The Voice of Primates: Neuro-evolutionary Aspects of Emotions

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Thesis

Reference

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.

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

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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

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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

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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

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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 !

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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?

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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 (IFG^tri) between the categorization and the discrimination of affects in all primate species vocalizations. Further analyses also demonstrated that the correct categorization of agonistic chimpanzee and bonobo calls as well as affiliative chimpanzee vocalizations were associated to a decrease of activity in bilateral PFC and IFG^tri. On the contrary, the accurate discrimination of agonistic chimpanzee vocalizations was correlated to bilateral enhancement of activity in the frontal regions. Finally, our behavioural results showed that to the exception of threatening bonobo calls, human participants were able to discriminate all affective cues in all primate species while for the categorization task, they were unable to do so for macaque vocalizations. Together, these findings point out the difference between discrimination and categorization processes as well as acoustic divergence between chimpanzee and bonobo vocalizations. Acoustical analyses are thus needed to better understand the recognition of emotions in NHP vocalizations.

In order to assess the role of acoustic features in cross-taxa recognition, Study 3 investigated using a phylogenetic and acoustic perspective perceptual decision-making mechanisms at play in the identification of affects in human and NHP vocalizations. The aim of this study was to demonstrate the importance of acoustic and phylogenetic proximities in such processes. For this purpose, sixty-eight participants performed the paradigm described in Study 2. Our analyses revealed the existence of a closer acoustic similarity between human and chimpanzee vocalizations than between human voices and calls expressed by bonobo and macaque species. Consequently, participants were more accurate to categorize and discriminate affective cues in chimpanzee vocalizations compared to bonobo or macaque calls. Interestingly, our behavioural results also showed the ability of human participants to identify distressful and affiliative macaque calls during discrimination while in the categorization task they were only capable of doing so for affiliative vocalizations. Overall,

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our findings support the distinction between categorization and discrimination mechanisms revealed in Studies 1 and 2. Furthermore, the difference of recognition performance between chimpanzee and bonobo – macaque vocalizations underline the importance of both acoustic and phylogenetic distances triggering an additional question:

are acoustic and phylogeny essential to involve brain regions usually associated with the processing of conspecific vocalizations?

To answer this question, Studies 4 and 5 explored the recognition of human and NHP species vocalizations in temporal voice areas (TVA) and IFG using functional magnetic resonance imaging (fMRI). Twenty-five participants were asked to categorize the species (human, chimpanzee, bonobo, and macaque) that expressed the vocalizations. Wholebrain analyses revealed i) the involvement of left TVA and pars triangularis, pars opercularis and pars orbitalis (excepted for bonobos) of bilateral IFG for the categorization of NHP vocalizations; ii) an enhancement of activity in all subparts of IFG for the correct recognition of chimpanzee and macaque calls (left pars orbitalis excluded for macaques); iii) an involvement of the pars triangularis of IFG for the correct categorization of bonobo screams; and iv) an increase of activity in bilateral TVA for the categorization of human and chimpanzee vocalizations compared to bonobo and macaque screams. Following this, functional connectivity analyses showed a similar coupling between right and left TVA for the identification of human voices and chimpanzee calls. Finally, our behavioural results demonstrated the capacity of human participants to accurately recognize all primate species, to the exception of bonobos. Hence, together, our results suggest that humans are capable of recognizing most of the primate species. However, phylogenetic, acoustic and behavioural proximities seem required to enhance activity in the TVA and all subparts of IFG.

Finally, in order to close the comparative loop, it was essential to investigate the auditory processing at play in NHP. The goal of Study 6 was, as a proof of concept, to demonstrate the suitability of fNIRS to explore vocal recognition mechanisms in NHP. For this purpose, we tested fNIRS on three female adult baboons anesthetized with a minimum amount of propofol. Two passive tasks were performed. In the first one, experimenters extended several times the right or left arm of the anesthetized subject. In the second task, using headphones, white noises, agonistic chimpanzee and baboon vocalizations were

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stimulations revealed for the three baboons contralateral activity of the motor cortex depending on the right or left arm movements. Similarly, for one subject, contralateral activity of the temporal cortex was found depending on the lateralization of the sounds. In addition, stimuli broadcast in stereo increase the oxygenated haemoglobin more in the right temporal cortex. Overall, our results support the suitability of fNIRS to assess the modulation of brain activity in NHP. Further analyses in Study 6, currently in process, will investigate vocal recognition processing in baboons.

In sum, using an evolutionary perspective, the present thesis significantly improves at the cerebral and behavioural levels our knowledge of emotional processing through the human recognition of affects in conspecific and heterospecific vocalizations. Importantly, the current project will lead to further non-invasive investigations in NHP.

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Abstract in French

Mentionné à juste titre par Pascal Belin « Les voix sont partout ». De la musique aux conversations sociales, la voix humaine a le pouvoir extraordinaire de communiquer quotidiennement nos émotions. Influencée par des millions d’années d’évolution, la reconnaissance vocale des émotions permet de guider les individus dans leur prise de décision.

La capacité d’exprimer vocalement puis identifier une émotion n’est pas une caractéristique d’Homo sapiens. En effet, dans le règne animal, la majorité des espèces possède également de telles aptitudes, permettant de maximiser leur chance de survie et leur succès reproducteur.

