Overt social interaction and resting state in young adult males with autism: core and contextual neural features

• Published in: Brain (London, England : 1878) Vol. 142; no. 3; pp. 808 - 822
• Main Authors: Jasmin, Kyle, Gotts, Stephen J, Xu, Yisheng, Liu, Siyuan, Riddell, Cameron D, Ingeholm, John E, Kenworthy, Lauren, Wallace, Gregory L, Braun, Allen R, Martin, Alex
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 01.03.2019
• Subjects: Adolescent; Adult; Autism Spectrum Disorder - physiopathology; Autistic Disorder - physiopathology; Brain - physiopathology; Brain Mapping - methods; Communication; Humans; Interpersonal Relations; Magnetic Resonance Imaging - methods; Male; Neural Pathways - physiopathology; Original; Prefrontal Cortex - physiopathology; Rest; Social Behavior; Social Skills; Verbal Behavior - physiology; Young Adult; fMRI; resting state; language; autism; conversation
• ISSN: 0006-8950; 1460-2156; 1460-2156
• DOI: 10.1093/brain/awz003

Autism is diagnosed via face-to-face spoken interactions. Using a novel face-to-face fMRI paradigm, Jasmin et al. report that cortical functional connectivity is heightened in social brain areas of men with autism during face-to-face conversations but not in the resting state, while subcortical-cortical connectivity is heightened in interaction and resting states. Abstract Conversation is an important and ubiquitous social behaviour. Individuals with autism spectrum disorder (autism) without intellectual disability often have normal structural language abilities but deficits in social aspects of communication like pragmatics, prosody, and eye contact. Previous studies of resting state activity suggest that intrinsic connections among neural circuits involved with social processing are disrupted in autism, but to date no neuroimaging study has examined neural activity during the most commonplace yet challenging social task: spontaneous conversation. Here we used functional MRI to scan autistic males (n = 19) without intellectual disability and age- and IQ-matched typically developing control subjects (n = 20) while they engaged in a total of 193 face-to-face interactions. Participants completed two kinds of tasks: conversation, which had high social demand, and repetition, which had low social demand. Autistic individuals showed abnormally increased task-driven interregional temporal correlation relative to controls, especially among social processing regions and during high social demand. Furthermore, these increased correlations were associated with parent ratings of participants' social impairments. These results were then compared with previously-acquired resting state data (56 autism, 62 control subjects). While some interregional correlation levels varied by task or rest context, others were strikingly similar across both task and rest, namely increased correlation among the thalamus, dorsal and ventral striatum, somatomotor, temporal and prefrontal cortex in the autistic individuals, relative to the control groups. These results suggest a basic distinction. Autistic cortico-cortical interactions vary by context, tending to increase relative to controls during task and decrease during test. In contrast, striato- and thalamocortical relationships with socially engaged brain regions are increased in both task and rest, and may be core to the condition of autism.