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.

Keywords: auditory; brain; children; reward; voice.

Fig. 1.

fMRI experimental design, acoustical analysis. and behavioral results. (A) Randomized, rapid event-related design: During fMRI data collection, three auditory nonsense words, produced by three different speakers, were presented to the child participants at a comfortable listening level. The three speakers consisted of the child’s mother and two female control voices. Nonspeech environmental sounds were also presented to enable baseline comparisons for the speech contrasts of interest. All auditory stimuli were 956 ms in duration and were equated for rms amplitude. (B) Acoustical analyses show that vocal samples produced by the participants’ mothers were similar to the female control voice samples for individual acoustical measures. (C) Results from behavioral ratings, collected in an independent cohort of children who did not participate in the fMRI study, show that female control voice samples were rated equally as pleasant as, and more exciting than, the mother’s voice samples. *P < 0.05; NS, not significant. (D) Children who participated in the fMRI study were able to identify their mother’s voice with high levels of accuracy, supporting the sensitivity of these young listeners to their mother’s voice. The horizontal line represents chance level for the mother’s voice identification task.

Fig. 2.

Brain activity in response to mother’s voice. Compared to female control voices, mother’s voice elicits greater activity in auditory brain structures in the midbrain and superior temporal cortex (Upper Left), including the bilateral IC and primary auditory cortex (mHG) and a wide extent of voice-selective STG (Upper Center) and STS. Mother’s voice also elicited greater activity in occipital cortex, including fusiform gyrus (FG) (Lower Left), and in heteromodal brain regions serving affective functions, anchored in the amygdala (Upper Right), core structures of the mesolimbic reward system, including NAc, OFC, and vmPFC (Lower Center), and structures of the salience network, including the AI and dACC (Lower Right). No voxels showed greater activity in response to female control voices compared to mother’s voice.

Fig. S1.

Signal levels in primary auditory regions (Upper) and voice-selective cortex (Lower) in response to mother’s voice and female control voices. Primary auditory regions were identified a priori from previous auditory studies (IC ROIs) (56) and from cytoarchitectonic maps (Te ROIs) (55), and voice-selective cortical regions were selected for signal-level analysis based on previous investigations of voice-selective cortex (bilateral pSTS; refs. 11, 37) or their identification in the [mother’s voice > female control voices] contrast (bilateral mSTS and aSTS; see Fig. 2 in the main text). Values plotted for mother’s voice and female control voices are referenced to duration and energy-matched environmental sounds, e.g., [mother’s voice > environmental sounds]. The signal-level analysis was performed because stimulus-based differences in fMRI activity can result from a number of different factors. Significant differences were inherent to this ROI analysis, because they are based on results from the whole-brain GLM analysis (52); however, results provide important information regarding the magnitude and sign of fMRI activity. **P < 0.01; *P < 0.05.

Fig. S2.

Signal levels in mesolimbic reward regions (Upper) and the amygdala and salience network (Lower) in response to mother’s voice and female control voices. Regions were selected for signal-level analysis based on their identification in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). Values plotted for mother’s voice and female control voices are referenced to duration- and energy-matched environmental sounds, e.g., [mother’s voice > environmental sounds]. NAc and amygdala ROIs are 2-mm spheres centered at the peak for these regions in the [mother’s voice > female control voices] contrast; all other ROIs in these bar graphs are 5-mm spheres centered at the peak for these regions in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). **P < 0.01; *P < 0.05.

Fig. S3.

Signal levels in default mode (Upper) and occipital (Lower) regions in response to mother’s voice and female control voices. Regions were selected for signal-level analysis based on their identification in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). Values plotted for mother’s voice and female control voices are referenced to duration- and energy-matched environmental sounds, e.g., [mother’s voice > environmental sounds]. All ROIs in these bar graphs are 5-mm spheres centered at the peak for these regions in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). **P < 0.01.

Fig. S4.

Signal levels in frontoparietal regions in response to mother’s voice and female control voices. Regions were selected for signal-level analysis based on their identification in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). Values plotted for mother’s voice and female control voices are referenced to duration- and energy-matched environmental sounds, e.g., [mother’s voice > environmental sounds]. All ROIs are 5-mm spheres centered at the peak for these regions in the [mother’s voice > female control voices] contrast (Fig. 2 in the main text). **P < 0.01.

Fig. S5.

Brain activity in response to female control voices compared to environmental sounds. Compared to environmental sounds, female control voices elicit greater activity throughout a wide extent of voice-selective STG and STS (Upper Center Left), bilateral amygdala (Upper Center Right) and supramarginal gyrus (Upper Right), and a small extent of left hemisphere mHG (Upper Left). In contrast to brain activity in response to mother’s voice, univariate results comparing female control voices to environmental sounds failed to identify brain regions in reward, salience, and face-processing regions or in the IC.

Fig. 3.

Connectivity of left-hemisphere voice-selective cortex and social communication abilities. The whole-brain connectivity map shows that children’s social communication scores covaried with the strength of functional coupling between the left-hemisphere aSTS (Top) and left-hemisphere NAc (Center Left), right-hemisphere amygdala (Center Right), right-hemisphere hippocampus (Bottom Left), and FG, which overlapped with the FG2 subregion (Bottom Right). Scatterplots show the distributions and covariation of aSTS connectivity strength in response to mother’s voice and standardized scores of social communication abilities. Greater social communication abilities, reflected by smaller social communication scores, are associated with greater brain connectivity between the STS and these brain regions. a.u., arbitrary units.

Fig. 4.

Connectivity of right-hemisphere voice-selective cortex and social communication abilities. The whole-brain connectivity map shows that children’s social communication scores covaried with the strength of functional coupling between the right-hemisphere pSTS (Upper Left) and OFC of the reward pathway (Upper Right) and between the AI and dACC of the salience network (Lower). Scatterplots show the distributions and covariation of STS connectivity strength in response to mother’s voice and standardized scores of social function. Greater social communication abilities, reflected by smaller social communication scores, are associated with greater brain connectivity between the STS and these brain regions.

Fig. S6.

Connectivity of left-hemisphere voice-selective cortex and language abilities. The whole-brain connectivity map shows that children’s CELF core language covaried with the strength of functional coupling between the left-hemisphere mSTS (Upper) and right-hemisphere HG (Lower Left) and BA 47 of inferior frontal gyrus (IFG) (Lower Right). Scatterplots show the distributions and covariation of mSTS connectivity strength in response to mother’s voice and standardized scores of language abilities in these children. Greater language scores are associated with greater brain connectivity between the STS and these brain regions.