Bien que l’Homme ait des traits communs avec les autres primates, rare sont les études utilisant une approche comparative afin de mieux comprendre les processus émotionnels en jeu dans la voix. Pour combler cette lacune, cette thèse a pour but d’explorer les mécanismes de prise de décision, à travers les vocalisations émotionnelles exprimées par des humains et des primates non-humains (NHP), nos plus proches cousins. Dans ce but, six études complémentaires analysant des données cérébrales et comportementales ont été réalisées.

L’Etude 1 a permis d’investiguer la reconnaissance vocale implicite et explicite des émotions à travers les voix humaines grâce à la Spectroscopie proche infrarouge fonctionnelle (fNIRS). L’objectif principal de cette première étude était de démontrer i) les mécanismes cérébraux et comportementaux liés à une prise de décision biaisée ou non biaisée ; et ii) la pertinence de la fNIRS dans l’évaluation des mécanismes émotionnels et décisionnels. Par conséquent, vingt-huit participants ont catégorisé (choix non biaisé) ou discriminé (choix biaisé) implicitement (reconnaissance sémantique) ou explicitement (reconnaissance émotionnelle) des pseudo-mots prononcés avec un ton de colère, de peur ou neutre. Les analyses fNIRS ont alors révélé une modulation de la réponse hémodynamique, dans le cortex frontal inférieur (IFC), selon la reconnaissance implicite ou explicite des émotions.

De même, les analyses ont démontré une modulation de l’activité dans l’IFC, liée à la tâche de catégorisation ou discrimination. Ces résultats sont confirmés par nos données comportementales. En effet, nous avons par exemple montré que les participants étaient plus performants dans la tâche de catégorisation explicite que dans la tâche de discrimination implicite. Dans l’ensemble, nos résultats soutiennent premièrement, l’existence de mécanismes distincts pour la reconnaissance implicite et explicite des

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complexité du choix influence donc la reconnaissance émotionnelle dans les voix humaines.

Mais qu’en est-il des vocalisations hétérospécifiques ?

Faisant suite aux résultats de l’Etude 1, l’Etude 2 a permis d’explorer avec la fNIRS, la catégorisation et la discrimination des émotions à travers les voix humaines et les vocalisations de NHP. Le but de cette expérience était d’investiguer les mécanismes de prise de décision, impliqués dans la reconnaissance des émotions exprimées par diverses espèces de primates. Pour cela, trente participants ont catégorisé ou discriminé l’affiliation (positif), la menace et la détresse dans des voix humaines, des vocalisations de grands singes (chimpanzé –Pan troglodytes, bonobo –Pan paniscus) et de singes (macaque –Macaca mulatta).

Les analyses fNIRS ont révélé une implication distincte du cortex préfrontal (PFC) et du pars triangularis du gyrus inferieur frontal (IFGtri) dans la catégorisation et la discrimination des affects à travers toutes les vocalisations primates. D’autres analyses ont aussi démontré que, la catégorisation des affects négatifs dans les vocalisations de chimpanzés et de bonobos, était associée à une baisse d’activité dans le PFC et l’IFG^tri. A l’inverse, la discrimination des affects négatifs dans les vocalisations de chimpanzés, était significativement corrélée à une hausse d’activité dans les régions frontales. Enfin, nos résultats comportementaux ont montré la capacité des participants à discriminer tous les affects à travers toutes les vocalisations (à l’exception de la menace dans les vocalisations de bonobos). A contrario, les participants ont été bien incapables de catégoriser les affects dans les vocalisations de macaques. Ensemble, nos résultats suggèrent des différences entre les processus de catégorisation et de discrimination, ainsi qu’une divergence acoustique entre les vocalisations de chimpanzés et de bonobos. Une analyse acoustique nous a donc semblé être nécessaire, pour mieux comprendre la reconnaissance humaine des émotions à travers les vocalisations des NHP.

Afin d’évaluer le rôle des composantes acoustiques dans de tels processus, l’Etude 3 a eu pour but d’explorer, grâce à une perspective phylogénétique et acoustique, les mécanismes de décision émotionnelle en jeu, dans l’identification des affects à travers les voix humaines et les vocalisations de NHP. Pour cela, soixante-huit participants ont réalisé le même paradigme que celui décrit dans l’Etude 2. Nos analyses ont alors révélé l’existence de similarités acoustiques plus importantes entre les voix humaines et les vocalisations de chimpanzés que pour les autres espèces. En conséquence, les participants furent meilleurs à

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intéressante, nos données comportementales ont aussi démontré la capacité des participants, à discriminer la détresse et l’affiliation dans les vocalisations de macaques.

Cependant, dans la tâche de catégorisation, seul le contenu affiliatif de ces vocalisations a pu être identifié par les participants. Par conséquent, nos résultats supportent une distinction entre les mécanismes de catégorisation et de discrimination révélés dans les Etudes 1 et 2. De plus, les différences de performances entre les vocalisations chimpanzés et les vocalisations bonobos, soulignent l’importance de la distance phylogénétique et acoustique dans ces processus. Mais ces deux facteurs sont-ils primordiaux pour impliquer des régions cérébrales habituellement associées aux vocalisations conspécifiques ?

