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.

Aligning evidence for the genesis of visual gamma oscillations

“…Together, these data suggest that stimuli which maximally drive gamma oscillations are typically associated with lowered, and more temporally synchronous, spiking patterns. This consistent set of findings from Shirhatti and colleagues [2] provides critical support for the center-surround prediction theory of gamma genesis [5], which was also recently tested for uniform color stimuli [7] and complex images [8]. These findings prompt us to reconsider prior theories, such that visual gamma's primary function may not be that of a general mechanism for coordinating visual circuit interactions, but rather, a contextually specific mechanism for the efficient processing of redundant (i.e., predictable) feature configurations in the visual world [5].…”

“…While a highly robust phenomenon across species, debate continues as to the functional significance of these visual gamma oscillations. In this issue of PLOS Biology , Shirhatti and colleagues [ 2 ] show that even subtle tweaks in the structure of specific gamma inducing stimuli greatly reduces the amplitude of this oscillation. These findings present important challenges for theories of gamma’s functional role in visual cortex.…”

“…In their work, Shirhatti and colleagues [ 2 ] directly tested this theory by quantifying changes in visual gamma during systematic manipulation of grating center-surround continuity, in spatial, orientation, phase, and contrast domains (see Fig 1C ). To do so, they first carefully mapped RFs within V1 of awake macaque monkeys via high-density intracortical microelectrode recording arrays.…”

“…What then are the specific circuit dynamics which underlie gamma genesis? Building on a large literature, Shirhatti and colleagues [ 2 ] show that a well-known model of coupled excitatory and inhibitory neurons is able to recapitulate many of their experimental results. However, such models lack specific incorporation of visual circuit connectivity and related center-surround computations, which are essential to generating new predictions of gamma genesis under more complex multifeature conditions [ 10 ] of natural vision.…”

“…Gratings that predominately fall on the surround and not the RF center will reduce gamma amplitude below baseline levels (4; likely due to a predominance of inhibition without RF excitatory drive) [6]. (C) Grating center-surround manipulations performed by Shirhatti and colleagues (2). Even if grating stimuli fall upon both RF center and surround, small spatial ( 5), orientation (6), phase (7) or contrast (8) discontinuities between the center-surround greatly attenuate gamma amplitude (B; lower) from levels observed for contiguous gratings of the same size (3).…”