Exploring the cerebral substrate of voice perception in primate brains

Abstract

One can consider human language to be the Swiss army knife of the vast domain of animal communication. There is now growing evidence suggesting that this technology may have emerged from already operational material instead of being a sudden innovation. Sharing ideas and thoughts with conspecifics via language constitutes an amazing ability, but what value would it hold if our conspecifics were not first detected and recognized? Conspecific voice (CV) perception is fundamental to communication and widely shared across the animal kingdom. Two questions that arise then are: is this apparently shared ability reflected in common cerebral substrate? And, how has this substrate evolved? The paper addresses these questions by examining studies on the cerebral basis of CV perception in humans' closest relatives, non-human primates. Neuroimaging studies, in particular, suggest the existence of a 'voice patch system', a network of interconnected cortical areas that can provide a common template for the cerebral processing of CV in primates. This article is part of the theme issue 'What can animal communication teach us about human language?'

Keywords: comparative neuroimaging; language evolution; primates; voice patch system; voice perception.

Figure 1.

Neuroimaging evidence of the temporal lobe regions showing sensitivity to conspecific voice (CV) in primates. A simplified phylogenetic tree of the species of interest is represented on the left (common marmoset, rhesus macaque, chimpanzee and human). On the right side, the table summarizes the regions found in neuroimaging studies (references in the last column) for the left and right hemispheres separately. The other columns indicate the main differences in the experimental procedures used in these studies (contrast of interest, anaesthesia and number of individuals). Three main categories of contrasts emerge: CV > non-CV (red), CV > acoustic controls (green) and identity sensitivity (orange). In black, we added recent results that we obtained in a comparative study between human and macaques. a, m, p, anterior, middle, posterior; Env, environmental sounds; HV, heterospecific voice; ITG, inferior temporal gyrus; LS, lateral sulcus; MTG, middle temporal gyrus; Ma, million years ago; STP, superior temporal plane; STG/S superior temporal gyrus/sulcus; TP, temporal pole.

Figure 2.

Organization of the conspecific voice (CV) patches along the temporal lobe in primates. The location of the regions is based on the selected neuroimaging studies in figure 1. Coloured spheres represent the location of a region more sensitive to CV than: non-CV (red), acoustic controls (green), a particular sensitivity to identity (orange) or to several of these contrasts (mixed colour). Black crosses illustrate the position of the newly identified CV-sensitive STS sites [82]. The regions are represented on white matter surfaces to reveal the inner part of the folds. The brain surfaces were modified from personal data for human, one individual image of the National Chimpanzee Brain Resource (NS092988) for chimpanzees, the NMT atlas white matter surface for macaques [83] and the segmented Brain/MINDS atlas for marmosets [84]. The black bar indicates 1 cm scale. L, left hemisphere; R, right hemisphere; a, m, p, anterior, middle, posterior; CV, conspecific voice; ITG, inferior temporal gyrus; LS, lateral sulcus; MTG, middle temporal gyrus; STP, superior temporal plane; STG/S, superior temporal gyrus/sulcus; TP, temporal pole.