Pour répondre à cette question, les Etudes 4 et 5 ont investigué, avec l’imagerie par résonnance magnétique fonctionnelle (IRMf), la reconnaissance des vocalisations humaines et NHP, dans les aires temporales de la voix (TVA) et l’IFG. Vingt-cinq participants ont donc catégorisé les vocalisations de quatre espèces de primates (humain, chimpanzé, bonobo et macaque). Les analyses d’imagerie cérébrale ont révélé i) l’implication des TVA gauches et du pars triangularis, pars opercularis et pars orbitalis (excepté pour les bonobos) de l’IFG, pour la catégorisation des vocalisations de tous les NHP ; ii) une augmentation de l’activité dans toutes les sous-parties de l’IFG (à l’exception du pars orbitalis gauche pour les macaques), pour la reconnaissance correcte des vocalisations de chimpanzés et macaques; iii) une implication du pars triangularis de l’IFG pour la catégorisation correcte des vocalisations de bonobos; et iv) l’activation des TVA pour la catégorisation des vocalisations humaines et de chimpanzés. De même, les analyses de connectivités fonctionnelles ont montré un couplage similaire entre les TVA des hémisphères droit et gauche, pour l’identification des voix humaines et des vocalisations de chimpanzés. Enfin, nos données comportementales ont démontré la capacité des participants à reconnaitre la majorité des espèces de primates. Ensemble, nos résultats suggèrent qu’une proximité phylogénétique, acoustique et comportementale est nécessaire pour impliquer les TVA et l’ensemble des sous parties de l’IFG.

Afin de clore la boucle comparative, il était essentiel d’investiguer les processus auditifs en jeu chez les NHP. Le but de l’Etude 6 était donc, en tant que preuve de concept, de démontrer la pertinence de la fNIRS pour explorer les mécanismes de reconnaissance vocale chez les NHP. Pour cela, nous avons testé la fNIRS sur trois femelles babouins adultes

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réalisées. Dans la première, les expérimentateurs ont mobilisé plusieurs fois le bras droit ou gauche du sujet anesthésié. Dans la deuxième tâche, à l’aide d’un casque audio, des bruits blancs ainsi que des vocalisations de chimpanzés et de babouins ont été diffusés en stéréo ou latéralisés dans l’oreille droite ou gauche. Les analyses fNIRS des stimulations motrices ont alors révélé, pour les trois babouins, une activité controlatérale du cortex moteur, en fonction des mouvements passifs du bras droit ou gauche. De même, pour un seul sujet, une activation controlatérale du cortex temporal a été démontrée selon la latéralisation des sons.

De plus, d’autres analyses ont montré que les stimuli diffusés en stéréo avaient significativement plus activé le cortex temporal droit de ce même sujet. Dans l’ensemble, nos résultats confirment la pertinence de la fNIRS pour mesurer l’activité cérébrale chez les NHP. De futures analyses dans l’Etude 6, toujours en cours, exploreront les processus impliqués dans l’exposition à des vocalisations de babouins et de chimpanzés.

En résumé, utilisant à la fois une perspective évolutionnaire et des données cérébro- comportementales, cette thèse contribue à améliorer la compréhension des processus émotionnels en jeu dans les vocalisations conspécifiques et hétérospécifiques. Enfin, ce projet conduira je l’espère, à de futures investigations non-invasive chez les NHP.

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Theoretical Part

« J’aime trop les humains ! J’aime qu’ils me servent, j’aime les regarder pleurer, j’aime les regarder souffrir, j’aime les regarder vivre, j’aime les savoir ignorants de ma tendresse à leur égard, j’aime les savoir convaincu de mon incompétence à comprendre leur monde, de mon incapacité à les écouter et partager leurs peines et leurs tristesses. Ne suis-je pas qu’un misérable singe […] le chimpanzé sympathique ? »

Wajdi Mouawad, Anima, Chapter II Bestiae Fabulosae, Pan Troglodytes.

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1. Abstract of Literature Review

Mechanisms underlying the human recognition of emotions are still misunderstood. Mainly focused on Homo oeconomicus and its rationality, studies on decision-making¹ processes have investigated only late how emotional experiences affect our daily choices.

Yet, for our survival², it is crucial to distinguish a friendly situation from an agonistic one, in order to approach or avoid the source of these emotions. Thus, this ability to recognize emotional signalling must rely on old evolutionary bases. In fact, identifying emotional cues in order to make adaptive choices is also primordial across the animal kingdom, with the effect of increasing survival chances of an individual from a given species.

Despite innate mechanisms and homologous traits between humans and other animals, only few studies have used a comparative approach to explore the possible capacity of humans to recognize emotions expressed by other animals, especially non-human primates, our closest relatives. Moreover, most of these studies have investigated such processes through facial expressions and little is known about the human recognition of emotions in primate vocalizations. The present thesis attempts to fill this gap, exploring behavioural and cerebral mechanisms underlying the human recognition of emotions in human voices, great ape and monkey calls.

