Luminance contrast shifts dominance balance between ON and OFF pathways in human vision

Human vision processes light and dark stimuli in visual scenes with separate ON and OFF neuronal pathways. In nature, stimuli lighter or darker than their local surround have different spatial properties and contrast distributions (Ratliff et al., 2010; Cooper and Norcia, 2015; Rahimi-Nasrabadi et al., 2021). Similarly, in human vision, we show that luminance contrast affects the perception of lights and darks differently. At high contrast, human subjects of both sexes locate dark stimuli faster and more accurately than light stimuli, consistently with a visual system dominated by the OFF pathway. However, at low contrast, they locate light stimuli faster and more accurately than dark stimuli, consistently with a visual system dominated by the ON pathway. Luminance contrast was strongly correlated with multiple ON/OFF dominance ratios estimated from light/dark ratios of performance errors, missed targets or reaction times. All correlations could be demonstrated at multiple eccentricities of the central visual field with an ON-OFF perimetry test implemented in a head-mounted visual display. We conclude that high contrast stimuli are processed faster and more accurately by OFF than ON pathways. However, the OFF dominance shifts towards ON dominance when stimulus contrast decreases, as expected from the higher contrast sensitivity of ON cortical pathways (Kremkow et al., 2014; Rahimi-Nasrabadi et al., 2021). The results highlight the importance of contrast polarity in visual field measurements and predict a loss of low-contrast vision in humans with ON pathway deficits, as demonstrated in animal models (Sarnaik et al., 2014).SIGNIFICANCE:ON and OFF retino-thalamo-cortical pathways respond differently to luminance contrast. In both animal models and humans, low contrasts drive stronger responses from ON pathways whereas high contrasts drive stronger responses from OFF pathways. We demonstrate that these ON-OFF pathway differences have a correlate in human vision. At low contrast, humans locate light targets faster and more accurately than dark targets but, as contrast increases, dark targets become more visible than light targets. We also demonstrate that contrast is strongly correlated with multiple light/dark ratios of visual performance in central vision. These results provide a link between neuronal physiology and human vision while emphasizing the importance of stimulus polarity in measurements of visual fields and contrast sensitivity.