Species-specific calls evoke asymmetric activity in the monkey's temporal poles

Abstract

It has often been proposed that the vocal calls of monkeys are precursors of human speech, in part because they provide critical information to other members of the species who rely on them for survival and social interactions. Both behavioural and lesion studies suggest that monkeys, like humans, use the auditory system of the left hemisphere preferentially to process vocalizations. To investigate the pattern of neural activity that might underlie this particular form of functional asymmetry in monkeys, we measured local cerebral metabolic activity while the animals listened passively to species-specific calls compared with a variety of other classes of sound. Within the superior temporal gyrus, significantly greater metabolic activity occurred on the left side than on the right, only in the region of the temporal pole and only in response to monkey calls. This functional asymmetry was absent when these regions were separated by forebrain commissurotomy, suggesting that the perception of vocalizations elicits concurrent interhemispheric interactions that focus the auditory processing within a specialized area of one hemisphere.

Wernicke's area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language

“…Functional imaging studies in non-human primates also indicate the existence of asymmetric hemispheric activation of auditory areas in the superior temporal gyrus, including area Tpt (Poremba et al 2003(Poremba et al , 2004. In particular, the posterior portion of the right superior temporal gyrus processes a wide variety of auditory stimuli in macaques (Poremba et al 2003(Poremba et al , 2004, whereas the left hemisphere is specifically involved in the analysis of species-specific vocalizations, which activates the dorsal temporal pole (Poremba et al 2004). In addition, vocal calls have been demonstrated to elicit increased activity in area Tpt of macaques (Gil-da-Costa et al 2006) with seemingly greater intensity in the left hemisphere, although this pattern appeared variable among the three subjects studied.…”

“…The thalamocortical afferents to area Tpt, arising from the medial geniculate complex, however, suggest that it is primarily associated with auditory processing ) and may play a role discriminating the spatial location of sounds (Leinonen et al 1980). Accordingly, area Tpt of the left and right hemispheres has been demonstrated to be involved in the processing of species-specific vocalizations in Old World monkeys (Poremba et al 2003(Poremba et al , 2004Gil-da-Costa et al 2006) and chimpanzees (Taglialatela et al 2009). …”

Voice processing in human and non-human primates

“…Yet, a left-lateralized pattern of activity was found in the dorsal temporal pole, the most anterior region of interest, only for the conditions where CVs were present (CVs or CVs mixed with other sounds). These findings were interpreted as suggesting that the temporal pole might constitute a precursor of a human acoustic language area (Poremba et al 2004). Of particular interest would have been a comparison of activity across the different classes of sounds within a same region.…”

“…Poremba et al (2004) used positron emission tomography (PET) to measure metabolic activity in rhesus macaques during passive listening to several classes of complex sounds, including CVs, human vocalizations, as well as non-vocal sounds from the environment (Poremba et al 2004). Each superior temporal gyrus was divided into five regions of interest, and metabolic activity in each region was compared across hemispheres.…”

Sex-dependent neurofunctional predictors of long-term maintenance of visual word learning

“…The larger isthmus might allow females to communicate more efficiently between the two hemispheres. On the other hand, one recent animal study suggests that interhemispheric interactions help to inhibit the activation in one hemisphere and thus increase the laterality when processing species-specific calls [16]. Further studies are required to examine how the two hemispheres interact with each other, in terms of competition and collaboration, and how this is modulated by sex differences in neuroanatomical connection.…”