Human behaviours, cognition or even emotions were shaped through millions of years of evolution. From our common ancestor with chimpanzees and bonobos 6-8 million years ago to Homo sapiens, human’s abilities have changed. Taking in consideration this extraordinary history has become crucial in affective sciences for a general understanding of emotional processing. However, evolutionary theories have been denied or ignored by most of the scientific community during a long time. Darwinism and its impact on human and animal³ research, especially in the affective domain, was only recognized late (Section 2.1). Scientists of the 20-21th centuries underlined the importance of evolution in human daily life, highlighting for example that arousal or emotional valence promote survival. Thus, researchers started to investigate affective communication in mammals, especially in primates, and comparative approaches emerged to explore cross-taxa recognition in humans (Section 2.2).

Evolution theories are part of the great human history (Section 2.1.1). Going back to Antiquity, most ancient civilizations already understood or believed that species change

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over time. Since this extraordinary period of knowledge, evolutionary thought continued to progress through ages, encountering criticisms and rejection from a part of the scientific community influenced by morality or religion (Section 2.1.1.1). However, during the 19^th century, scientists such as Darwin and Wallace underlined once again the importance of evolutionary mechanisms, specifically natural selection, to understand the global history of mankind. The latter theory is the basis of a modern view of evolutionary thought (Section 2.1.1.2). Since the 20th century, the scientific community accepts the modern synthesis of evolution. Theories in psychology, especially in affective sciences (Section 2.1.2), have integrated this new point of view to investigate the evolution of emotional processing in human (Section 2.1.2.1) but also in other animals (Section 2.1.2.2).

Emotions and evolution are closely related. Affective processes rely on vocalisations in humans and other species to promote the survival of individuals (Section 2.2.1). In fact, the prosodic modulation of utterances in human voices can signal, among other things, emotional cues from a speaker to a receiver, allowing the latter to react adequately to a potential danger conveyed for instance, by a fearful or an angry prosody in the speaker’s voice (Section 2.2.1.1). Since the last decade, comparative approaches have emerged in neurosciences and psychology to explore the human identification of affects in other species’ vocalizations (Section 2.2.1.2). However, studies on this topic are still scarce and none of them have investigated at both the behavioural and cerebral levels the differences of mechanisms related for instance to the identification task itself (e.g. categorisation or discrimination processing). Consequently, research to fill this gap is mandatory. Moreover, emotional processing being crucial to attention, social interaction and more generally to survival, affective mechanisms can also be found in other primate vocalizations (Section 2.2.2) at the acoustic (Section 2.2.2.1) and cerebral level (Section 2.2.2.2).

2. Literature review

2.1. A Brief history of Evolutionary Theory 2.1.1. Development of Evolutionary Thought

From Antiquity to the 21th century, evolutionary thought has been discussed through the ages. In the Ancient Greece and the Roman Empire, philosophers, scientists and poets of their time debated the origin of humankind. Despite the fact that the first evolutionary

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ideas were emerging, they were not sufficient to explain the appearance of human and animal beings on Earth, facing the strong belief in divine intervention for the creation of life. Due to the power of religion, evolutionary thought was thus ignored until the Age of Enlightenment. The 18^th century was indeed the time of an important philosophical revolution, in which the thirst for knowledge enabled the theory of evolution to finally reach a milestone. Following this great period of scientific knowledge, the first conceptualizations of evolutionary mechanisms emerged in the 19^th century with the concepts of transmutation of species and natural selection, made by Jean-Baptiste Lamarck and Charles Darwin respectively. Nevertheless, Darwin’s ideas of fitness and phylogenetic branches initiated the

“Darwinian revolution”, in which the fact that humans are primates and thus animals among others is finally recognized in sciences. His theories were strongly debated across the scientific community, even if his friend, Thomas Henry Huxley strongly supported him.

Nowadays, through the modern synthesis of evolution, evolutionary mechanisms are recognized as key factors to explain physiological and behavioural processes in humans and other animals.

2.1.1.1. At the Origins of Sciences

The intuition that species change over time and descend from a common animal is not a modern theory. In fact, it is probably one of the oldest concepts in science. Indeed, Anaximander of Miletus (610 – 546 BC), often considered as the first evolutionist, already suggested that the first animal on Earth lived in water and that humans could be the descendants of a primitive fish (Kočandrle & Kleisner, 2013). However, influential philosophers such as Plato (428 – 648 BC) and Aristotle (384 – 322 BC), who believed in a divine intervention for the creation of life, questioned this first evolutionary perspective. In the same way, later in the Roman Empire, Lucretius (99 – 55 BC) described in his poems “De rerum natura”, survival mechanisms in the development of life (Holmes, 2007). Nevertheless, he was also criticized by Cicero (106 – 43 BC), a major philosopher at that time, strongly influenced by religion (Cicero, 2003).

Crossing the Middle-Age and the Renaissance period, evolutionary thought finally reached a milestone during the Age of Enlightenment (18th). Indeed, the word “evolution” took on its full meaning of progression with Charles Bonnet, in his concept of future generation development: the theory of pre-formation, in which female carry within them all future

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generation in a miniature form (Pallen, 2011).

Additionally to this, Pierre Louis Moreau de Maupertuis was the first to describe in his book “Venus Physique” the mechanism of “natural selection” conceptualized later by Charles Darwin: “In the fortuitous combinations of the productions of nature, none but those that found themselves in certain relations of fitness could subsist, is it not wonderful that this fitness is present in all species that are currently in existence?” (Maupertuis, 1745, p. 197).

