Altered Gamma Oscillations during Motor Control in Children with Autism Spectrum Disorder

Abstract

Autism is hypothesized to result in a cortical excitatory and inhibitory imbalance driven by inhibitory interneuron dysfunction, which is associated with the generation of gamma oscillations. On the other hand, impaired motor control has been widely reported in autism. However, no study has focused on the gamma oscillations during motor control in autism. In the present study, we investigated the motor-related gamma oscillations in autism using magnetoencephalography. Magnetoencephalographic signals were recorded from 14 right-handed human children with autism (5 female), aged 5–7 years, and age- and IQ-matched 15 typically developing children during a motor task using their right index finger. Consistent with previous studies, the autism group showed a significantly longer button response time and reduced amplitude of motor-evoked magnetic fields. We observed that the autism group exhibited a low peak frequency of motor-related gamma oscillations from the contralateral primary motor cortex, and these were associated with the severity of autism symptoms. The autism group showed a reduced power of motor-related gamma oscillations in the bilateral primary motor cortex. A linear discriminant analysis using the button response time and gamma oscillations showed a high classification performance (86.2% accuracy). The alterations of the gamma oscillations in autism might reflect the cortical excitatory and inhibitory imbalance. Our findings provide an important clue into the behavioral and neurophysiological alterations in autism and a potential biomarker for autism.SIGNIFICANCE STATEMENT Currently, the diagnosis of autism has been based on behavioral assessments, and a crucial issue in the diagnosis of autism is to identify objective and quantifiable clinical biomarkers. A key hypothesis of the neurophysiology of autism is an excitatory and inhibitory imbalance in the brain, which is associated with the generation of gamma oscillations. On the other hand, motor deficits have also been widely reported in autism. This is the first study to demonstrate low motor performance and altered motor-related gamma oscillations in autism, reflecting a brain excitatory and inhibitory imbalance. Using these behavioral and neurophysiological parameters, we classified autism and control group with good accuracy. This work provides important information on behavioral and neurophysiological alterations in patients with autism.

Brain Oscillatory Coupling during Motor Control as a Potential Biomarker for Autism Spectrum Disorders: a comparative study

“…We con rmed that motor-related gamma oscillations were reduced in ASD, consistent with our previous ndings (20). The power of gamma oscillations is reported to be increased immediately after movement onset in adults (13,15) and children (34,35).…”

“…In addition, the power of beta oscillations begins to decrease prior to movement onset and is maintained during movement execution, and these pre-movement beta decreases are thought to be related to motor planning and movement preparation (16)(17)(18)(19). In our previous study, we found that motor-related gamma oscillations were altered in children with ASD, suggesting a potential biomarker for ASD using gamma oscillatory changes as a neurophysiological index and button response time as a behavioral index (20).…”

“…To investigate motor-related oscillatory changes and oscillatory coupling, we used a video-game-like motor task developed in our previous study (20). The experimental paradigm for the video-game-like motor task is shown in Fig.…”

“…MEG signals were digitized at 2000 Hz and low-pass ltered at 200 Hz. MEG recording conditions were similar to those detailed in our previous studies (20). Prior to the experiment, we explained the experimental paradigm and procedures to participants and their parents.…”

“…Brain oscillations are rhythmic patterns of neural activity, and motor control modulates typical brain oscillations, particularly in the beta (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) and gamma frequency bands (60-90 Hz). Gamma oscillations are known to increase immediately after movement onset, and these motor-related gamma oscillations are thought to be associated with motor execution and initiation (13)(14)(15)(16).…”