Theoretical implications

were found for the baboon Chet only with additionally, a right hemisphere bias for the sounds broadcasted in stereo (Figure 65). The lack of results in the two other baboons could be explain by their handedness in communicative gesture. In fact, our left-handed subject Talma, showed a clear right hemisphere bias for most of the stimuli whereas right-handed Rubis showed a stronger bias toward the left hemisphere for the sounds broadcasted in right and left ears. Yet, findings for stereo stimuli are consistent with the literature on human and NHP auditory pathway showing a rightward asymmetry for stereo sounds (Jäncke et al., 2002; Joly et al., 2012; Kaiser et al., 2000; Petkov et al., 2008).

Overall, this last study upholds the suitability of fNIRS to assess brain mechanisms in NHP, and opens new avenues of research in free-ranging primates.

Findings from Study 1 to Study 6 will hopefully contribute to a better understanding of i) the human recognition of affects in heterospecific vocalizations; ii) the evolutionary continuity between human and NHP brains; and iii) the development of non-invasive protocols in animal research.

2. Theoretical Implications

In light of evolutionary thought, the present thesis uncovered new findings that could be valuable in affective sciences, psychology, neurosciences or even primatology (see Table 16).

First, the congruent results found across Study 2 to Study 5, highlight the importance for future comparative studies on vocal recognition, to consider both phylogenetic and acoustic proximity in such matter (see Figure 66). Yet, rare are the studies investigating the link between the acoustic structure of the calls and the behavioural or cerebral response of human participants. In fact, to our knowledge, only three studies used this approach (Filippi et al., 2017; Fritz et al., 2018; Kelly et al., 2017) emphasizing the crucial role of frequency parameters in the identification of affects in heterospecific vocalizations. Despite the existence of few interesting findings, Study 3 was the first to extensively assess the influence of phylogenetic and acoustic proximities in vocal affective recognition. Thus, for the first time, we demonstrated that vocalizations expressed by chimpanzees, our closest relatives, were significantly closer in acoustic distance to the human voice than they were to bonobo (great ape) and macaque (monkey) calls. Moreover, results in Study 3 revealed that acoustic similarities between human and chimpanzee vocalizations had a direct impact on the

human recognition of affects in chimpanzee screams. Furthermore, similar brain mechanisms were also found at play in Study 4 and 5 for the categorization of NHP calls.

Despite bonobos belonging to the great ape family, the higher acoustic distance of their calls from the human voice as well as their behavioural differences seems to prevent the involvement of such mechanisms in human recognition of bonobo vocalizations.

Hence, both phylogenetic and acoustic factors are essential to the human perceptual decision-making in heterospecific vocalizations. Yet, the kinds of process related to decision-making itself seem also primordial in such paradigms. In fact, previous fMRI findings (Dricu et al., 2017) and results found in Study 1 demonstrated the difference of mechanisms between the categorization and discrimination tasks, depending on the level of complexity (number) of possible choices. However, to our knowledge, Study 2 and Study 3 constitute the only comparative research considering the choice complexity in cross-taxa recognition. We thus importantly revealed, for the first time, the distinction between the categorization and discrimination of affect in NHP vocalizations at cerebral and behavioural levels. Therefore, future studies on this matter should carefully investigate sub processes involved in decision-making mechanisms at play in cross-taxa recognition.

Interestingly and unexpectedly, findings in Studies 2 to 5 support the hypothesis of an evolutionary divergence between chimpanzee and bonobo species. The self-domestication hypothesis conceptualized by Hare and collaborators, indeed suggests a distinct evolutionary pathway for bonobos compared to chimpanzees due to selection against aggression, despite their common affiliation to the great ape family (Hare et al., 2012). In line with previous studies showing morphological (Grawunder et al., 2018), neuroanatomical (Staes et al., 2018), and behavioural (Gruber & Clay, 2016) differences between both species, our results also point out the existence of divergence in their vocal expression of affects.

Together, these findings support the fact that bonobo vocalizations, are particularly of interest for future comparative studies investigating both, phylogenetic and acoustic distances.

Figure 66: Human perceptual decision-making tree for affective conspecific and heterospecific vocalizations. Summary of the findings from Study 1 to Study 5. In green are represented the factors of choice. In red are indicated the behavioural and cerebral consequences. Decision processing start from the bottom and end at the top of the tree.

Table 16: Summary of the findings from Study 1 to Study 6 depending on the five thesis objectives (see p.63).