Similarly, Georges-Louis Leclerc, Comte de Buffon, like his future successor Jean-Baptiste Lamarck, argued that species are varieties modified by environmental factors from one original individual. He even suggested that humans and apes had a common ancestor.

However, the Comte de Buffon also believed that each species had an original form arisen through spontaneous generation and thus, that modifications specific to each species were limited (Pallen, 2011).

Finally, James Burnett, Lord Monboddo, probably ahead of his time, already suggested in the late 18^th century, that humans were the descendants of other primates and often compared the human species to other great apes such as chimpanzees or orangutans in his book “Of the Origin and Progress of Language”: “The orangutan is an animal of the human form, inside as well as outside: That he has the human intelligence, as much as can be expected in an animal living without civility or arts: That he has a disposition of mind, mild, docile and human:

That he has the sentiments and affections peculiar to our species” (Monboddo, 1774, p. 289).

Interestingly, such writings impacted scientific theories as well as popular thoughts, starting to influence the theatrical art (see Figure1) and the poetic literature of the 18^th and 19^th centuries (E. Darwin, 1803).

Figure 1: Illustration of Mazurier’s ape costume for his role of Joko at the Theatre de la porte-

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Emerging in the early 19^th, the first comprehensive theory of evolution known as Lamarckism as well as Transformationism emphasized the importance of environmental adaptation in species complexity. In fact, even if Jean-Baptiste Lamarck in his theory of the transmutation of species believed in spontaneous generation and then, rejected the idea of a common ancestor (Lamarck, 1809), his concept of inheritance of acquired characteristics in species strongly influenced evolutionary thinkers. Professor in zoology, Lamarck famously illustrated his theory using the giraffe’s neck adaptation as one example (see Figure 2) in his books of 1802 and then 1809: “In regard to habits, it is interesting to observe a product of them in the particular form and height of the giraffe. […] the earth is nearly always arid and without herbage, obliging it to browse on the leaves of trees and to continually strive to reach up to them. It was resulted from this habit, maintained for a long time by all individuals of the race that the forelegs have become longer than the hind legs and its necks has so lengthened itself” (Lamarck, 1809, p. 219).

Figure 2: Drawing by Lamarck depicting the giraffe’s neck adaptation. He suggested that, over generations the long neck of the giraffe evolved to reach higher leaves, which are unattainable by any other herbivore. (Lamarck, 1802)^.

Hence, in response to modifications in their environment, a given species adopted new habits leading to new structures (e.g. muscles) accumulated across the future generations and resulting at some point in a new species. Despite the fact that Lamarck’s theory was well conceptualized, he did not explain explicitly how the acquired characters were

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transmitted within the next generation. Nevertheless, even if he never pronounced the word

“heredity”, Lamarck yet referred to sexual reproduction and shared characters between both parents (Burkhardt, 2013).

The main opponent to the theory of transmutation of species was George Cuvier, who believed like Aristotle at this time in the fixity of species. According to him, a species could only change after an extinction or a catastrophic episode leading to a new period of creation. Cuvier’s theory came from his work as a palaeontologist, for which he is often considered the funder of the discipline as well as that of comparative anatomy (Bowler, 2003).

Nowadays, some researchers still claim a Lamarckism point of view in modern fields such as developmental plasticity or epigenetic inheritance, mainly focusing on the developmental aspect of Lamarck’s theory (Gissis et al., 2011).

From the Antiquity with Anaximander of Miletus to the early 19^th century with Jean–

Baptiste Lamarck, many concepts of Darwin’s theory were already claimed. Nevertheless, the “Darwinian revolution” (Burkhardt, 2013) enabled for the first time the conceptualization of all relevant hypotheses in one comprehensive theory that is currently the base of a modern view of evolution.

2.1.1.2. Darwinism & Modern view of Evolution

Travelling across the globe aboard to the HMS Beagle during five years, the young naturalist Charles Darwin collected fossils and geological artifacts, while precisely describing his surrounding environment. Writing his discoveries on a personal notebook

“The voyage of the Beagle”, Darwin started to question the fixity of species, encouraged by the Captain of the HMS Beagle, Robert Fitzroy, who gave him the first volume of

“Principles of Geology” wrote by Charles Lyell, a famous geologist of his time, supporting the idea of slow and long periods of modifications for the development of earth, totally rejecting the theory of George Cuvier. Influenced by his observations and Lyell’s ideas, Darwin secretly modelled the concept of transmutation of species that he described in opposition to Lamarck as a process of divergence and branching between species. While Darwin already built the foundations of his concept of natural selection, named so in opposite to artificial selection made by humans (Huxley, 1881), at the time of his travels (see

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Figure 3: Illustration of Darwin’ Finches, observed in Galapagos Island (1835). Darwin described his concept of natural selection using the evolutionary mechanisms that were at play in Finches.

According to Darwin, the different species of Finches have different beaks because they are adapted to eat different kinds of food (e.g. nuts, insects) but they all descend from of a common ancestor due to their important behavioural and anatomical similarities.

