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

Abstract

Autism spectrum disorder (ASD) is a clinical condition that is associated with deficient processing of communication signals. To-date, most neuroscience research on ASD focuses on explaining these symptoms at the cerebral cortex level or in limbic structures. This research implicitly or explicitly assumes that the subcortical sensory pathways are intact in ASD. To date, however, the integrity of subcortical sensory pathway nuclei in ASD has never been investigated in humans in vivo. Here, we assessed the functional integrity of auditory sensory pathway nuclei in ASD in three independent functional magnetic resonance imaging (fMRI) experiments. We focused on two aspects of auditory communication that are impaired in ASD: voice identity perception, and recognising speech-in noise. Adults with ASD (n = 16 in experiments 1 and 2 and n = 17 in another sample in experiment 3) and typically developed control groups were pairwise matched on sex, age, handedness, and full-scale IQ. We found reduced processing in the ASD as compared to the control groups in the central midbrain structure of the auditory pathway (inferior colliculus, IC; all results FWE corrected and Bonferroni corrected for the number of regions tested). The right IC responded less in the ASD as compared to the control group for voice identity recognition, in contrast to a speech recognition task. The right IC also responded less in the ASD as compared to the control group when passively listening to vocal sounds in contrast to non-vocal sounds. For speech-in-noise recognition, we found that within the control group, the left and right IC responded more when performing a speech-in-noise recognition task as compared to when performing a speech recognition task without additional noise. In the ASD group, this was only the case in the left, but not the right IC. There was no interaction between noise and group. 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 social communication difficulties, which are at the core of ASD.

Intrinsic Neural Timescales in Autism Spectrum Disorder and Schizophrenia. A Replication and Direct Comparison Study

“…Information integration requires fast and accurate information processing and transmission, but this is impaired in clinical samples. Patients diagnosed with schizophrenia (SZ) or autism spectrum disorder (ASD) show alterations in basic visual and auditory processing (e.g., Gold et al, 2012; Javitt and Freedman, 2015; Schelinski, Roswandowitz, & von Kriegstein, 2017; Schelinski & von Kriegstein, 2019; Schelinski et al, 2020), as well as motion detection (Chen et al 2003) and object recognition (Kronbichler et al 2018). Furthermore, multisensory integration has also been shown to be impaired in ASD and SZ.…”

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

“…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 speech-in-noise perception in ASD (Russo, Zecker, Trommer, Chen, & Kraus, 2009;Schelinski, Tabas, & von Kriegstein, 2020). These studies focused on alteration and reduction of responses in subcortical sensory structures (Russo et al, 2009;.…”

“…Only a few studies investigated the neural processing of speech‐in‐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.…”

“…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).…”