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

Abstract

Cortical gamma oscillations are generated in circuits that include excitatory (E) and inhibitory (I) neurons. Prominent MEG/EEG gamma oscillations in visual cortex can be induced by static or moving high-contrast edges stimuli. In a previous study in children, we observed that increasing velocity of visual motion substantially accelerated gamma oscillations, and led to the suppression of gamma response magnitude. These velocityrelated modulations might reflect the balance between neural excitation induced by increasing excitatory drive, and efficacy of inhibition.Here, we searched for functional correlates of visual gamma modulations and assessed their development in 75 typically developing individuals aged 7-40 years. Gamma oscillations were measured with MEG in response to high-contrast annular gratings drifting at 1.2, 3.6, or 6.0°/s. In adults, we also recorded pupillary constriction as an indirect measure of excitatory drive.Pupil constriction increased with increasing velocity, thus suggesting increased excitatory drive to the cortex. Despite drastic developmental changes in gamma frequency and response strength, the magnitude of the velocity-related gamma modulations -a shift to higher frequency and amplitude suppression -remained remarkably stable. Based on the previous simulation studies, we hypothesized that gamma suppression might result from excessively strong excitatory drive caused by increasing motion velocity and reflects a tradeoff between overexcited excitatory and inhibitory circuitry. In children, the stronger gamma suppression correlated with higher IQ, suggesting importance of an optimal E/I balance for cognitive functioning.The velocity-related changes in gamma response may appear useful to assess E/I balance in the visual cortex.

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

“…In both NT and ASD subjects, the increase in velocity of the visual motion from 1.2 to 6°/s elicited a strong and reliable suppression of the visual gamma response accompanied by a substantial increase in gamma frequency for almost 15 Hz (Fig 3). These findings extend our previous results on the velocity-related changes of visual gamma response in NT subjects (Orekhova et al, 2015; Orekhova et al, 2018) and children with ASD (Stroganova et al, 2015) by replicating these findings in a group of adult ASD individuals.…”

“…Increasing motion velocity of full-contrast visual gratings up to 6.0°/s likely promotes excitation of interconnected excitatory and inhibitory neurons in the visual cortical areas (see (Orekhova et al, 2018) for discussion). According to the computational modeling results of Borgers and colleagues, increasing excitation of the l-neurons above some critical threshold leads to neuronal de-synchronization and thus suppression of gamma oscillations (Borgers and Kopell, 2005; Borgers and Walker, 2013; Cannon et al, 2014).…”

“…In a previous study we put forward the idea that it is possible to estimate efficiency of the E/I balance regulation in the visual cortex through probing input-output gain in the strength of the visual gamma oscillations recorded by MEG (Orekhova et al, 2018). Response gain control is a basic property of neural networks that works to both amplify the neuronal responses to weak sensory signals and to saturate/suppress these responses under conditions of excessive input (e.g.…”

“…(Peirce, 2007)). The strength of visually induced gamma oscillations is controlled in accord with this mechanism, in both animals (Jia et al, 2011; Jia et al, 2013; Roberts et al, 2013; Salelkar et al, 2018) and humans (Orekhova et al, 2018), wherein a gradual increase in excitatory drive elicits an increase in gamma power up to a certain ′transition′ point, and a stimulation intensity past that point leads to suppression of the gamma response.…”

“…In regard to humans, these considerations imply that the brain of individuals exhibiting weaker suppression of the visual MEG gamma response is characterized by less efficient inhibitory-based capacity to down-regulate the rising excitation, i.e. by an E/I ratio shifted towards excitation (see (Orekhova et al, 2018) for discussion).…”