In parallel to Darwin, Alfred Russel Wallace, a naturalist, also believed in the transmutation of species after his own observations in South America and Malay Archipelago. He also suggested in his early writings that the evolution of species, would be explain by branching mechanisms (Pallen, 2011). Like Darwin, Wallace was strongly influenced by a clergyman, Thomas Robert Malthus and his concept of “struggle for existence” (Bowler, 2003). Advised by Lyell and Joseph Dalton Hooker, Darwin allowed them to present conjointly his own work on natural selection as well as Wallace theory to the Linnean Society in 1858 (Wyhe &

Rookmaaker, 2012). Yet, one year later, the Darwinian revolution was fully realized after the first publication of Darwin’s famous book “On the Origin of Species” (Darwin, 1859).

Darwin’s theory on natural selection and branching always provoked intense debates in the scientific community of the 19th century. In fact, the concept of branching claimed by Darwin suggested that humans and other great apes were together on the same evolutionary tree. Triggering a philosophical revolution, scientists such as Cuvier or even Darwin’

friends Lyell and Wallace questioned its perspective. Indeed, in Cuvier’s theory, humans are from a different order of mammals and thus, cannot be compared to any other species.

Similarly, Lyell and Wallace effectively defended the idea of a physical ancestor between humans and other great apes but totally disproved the continuity between some aspects of their minds.

The debate became even more intense with the successive publications of “The Descent of Man and Selection in Relation to Sex” (Darwin, 1871) and “The Expression of Emotions in Man and Animals” (Darwin, 1872) in which Darwin clearly compared humans to other

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animals from a biological point of view to an intellectual and emotional one. Read by the non-scientific community as well, the news-papers of its period often caricatured Darwin as a primitive monkey (see Figure 4). Nevertheless, its caricatures finally contributed to the popularity of Darwin in evolutionary theories.

Figure 4: Darwin caricatures in 19^th century’ new papers (Cavin & Vallotton, 2009)

Moreover, Thomas Henry Huxley, positioning himself as “Darwin Bulldog”, defended against old odds Darwin’s hypotheses in demonstrating for instance, how humans and apes were close anatomically speaking, even in their brain structures. He also pointed out the fact that, in opposite to Lamarck’s or Cuvier’s theories, Darwin was the first to describe evolutionary mechanisms without any divine or supernatural intervention. Visionary, Huxley concluded in his book “On the Origin of Species: Or, The Causes of the Phenomena of Organic Nature”: “Mr. Darwin’s work is the greatest contribution which has been made to biological science […] and I believe that, if you take it as the embodiment of a hypothesis, it is destined to be the guide of a biological and psychological speculation for the next three or four generations.” (Huxley, 1881, p. 144).

As Huxley predicted, nowadays, Darwinian theories of evolution are strongly supported by the emerging cross-disciplinary consensus of the early 20^th and 21^st centuries (see Figure 5).

His grandson, Julian Huxley, also biologist, was the first to name this consensus “the modern synthesis of evolution” (Huxley, 1942).

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Figure 5: Diagram of the idea brought together in the “Modern Synthesis” in evolutionary biology (modified from Ian, 2020).

Therefore, influencing scientists and thinkers from the 19^th to the 21^st centuries, Darwinian theories were the keystones of evolutionary thought. Darwin indeed initiated a philosophical revolution in which other animals, like humans, expressed and felt emotions.

Section 2.1.2. will develop how this perspective influences current theories of emotion.

2.1.2. Evolution in Theories of Emotion

The definition of emotion may be one of the most debated concepts in research. Despite the fact that the lack of consensus led few psychologists to even doubt of the necessity of a definition (Frijda, 2007; LeDoux, 2012), we will consider in the next sections that “emotion”

is a rapid process, focused on a specific event and involving i) elicitation mechanisms based on stimuli relevance; and ii) multiple emotional response processes (action tendency, autonomic reaction, expression and feeling components - Sander, 2013).

While the definition of emotion is still discussed, its evolutionary basis is now recognized by most scientists in the affective domain. From the theories of Nesse to Frijda, Ekman or more recently Scherer’s model, evolution is key to understand the genesis of emotions in humans. Moreover, if old evolutionary mechanisms are really at play in our emotional experiences, we can assume that emotional processes are also present in other animals, especially in phylogenetically close species such as non-human primates. In spite of intense debates on this last perspective, research however often described the existence of more or less complex affective lives in multiple species across the animal kingdom.

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2.1.2.1. Evolution of Emotion

Darwin in “The expression of the emotions in man and animals” (Darwin, 1872) was the first to truly emphasize the key role of evolutionary mechanisms in emotional processing.

Nowadays, it is accepted that emotions have an evolutionary history. Randolph Nesse, for example, writes in 2009 that “Natural selection shaped emotions and the mechanisms that regulate them” (Nesse, 2009, p. 159), referring to the role of natural selection in first, the subdivision of emotional types, and second, in the organization of psychological and physiological processes that facilitate an adaptive response to a particular situation (Al- Shawaf & Lewis, 2017; Nesse, 1990 - see Figure 6). In fact, different emotions were probably shaped by natural selection because each specific situation elicited different sets of adaptive responses. However, in our modern environment, emotions are not always adapted (Greenberg, 2002). Johan Bolhuis and Clive Wynne explained this, with a practical and quite comical example: “The tendency of modern humans to spontaneously fear spiders rather than cars, which are far more dangerous, is thought to stem form the prevalence of poisonous arachnids, rather than dangerous driving, during the Pleistocene.” (Bolhuis & Wynne, 2009, p. 832). Yet, emotions enable to react differently to a threatening or a joyful situation for instance. This last process was well conceptualized by Nico Frijda with his notion of action readiness, referring to motivational aspect of emotions (Frijda, 2007, 2016). In fact, specific motives would appear to “move” animals to achieve their biosocial goals (e.g. reproduction) and to guide them to pay attention or be emotionally aroused in a certain situation (Gilbert, 2015).

