MEG Gamma Oscillations and Directional Sensitivity to Visual Motion in Children with ASD: Two Sides of the Inhibition Deficit.

Background: Altered balance between excitation (E) and inhibition (I) in neural networks is thought to underlie core symptoms of ASD, including sensory processing abnormalities. In line with this hypothesis we have recently found in children with ASD a reduction of spatial suppression (SS) – a perceptual phenomenon that depends on the efficacy of inhibition in the visual cortex. If present, the E/I imbalance in ASD may affect neural gain control (i.e. the rate at which inhibition shapes neuronal firing in response to increasing excitatory input) and result in an altered pattern of intensity-related changes of gamma oscillations (30-100Hz) – the populational neural activity that is highly sensitive to the E/I ratio.

Objectives: We tested the hypothesis that the E/I imbalance is a common factor that alters both directional sensitivity to visual motion and the intensity-related changes in MEG gamma oscillations in ASD.

Methods: MEG was recorded in 43 neuro-typical (NT) boys and 36 boys with ASD aged 6-15 years. Children watched high-contrast concentric circular gratings moving at a visual angular velocity of 1.2(slow), 3.6(medium) or 6.0(fast) °/sec. To assess the neural gain control we calculated the velocity-related change in gamma response power in the 'slow' vs. 'fast' conditions – gamma suppression magnitude (gSM). Greater gSM reflects a greater reduction in the gamma power with increasing motion intensity, i.e. stronger gain control. SS has been tested in a separate psychophysical experiment wherein subjects detected the direction of motion of a small (1°) and large (12°) gratings presented for a short time. The direction discrimination deteriorates with increasing stimulus size as the result of the top-down modulated inhibition in the primary visual cortex (V1). The SS was calculated as a difference between log discrimination thresholds for the large vs. small stimuli.

Results: The power of gamma oscillations decreased with increasing visual motion. As expected, velocity-related suppression of the visual gamma response was reduced in the ASD group. The perceptual SS effect was diminished in boys with ASD mainly due to their abnormally elevated direction discrimination threshold for the small gratings. In the NT boys gSM correlated with the SS and with their discrimination threshold for the large gratings. In boys with ASD, the correlation with the SS was also present, but it was mainly due to impaired direction discrimination for the small gratings in those with low gSM.

Conclusions: The significant correlations between the neural gain regulation index and measures of motion direction sensitivity supports the hypothesis that the E/I balance is a common underlying factor for both. Our findings suggest that the normal variations in the E/I balance have a role for the top-down suppression effects associated with increasing stimulus size. In children with ASD, on the other hand, the E/I imbalance affects motion direction discrimination mainly for the small gratings suggesting impairment of the local inhibition in V1. By showing the role of E/I imbalance in abnormal directional discrimination in ASD, our findings extend the recent evidence for a broadening of the population receptive fields in V1 in ASD individuals.