Atypical sound discrimination in children with ASD as indicated by cortical ERPs

Abstract

Background: Individuals with autism spectrum disorder (ASD) show a relative indifference to the human voice. Accordingly, and contrarily to their typically developed peers, adults with autism do not show a preferential response to voices in the superior temporal sulcus; this lack of voice-specific response was previously linked to atypical processing of voices. In electroencephalography, a slow event-related potential (ERP) called the fronto-temporal positivity to voice (FTPV) is larger for vocal than for non-vocal sounds, resulting in a voice-sensitive response over right fronto-temporal sites. Here, we investigated the neurophysiological correlates of voice perception in children with and without ASD.

Methods: Sixteen children with autism and 16 age-matched typically developing children heard vocal (speech and non-speech) and non-vocal sounds while their electroencephalographic activity was recorded; overall IQ was smaller in the group of children with ASD. ERP amplitudes were compared using non-parametric statistical tests at each electrode and in successive 20-ms time windows. Within each group, differences between conditions were assessed using a non-parametric Quade test between 0 and 400 ms post-stimulus. Inter-group comparisons of ERP amplitudes were performed using non-paired Kruskal-Wallis tests between 140 and 180 ms post-stimulus.

Results: Typically developing children showed the classical voice-sensitive response over right fronto-temporal electrodes, for both speech and non-speech vocal sounds. Children with ASD did not show a preferential response to vocal sounds. Inter-group analysis showed no difference in the processing of vocal sounds, both speech and non-speech, but significant differences in the processing of non-vocal sounds over right fronto-temporal sites.

Conclusions: Our results demonstrate a lack of voice-preferential response in children with autism spectrum disorders. In contrast to observations in adults with ASD, the lack of voice-preferential response was attributed to an atypical response to non-vocal sounds, which was overall more similar to the event-related potentials evoked by vocal sounds in both groups. This result suggests atypical maturation processes in ASD impeding the specialization of temporal regions in voice processing.

Keywords: Auditory; Autism; Development; FTPV; Speech; Voice.

Fig. 1

Acoustical differences between sound categories. a Power analysis in time: average power of each sound category over the 500 ms sound duration. b Power analysis in frequency: average power spectrum of each sound category. Statistical differences between sound categories are indicated by gray bars

Fig. 2

ERPs evoked by vocal sounds (either non-speech: Voc^NSp, or speech: Voc^Sp) and non-vocal sounds (NVoc) at fronto-temporal, temporo-mastoïd, and central electrode sites in TD children (a) and children with ASD (b). Significant differences between conditions according to the Quade test (after Bonferroni correction) are indicated by gray bars

Fig. 3

ERPs evoked by vocal sounds (either non-speech: Voc^NSp, or speech: Voc^Sp) and non-vocal sounds (NVoc) at left and right frontal (F7 and F8, respectively), temporal (T7 and T8, respectively), and central (Cz) electrode sites in TD children (black lines) and children with ASD (red lines). Significant differences (gray bars) between children with ASD and TD children were only found for the NVoc sounds

Fig. 4

Scalp potential distributions (top view) of responses to vocal (either non-speech: Voc^NSp, or speech: Voc^Sp) and non-vocal (NVoc) stimuli in the 140–180-ms time window in 16 children with ASD (middle row) and 16 age- and gender-matched TD children (top row). The 140–180-ms time window corresponds to the significant voice effect at right fronto-temporal electrode sites in TD children. Bottom row: topographies of the p value resulting from the group comparison between TD and ASD children for each type of stimuli between 140 and 180 ms