Abstract

SummaryBackgroundIn bright light, mammals use a distinct photopigment (melanopsin) to measure irradiance for centrally mediated responses such as circadian entrainment. We aimed to determine whether the information generated by melanopsin is also used by the visual system as a signal for light adaptation. To this end, we compared retinal and thalamic responses to a range of artificial and natural visual stimuli presented using spectral compositions that either approximate the mouse’s experience of natural daylight (“daylight”) or are selectively depleted of wavelengths to which melanopsin is most sensitive (“mel-low”).ResultsWe found reproducible and reversible changes in the flash electroretinogram between daylight and mel-low. Simultaneous recording in the dorsal lateral geniculate nucleus (dLGN) revealed that these reflect changes in feature selectivity of visual circuits in both temporal and spatial dimensions. A substantial fraction of units preferred finer spatial patterns in the daylight condition, while the population of direction-sensitive units became tuned to faster motion. The dLGN contained a richer, more reliable encoding of natural scenes in the daylight condition. These effects were absent in mice lacking melanopsin.ConclusionsThe feature selectivity of many neurons in the mouse dLGN is adjusted according to a melanopsin-dependent measure of environmental brightness. These changes originate, at least in part, within the retina. Melanopsin performs a role analogous to a photographer’s light meter, providing an independent measure of irradiance that determines optimal setting for visual circuits.

Highlights

  • The visual system is charged with encoding visual information across the >109-fold change in background light intensity from starlight to cloudless midday

  • One might expect that adaptation state would be defined by the most accurate available measure of irradiance; under many circumstances, this is provided by a particular class of retinal ganglion cell [5,6,7,8]

  • These intrinsically photosensitive retinal ganglion cells have their own melanopsin-dependent phototransduction mechanism [9,10,11], and employ this, along with extrinsic signals originating with rods and cones, to encode light levels over many decimal orders [6]

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Summary

Introduction

The visual system is charged with encoding visual information across the >109-fold change in background light intensity from starlight to cloudless midday. The behavior of circuits in the retina is critical, with multiple examples of visual signals being shifted between parallel pathways with different computational characteristics, and of the behavior of individual elements within these pathways changing as a function of irradiance [1, 2] Such network changes do not merely adjust sensitivity and avoid saturation, but optimize circuit behavior to ensure efficient extraction of visual information (see [3, 4]). One might expect that adaptation state would be defined by the most accurate available measure of irradiance; under many circumstances, this is provided by a particular class of retinal ganglion cell [5,6,7,8] These intrinsically photosensitive retinal ganglion cells (ipRGCs) have their own melanopsin-dependent phototransduction mechanism [9,10,11], and employ this, along with extrinsic signals originating with rods and cones, to encode light levels over many decimal orders [6]

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