Both stronger and weaker cerebro-cerebellar functional connectivity patterns during processing of spoken sentences in autism spectrum disorder

• Published in: Human brain mapping 2023-12, Vol.44 (17), p.5810-5827
• Main Authors: Alho, Jussi, Samuelsson, John G, Khan, Sheraz, Mamashli, Fahimeh, Bharadwaj, Hari, Losh, Ainsley, McGuiggan, Nicole M, Graham, Steven, Nayal, Zein, Perrachione, Tyler K, Joseph, Robert M, Stoodley, Catherine J, Hämäläinen, Matti S, Kenet, Tal
• Format: Article
• Language: English
• Subjects: Auditory perception; Autism; Autism Spectrum Disorder - diagnostic imaging; Brain Mapping; Cerebellum; Cerebellum - diagnostic imaging; Child; Children; Communication; Hemispheric laterality; Humans; Intelligence tests; Language; Localization; Magnetic Resonance Imaging; Magnetoencephalography; Natural language processing; Neural networks; Questionnaires; Semantics; Sensorimotor system; Sentences; Speech; Speech processing; Windows (intervals)
• ISSN: 1065-9471; 1097-0193
• DOI: 10.1002/hbm.26478

Cerebellar differences have long been documented in autism spectrum disorder (ASD), yet the extent to which such differences might impact language processing in ASD remains unknown. To investigate this, we recorded brain activity with magnetoencephalography (MEG) while ASD and age-matched typically developing (TD) children passively processed spoken meaningful English and meaningless Jabberwocky sentences. Using a novel source localization approach that allows higher resolution MEG source localization of cerebellar activity, we found that, unlike TD children, ASD children showed no difference between evoked responses to meaningful versus meaningless sentences in right cerebellar lobule VI. ASD children also had atypically weak functional connectivity in the meaningful versus meaningless speech condition between right cerebellar lobule VI and several left-hemisphere sensorimotor and language regions in later time windows. In contrast, ASD children had atypically strong functional connectivity for in the meaningful versus meaningless speech condition between right cerebellar lobule VI and primary auditory cortical areas in an earlier time window. The atypical functional connectivity patterns in ASD correlated with ASD severity and the ability to inhibit involuntary attention. These findings align with a model where cerebro-cerebellar speech processing mechanisms in ASD are impacted by aberrant stimulus-driven attention, which could result from atypical temporal information and predictions of auditory sensory events by right cerebellar lobule VI.