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Debracque, C.

Publications and source records attributed to Debracque, C..

8 recordsLinked to original sources

Sensitivity of the human temporal voice areas to nonhuman primate vocalizations

In recent years, research on voice processing in the human brain, particularly the study of temporal voice areas (TVA), was dedicated almost exclusively to conspecific vocalizations. To characterize commonalities and differences regarding primate vocalization representations in the human brain, the inclusion of closely related nonhuman primates, namely chimpanzees and bonobos, is needed. We hypothesized that neural commonalities would depend on both phylogenetic and acoustic proximities, with chimpanzees ranking closest to Homo. Presenting human participants (N=23) with the vocalizations of four primate species (rhesus macaques, chimpanzees, bonobos and humans) and regressing-out relevant acoustic parameters using three distinct analyses, we observed within-TVA, sample-specific, bilateral anterior superior temporal gyrus activity for chimpanzee vocalizations compared to: all other species; nonhuman primates; human vocalizations. Within-TVA activity was also observed for macaque vocalizations. Our results provide evidence for subregions of the TVA that respond principally, but not exclusively, to phylogenetically and acoustically close nonhuman primate vocalizations, namely those of chimpanzees.

neuroscience↗

Model-based frontal cortex analysis reveals origins of human non-verbal communication

The ability to process verbal language seems unique to humans and relies not only on semantics but on other forms of communication such as affective vocalisations, that we share with other primate species--particularly great apes (Hominidae). To better understand these processes at the behavioural and brain level, we asked human participants to categorize vocalizations of four primate species including human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) during MRI acquisition. Classification was above chance level for all species but bonobo vocalizations. Imaging analyses were computed using a participant-specific, trial-by-trial fitted probability categorization value in a model-based style of data analysis. Model-based analyses revealed the implication of the bilateral orbitofrontal cortex and inferior frontal gyrus pars triangularis (IFGtri) respectively correlating and anti-correlating with the fitted probability of accurate species classification. Further conjunction analyses revealed enhanced activity in a sub-area of the left IFGtri specifically for the accurate classification of chimpanzee calls compared to human voices. Our data therefore reveal distinct frontal mechanisms that shed light on how the human brain evolved to process non-verbal language. Author contributionsCD and LC were involved in every steps of the study including experimental design, programming, data acquisition, data analysis and redaction of the first draft of the manuscript and subsequent editing. EP helped design the model-based MRI analyses and interpret the results. TG and DG were involved in the experimental design and study planification. All authors wrote and edited the manuscript.

neuroscience↗

Cerebral activity in monkeys Papio anubis during the perception of conspecific and heterospecific agonistic vocalizations: A functional Near Infrared Spectroscopy study

Are conspecific emotional vocalizations special? Although often investigated in non-human primates using functional magnetic resonance imaging or positron emission tomography, it remains unclear whether the listening of conspecific vocal emotions leads to similar or different cerebral activations when compared to heterospecific calls (i.e. expressed by another primate species). Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy (fNIRS), the present study investigated cortical temporal activities during exposure to both conspecific and heterospecific calls in three female adult baboons (Papio anubis). The three subjects were lightly anesthetized and passively exposed to agonistic baboon and chimpanzee (Pan troglodytes) vocalizations, as well as energy matched white noises in order to control for this low-level acoustic feature. Despite inter-individual variabilities, permutation test analyses on the extracted OxyHemoglobin signal revealed for two subjects out of three significant differences between the passive listening of baboon versus chimpanzee stimuli. Additionally, in one subject, a modulation of the left temporal cortex activity was found for the perception of baboon calls contrasted to chimpanzee vocalizations as well as for the passive listening of baboon white noises compared to chimpanzee ones. Although the lack of generalization of those findings in all three subjects prevents us to drawn any conclusion and that more subjects would be needed, the hypothesis that baboons cortical temporal regions may be more sensitive to the processing of conspecific sounds compared to heterospecific stimuli is not excluded. Our study highlights that fNIRS may be a promising alternative to further investigate the auditory mechanisms at play in the right and left baboons temporal cortices for the processing of emotional vocalizations.

neuroscience↗

Categorization and discrimination of human and non-human primate affective vocalizations: investigation of the frontal cortex activity through fNIRS.

Many species, including humans and non-human primates, react differently to threatening or pleasant situations. Because of its adaptiveness, recognizing affective signals is likely to be reflected in a capability of modern humans to recognize other closely related species call content. However, at both behavioural and neural levels, only few studies have used a comparative approach to understand affective decoding processes in humans, particularly with respect to affective vocalizations. Previous research in neuroscience about the recognition of human affective vocalizations has shown the critical involvement of temporal and frontal regions. In particular, frontal regions have been reported as crucial in the explicit decoding of vocal emotions especially in different task complexity such as discrimination or categorization. The aim of this study using functional Near Infrared Spectroscopy (fNIRS) was to specifically investigate the neural activity of the inferior frontal cortex pars triangularis (IFGtri) and the prefrontal cortex (PFC) underlying categorization (A versus B) and discrimination (A versus non-A) mechanisms of positive and negative affects in human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) vocalizations. We also analysed participants behavioural responses and correlated them with the recorded frontal activations. While performing the tasks, fNIRS data revealed a clear distinction between the two frontal regions, with a general positive activation of IFGtri compared to a decrease of PFC activity. We also found a modulation of IFGtri and PFC activations depending on both the species considered and on task complexity; with generally more activity in the IFGtri during discrimination compared to categorization, and a more intense decrease of the PFC in categorization compared to discrimination. Behaviourally, participants recognized almost all affective cues in all species vocalizations at above chance levels in the discrimination task (except for threatening bonobo calls). For categorization, they mostly correctly identified at levels significantly above chance affective contents in human and great ape vocalizations but not in macaque calls. Overall, these findings support the hypothesis of a pre-human origin of affective recognition processing inherited from our common ancestor with other great apes and processed in the frontal cortex. Our results also highlight behavioural differences related to task complexity, i.e. between categorization and discrimination processes, and the differential involvement of the PFC and the IFGtri, which seems necessary to explicitly decode affects in all primate vocalizations.

