Differential cortical and subcortical visual processing with eyes shut

Abstract

AbstractClosing our eyes largely shuts down our ability to see. That said, our eyelids still pass some light, allowing our visual system to coarsely process information about visual scenes, such as changes in luminance. However, the specific impact of eye closure on processing within the early visual system remains largely unknown. To understand how visual processing is modulated when eyes are shut, we used functional magnetic resonance imaging (fMRI) to measure responses to a flickering visual stimulus at high (100%) and low (10%) temporal contrasts, while participants viewed the stimuli with their eyes open or closed. Interestingly, we discovered that eye closure produced a qualitatively distinct pattern of effects across the visual thalamus and visual cortex. We found that with eyes open, low temporal contrast stimuli produced smaller responses, across the lateral geniculate nucleus (LGN), primary (V1) and extrastriate visual cortex (V2). However, with eyes closed, we discovered that the LGN and V1 maintained similar BOLD responses as the eyes open condition, despite the suppressed visual input through the eyelid. In contrast, V2 and V3 had strongly attenuated BOLD response when eyes were closed, regardless of temporal contrast. Our findings reveal a qualitative distinct pattern of visual processing when the eyes are closed – one that is not simply an overall attenuation, but rather reflects distinct responses across visual thalamocortical networks, wherein the earliest stages of processing preserves information about stimuli but is then gated off downstream in visual cortex.Significance statementWhen we close our eyes, not all information is blocked out. Coarse luminance information is still accessible for processing by the visual system, even when our eyes are closed. Using functional magnetic resonance imaging (fMRI), we examined whether eyelid closure plays a unique role in visual processing. We discovered that while the thalamus and primary visual cortex (V1) show equivalent luminance-dependent responses both when the eyes are open and closed, extrastriate cortex exhibited a qualitatively distinct pattern of responses. Specifically, eye closure attenuated luminance responses in extrastriate cortices, but responses were preserved in LGN and V1. This pattern suggests that during brain states where the eyes are closed, visual information is still accessible to the very earliest stages of visual processing, but that downstream visual processing areas appear to become blind to this information.