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

Abstract

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.

Keywords: Agonistic vocalizations; Cerebral activity; Conspecific; Heterospecific; Monkey; fNIRS.

Fig. 1

Representative waveforms and spectrograms of 20 s-long agonistic a baboon and b chimpanzee vocalizations used as stimuli in the present study. These graphical representations were extracted using the PhonTools package (Barreda, 2015) on R. studio (Team, 2020)

Fig. 2

fNIRS optode and channel locations according to 89 baboons T1 MRI template (Love et al., 2016). Blue and green crosses represent optical receivers and transmitters, respectively. Ch1, Ch2, and Ch3 indicate the three channels on the right and left temporal cortex

Fig. 3

Right and left temporal cortex activations for the baboons a Talma, b Chet, and c Rubis during the perception of agonistic baboon (conspecific) and chimpanzee (heterospecific) vocalizations as well as their energy-matched white noises. The mean concentration changes of O₂Hb (y axis) are represented in micromolar (µM) for each fNIRS channel (x axis). Colorful dots and dark lines represent stimuli and confidence intervals respectively. Results of the permutation tests within channels are shown with *p < 0.05; p = 0.07. The ggplot2 package (Wickham et al., 2021) on R.studio (Team, 2020) was used for visualizing the data