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J Neurosci. 2019 Aug 26. pii: 0836-19. doi: 10.1523/JNEUROSCI.0836-19.2019. [Epub ahead of print]

GABAergic inhibition gates perceptual awareness during binocular rivalry.

Author information

1
Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755, USA.
2
McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
3
School of Medicine, Johns Hopkins University, Baltimore, MD, 21205.
4
Clinical Research Center, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
5
Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755, USA caroline.e.robertson@dartmouth.edu.

Abstract

Binocular rivalry is a classic experimental tool to probe the neural machinery of perceptual awareness. During rivalry, perception alternates between the two eyes, and the ebb and flow of perception is modeled to rely on the strength of inhibitory interactions between competitive neuronal populations in visual cortex. As a result, rivalry has been suggested as a non-invasive perceptual marker of inhibitory signaling in visual cortex, and its putative disturbance in psychiatric conditions, including autism. Yet, direct evidence causally implicating inhibitory signaling in the dynamics of binocular rivalry is currently lacking. We previously found that people with higher GABA levels in visual cortex, measured using magnetic resonance spectroscopy, have stronger perceptual suppression during rivalry. Here, we present direct causal tests of the impact of GABAergic inhibition on rivalry dynamics, and the contribution of specific GABA receptors to these dynamics. In a crossover pharmacological design with male and female adult participants, we found that drugs that affect the two dominant GABA receptor types in the brain - GABAA (clobazam) and GABAB (arbaclofen) - increase perceptual suppression during rivalry relative to a placebo. Crucially, these results could not be explained by changes in reaction times or response criteria, as determined through rivalry simulation trials, suggesting a direct and specific influence of GABA on perceptual suppression. A full replication study of the GABAB modulator reinforces these findings. These results provide causal evidence for a link between the strength of inhibition in the brain and perceptual suppression during rivalry and have implications for psychiatric conditions including autism.SIGNIFICANCE STATEMENTHow does the brain accomplish perceptual gating? Here we use a direct and causal pharmacological manipulation to present insight into the neural machinery of a classic illusion of perceptual awareness: binocular rivalry. We show that drugs that increase GABAergic inhibition in the brain - clobazam (GABAA modulator) and arbaclofen (GABAB modulator) - increase perceptual suppression during rivalry relative to a placebo. These results present the first causal link between GABAergic inhibition and binocular rivalry in humans, complementing classic models of binocular rivalry, and have implications for our understanding of psychiatric conditions such as autism where binocular rivalry is posited as a behavioral marker of disruptions in inhibitory signaling in the brain.

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