GABAergic inhibition in the human visual cortex relates to eye dominance

Abstract

Our binocular world is seamlessly assembled from two retinal images that remain segregated until the cerebral cortex. Despite the coherence of this input, there is often an imbalance between the strength of these connections in the brain. ‘Eye dominance’ provides a measure of the perceptual dominance of one eye over the other. Theoretical models suggest that eye dominance is related to reciprocal inhibition between monocular units in the primary visual cortex, the first location where the binocular input is combined. As the specific inhibitory interactions in the binocular visual system critically depend on the presence of visual input, we sought to test the role of inhibition by measuring the concentrations of inhibitory (GABA) neurotransmitters during monocular visual stimulation of the dominant and the non-dominant eye. GABA-levels were acquired in V1 using a combined functional magnetic resonance imaging (fMRI) and magnetic resonance spectroscopy (MRS) sequence on a 7-Tesla MRI scanner. Individuals with stronger eye dominance had a greater difference in GABAergic inhibition between the eyes. This relationship was present only when the visual system was actively processing sensory input and was not present at rest. We provide the first evidence that imbalances in GABA levels during ongoing sensory processing are related to eye dominance in the human visual cortex. This provides strong support to the view that intracortical inhibition underlies normal eye dominance.SIGNIFICANCE STATEMENTWhat we see is shaped by excitation and inhibition in our brain. We investigated how eye dominance, the perceptual preference of one eye’s input over the other, is related to levels of inhibitory neurotransmitter GABA during monocular visual stimulation. GABAergic inhibition is related to eye dominance, but only when the visual system is actively processing sensory input. This provides key support for the view that imbalances in visual competition that are observed in the normal visual system arise from an inability of GABA signalling to suppress the stronger sensory representation.

Ocular Dominance in Open-angle Glaucoma: The Shifting Trend Depending on Stage of the Disease

“…Ganglion cells are densely located in the central retina and relatively less dense in the periphery of retina. Moreover, cones are mostly one to one connected to ganglion cells, in other words they have low convergence, in the fovea of macula in order to provide high-resolution images [27]. In this regard, the central VF corresponding to macula seem to be advantageous for assessing the effect of ocular dominance.…”

“…Moreover, macula area processed in the contralateral hemisphere was thicker in dominant eyes compared with non-dominant eyes [2]. The underlying mechanism in ocular dominance involves the imbalances in GABA levels in the human visual cortex [7]. These evidences suggest a possibility of reciprocal feedback mechanism related to ocular dominance in the visual cortex and retina.…”

Developmental hearing loss-induced perceptual deficits are rescued by cortical expression of GABABreceptors

“…There is indirect support for the premise that normal perceptual performance is associated with appropriate levels of cortical inhibition in adults. For example, magnetic resonance spectroscopy measurements in humans demonstrate that performance on visual or auditory perceptual tasks are correlated with a higher GABA concentration (Edden et al, 2009; Dobri and Ross, 2021; Ip et al, 2021). Furthermore, a pharmacological manipulation that enhances GABAergic inhibition during behavioral testing leads to improved performance on an auditory temporal perception task in senescent gerbils and improved visual coding in senescent monkeys (Gleich et al, 2003; Leventhal et al 2003).…”

Metaplasticity: Dark exposure boosts excitability and visual plasticity in adult human cortex

“…This protocol mirrors that of animal studies, which assess the susceptibility of the visual cortex to long-term MD as an index of cortical plasticity. The susceptibility in humans to short-term MD is measured as the degree of the shift in ocular dominance that is observed after MD, which favors the deprived eye and is thought to involve homeostatic plasticity that regulates the intracortical excitatory/inhibitory (E/I) balance [12]. Moreover, GABA is decreased in regions within the primary visual cortex (V1) associated with the previously deprived eye [13], suggesting a clear relationship between the perceptual gain of the deprived eye and its reduced GABAergic inhibition in pertinent areas within adult V1.…”