Abstract
SummaryMelanopsin photoreception enhances retinal responses to variations in ambient light (irradiance) and drives non-image-forming visual reflexes such as circadian entrainment [1, 2, 3, 4, 5, 6]. Melanopsin signals also reach brain regions responsible for form vision [7, 8, 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.
Highlights
As our first question was whether melanopsin was able to encode patterns, we used the light engine to produce a pair of spectra of equivalent effective intensity for rod and cone opsins but differing for melanopsin ($52% Michelson contrast)
In generating visual images that provide spatiotemporal contrast to rods and cones versus melanopsin, we have shown that melanopsin signals have sufficient spatiotemporal resolution to encode spatial patterns
Our description of melanopsin spatial receptive fields (RFs) in the mouse dorsal lateral geniculate nucleus (dLGN) show that its spatial resolution is modest (RF diameters $13), but that is true for mouse vision in general, and this feature is likely to be species-specific
Summary
Melanopsin photoreception enhances retinal responses to variations in ambient light (irradiance) and drives non-image-forming visual reflexes such as circadian entrainment [1,2,3,4,5,6]. In MR units (Figure 3E), correlation coefficients were significantly larger when the changes in shade were visible to all photoreceptors than only rods and cones and equivalent for ‘‘melanopsin-less’’ and ‘‘melanopsin-only’’ stimuli These data indicate that melanopsin enhances the ability of MR units to encode maintained differences in local radiance. Using these ‘‘all-photoreceptor’’ and ‘‘melanopsin-less’’ linear filters, we were able to adequately describe the activity of individual dLGN units over time under the simulated natural view experiment (Figure S3G) We applied these models to a simulated group of MR units tiling the visual scene in order to predict the representation of spatial patterns by the dLGN population under different viewing conditions.
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