Melanopsin-Driven Light Adaptation in Mouse Vision

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.

Modulation of Fast Narrowband Oscillations in the Mouse Retina and dLGN According to Background Light Intensity

“…Within the retina, the melanopsin-expressing ipRGCs are thought to provide the primary irradiance signal (Wong, 2012). The ipRGC irradiance code is already known to impact conventional vision by setting pupil size (Lucas et al, 2003), adapting visual circuits (Allen et al, 2014;Hankins and Lucas, 2002;Zhang et al, 2008), and regulating maintained firing (Brown et al, 2010). Our demonstration that irradiance control of oscillations can be modulated by changes in spectral power density targeting melanopsin and is impaired in melanopsin knockouts argues that melanopsin (and thus ipRGCs) also plays a central role in this aspect of vision.…”

“…This stimulus features a spatially diffuse, very gradual 1,0003 increase in irradiance (rise time = 13 min). Because its spectral composition recreates the balance of photoreceptor activations produced by daylight (Allen et al, 2014), we term it a ''daylight'' ramp. Both the normalized peak power and frequency of narrowband oscillations in the dLGN of anesthetized mice increased across this ramp (Figures 3A-3C; p = 4*10…”

Signalling by melanopsin (OPN4) expressing photosensitive retinal ganglion cells

“…The nature and properties of light responses recorded from cells within the dLGN have suggested a role for melanopsin in encoding changes in background [18][19][20] and the modulation of visual responses, with melanopsin reportedly driving adaptation of visual responses, modulating visual feature selectivity and facilitating a more reliable encoding of complex visual signals. 22,23 Based on retrograde labelling studies, it would seem that M4-type pRGCs project almost exclusively to the dLGN, 39 and would, therefore, seem to be predominantly tasked with providing input to visual pathways. In keeping with this hypothesis, M4-type pRGCs have now been identified as a subset of alpha ON ganglion cells, 21,39 a type of retinal ganglion cell known to be involved in the processing of visual information and contrast sensitivity.…”

“…Melanopsin provides visual centres with information regarding overall levels of environmental light, and performs roles in irradiance coding and brightness discrimination, [18][19][20] contrast detection, 21 and adaptation of visual responses. 22 Melanopsin also acts as an irradiance detector for the retina, 22,23 providing measures of overall illuminance and facilitating the adaptation of cone photoresponses under bright-light conditions. 22,24 Intraretinal signalling from pRGCs is also known to influence the activity of dopaminergic amacrine cells, [25][26][27] and displaced AII amacrine cells.…”

“…22 Melanopsin also acts as an irradiance detector for the retina, 22,23 providing measures of overall illuminance and facilitating the adaptation of cone photoresponses under bright-light conditions. 22,24 Intraretinal signalling from pRGCs is also known to influence the activity of dopaminergic amacrine cells, [25][26][27] and displaced AII amacrine cells. 28 During development, melanopsin-driven light responses influence the nature of calcium waves that spread across the developing retina and promote the segregation and refinement of retinofugal projections 29 (see also, Kirkby and Feller 30 ) and also regulate the formation and patterning of retinal blood vessels that ultimately influence retinal cell numbers.…”