Artists and astronomers noticed centuries ago that humans perceive dark features in an image differently from light ones; however, the neuronal mechanisms underlying these dark/light asymmetries remained unknown. Based on computational modeling of neuronal responses, we have previously proposed that such perceptual dark/light asymmetries originate from a luminance/response saturation within the ON retinal pathway. Consistent with this prediction, here we show that stimulus conditions that increase ON luminance/response saturation (e.g., dark backgrounds) or its effect on light stimuli (e.g., optical blur) impair the perceptual discrimination and salience of light targets more than dark targets in human vision. We also show that, in cat visual cortex, the magnitude of the ON luminance/response saturation remains relatively constant under a wide range of luminance conditions that are common indoors, and only shifts away from the lowest luminance contrasts under low mesopic light. Finally, we show that the ON luminance/response saturation affects visual salience mostly when the high spatial frequencies of the image are reduced by poor illumination or optical blur. Because both low luminance and optical blur are risk factors in myopia, our results suggest a possible neuronal mechanism linking myopia progression with the function of the ON visual pathway.

SUMMARY Accurate measures of contrast sensitivity are important for evaluating visual disease progression and for navigation safety. Previous measures suggested that cortical contrast sensitivity was constant across widely different luminance ranges experienced indoors and outdoors. Against this notion, here, we show that luminance range changes contrast sensitivity in both cat and human cortex, and the changes are different for dark and light stimuli. As luminance range increases, contrast sensitivity increases more within cortical pathways signaling lights than those signaling darks. Conversely, when the luminance range is constant, light-dark differences in contrast sensitivity remain relatively constant even if background luminance changes. We show that a Naka-Rushton function modified to include luminance range and light-dark polarity accurately replicates both the statistics of light-dark features in natural scenes and the cortical responses to multiple combinations of contrast and luminance. We conclude that differences in light-dark contrast increase with luminance range and are largest in bright environments.

Graphical AbstractHighlights d Small fast stimuli drive stronger OFF than ON cortical responses.d Large long-lasting stimuli suppress more OFF than ON cortical responses.d ON/OFF spatiotemporal asymmetries are preserved across a wide luminance range.d ON and OFF cortical pathways are specialized in global-slow and local-fast vision. SUMMARYVisual information is processed in the cortex by ON and OFF pathways that respond to light and dark stimuli. Responses to darks are stronger, faster, and driven by a larger number of cortical neurons than responses to lights. Here, we demonstrate that these light-dark cortical asymmetries reflect a functional specialization of ON and OFF pathways for different stimulus properties. We show that large long-lasting stimuli drive stronger cortical responses when they are light, whereas small fast stimuli drive stronger cortical responses when they are dark. Moreover, we show that these light-dark asymmetries are preserved under a wide variety of luminance conditions that range from photopic to low mesopic light. Our results suggest that ON and OFF pathways extract different spatiotemporal information from visual scenes, making OFF local-fast signals better suited to maximize visual acuity and ON globalslow signals better suited to guide the eye movements needed for retinal image stabilization.