The Biological Mechanisms and Behavioral Functions of Opsin-Based Light Detection by the Skin

Abstract

Light detection not only forms the basis of vision (via visual retinal photoreceptors), but can also occur in other parts of the body, including many non-rod/non-cone ocular cells, the pineal complex, the deep brain, and the skin. Indeed, many of the photopigments (an opsin linked to a light-sensitive 11-cis retinal chromophore) that mediate color vision in the eyes of vertebrates are also present in the skin of animals such as reptiles, amphibians, crustaceans and fishes (with related photoreceptive molecules present in cephalopods), providing a localized mechanism for light detection across the surface of the body. This form of non-visual photosensitivity may be particularly important for animals that can change their coloration by altering the dispersion of pigments within the chromatophores (pigment containing cells) of the skin. Thus, skin coloration may be directly color matched or "tuned" to both the luminance and spectral properties of the local background environment, thereby facilitating behavioral functions such as camouflage, thermoregulation, and social signaling. This review examines the diversity and sensitivity of opsin-based photopigments present in the skin and considers their putative functional roles in mediating animal behavior. Furthermore, it discusses the potential underlying biochemical and molecular pathways that link shifts in environmental light to both photopigment expression and chromatophore photoresponses. Although photoreception that occurs independently of image formation remains poorly understood, this review highlights the important role of non-visual light detection in facilitating the multiple functions of animal coloration.

The expression of opsins in the human skin and its implications for photobiomodulation: A Systematic Review

“…Continuous investigations in dermal photoreception have identified mitochondrial cytochrome c oxidase (CCO), nitrosated proteins, flavoproteins generating reactive oxygen species (ROS), and light‐activated calcium ion channels as endogenous photosensors 10 . More recently, opsins, which are key phototransducing molecules found in the retina, have emerged as new photosensors in the skin as several lines of scientific evidence support their expression in both nonhuman animal and human skin 11,12 …”

Phototactic tails: Evolution and molecular basis of a novel sensory trait in sea snakes

“…The role of opn4x is understudied but it is expressed in a wide range of tissues including the brain and eye of fish, amphibians, reptiles, turtles and birds (reviewed by Davies et al, 2014). Because opn4x is expressed in dermal melanophores of fish and amphibians (Bertolesi & McFarlane, ; Oshima, ; Provencio et al, ) and neuromasts of the lateral line system in Xenopus tadpoles (Baker et al, ), it is a good candidate pigment for nonvisual light detection pathways in nonmammalian vertebrates such as sea snakes (Kelley & Davies, ).…”

“…The mammal-like class of melanopsin (opn4m) is present in the ipRGCs of the eye (Bellingham et al, 2006;Provencio & Warthen, 2012) and some cranial nerves (Matynia et al, 2016), and has a range of photosensory functions including photoentrainment of molecular clocks, local pupil light reflex, DNA repair and melatonin synthesis (reviewed by Peirson et al, 2009;Bertolesi & McFarlane, 2018). The role of opn4x is understudied but it is expressed in a wide range of tissues including the brain and eye (Bertolesi & McFarlane, 2018;Oshima, 2001;Provencio et al, 1998) and neuromasts of the lateral line system in Xenopus tadpoles (Baker et al, 2015), it is a good candidate pigment for nonvisual light detection pathways in nonmammalian vertebrates such as sea snakes (Kelley & Davies, 2016).…”

“…Various cephalic or "extraocular" tissues have been linked to nonvisual photoreception, such as the parietal organ and pineal complex (Foster & Soni, 1998). In organisms lacking fur or feathers, the skin also provides a primary site for nonvisual photoreception (Kelley & Davies, 2016).…”

Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

“…Most animals possess eyes as specialized sensory organs for photoreception. However, the presence of non-ocular photosensory systems, such as photosensitive brain neurons and dermal photosensing systems, has been reported in several invertebrate species (reviewed in Yoshida, 1979;Kartelija et al, 2003;Gotow and Nishi, 2009;Ramirez et al, 2011;García-Fernández et al, 2015;Kelley and Davies, 2016). Of these, photosensing by the brain is of special interest because of its possible direct involvement in light-evoked behavioural changes.…”