Melanopsin contributions to the representation of images in the early visual system

Melanopsin photoreception enhances retinal responses to variations in ambient light (irradiance) and drives non-image forming visual reflexes such as circadian entrainment[1-6]. Melanopsin signals also reach brain regions responsible for form vision[7-9], but melanopsin’s contribution, if any, to encoding visual images remains unclear. We addressed this deficit using principles of receptor silent substitution to present images in which visibility for melanopsin vs rods+cones was independently modulated, and recorded evoked responses in the mouse dorsal lateral geniculate nucleus (dLGN; thalamic relay for cortical vision). ~20% of dLGN units responded to patterns visible only to melanopsin, revealing that melanopsin signals alone can convey spatial information. Spatial receptive fields (RFs) mapped using melanopsin-isolating stimuli had ON-centres, with diameters ~13°. Melanopsin and rod+cone responses differed in the temporal domain, and responses to slow changes in radiance (<0.9Hz) and stationary images were deficient when stimuli were rendered invisible for melanopsin. We employ these data to devise and test a mathematical model of melanopsin’s involvement in form vision and applied it, along with further experimental recordings, to explore melanopsin signals under simulated active view of natural scenes. These reveal that melanopsin enhances the thalamic representation of scenes containing local correlations in radiance, compensating for the high temporal frequency bias of cone vision and the negative correlation between magnitude and frequency for changes in direction of view. Together these data reveal a distinct melanopsin contribution to encoding visual images, predicting that, under natural view, melanopsin augments the early visual system’s ability to encode patterns over moderate spatial scales.