Melanopsin Contributions to the Representation of Images in the Early Visual System

• Published in: Current biology Vol. 27; no. 11; pp. 1623 - 1632.e4
• Main Authors: Allen, Annette E., Storchi, Riccardo, Martial, Franck P., Bedford, Robert A., Lucas, Robert J.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 05-06-2017; Cell Press
• Subjects: Animals; Brain Mapping; dorsal lateral geniculate nucleus; Geniculate Bodies - physiology; intrinsically photosensitive retinal ganglion cells; Male; melanopsin; metameric light stimuli; Mice; Mice, Inbred C57BL; Mice, Knockout; Models, Animal; Models, Biological; mouse vision; Photic Stimulation; receptive fields; receptor silent substitution; Retina - cytology; Retina - physiology; Retinal Cone Photoreceptor Cells - physiology; Retinal Rod Photoreceptor Cells - physiology; Rod Opsins - genetics; Rod Opsins - metabolism; Rod Opsins - physiology; Software; spatial vision; Vision, Ocular - physiology; Visual Cortex - physiology; melanopsin; intrinsically photosensitive retinal ganglion cells; mouse vision; dorsal lateral geniculate nucleus; metameric light stimuli; spatial vision; receptor silent substitution; receptive fields
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.04.046

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 versus rods+cones was independently modulated, and we recorded evoked responses in the mouse dorsal lateral geniculate nucleus (dLGN; thalamic relay for cortical vision). Approximately 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 centers with diameters ∼13°. Melanopsin and rod+cone responses differed in the temporal domain, and responses to slow changes in radiance (<0.9 Hz) and stationary images were deficient when stimuli were rendered invisible for melanopsin. We employed 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. Our findings 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.
•A five-primary display is used to define melanopsin’s contribution to form vision•Melanopsin extends the spatiotemporal range of the mouse early visual system•The representation of spatial patterns is deficient when melanopsin is not engaged•A linear model predicting melanopsin’s contribution to pattern vision is defined
Allen et al. probe the origins of form vision and show that the inner retinal photoreceptor, melanopsin, extends its spatiotemporal range. Melanopsin augments the representation of patterns whose spatial scale is larger than that of ongoing changes in direction of view.