neuroscience↗

Humans recognize affective cues in primate vocalizations: Acoustic and phylogenetic perspectives

Humans are adept in extracting affective information from the vocalisations of not only humans but also other animals. Current research has mainly focused on phylogenetic proximity to explain such cross-species emotion recognition abilities. However, because research protocols are inconsistent across studies, it remains unclear whether human recognition of vocal affective cues of other species is due to cross-taxa similarities between acoustic parameters, the phylogenetic distances between species, or a combination of both. To address this, we first analysed acoustic variation in 96 affective vocalizations, including agonistic and affiliative contexts, of humans and three other primate species - rhesus macaques, chimpanzees and bonobos - the latter two being equally phylogenetically distant from humans. Using Mahalanobis distances, we found that chimpanzee vocalizations were acoustically closer to those of humans than to those of bonobos, confirming a potential derived vocal evolution in the bonobo lineage. Second, we investigated whether 68 human participants recognized the affective basis of vocalisations through tasks by asking them to categorize ( A vs B) or discriminate ( A vs non-A) vocalisations based on their affective content. Results showed that participants could reliably categorize and discriminate most of the affective vocal cues expressed by other primates, except threat calls by bonobos and macaques. Overall, participants showed greatest accuracy in detecting chimpanzee vocalizations; but not bonobo vocalizations, which provides support for both the phylogenetic proximity and acoustic similarity hypotheses. Our results highlight for the first time the importance of both phylogenetic and acoustic parameter level explanations in cross-species affective perception, drawing a more complex picture to explain our natural understanding of animal signals.

animal behavior and cognition↗

Human temporal voice areas are sensitive to chimpanzee vocalizations

Withdrawal StatementThe authors have withdrawn this manuscript due to a duplicate posting of manuscript number BIORXIV/2025/677258. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author. The correct preprint can be found at doi: 10.1101/2025.09.19.677258

neuroscience↗

Brain activation lateralization in monkeys (Papio Anubis) following asymmetric motor and auditory stimulations through functional Near Infrared Spectroscopy

Hemispheric asymmetries have long been seen as characterizing the human brain; yet, an increasing number of reports suggest the presence of such brain asymmetries in our closest primate relatives. However, most available data in non-human primates have so far been acquired as part of neurostructural approaches such as MRI, while comparative data in humans are often dynamically acquired as part of neurofunctional studies. In the present exploratory study in baboons (Papio Anubis), we tested whether brain lateralization could be recorded non-invasively using a functional Near-Infrared Spectroscopy (fNIRS) device in two contexts: motor and auditory passive stimulations. Under light propofol anaesthesia monitoring, three adult female baboons were exposed to a series of (1) left-versus right-arm passive movement stimulations; and (2) left-versus right-ear versus stereo auditory stimulations while recording fNIRS signals in the related brain areas (i.e., motor central sulcus and superior temporal cortices respectively). For the motor condition our results show that left-arm versus right-arm stimulations induced typical contralateral difference in hemispheric activation asymmetries in the three subjects for all three channels. For the auditory condition, we also revealed typical human-like patterns of hemispheric asymmetries in one subject for all three channels, namely (1) typical contralateral differences in hemispheric asymmetry between left-ear versus right-ear stimulations, and (2) a rightward asymmetry for stereo stimulations. Overall, our findings support the use of fNIRS to investigate brain processing in non-human primates from a functional perspective, opening the way for the development of non-invasive procedures in non-human primate brain research.

neuroscience↗

Human discrimination and categorization of emotions in voices: a functional Near-Infrared Spectroscopy (fNIRS) study

Variations of the vocal tone of the voice during speech production, known as prosody, provide information about the emotional state of the speaker. In recent years, functional imaging has suggested a role of both right and left inferior frontal cortices in attentive decoding and cognitive evaluation of emotional cues in human vocalizations. Here, we investigated the suitability of functional Near-Infrared Spectroscopy (fNIRS) to study frontal lateralization of human emotion vocalization processing during explicit and implicit categorization and discrimination. Participants listened to speech-like but semantically meaningless words spoken in a neutral, angry or fearful tone and had to categorize or discriminate them based on their emotional or linguistic content. Behaviorally, participants were faster to discriminate than to categorize and they processed the linguistic content of stimuli faster than their emotional content, while an interaction between condition (emotion/word) and task (discrimination/categorization) influenced accuracy. At the brain level, we found a four-way interaction in the fNIRS signal between condition, task, emotion and channel, highlighting the involvement of the right hemisphere to process fear stimuli, and of both hemispheres to treat anger stimuli. Our results show that fNIRS is suitable to study vocal emotion evaluation in humans, fostering its application to study emotional appraisal.

neuroscience↗