Input-dependent modulation of MEG gamma oscillations reflects gain control in the visual cortex

Abstract

Gamma-band oscillations arise from the interplay between neural excitation (E) and inhibition (I) and may provide a non-invasive window into the state of cortical circuitry. A bell-shaped modulation of gamma response power by increasing the intensity of sensory input was observed in animals and is thought to reflect neural gain control. Here we sought to find a similar input-output relationship in humans with MEG via modulating the intensity of a visual stimulation by changing the velocity/temporal-frequency of visual motion. In the first experiment, adult participants observed static and moving gratings. The frequency of the MEG gamma response monotonically increased with motion velocity whereas power followed a bell-shape. In the second experiment, on a large group of children and adults, we found that despite drastic developmental changes in frequency and power of gamma oscillations, the relative suppression at high motion velocities was scaled to the same range of values across the life-span. In light of animal and modeling studies, the modulation of gamma power and frequency at high stimulation intensities characterizes the capacity of inhibitory neurons to counterbalance increasing excitation in visual networks. Gamma suppression may thus provide a non-invasive measure of inhibitory-based gain control in the healthy and diseased brain.

Additive effect of contrast and velocity proves the role of strong excitatory drive in suppression of visual gamma response

“…Also in accordance with our previous results—and those of others— (Muthukumaraswamy and Singh, 2013; Orekhova et al, 2015; Orekhova et al, 2018b; Swettenham et al, 2009; van Pelt et al, 2018), we found that the peak frequency of the MEG GR prominently increased (17 Hz on average for the 100% contrast) with increasing motion velocity from 0 to 6 °/s, which corresponds to 0 - 10 Hz of temporal frequency in our study (Fig 4A). No saturation effect has been observed for the gamma frequency even at the highest speeds of stimulation.…”

“…The same changes in the stimulation properties that induce a linear increase in gamma frequency lead to nonlinear --- often bell-shaped --- changes in gamma power in monkey LFP (Hadjipapas et al, 2015; Jia et al, 2011; Jia et al, 2013; Lowet et al, 2015; Salelkar et al, 2018). In a recent MEG study (Orekhova et al, 2018b), we applied high-contrast gratings drifting at different rates (motion velocities) and found the same bell-shaped changes in the gamma response power as those described in the LFP studies on monkeys. The majority of our healthy subjects increased visual GR power from the static to the slowly moving (1.2°/s) stimulus and then suppressed the response at higher velocities of 3.6 °/s and 6.0 °/s.…”

“…Specifically, the transition to suppression of the gamma response at a relatively higher level of excitatory drive and/or the shallower slope of this suppression would reflect less effective inhibition. In indirect support of this assumption, we have recently described a lack of velocity-related gamma suppression in a subject with epilepsy and occipital spikes (Orekhova et al, 2018b), who might have an elevated E-I ratio in the visual cortex. The causal link between the E-I ratio and the gamma suppression transition point could, in the future, be proved directly using pharmacological or other (e.g.…”

“…In order to investigate if the power and frequency of GR measured in one experimental condition predicts the subject’s rank position in another experimental condition, we calculated two types of correlations: 1) between contrasts for the respective velocity conditions and 2) between velocities, separately for each of the contrasts. Since frequency, but not power, of the visual gamma oscillations is strongly affected by age in adults (Gaetz et al, 2012; Orekhova et al, 2018b), we calculated partial correlations taking age as a nuisance variable with frequency.…”

“…Interestingly, the intensity of visual stimulation has a different impact on the frequency and power of induced gamma oscillations in both monkeys and humans. The frequency of gamma oscillations nearly linearly increases with increasing visual input strength (Hadjipapas et al, 2015; Jia et al, 2013; Murty et al, 2018; Orekhova et al, 2015; Perry et al, 2015; Ray and Maunsell, 2010; van Pelt et al, 2018) while gamma power undergoes nonlinear changes (Jia et al, 2013; Orekhova et al, 2018b; Salelkar et al, 2018).…”