Gamma oscillations in primate primary visual cortex are severely attenuated by small stimulus discontinuities

Abstract

Gamma oscillations (30 to 80 Hz) have been hypothesized to play an important role in feature binding, based on the observation that continuous long bars induce stronger gamma in the visual cortex than bars with a small gap. Recently, many studies have shown that natural images, which have discontinuities in several low-level features, do not induce strong gamma oscillations, questioning their role in feature binding. However, the effect of different discontinuities on gamma has not been well studied. To address this, we recorded spikes and local field potential from 2 monkeys while they were shown gratings with discontinuities in 4 attributes: space, orientation, phase, or contrast. We found that while these discontinuities only had a modest effect on spiking activity, gamma power drastically reduced in all cases, suggesting that gamma could be a resonant phenomenon. An excitatory–inhibitory population model with stimulus-tuned recurrent inputs showed such resonant properties. Therefore, gamma could be a signature of excitation–inhibition balance, which gets disrupted due to discontinuities. Gamma oscillations (30-80 Hz) in visual cortex have been hypothesized to play an important role in feature binding, but this role has recently been questioned. This study shows that visual stimulus-induced gamma oscillations are highly attenuated with even small discontinuities in the stimulus. This "resonant" behaviour can be explained by a simple excitatory-inhibitory model in which discontinuities lead to a small reduction in lateral inputs.