Findings

Objective 1 Brain data: distinct involvement of bilateral IFC in affective categorisation and discrimination for implicit and explicit decoding

Behavioural recognition: explicit categorization (cat) > implicit discrimination (dis) > implicit cat > explicit dis

Objective 2 Brain data: distinct involvement of IFCtri and PFC in affective categorization and discrimination for all NHP calls

Behavioural recognition: discrimination of all stimuli (threatening bonobo screams excepted) + categorization of all affective calls expressed by great apes

Brain * behaviour: categorization agonistic chimpanzee and bonobo &

affiliative chimpanzee calls = ↘ PFC-IFC. discrimination agonistic

chimpanzee screams = ↗ PFC-IFC

Objective 3 Mahalanobis: human < chimpanzee < bonobo < macaque calls

Behavioural recognition: discrimination of all stimuli, (threatening bonobo and macaque screams excepted) + categorization of all stimuli (agonistic macaque vocalizations and threatening bonobo screams excluded)

Mahalanobis * behaviour: ↗ recognition for chimpanzee calls

Objective 4 Brain data: ↗ left TVA and bilateral IFGtri – ope - orb for the categorization of chimpanzee vocalizations + similar brain networks between human voices and chimpanzee calls within bilateral TVA + IFGtri for the categorization of NHP

Behavioural recognition: chimpanzee > macaque. ∅ bonobo

Objective 5 Brain data: Contralateral activations in the motor (for all baboons) and temporal cortices (for one subject)

A second important aspect of the present thesis is the successful investigation of preserved mechanisms in the humans’ frontal and temporal cortices. In fact, despite a larger and more folded brain compared to the other great apes species (Heuer et al., 2019), human neuroanatomical traits are mainly considered as a continuum in the primate brain evolution (Herculano-Houzel, 2009; Semendeferi et al., 2002). It is thus unlikely that 18 millions of years of common evolution (Perelman et al., 2011) did not affect modern human abilities.

From this assessment, Studies 2, 4 and 5 explored in humans the processing of cross-taxa recognition within TVA, PFC and IFG areas. In line with the few existing fMRI findings showing an increase of activity in frontal regions for the identification of affective valence in macaque (Belin et al., 2008) and chimpanzee calls (Fritz et al., 2018), results in Study 2 revealed for the first time the involvement of bilateral IFG and PFC in the recognition of affective contents in human and NHP vocalizations (with the crucial addition of bonobos).

Following this, fMRI data in Study 5 demonstrated the enhancement of activity in bilateral IFG for the recognition of NHP species. Finally and most importantly, wholebrain and functional connectivity analyses in Study 4 showed the involvement of TVA for the perception of chimpanzee vocalizations only. Usually associated to the processing of human voice (Belin et al., 2000), Joly and collaborators did not find such activity in TVA for human participants listening to macaque calls (Joly et al., 2012). Yet, this lack of result is not surprising in view of the large phylogenetic distance between macaque species and Homo sapiens. Therefore, Study 4 is the first to demonstrate the involvement of TVA for the

listening of heterospecific vocalizations, namely chimpanzee calls.

Third, Study 6 will hopefully have a positive impact on ethical standards in animal research.

In fact, our findings in both motor and auditory paradigms demonstrate for the first time the suitability of fNIRS to assess the hemodynamic responses of the baboon brain.

fNIRS is indeed a relatively new brain imaging technique. Using the principle of tissue transillumination (Bright, 1831), fNIRS measures via near infrared lights, blood oxygenation changes (e.g. Hoshi, 2016; Jöbsis, 1977) related to the HRF constituted of oxygenated haemoglobin and deoxygenated haemoglobin. Considering that fNIRS is a lower-cost option and less sensitive to motion artefacts (Balardin et al., 2017) than other non-invasive techniques (e.g. MRI, EEG), it might be an excellent methodology to study cognitive functions of NHP under more ecologically relevant testing conditions using a wireless and wearable device. In fact, few fNIRS studies on NHP are emerging but the research have been only focused on macaques and on cross-validating the technique with other well established but invasive methods such as the electrophysiology (Kim et al., 2017).

Nevertheless, fNIRS was successfully used on macaques as the only technique to explore PFC (Lee et al., 2017), occipital and frontal activations (Wakita et al., 2010) elicited by visual stimuli. Therefore, together Study 6 and the existing literature support an extensive using of fNIRS in the future to investigate brain processing in NHP in ecological conditions.

Overall, the present thesis led to various new findings that should especially improve our knowledge on perceptual affective decision-making in heterospecific vocalizations as well as fNIRS suitability for the NHP brain investigations. Yet, additional experiment are still needed to extend our findings in more ecological conditions, especially during social interactions or specific tasks.