Neural gain control measured through cortical gamma oscillations is associated with sensory sensitivity

Abstract

Gamma oscillations facilitate information processing by shaping the excitatory input/output of neuronal populations. Recent studies in humans and nonhuman primates have shown that strong excitatory drive to the visual cortex leads to suppression of induced gamma oscillations, which may reflect inhibitory-based gain control of network excitation. The efficiency of the gain control measured through gamma oscillations may in turn affect sensory sensitivity in everyday life. To test this prediction, we assessed the link between self-reported sensitivity and changes in magneto-encephalographic gamma oscillations as a function of motion velocity of high-contrast visual gratings. The induced gamma oscillations increased in frequency and decreased in power with increasing stimulation intensity. As expected, weaker suppression of the gamma response correlated with sensory hypersensitivity. Robustness of this result was confirmed by its replication in the two samples: neurotypical subjects and people with autism, who had generally elevated sensory sensitivity. We conclude that intensity-related suppression of gamma response is a promising biomarker of homeostatic control of the excitation-inhibition balance in the visual cortex.

Keywords: autism spectrum disorders; gamma oscillations; magneto-encephalography; response gain control; sensory sensitivity; visual motion.

Conflict of interest statement

The authors declare that they have no conflicts of interest.

© 2018 Wiley Periodicals, Inc.

Figures

Figure 1

Experimental design. Each trial began with presentation of a fixation cross that was followed by an annular grating drifting inward for 1.2–3 s at one of the three velocities: 1.2, 3.6, 6.0°/s. Hereafter, we referred to these velocities as “slow,” “medium,” and “fast.” Arrows indicate direction of the motion. Participants responded to the termination of motion with a button press. Short (3–6 s) animated cartoon characters were presented randomly between every 2–5 stimuli to sustain vigilance and reduce visual fatigue [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Gamma suppression slope (GSS). The left panel shows spectra of gamma power ratios: (stimulus–baseline)/baseline for two subjects. The right panel demonstrates corresponding GSSs. Subject a shows a strong suppression of gamma response power with increasing motion velocity reflected in strongly negative slope of the regression line. Subject b has a less prominent gamma suppression corresponding to less negative GSS value [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Grand average source localization of the visual gamma responses in ASD and NT individuals. Here and hereafter the magnitude of the gamma response was calculated as the ratio: (stimulus − baseline)/baseline. In both groups and under all the three velocity conditions the gamma power ratio was maximal in the calcarine sulcus (marked with a blue crosshair) [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Magnitude (a) and peak frequency (b) of gamma responses to moving gratings in NT and ASD individuals. Parameters of the gamma response were measured in its focus in the visual cortex (see Materials and Methods for details). Vertical bars denote 0.95 confidence intervals [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

The relationship between gamma suppression slope and sensory sensitivity (a), visual low threshold (b), and visual motion sensitivity (c) in the combined sample of ASD (read squares) and NT (blue circles) individuals [Color figure can be viewed at http://wileyonlinelibrary.com]