Atypical excitation-inhibition balance in autism captured by the gamma response to contextual modulation

Abstract

Atypical visual perception in people with autism spectrum disorders (ASD) is hypothesized to stem from an imbalance in excitatory and inhibitory processes in the brain. We used neuronal oscillations in the gamma frequency range (30-90 Hz), which emerge from a balanced interaction of excitation and inhibition in the brain, to assess contextual modulation processes in early visual perception. Electroencephalography was recorded in 12 high-functioning adults with ASD and 12 age- and IQ-matched control participants. Oscillations in the gamma frequency range were analyzed in response to stimuli consisting of small line-like elements. Orientation-specific contextual modulation was manipulated by parametrically increasing the amount of homogeneously oriented elements in the stimuli. The stimuli elicited a strong steady-state gamma response around the refresh-rate of 60 Hz, which was larger for controls than for participants with ASD. The amount of orientation homogeneity (contextual modulation) influenced the gamma response in control subjects, while for subjects with ASD this was not the case. The atypical steady-state gamma response to contextual modulation in subjects with ASD may capture the link between an imbalance in excitatory and inhibitory neuronal processing and atypical visual processing in ASD.

Keywords: Asperger's disorder; EEG; GABA; Gamma oscillations; Surround suppression; Visual perception.

Fig. 1

Inhomogeneous (IH-25), intermediate (inter-62), and homogeneous (H-100) example stimuli.

Fig. 2

Normalized gamma power elicited by the experimental stimuli (all conditions combined) compared to an absolute baseline of 300–100 ms before stimulus onset, for controls (left) and subjects with autism spectrum disorders (ASD, right). Color codes represent z-values. Top: time–frequency representation averaged over six parieto-occipital electrodes (PO3, O1, Oz, POz, PO4, O2, shown with ‘x’ in lower panel). Bottom: topography of the effect of stimulus presentation, at 58–62 Hz, 100–800 ms after stimulus onset. Starred electrodes showed a larger effect in control subjects compared to subjects with ASD (p = .023, corrected for multiple comparisons with cluster randomization routine).

Fig. 3

Time–frequency representation for the three different contextual-modulation conditions (inhomogeneous IH-25, intermediate inter-62, and homogeneous H-100) for control subjects (top) and subjects with autism spectrum disorders (ASD, bottom). Gamma power is compared to an absolute baseline of 300–100 ms before stimulus onset, and averaged over six parieto-occipital electrodes (PO3, O1, Oz, POz, PO4, O2, shown with ‘x’ in Fig. 2). Color codes represent z-values. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Normalized power difference for inter-62 compared to IH-25 conditions for controls (upper panel) and subjects with autism spectrum disorders (ASD, lower panel). Color codes represent z-values. Left: topography of the effect at 58–62 Hz, 250–650 ms after stimulus onset. Electrodes showing a significant effect in control subjects are marked with * (p < .05 corrected for multiple comparisons with cluster randomization routine). Right: time–frequency representation of the effect averaged over electrodes showing a group difference (marked with + in left panel). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)