Effects of Age and Social Function on Voice-Processing Systems in Autism

Background:

Children with autism spectrum disorders (ASD) often show a lack of engagement with social communication cues, including speech, perhaps due to diminished attribution of reward to social stimuli, which may impact the development of social skills. In adolescence, increased importance is placed on social interactions as individuals begin to make a world for themselves outside of the home. Social communication impairments thus may leave individuals with ASD uniquely vulnerable during the transition from childhood to adulthood. Neuroimaging research suggests that children with ASD show weaker connectivity between voice-selective superior temporal sulcus and reward and affective brain regions compared to typically developing (TD) children, and that the strength of connectivity is associated with individual differences in social communication abilities. However, little is known about the development of speech processing in the social brain during adolescence, or its relationship to social communication deficits in ASD.  

Objectives:  

We examined the neural basis of 1) processing unfamiliar voices compared to non-vocal sounds and 2) processing unfamiliar voices compared to mother’s voice, a familiar vocal source associated with the home environment, in children and adolescents with ASD compared to their TD peers. Specifically, we explored age- and social function-related effects to better understand how voice processing in ASD deviates from typical development and correlates with social communication abilities.

Methods:  

We used fMRI to measure brain activity in 31 individuals with high-functioning ASD (8-18 y/o) and 39 age- and IQ-matched TD controls (7-17 y/o) in response to nonsense words produced by both unfamiliar female speakers and their own mothers, as well as energy- and duration-matched non-vocal environmental sounds. We also administered the social responsiveness scale (SRS) to measure social function.

Results:  

The ASD group showed less activity in reward and social brain regions compared to the TD group in response to vocal stimuli. Moreover, unfamiliar voices, compared to both environmental sounds and mother’s voice, elicited increased activity in the brain’s reward circuit as a function of age in the TD group, suggesting increased reward attribution to novel vocal sources in adolescence.  This relationship was absent in the ASD group, who showed no age-related change but did show variability in brain activity in voice-selective and affective regions as a function of SRS score, with increased activity correlating with more severe social impairments. 

Conclusions:  

Our results support previous findings by showing that both familiar and unfamiliar vocal sources elicit reduced brain activity in reward and affective circuits in individuals with ASD compared to their TD peers. Moreover, the absence of age-related changes in response to unfamiliar voices in the ASD group suggests a deviation from typical development. Such impairments may play a role in the ability of adolescents with ASD to experience novel vocal sources as salient and pleasurable stimuli, thereby impacting social skill development in this population. Our results also suggest a neural basis for individual differences in social function in ASD, with immature brain responses correlating with behavioral impairments.