Atypical processing of voice sounds in infants at risk for autism spectrum disorder

Declan G.M Murphy,Evelyne Mercure,Mark H Johnson,Anna Blasi,Lynne Murray,Vaheshta Sethna,Andrew Simmons,Steven C.R Williams,Michael J Brammer,Sarah Lloyd-Fox

doi:10.1016/j.cortex.2015.06.015

Abstract

Adults diagnosed with autism spectrum disorder (ASD) show a reduced sensitivity (degree of selective response) to social stimuli such as human voices. In order to determine whether this reduced sensitivity is a consequence of years of poor social interaction and communication or is present prior to significant experience, we used functional MRI to examine cortical sensitivity to auditory stimuli in infants at high familial risk for later emerging ASD (HR group, N = 15), and compared this to infants with no family history of ASD (LR group, N = 18). The infants (aged between 4 and 7 months) were presented with voice and environmental sounds while asleep in the scanner and their behaviour was also examined in the context of observed parent–infant interaction. Whereas LR infants showed early specialisation for human voice processing in right temporal and medial frontal regions, the HR infants did not. Similarly, LR infants showed stronger sensitivity than HR infants to sad vocalisations in the right fusiform gyrus and left hippocampus. Also, in the HR group only, there was an association between each infant's degree of engagement during social interaction and the degree of voice sensitivity in key cortical regions. These results suggest that at least some infants at high-risk for ASD have atypical neural responses to human voice with and without emotional valence. Further exploration of the relationship between behaviour during social interaction and voice processing may help better understand the mechanisms that lead to different outcomes in at risk populations.

Highlights

One of the basic foundations for social communication is the human voice, which is arguably the most important acoustic stimulus in an individuals' social environment as it carries important cues such as speaker identity and emotional state
Voice-processing in high risk (HR) and low risk (LR) infants. In this functional magnetic resonance imaging (fMRI) study, infants in the high-risk group show a striking atypicality in human voice selectivity
Adding to these previous studies, we have established that between 4 and 7 months there is already voice specialisation along the superior temporal sulcus (STS), and in other brain regions such as the inferior frontal and fusiform cortex

Summary

Introduction

One of the basic foundations for social communication is the human voice, which is arguably the most important acoustic stimulus in an individuals' social environment as it carries important cues such as speaker identity and emotional state. Research with adults has revealed that cortical regions along the superior temporal sulcus (STS) show stronger activation when participants listen to human vocalisations (speech, laughter, crying, coughing, etc.) as compared to nonvocal environmental sounds and acoustically matched stimuli (Belin, Zatorre, Lafaille, Ahad, & Pike, 2000) Activation of these temporal voice-selective areas can be modulated by emotional information carried on the voice (Grandjean et al, 2005), as can activation in other areas such as inferior prefrontal cortex (Fecteau, 2005), premotor cortical regions (Warren et al, 2006) and the amygdala (Fecteau, Belin, Joanette, & Armony, 2007), insula and orbitofrontal cortex (Chikazoe, Lee, Kriegeskorte, & Anderson, 2014). The data collected in our previous study has contributed to the LR group in the current study with the exception of three participants who had to be excluded from the current analysis (see the Methods section)

Methods

Results

Conclusion