Altered processing of communication signals in the subcortical auditory sensory pathway in autism

Abstract

Autism spectrum disorder (ASD) is characterised by social communication difficulties.These difficulties have been mainly explained by cognitive, motivational, and emotional alterations in ASD. The communication difficulties could, however, also be associated with altered sensory processing of communication signals. Here, we assessed the functional integrity of auditory sensory pathway nuclei in ASD in three independent functional magnetic resonance imaging experiments. We focused on two aspects of auditory communication that are impaired in ASD: voice identity perception, and recognising speech-in-noise. We found reduced processing in adults with ASD as compared to typically developed control groups (pairwise matched on sex, age, and full-scale IQ) in the central midbrain structure of the auditory pathway (inferior colliculus [IC]). The right IC responded less in the ASD as compared to the control group for voice identity, in contrast to speech recognition. The right IC also responded less in the ASD as compared to the control group when passively listening to vocal in contrast to non-vocal sounds. Within the control group, the left and right IC responded more when recognising speech-in-noise as compared to when recognising speech without additional noise. In the ASD group, this was only the case in the left, but not the right IC. The results show that communication signal processing in ASD is associated with reduced subcortical sensory functioning in the midbrain. The results highlight the importance of considering sensory processing alterations in explaining communication difficulties, which are at the core of ASD.

Responses in left inferior frontal gyrus are altered for speech‐in‐noise processing, but not for clear speech in autism

“…This point is critical, because differences in task instruction in speech-innoise perception lead to the recruitment of different brain mechanism (Wild et al, 2012). Evidence that neural processing is altered when performing a speech recognition task comes from a previous study which included the same ASD and TD group participants as reported here (Schelinski et al, 2022). In that study, the TD group but not the ASD group showed enhanced responses in the right IC for speech-in-noise recognition as compared to speech recognition without noise.…”

“…We provide novel evidence that processes related to speech-innoise recognition in ASD are particularly altered in the left IFG. Only a few studies investigated the neural processing of speech-in-noise in ASD (Hernandez et al, 2020;Lin et al, 2021;Russo et al, 2009;Schelinski et al, 2022). Russo et al (2009) found altered brainstem responses in children with ASD as compared to typically developing children when passively listening to speech (i.e., syllables) when the speech signal was presented with and without additional noise (i.e., presented together with white noise).…”

“…To investigate neural responses to speech-in-noise, participants performed an auditory-only speech recognition task for speech that was either presented with or without additional noise during MRI (speechin-noise recognition experiment, Figure 1a,b). Design and raw data for the speech-in-noise recognition experiment are the same as described in Schelinski et al (2022). For participants who never had MRI before, we conducted a mock MRI to familiarize the participants with the MRI environment.…”

“…Only a few studies investigated the neural processing of speechin-noise perception in ASD (Hernandez et al, 2020;Lin et al, 2021;Russo et al, 2009;Schelinski et al, 2022). These studies focused on alteration and reduction of responses in subcortical sensory structures (Russo et al, 2009;Schelinski et al, 2022) and/or did not include a speech recognition task (Hernandez et al, 2020;Lin et al, 2021;Russo et al, 2009). Russo et al (2009) found altered brainstem responses in children with ASD as compared to typically developing children when passively listening to speech (i.e., syllables).…”

“…These alterations were present both for speech without noise as well as when speech was presented with additional white noise. Schelinski et al (2022) showed enhanced responses within a typically developed control group, when performing a speech recognition task when the speech signal was presented with noise versus no noise in the left and right inferior colliculus (IC). The IC is a nucleus of the subcortical auditory pathway associated with processing of spectro-temporal voice acoustic features (e.g., Baumann et al, 2011;Griffiths et al, 2001; for review see Pannese et al, 2015).…”