MEG Theta during Lexico-Semantic and Executive Processing Is Altered in High-Functioning Adolescents with Autism

Abstract

Neuroimaging studies have revealed atypical activation during language and executive tasks in individuals with autism spectrum disorders (ASD). However, the spatiotemporal stages of processing associated with these dysfunctions remain poorly understood. Using an anatomically constrained magnetoencephalography approach, we examined event-related theta oscillations during a double-duty lexical decision task that combined demands on lexico-semantic processing and executive functions. Relative to typically developing peers, high-functioning adolescents with ASD had lower performance accuracy on trials engaging selective semantic retrieval and cognitive control. They showed an early overall theta increase in the left fusiform cortex followed by greater activity in the left-lateralized temporal (starting at ~250 ms) and frontal cortical areas (after ~450 ms) known to contribute to language processing. During response preparation and execution, the ASD group exhibited elevated theta in the anterior cingulate cortex, indicative of greater engagement of cognitive control. Simultaneously increased activity in the ipsilateral motor cortex may reflect a less lateralized and suboptimally organized motor circuitry. Spanning early sensory-specific and late response selection stages, the higher event-related theta responsivity in ASD may indicate compensatory recruitment to offset inefficient lexico-semantic retrieval under cognitively demanding conditions. Together, these findings provide further support for atypical language and executive functions in high-functioning ASD.

fMRI BOLD and MEG theta power reflect complementary aspects of activity during lexicosemantic decision in adolescents with ASD

“…Presence of comorbidities and use of psychotropic medications were not considered exclusionary as they are common in adolescents with ASD and their exclusion would have rendered the sample less representative of the broader ASD population ( Gurney et al, 2006 ). There was some overlap between this study and You et al (2020) . Fourteen ASD and 16 TD participants were included in both You et al (2020) and the current study.…”

“…There was some overlap between this study and You et al (2020) . Fourteen ASD and 16 TD participants were included in both You et al (2020) and the current study. Five ASD and 4 TD participants were included in You et al (2020) , but not in the current study.…”

“…Research using MEG to examine theta power in ASD has been minimal. In one of the few MEG studies on lexicosemantic processing in ASD, members of our group recently reported atypically increased event-related theta power in adolescents with ASD in multiple fronto-temporal brain regions ( You et al, 2020 ). This appears to be in partial contrast to BOLD fMRI findings of atypically reduced frontal activity in ASD ( Gaffrey et al, 2007 ; Harris et al, 2006 ; Just et al, 2004 ; Knaus et al, 2017 ), which raises the question whether MEG and fMRI, when implemented in isolation (as has been standard practice), can provide comprehensive assays of neurofunctional differences between ASD and TD samples.…”

“…Following up on our unimodal (anatomically-constrained MEG [aMEG]) report ( You et al, 2020 ), the current study, which included an expanded, but partially overlapping sample, investigated the relation between BOLD signal and event-related theta power during lexicosemantic decision in two sets of regions that were (1) reported to show aMEG activity by You et al (2020) , and (2) identified based on increases in task-driven fMRI BOLD signal.…”

Brain Waves Reflect Cognition-Emotion State as a Diagnostic Tool for Intervention in Dysfunctional States: A Real-World Evidence

“…An increase in theta activity in the prefrontal cortex related to emotional experience has been associated with orbitofrontal cortex activation [40]. The higher theta responsivity in autistic spectrum disorder may indicate compensatory activity to a cognitively demanding condition as a stressor [41]. Delta (0-4 Hz) and theta (4-8 Hz) rhythms are associated with hypoactive cortical states, in contrast to alpha (8-12 Hz) which is associated with cortical activated states.…”