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

Abstract

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.