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Edited by Michael I. Posner, University of Oregon, Eugene, OR, and approved April 1, 2016 (received for review February 24, 2016)
Significance
The human voice provides a wealth of social information, including who is speaking. A salient voice in a child’s life is mother's voice, which guides social function during development. Here we identify brain circuits that are selectively engaged in children by their mother’s voice and show that this brain activity predicts social communication abilities. Nonsense words produced by mother activate multiple brain systems, including reward, emotion, and face-processing centers, reflecting how widely mother’s voice is broadcast throughout a child’s brain. Importantly, this activity provides a neural fingerprint of children’s social communication abilities. This approach provides a template for investigating social function in clinical disorders, e.g., autism, in which perception of biologically salient voices may be impaired.
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.
Footnotes
- ↵1To whom correspondence may be addressed. Email: daa{at}stanford.edu or menon{at}stanford.edu.
Author contributions: D.A.A. and V.M. designed research; D.A.A., P.O., K.M.C., A.E.B., and A.P. performed research; D.A.A., T.C., A.E.B., S.R., and V.M. contributed new reagents/analytic tools; D.A.A., T.C., P.O., A.E.B., and J.K. analyzed data; and D.A.A., C.F., and V.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1602948113/-/DCSupplemental.
Freely available online through the PNAS open access option.
References
Neural circuits for mother's voice
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