Abnormal MEG Gamma Oscillations Induced By Visual Motion in Children with ASD

Background:   A large body of evidence suggests that alternation of the balance between neural excitation and inhibition (E/I balance) in direction of excitation is an important factor leading to development of autism spectrum disorders (ASD).  When present in visual cortex, the altered E/I balance may account for visual perceptual abnormalities frequently reported in ASD. The high-frequency (gamma) oscillations are crucially dependent on functioning of fast-spiking, parvalbumin-positive GABAergic inhibitory interneurons and may appear valuable correlates of the altered E/I balance.  The frequency of the visual gamma oscillations reflects kinetics of inhibitory processes in neural networks and according to the animal studies is modulated by properties of visual stimulation, e.g. by velocity of visual motion. The velocity-related changes in gamma frequency may provide valuable information about inhibitory processes in visual cortex in children with ASD.

Objectives:   We aimed to study whether the modulation of gamma oscillations frequency by velocity of visual motion is altered in children with ASD as compared to the typically developing control children. We also investigated whether such alternations, if present, are related to performance of a visual orientation discrimination task that is particularly sensitive to neural inhibitory function.

Methods:   We studied 27 boys with ASD (IQ>60) aged 8-15 years and 27 age-matched typically developing (TD) boys using whole head Magnetoencephalography (MEG). Participants watched high-contrast annual gratings moving with different speeds while performing a simple detection task.   The gamma individual peak frequency (IPF) was identified for each participant and for each stimulus velocity at the occipital MEG sensor with the greatest gamma response amplitude. After the MEG session the oblique grating orientation discrimination threshold has been measured in 13 ASD and 18 TD participants in a psychophysical experiment.

Results:   Gamma frequency significantly increased with stimulus velocity in both TD and ASD participants. The difference in gamma IPF between the fastest and slowest stimulus velocity (i.e. gamma dynamic range) was significantly smaller in the ASD then in the TD group, suggesting impaired velocity-related modulation of inhibitory processes in visual cortical areas.  Both the gamma IPF to the fast moving stimuli and the gamma dynamic range correlated positively with IQ, but did not correlate with the autism quotient. In the ASD, but not in the TD children the broader dynamic range of gamma frequency predicted better capacity for discrimination of oblique grating orientation. 

Conclusions:   The narrow dynamic range of  gamma oscillations frequency in children with ASD suggests abnormally slow kinetics of neural inhibition in visual cortex under high functional load.  This physiological abnormality may affect basic visual processes in children with ASD.