Neural circuits underlying mother’s voice perception predict social communication abilities in children

Abstract

The human voice is a critical social cue, and listeners are extremely sensitive to the voices in their environment. One of the most salient voices in a child's life is mother's voice: Infants discriminate their mother's voice from the first days of life, and this stimulus is associated with guiding emotional and social function during development. Little is known regarding the functional circuits that are selectively engaged in children by biologically salient voices such as mother's voice or whether this brain activity is related to children's social communication abilities. We used functional MRI to measure brain activity in 24 healthy children (mean age, 10.2 y) while they attended to brief (<1 s) nonsense words produced by their biological mother and two female control voices and explored relationships between speech-evoked neural activity and social function. Compared to female control voices, mother's voice elicited greater activity in primary auditory regions in the midbrain and cortex; voice-selective superior temporal sulcus (STS); the amygdala, which is crucial for processing of affect; nucleus accumbens and orbitofrontal cortex of the reward circuit; anterior insula and cingulate of the salience network; and a subregion of fusiform gyrus associated with face perception. The strength of brain connectivity between voice-selective STS and reward, affective, salience, memory, and face-processing regions during mother's voice perception predicted social communication skills. Our findings provide a novel neurobiological template for investigation of typical social development as well as clinical disorders, such as autism, in which perception of biologically and socially salient voices may be impaired.

Longitudinal relationships among depressive symptoms, cortisol, and brain atrophy in the neocortex and the hippocampus

“…All the depression‐related regions observed in our study are engaged during processing of familiar faces and voices, especially of significant others . STC is also activated by a gentle touch .…”

Functional connectivity within the voice perception network and its behavioural relevance

“…Finally, this is the first study documenting a relationship between FC and behavioural performance in voice perception in healthy subjects; yet, a positive correlation between right fronto-temporal FC and voice recognition abilities has been previously observed in the clinical domain, namely in schizophrenic patients characterized by auditory hallucinations ( Mou et al., 2013 ). The importance of looking at FC during voice perception is also supported by a recent study that found that fronto-temporal FC during mother's voice perception could predict future social communication skills as measured by a standardized scale ( Abrams et al., 2016 ). Even if a systematic comparison between these studies and ours is not possible since we are in presence of different populations, these very similar findings can confirm the importance of looking at FC (in particular between regions of the core and extended voice perception network) when investigating individual differences in social processes such as voice perception.…”

Evolution of vertebrate survival circuits

“…Similarly, visual displays or simple conspecific visual stimuli in primates (including humans) might constitute rewarding social stimuli (that we, humans, judge as beautiful) and it has been shown that they activate, among other structures, portions of the amygdala and ventral striatum [37]. Activation of amygdalo-striatal pathways is also likely to have a causal role in reward induced by other social stimuli in humans [38].…”