Frontal mechanisms underlying primate calls recognition by humans.

Introduction: 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 vocalizations, that we share with other primate species-particularly great apes (Hominidae). Methods: To better understand these processes at the behavioral 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. Results: 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. Discussion: Our data-that are controlled for acoustic variability between species-therefore reveal distinct frontal mechanisms that shed light on how the human brain evolved to process vocal signals.

Cerebral Activity in Female Baboons (Papio anubis) During the Perception of Conspecific and Heterospecific Agonistic Vocalizations: a Functional Near Infrared Spectroscopy Study.

The "voice areas" in the superior temporal cortex have been identified in both humans and non-human primates as selective to conspecific vocalizations only (i.e., expressed by members of our own species), suggesting its old evolutionary roots across the primate lineage. With respect to non-human primate species, it remains unclear whether the listening of vocal emotions from conspecifics leads to similar or different cerebral activations when compared to heterospecific calls (i.e., expressed by another primate species) triggered by the same emotion. Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy, the present study investigated in three lightly anesthetized female baboons (Papio anubis), temporal cortex activities during exposure to agonistic vocalizations from conspecifics and from other primates (chimpanzees-Pan troglodytes), and energy matched white noises in order to control for this low-level acoustic feature. Permutation test analyses on the extracted OxyHemoglobin signal revealed great inter-individual differences on how conspecific and heterospecific vocal stimuli were processed in baboon brains with a cortical response recorded either in the right or the left temporal cortex. No difference was found between emotional vocalizations and their energy-matched white noises. Despite the phylogenetic gap between Homo sapiens and African monkeys, modern humans and baboons both showed a highly heterogeneous brain process for the perception of vocal and emotional stimuli. The results of this study do not exclude that old evolutionary mechanisms for vocal emotional processing may be shared and inherited from our common ancestor. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00164-z.

Validating the use of functional Near-Infrared Spectroscopy in monkeys: The case of brain activation lateralization in Papio anubis.

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 sensorimotor condition our results show that left-arm versus right-arm stimulations induced typical contralateral difference in hemispheric activation asymmetries in the three subjects. For the auditory condition, we also revealed typical human-like patterns of hemispheric asymmetries in one subject, namely a leftward lateralization for right ear stimulations for all three channels. 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.

Human Discrimination and Categorization of Emotions in Voices: A Functional Near-Infrared Spectroscopy (fNIRS) Study.

Functional Near-Infrared spectroscopy (fNIRS) is a neuroimaging tool that has been recently used in a variety of cognitive paradigms. Yet, it remains unclear whether fNIRS is suitable to study complex cognitive processes such as categorization or discrimination. Previously, functional imaging has suggested a role of both inferior frontal cortices in attentive decoding and cognitive evaluation of emotional cues in human vocalizations. Here, we extended paradigms used in functional magnetic resonance imaging (fMRI) to investigate the suitability of fNIRS to study frontal lateralization of human emotion vocalization processing during explicit and implicit categorization and discrimination using mini-blocks and event-related stimuli. Participants heard speech-like but semantically meaningless pseudowords spoken in various tones and evaluated them based on their emotional or linguistic content. Behaviorally, participants were faster to discriminate than to categorize; and processed the linguistic faster than the emotional content of stimuli. Interactions between condition (emotion/word), task (discrimination/categorization) and emotion content (anger, fear, neutral) influenced accuracy and reaction time. At the brain level, we found a modulation of the Oxy-Hb changes in IFG depending on condition, task, emotion and hemisphere (right or left), 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, fostering its application to complex cognitive paradigms.

DJINNI: A Novel Technology Supported Exposure Therapy Paradigm for SAD Combining Virtual Reality and Augmented Reality.

The present paper explores the benefits and the capabilities of various emerging state-of-the-art interactive 3D and Internet of Things technologies and investigates how these technologies can be exploited to develop a more effective technology supported exposure therapy solution for social anxiety disorder. "DJINNI" is a conceptual design of an in vivo augmented reality (AR) exposure therapy mobile support system that exploits several capturing technologies and integrates the patient's state and situation by vision-based, audio-based, and physiology-based analysis as well as by indoor/outdoor localization techniques. DJINNI also comprises an innovative virtual reality exposure therapy system that is adaptive and customizable to the demands of the in vivo experience and therapeutic progress. DJINNI follows a gamification approach where rewards and achievements are utilized to motivate the patient to progress in her/his treatment. The current paper reviews the state of the art of technologies needed for such a solution and recommends how these technologies could be integrated in the development of an individually tailored and yet feasible and effective AR/virtual reality-based exposure therapy. Finally, the paper outlines how DJINNI could be part of classical cognitive behavioral treatment and how to validate such a setup.