Luminance Information Is Required for the Accurate Estimation of Contrast in Rapidly Changing Visual Contexts

Visual perception scales with changes in the visual stimulus, or contrast, irrespective of background illumination. However, visual perception is challenged when adaptation is not fast enough to deal with sudden declines in overall illumination, for example, when gaze follows a moving object from bright sunlight into a shaded area. Here, we show that the visual system of the fly employs a solution by propagating a corrective luminance-sensitive signal. We use in vivo 2-photon imaging and behavioral analyses to demonstrate that distinct OFF-pathway inputs encode contrast and luminance. Predictions of contrast-sensitive neuronal responses show that contrast information alone cannot explain behavioral responses in sudden dim light. The luminance-sensitive pathway via the L3 neuron is required for visual processing in such rapidly changing light conditions, ensuring contrast constancy when pure contrast sensitivity underestimates a stimulus. Thus, retaining a peripheral feature, luminance, in visual processing is required for robust behavioral responses. [Display omitted] •Lamina neurons underestimate contrast when light levels suddenly decline•Distinct visual pathways postsynaptic to photoreceptors encode contrast and luminance•The luminance-sensitive pathway via L3 is necessary for behavior in sudden dim light•L3 scales behavioral responses in contextual dim light across adaptation states Ketkar and Sporar et al. reveal a novel mechanism in which visual systems can mediate accurate behavioral responses to visual cues under changing light conditions. Luminance information is preserved in a distinct pathway past photoreceptors. This pathway is required for visual behavior when pure contrast-sensitivity underestimates a visual stimulus.