementary studies were performed using imaging as well as behavioral paradigms. Reference DEBRACQUE, Coralie. The Voice of Primates: Neuro-evolutionary Aspects of Emotions. Thèse de doctorat : Univ. Genève et Lausanne, 2020, no. Neur. 278 DOI : 10.13097/archive-ouverte/unige:143258 URN : urn:nbn:ch:unige-1432583 Available at: http://archive-ouverte.unige.ch/unige:143258 Disclaimer: layout of this document may differ from the published version. 1 / 1 DOCTORAT EN NEUROSCIENCES des Universités de Genève et de Lausanne UNIVERSITE DE GENEVE SECTION DE PSYCHOLOGIE Professeur Grandjean Didier, directeur de thèse Professeur Gruber Thibaud, co-directeur de thèse THE VOICE OF PRIMATES: NEURO-EVOLUTIONARY ASPECTS OF EMOTIONS THESE Présentée à la Faculté de Psychologie et des Sciences de l’Education de l’Université de Genève pour obtenir le grade de Docteure en Neurosciences par Coralie DEBRACQUE de Cormeilles en Parisis (France) Thèse N°278 Genève Imprimeur : Université de Genève 2020 2 Published articles Gruber, T*., Debracque, C*., Ceravolo, L., Igloi, K., Marin Bosch, B., Frühholz, S., & Grandjean, D. (2020). Human Discrimination and Categorization of Emotions in Voices: A Functional Near-Infrared Spectroscopy (fNIRS) Study. Frontiers in Neuroscience, 14. https://doi.org/10.3389/fnins.2020.00570 *joint first authors Additional paper Ben-Moussa M*, Debracque C*, Rubo M*, Lange WG*. (2017) DJINNI: A Novel Technology Supported Exposure Therapy Paradigm for SAD Combining Virtual Reality and Augmented Reality. Frontiers in Psychiatry, 8:26. https://doi:10.3389/fpsyt.2017.00026 *all authors contributed equally 3 Remerciements Peu douée pour exprimer mes émotions (les cordonniers sont-ils véritablement les plus mal chaussés ?), c’est pourtant avec une facilité déconcertante que je vous remercie toutes et tous aujourd’hui, pour votre incroyable contribution à ce projet de thèse. Premièrement, je tiens à remercier le Prof. Didier Grandjean, superviseur émérite, qui part ses conseils toujours avisés et sa bonne humeur permanente, m’a fait grandir en tant que chercheur mais aussi en tant que personne. Les soirées mémorables que nous avons passées ensemble m’ont rappelé à quel point il était important de vivre ! J’aimerais également remercier mon co-superviseur, le Prof. Thibaud Gruber, qui m’a apporté une aide cruciale lors de la rédaction des articles. De plus, il m’a permis de découvrir la recherche en primatologie, univers fascinant qui rappel à l’Homme, qu’il n’ait finalement qu’un grand primate parmi tant d’autres. Un grand merci au Dr. Adrien Meguerditchian, mon « co-co-superviseur marseillais » comme j’aime l’appeler, pour cette dernière et quatrième année de thèse. Grâce à sa gentillesse et ses retards légendaires, j’ai eu l’unique opportunité de travailler avec des primates non-humains qui ont rapidement compris comment me manipuler ... Je souhaiterais également remercier les jurés présents lors de mon examen intermédiaire, mon introduction privée et finalement lors de ma défense publique: Prof. David Sander, Prof. Pascal Belin, Prof. Klaus Zuberbühler, Prof. Anne-Lise Giraud et le Dr. Roland Maurer, pour leur bienveillance et leurs questions pertinentes sur le projet. Je dois également beaucoup à mes chères et chers collègues qui ont malgré eux supporté mes blagues et mes sarcasmes durant quatre années. Vous reconnaitrez tout de même que cela animait l’open space du campus biotech! J’aimerais particulièrement remercier le Dr. Leonardo Ceravolo, pour son incroyable gentillesse et son aide plus que précieuse à la fois, dans cette thèse et dans mes essais (ratés ?) à la natation. Un grand merci à Blanca Marin Bosch, la seconde et dernière « NIRS girl » de toute la Suisse romande… Nous avons commencé la fNIRS en même temps, nous finirons avec gloire et honneur au même moment ! Dédicace particulière au Dr. Damien Benis, avec qui je débâterai encore longuement de l’utilisation d’électrodes intra corticales chez les singes et autres animaux de laboratoire. Je 4 dois cependant reconnaitre que nous sommes tous deux d’accord en ce qui concerne l’intra chez l’espèce humaine (pour ceux qui comprendront). Dans un souci de synthèse, je tenais à remercier: Dr. Simon Schaerlaeken (extraordinaire), Dr. Raphaël Thézé (Pandore), Dr. Donald Glowinski (musique), Dr. Manuella Philippa (douce), Dr. Ben Meuleman (statistiques), Patricia Cernadas (extraordinaire bis), Alexandra Zaharia (résiliente), Cyrielle Chappuis (tinder), Marion Gumy (choupinette), Sylvain Tailamée (S.A.V.) et Carole Varone (culture) pour les nombreux moments passés ensemble à discuter, rire et profiter tout simplement. Les meilleurs pour la fin ! Je remercie sincèrement mes parents pour leur soutien indéfectible durant ces 30 dernières années. Je sais d’expérience que mon sale caractère (si si ! je vous jure !) ainsi que mes changements d’humeur chaotiques, n’ont pas toujours été évident à supporter. Finalement, un remerciement un peu spécial pour mes fidèles et très chers compagnons, sans lesquels ma vie aurait été bien différente: Mr Pim’s, Cacahuète, Galac et Petit-Chat, qui ne sont malheureusement plus parmi nous ; Patapon, Pixelle et Plume, toujours en vie et heureux de l’être ! 5 Abstract in English Rightly emphasized by Pascal Belin “Voices are everywhere”. From music to social conversation, the human voice has indeed the extraordinary power to communicate our everyday emotions. Shaped by millions of years of evolution, the vocal recognition of emotions guides individuals in the best decision to take. The capacity to vocally express and then identify an emotion is not a distinctive characteristic of Homo sapiens. In fact, most species in the animal kingdom have such abilities that maximize their chances of survival and reproductive success. Despite homologous traits between humans and other animals, rare are the studies using a comparative approach to better understand emotional processing in voices. To fill this gap, the present thesis aims to investigate perceptual decision-making mechanisms through emotional vocalizations expressed by humans and non-human primates (NHP), our closest relatives. According to this goal, six complementary studies were performed using imaging as well as behavioural paradigms. Study 1 investigated the vocal recognition of emotions in human voices in implicit and explicit decoding using functional near infrared spectroscopy (fNIRS). The main objective of this first study was to demonstrate i) the involvement of distinct cerebral and behavioural mechanisms at play in biased and unbiased choices; and ii) the suitability of fNIRS to assess decision-making and emotional mechanisms. Therefore, twenty-eight participants categorized (unbiased choice) or discriminated (biased choice) angry, fearful and neutral pseudo-words in implicit (word recognition) or explicit (emotional content) decoding of emotions. fNIRS analyses revealed differences in the hemodynamic responses of the bilateral inferior frontal cortex (IFC) between the implicit and explicit decoding of emotions as well as a modulation of IFC activity depending on the categorization and discrimination tasks. These findings are supported by our behavioural data showing that participants were more accurate for explicit categorization and implicit discrimination compared to implicit categorization and explicit discrimination. Overall, our results suggest first, the existence of distinct mechanisms for both, the implicit and explicit decoding of emotions; and second, the suitability of fNIRS to assess such mechanisms in humans. The level of complexity in affective decision-making is thus at play for human voices. But do we have the same mechanisms for the processing of heterospecific vocalizations? 6 Following upon the findings of Study 1, Study 2 explored the categorization and discrimination of emotions in human voice and NHP vocalizations using fNIRS. The main aim of this experiment was to explore the involvement of similar decision-making mechanisms in cross-taxa recognition. Hence, thirty participants categorized or discriminated threatening, distressful, and affiliative contents in human voices, great ape (chimpanzee –Pan troglodytes, bonobo –Pan paniscus) and monkey (macaques –Macaca mulatta) vocalizations. fNIRS analyses interestingly revealed a distinct involvement of the prefrontal cortex (PFC) and the pars triangularis of the inferior frontal gyrus IFG (IFGtri) between the categorization and the discrimination of affects in all primate species vocalizations. Further
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