Thus, most emotions may involve a position toward a specific object (e.g. rejection) and readiness to implement that position in action (e.g. by moving away). Furthermore, states of action readiness would involve activation and deactivation states as well as action tendency (theorized by Arnold, 1960) to avoid or approach an object in a peculiar context. Action tendency relies on specific brain networks in the human brain involving bilateral prefrontal cortex (PFC), amygdala-motor pathway, right inferior frontal gyrus (IFG), anterior cingulate cortex (ACC), periaqueductal grey area (PAG) and basal ganglia (See Section 2.2.1.1 for a more detailed description of neural networks involved in emotion in humans and Section 2.2.2.2 for a review in non-human primates). Moreover, in his concept of approach- withdrawal, Richard Davidson demonstrated the distinct involvement of the right and left PFC depending on approach or avoidance behaviours elicited by the type of emotion (Davidson et al., 1990). Davidson and collaborators indeed demonstrated a stronger

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activation of anterior fronto-temporal regions in the right hemisphere for fear and disgust faces (withdrawal emotions) compared to higher neural activity in the left hemisphere for happy faces normally triggering approach behaviours (Davidson et al., 1990; Davidson, 1992).

Figure 6: Phylogeny of emotions shaped by natural selection. Resources are represented in upright font, emotions in italic and situations in capitals. Natural selection gradually differentiated responses to increase the ability of individuals to obtain the three main types of resources: personal, reproductive and social effort. Emotions were thus shaped to deal with situations arising from the pursuit of specific goals (Nesse, 2004).

As illustrated in Figure 6, different situations can have adaptive challenges in common.

Consequently, emotions can be classified using two dimensional aspects with i) arousal and ii) valence (Nesse, 2009). “Arousal” refers to a short-term increase in some processes that can be viewed as involving excitatory mechanisms (increase in behaviour or physiological activity) (Fowles, 2009). For instance, a massive increase in sympathetic nervous system (e.g.

cardiac or respiratory rhythm) triggered by a phobic stimulus (e.g. spider). “Valence” refers to the pleasant or unpleasant characters of emotions (e.g. Frijda, 1987; Scherer, 2003). For example, happiness is classified as a positive emotion whereas threat is recognized as a negative one. Positive emotions should elicit approach behaviours whereas negative emotions should trigger avoidance behaviours.

These two dimensions are highly correlated and thus, both are often used for the modelling of emotions (starting from Russell, 1980). Nevertheless, other dimensional aspects exist to represent emotional experiences (Fontaine et al., 2007). In fact, the individual sense of power

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or control to represent emotions (potency – control) was also well described in the literature.

For example, anger is expected to score highly in this dimension whereas fear is expected to score extremely low (Goudbeek & Scherer, 2010). Interestingly, Fontaine and collaborators highlighted as well the importance of a fourth dimension in the representation of emotions.

This last dimension, characterized by the unpredictability of an emotional event, would be indeed particularly essential to explain the ambivalent status of surprise (Fontaine et al., 2007).

Moreover, most of the theories of emotions involve complex psychological and physiological processes as well as evolutionary mechanisms (Sander et al., 2018). For instance, Paul Ekman and David Matsumoto define emotions as “Transient, bio-psychosocial reactions designed to aid individuals in adapting to and coping with events that have implications for survival and well-being” (Ekman & Matsumoto, 2009, p. 69). Hence, their definition highlights the key role of emotions in psychological and physiological processes enabling to maximize the chance of survival of an individual. Furthermore, Ekman in his theory of Basic emotions (Ekman, 1999), underlines the existence of an “Emotion alert database” storing schemas information and enabling individuals to react adaptively. He gives as an example the perception of a coiled object that could match with the schema of snake and thus trigger the emotion of fear. Importantly, he also emphasizes that the universality of seven emotional expressions relies on brain regions such as the amygdala and the insula (Sander et al., 2018) for anger, disgust, fear, happiness, sadness, contempt and surprise (see Figure 7), suggesting inherited mechanisms from our evolutionary history (Ekman, 2003). For instance, happiness would correspond to sub-goals being achieved, anger to an active plan being obstructed, sadness to the failure of a major plan or loss of an active goal, fear to self- preservation goal being threatened or goal conflict and disgust to gustatory goal violated (Juslin & Laukka, 2003). Yet, the universality of emotions is controversial in the literature.

