Familiar Speech Sounds Elicit Reduced Brain Activity in the Reward Circuit and Amygdala in Children with Autism
The human voice is a critical communication signal for children: speech serves as a primary source for language learning, provides emotional comfort to young listeners and promotes bonding between parents and children. Children with autism spectrum disorders (ASD) often have difficulty orienting to speech in their environment, including highly familiar voices, and it is thought that this deficit plays a key role in communication deficits in this population. Our recent study showed that children with ASD have weak brain connectivity between voice-selective regions of cortex and the distributed reward circuit and amygdala, and the strength of these speech-reward brain connections predicts social communication abilities in these children (Abrams et al., PNAS, 2013). These results provide novel support for the Social Motivation Hypothesis, which states that deficits in representing the reward value of social stimuli, including speech, impede children with ASD from actively engaging with these stimuli, and consequently impair social skill development.
Objectives: To further test the Social Motivation Hypothesis in the context of speech perception, we examined brain structures and networks that become active in response to familiar and rewarding speech sounds in children with ASD compared to typically developing children (TD). The Social Motivation Hypothesis predicts that familiar and rewarding speech sounds would elicit reduced neural activity in the brain’s reward circuitry in children with ASD compared to control children.
Methods: We used fMRI to measure brain activity in high-functioning children with ASD (n=23) and TD children (n=23) matched for age, gender and IQ. Participants listened to brief (< 1 sec), meaningless speech samples produced by their mothers (“Mother’s voice”) and two control mothers whose voices were unfamiliar to the participants. We also measured the children’s ability to identify their mother’s voice using these brief speech samples.
Results: All children included in the study were able to identify their Mother’s voice with a high degree of accuracy. In TD children, brain responses showed greater activity for Mother’s voice compared to unfamiliar mother’s voices in voice selective superior temporal cortex, the amygdala, which is crucial for processing of social and affective information, the ventral tegmental area, nucleus accumbens, orbitofrontal cortex, and medial prefrontal cortex of the reward circuit. Preliminary results from children with ASD indicate that Mother’s voice elicits significantly reduced neural activity in voice-selective cortex, structures of the reward circuit, including bilateral ventral tegmental area, and structures of the “social brain,” including the amygdala and insula.
Conclusions: Results suggest that impaired signaling between voice-selective areas of the brain and the reward circuit plays a role in the ability of children with ASD to experience speech as a pleasurable stimulus, which may impact social skill development in this population. Results strongly support the Social Motivation Hypothesis by showing that Mother’s voice, a familiar and rewarding sound source to TD children, elicits reduced brain activity in the reward circuit and amygdala in children with ASD.