Distinct Contributions of Rod, Cone, and Melanopsin Photoreceptors to Encoding Irradiance

Abstract

SummaryPhotoreceptive, melanopsin-expressing retinal ganglion cells (mRGCs) encode ambient light (irradiance) for the circadian clock, the pupillomotor system, and other influential behavioral/physiological responses. mRGCs are activated both by their intrinsic phototransduction cascade and by the rods and cones. However, the individual contribution of each photoreceptor class to irradiance responses remains unclear. We address this deficit using mice expressing human red cone opsin, in which rod-, cone-, and melanopsin-dependent responses can be identified by their distinct spectral sensitivity. Our data reveal an unexpectedly important role for rods. These photoreceptors define circadian responses at very dim “scotopic” light levels but also at irradiances at which pattern vision relies heavily on cones. By contrast, cone input to irradiance responses dissipates following light adaptation to the extent that these receptors make a very limited contribution to circadian and pupillary light responses under these conditions. Our data provide new insight into retinal circuitry upstream of mRGCs and optimal stimuli for eliciting irradiance responses.

Predicting Human Nocturnal Nonvisual Responses to Monochromatic and Polychromatic Light With a Melanopsin Photosensitivity Function

“…The irradiances used in the current study were within the melanopsin operating range (> 10 13 photons/cm 2 /sec) and thus, if melanopsin is the 13 predominant photopigment driving the response then it is possible that any additional influence of cones was not able to be detected. Similar findings have been observed in mice whereby the magnitude of the pupil constriction response is accounted for solely by melanopsin once the light irradiance is within the melanopsin operating range and melanopsin is activated under a 'winner takes all' arrangement (Lall et al, 2010). However, previous human studies using long duration nocturnal light stimuli of similar photon densities to those used here (2.8 x 10 13 photons/cm 2 /sec) have implicated a role for cones in the melatonin suppression response (Lockley et al, 2003).…”

“…Work in transgenic mice has demonstrated that whilst melanopsin-pRGCS are sufficient to sustain non-visual responses to light (Lucas et al, 2001;Hattar et al, 2003) it appears that both the rod and cone visual photopigments also contribute (Ruby et al, 2002;Lucas et al, 2003) primarily via the pRGCs . The relative contribution of rods, cones and melanopsin to nonvisual responses appears to be context dependent and varies with the nature of the light stimulus (Lall et al, 2010).…”

“…However, to date, lighting has not been optimised for the non-visual system and this will likely be a highly complex procedure. Firstly, it has been demonstrated, via physiological and behavioural studies in transgenic mice lacking specific photopigments, that the three photopigment classes contribute differentially to different non-visual responses Altimus et al, 2008;Lupi et al, 2008;Thompson et al, 2008;Tsai et al, 2009;Lall et al, 2010). Thus, optimal light for one situation/environment/population may not be effective or appropriate for another.…”

The retinal clock in mammals: role in health and disease

“…[26][27][28] It is now clear that ipRGCs combine their direct intrinsic responses with signals derived from rods and cones to regulate diverse non-image-forming responses, 29 with each photoreceptor encoding distinct parameters of the light. [30][31][32][33][34] However, we currently lack a comprehensive understanding of how light regulates the retinal clock in mammals and of the role of the different photoreceptors.…”

An insight into light as a chronobiological therapy in affective disorders

“…These act to drive non-image-forming (NIF) responses of circadian photoentrainment, pupillary light reflex, pineal melatonin suppression, and sleep propensity. [12][13][14] However, the communicated photic information is not defined simply by duration of light, as retinal sensitivity is subject to irradiance and spectral composition. 11,15 It has been shown experimentally that the rod class of photoreceptor has the greatest sensitivity to light, with very low illumination still able to contribute to photoentrainment in the absence of other NIF responses.…”