Categorization and discrimination of human and non-human primate affective vocalizations: Investigation of frontal...

Previous research has highlighted the involvement of frontal regions in human participants while they engaged in the explicit decoding, such as categorization (AvsB) and discrimination (Avsnon-A), of affective signals. Given its adaptive value and deep evolutionary history, this human capacity to recognize the affective content in human calls is likely to extend to the vocalizations of other closely related species, such as non-human primates. However, few comparative studies have thus far investigated this process at both the behavioral and neural levels. Here, we aimed to study the role of frontal regions in human participants while they engaged in the explicit affective content decoding of primate calls using functional Near Infrared Spectroscopy (fNIRS). Specifically, we recorded frontal regions of participants while they categorized or discriminated positive and negatively valenced vocal signals produced by four different primates: humans, chimpanzee and bonobo (both great apes species), and rhesus macaques (a more distant species). We also analyzed whether behavioral responses correlated with recorded frontal activations. fNIRS data revealed more activations within the inferior frontal cortexpars triangularis(IFC_tri), the frontopolar (FPC), and middle frontal cortices (MFC) during discrimination compared with categorization. Activity in these regions was modulated by both the species and the type of task, with greater activity during the discrimination of agonistic chimpanzee calls compared with categorization. Categorization was itself characterized by a decrease of frontal activity during the correct recognition of all chimpanzee calls, and of affiliative rhesus macaque and agonistic bonobo vocalizations. Our results also highlighted behavioral differences related to the type of task. Participants discriminated almost all affective cues of all four species vocalizations above chance level. In comparison, they correctly categorized the affective content of most human and great ape vocalizations above chance level, but not those of rhesus macaque calls, highlighting an effect of both phylogenetic relatedness and the type of task. Overall, these findings support the hypothesis of an evolutionary ancient affective recognition processing system situated in the frontal cortex, inherited from our last common ancestor with other great apes.