Cholinergic Modulation of Binocular Vision

J Neurosci. 2020 Jul 1;40(27):5208-5213. doi: 10.1523/JNEUROSCI.2484-19.2020. Epub 2020 May 26.

Abstract

The endogenous neurotransmitter acetylcholine (ACh) is known to affect the excitatory/inhibitory (E/I) balance of primate visual cortex, enhancing feedforward thalamocortical gain while suppressing corticocortical synapses. Recent advances in the study of the human visual system suggest that ACh is a likely component underlying interocular interactions. However, our understanding of its precise role in binocular processes is currently lacking. Here we use binocular rivalry as a probe of interocular dynamics to determine ACh's effects, via the acetylcholinesterase inhibitor (AChEI) donepezil, on the binocular visual system. A total of 23 subjects (13 male) completed two crossover experimental sessions where binocular rivalry measurements were obtained before and after taking either donepezil (5 mg) or a placebo (lactose) pill. We report that enhanced cholinergic potentiation attenuates perceptual suppression during binocular rivalry, reducing the overall rate of interocular competition while enhancing the visibility of superimposition mixed percepts. Considering recent evidence that perceptual suppression during binocular rivalry is causally modulated by the inhibitory neurotransmitter GABA, our results suggest that cholinergic activity counteracts the effect of GABA with regards to interocular dynamics and may modulate the inhibitory drive within the visual cortex.SIGNIFICANCE STATEMENT Our research demonstrates that the cholinergic system is implicated in modulating binocular interactions in the human visual cortex. Potentiating the transmission of acetylcholine (ACh) via the cholinergic drug donepezil reduces the extent to which the eyes compete for perceptual dominance when presented two separate, incongruent images.

Keywords: acetylcholinesterase inhibitors; binocular rivalry; binocular vision; cholinergic modulation; excitatory/inhibitory balance; visual cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Adult
  • Cholinergic Agents / pharmacology
  • Cholinesterase Inhibitors / pharmacology
  • Cross-Over Studies
  • Donepezil / pharmacology
  • Female
  • Functional Laterality / drug effects
  • Humans
  • Male
  • Parasympathetic Nervous System / drug effects
  • Parasympathetic Nervous System / physiology*
  • Photic Stimulation
  • Psychomotor Performance / drug effects
  • Vision Disparity
  • Vision, Binocular / drug effects
  • Vision, Binocular / physiology*
  • Young Adult
  • gamma-Aminobutyric Acid / physiology

Substances

  • Cholinergic Agents
  • Cholinesterase Inhibitors
  • gamma-Aminobutyric Acid
  • Donepezil
  • Acetylcholine