Using naturalistic utterances to investigate vocal communication processing and development in human and non-human primates

Abstract

Humans and several non-human primates possess cortical regions that are most sensitive to vocalizations produced by their own kind (conspecifics). However, the use of speech and other broadly defined categories of behaviorally relevant natural sounds has led to many discrepancies regarding where voice-sensitivity occurs, and more generally the identification of cortical networks, “proto-networks” or protolanguage networks, and pathways that may be sensitive or selective for certain aspects of vocalization processing. In this prospective review we examine different approaches for exploring vocal communication processing, including pathways that may be, or become, specialized for conspecific utterances. In particular, we address the use of naturally produced non-stereotypical vocalizations (mimicry of other animal calls) as another category of vocalization for use with human and non-human primate auditory systems. We focus this review on two main themes, including progress and future ideas for studying vocalization processing in great apes (chimpanzees) and in very early stages of human development, including infants and fetuses. Advancing our understanding of the fundamental principles that govern the evolution and early development of cortical pathways for processing non-verbal communication utterances is expected to lead to better diagnoses and early intervention strategies in children with communication disorders, improve rehabilitation of communication disorders resulting from brain injury, and develop new strategies for intelligent hearing aid and implant design that can better enhance speech signals in noisy environments.

Hearing and orally mimicking different acoustic-semantic categories of natural sound engage distinct left hemisphere cortical regions

“…Vocal-acoustic communication forms have obvious advantages relative to visiondominated manual gestures and sign languages, in that they are known to be faster, not require a need of being in line of sight, can be communicated in total darkness and over longer distances, and allow mothers rearing infants to have more freedom with the hands for foraging at a distance (Hewes, 1973). Lateralizations for processing certain classes of vocal calls have been reported in other primate species (Poremba et al, 2004; Taglialatela, Russell, Schaeffer, & Hopkins, 2009; Talkington et al, 2012; Talkington, Taglialatela, & Lewis, 2013), supporting the idea that more advanced vocalization processing and decoding is associated with brain asymmetries. However, assuming that improvements in oral mimicry of real-world natural sound-producing events were critical to oral communication evolution, what sounds were most likely needed to be imitated in early stages of hominin evolution?…”

Cooperation came first: Evolution and human cognition

“…Before we explore the evolutionary sense of that claim, however, we need to bring in a small set of related behavioral skills, some of which are supported by cooperation and eusociality. Although even human infants generally outperform nonhuman primates on each of the tasks we will describe in the sections that follow (e.g., Caron, Kiel, Dayton, and Butler, 2002;Mumme, Fernald, & Herrera, 1996;Talkington, Taglialatela, & Lewis, 2013), these abilities are shared with other nonhuman animals.…”

Auditory object perception: A neurobiological model and prospective review

“…2e, colored ovals and boxes) can at least roughly be organized along a continuum of harmonic structure (Lewis et al, 2009). The lower end of the harmonic content scale includes hisses, growls, grunts, and groans, which are mostly associated with threat warnings and phatic utterances expressing negative emotional valence (Austin, 1975; Lewis et al, 2009; Talkington et al, 2013). At the other extreme, whistling, howls, and vocal singing are characterized by relatively higher harmonic content.…”