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Abstract:
Humans and non-human primates such as macaques possess brain regions dedicated to segregating and processing vocal communication sounds from the environment and encoding their meaning. Brain regions that are strongly activated by conspecific vocalizations encompass the auditory cortices and higher-level regions in the temporal and frontal lobes. However, human imaging studies also implicate other brain regions in processing complex sounds and vocal and non-vocal communication signals such as speech or music. Hence our overall goal is to investigate the neural basis of how communication signals are processed across these regions.
One such area activated to speech is the insular cortex. Studying a vocal primate we identified a predominantly auditory region in the caudal insula where neurons, when probed with a range of natural sounds, responded preferentially to conspecific vocalizations. This preference also existed over acoustically manipulated versions of these vocalizations, demonstrating insula sensitivity to the spectral and temporal features of these sounds. These findings characterize the caudal insula as an auditory region preferentially responding to vocal communication sounds.
We also identified a sub-region within the claustrum, a structure located beneath the insula and reciprocally connected to the entire cortex, which responded to acoustic stimuli. Neurons here displayed increased firing rates at the onset of stimulus presentation and not integrate audio-visual information. They did however respond preferentially to vocalizations or events that were highly salient suggesting a role for the claustrum in saliency detection.
Human acoustic communication is not restricted to vocal sounds, but also includes non-vocal sounds or acoustic gestures. Here we report that macaque monkeys display drumming behaviors that not only attract the attention of listening monkeys as similarly as conspecific vocalizations but also influence their social interactions. Using high-resolution functional imaging we identified brain regions preferentially activated by drumming sounds or vocalizations, and found that they are both represented in higher-order regions within the auditory cortex and the amygdala. These results suggest a common origin of primate vocal and non-vocal communication systems and a likely common origin of human speech and music.
Overall, we show that vocal communication sounds are processed not only in the auditory cortices but also in the insula and claustrum. Furthermore, specialized networks that evolved to process vocalizations are also used to process non-vocal communication sounds in a similar manner.