Some findings indeed demonstrate cross-cultural emotional basis (e.g. Sauter et al., 2010;

Scherer et al., 2001) whereas others do not (e.g. Crivelli et al., 2016; Jack et al., 2016). Despite the fact that the results found by Carlos Crivelli and collaborators on cultural variation of emotional expression are highly debated (Kret & Straffon, 2018), other findings on facial expressions of emotions also suggest cross-cultural differences. According to Jack and collaborators, Ekman’s work was indeed biased by the use of static images excluding the temporal dynamic of facial expression for instance (Jack et al., 2014). The authors decided thus to investigate across three different studies, the conceptual mapping, the dynamics and

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the similarities of facial expressions of emotions between two cultures. Unlike Ekman, they revealed that only four latent emotional patterns were universal (rage, shame, joy and ecstatic), suggesting cultural differences for certain types of emotion (Jack et al., 2016).

Figure 7: The seven basic emotions and their universal expressions (Matsumoto et al., 2008).

In line with the appraisal mechanisms described by Frijda or Phoebe Ellsworth (Ellsworth &

Scherer, 2003) and the components of emotions of Ekman, Klaus Scherer conceptualized in his component process model (CPM; see Figure 8) the cognitive and physiological sequences that shaped the genesis of emotions (Scherer, 1982, 2001). The rapid cognitive evaluation of an event would enable the facilitation of adaptive mechanisms in case of emergency situations. In fact, in 2009 the psychologist described the CPM model as “Based on the idea that during evolution, emotion replaced instincts in order to allow for more flexible response to events in a complex environments, and it did so by introducing an interrupt for further processing into the stimulus-response chain.” (Scherer, 2009, p. 93). Moreover, according to the author, emotions would have been optimized i) to evaluate an object or an event, ii) to regulate the process, iii) to prepare and guide action, iv) to communicate reaction, behavioural intention; and v) to monitor internal states and organism-environment interaction (Scherer, 2001, 2009).

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Figure 8: Comprehensive illustration of the component processes of emotion (Sander et al., 2005; Scherer, 2001). In summary, in individuals an emotion is determined by i) the filtering of a relevant stimulus or event; ii) the evaluation of the organism’s implication; iii) the level of control and adjustment to this event; and iv) the response suitability to personal and social norms. In addition, for each sequential stage of assessment, there are two outputs (represented with the arrows): a modification of the cognitive – motivational mechanisms that have influenced the appraisal process and efferent effects on the periphery.

Importantly, Scherer also attempted to conceptualize mechanisms involved in the vocal communication of emotions between a speaker and a listener. For this purpose, he revised the Organon model of Karl Bühler on linguistic signs (Bühler, 1990) who postulated that any sign of language has three adaptive functions including i) “the symptom” of the speaker’

states; ii) “the symbol” of socially shared meaning category; and iii) “the appeal” that refers to a social message toward others. Adapting these three functions to the vocal expression of emotions, Scherer thus describes the symptom as the mechanisms underlying the sender’s cognitive and emotional states; the symbol as the concept of emotions and the appeal as the listener’s reactions with approach or avoidance behaviours (Scherer, 1988, 1992, 2009b).

Furthermore, based on Bühler and Brunswik’ model of emotional encoding – decoding processing (Brunswik, 1956), Scherer also crucially emphasizes “the strong pressure exerted by impression (pull) factors on expression (push) factors during the course of evolution of communication in socially living species” (Scherer, 2009c, p. 168). For example, an individual from any social species gives the impression of strength and power by producing loud and low-frequency vocalizations relying on vocal tracts tension. Hence, both psychobiological

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mechanisms (internal push effects) and social norms (external pull effects) would influence the encoding and the decoding of the vocal expression of emotions in human and other animals (Grandjean et al., 2006; Scherer, 1988, 2009c; see Figure 9).

Figure 9: Adaptation of Brunswik’s lens model, including the influences of conventions, norms and display rules - pull effects - and psychobiological mechanisms - push effects - on the encoding of emotional vocalizations produced by the speaker and the decoding made by the listener on reciprocal influences of these two aspects on attributions. An emotional content is thus expressed by distal indicators cues (e.g. acoustic features) that are perceived by a listener who on the basis of proximal percept and contextual information makes a subjective attribution of the speaker’s emotional states (Grandjean et al., 2006).

Affective sciences through the main theories of emotions, recognized the crucial role of evolutionary processing such as natural selection in the emergence of emotions. For instance, despite the current debate, the universality of basic emotions suggests inherited mechanisms based on human evolution. If this hypothesis of inheritance is correct, similar processes should be found in other species as well, in particular in non-human primates (NHP), our closest relatives.

2.1.2.2. Emotions in Animals: The end of a Debate?

Based on René Descartes’ words, “Animals are like robots: they cannot reason or feel pain.”

(Proctor et al., 2013, p. 883). Hopefully, in the 21^st century, this Cartesian point of view is no longer shared in affective sciences. However, the necessity to define or even study emotions

The Voice of Primates: Neuro-evolutionary Aspects of Emotions

Thesis

Reference

The Voice of Primates: Neuro-evolutionary Aspects of Emotions

THE VOICE OF PRIMATES:

NEURO-EVOLUTIONARY ASPECTS OF EMOTIONS

Coralie DEBRACQUE

Published articles

Remerciements

Abstract in English

Abstract in French

Table of Contents

Theoretical Part

1. Abstract of Literature Review

2. Literature review