The evolution of non-visual photopigments in the central nervous system of vertebrates

Abstract

In addition to classical image-forming vision, the vertebrates exhibit a range of non-image-forming light detection systems that utilise opsin photopigments. Within the CNS these systems are present in a range of anatomical locations that include both eye and brain. In mammals the eye is both responsible and required for all commonly measured responses to light. By contrast, non-mammalian vertebrates possess a wide range of intrinsically photoreceptive sites. Members of the non-visual opsin family include exorhodopsin, pinopsin, vertebrate ancient opsin (VA), parietopsin, parapinopsin, teleost multiple tissue opsin (TMT), encephalopsin (OPN3), neuropsin (OPN5), peropsin, retinal G protein-coupled receptor (RGR) and melanopsin (OPN4). Opsin-based photopigments have evolved to mediate specific photoreceptive tasks in different light environments, each exhibit functional properties that are tuned to the biological task in which they are involved. Examination of the classes of opsin involved reveals a range of adaptions particularly in spectral sensitivity, chromophore handling and signalling mechanisms. The loss of extraocular light detection in the mammals is associated with an evolutionary reduction in the non-visual opsin representation in the mammalian genome. One clear exception to this is the retention of the melanopsin (OPN4M) gene and the expression of this opsin protein in a single class of mammalian retinal ganglion cell. Exploring the diversity of melanopsin proteins in the lower vertebrates suggests that the property of chromophore biochemistry and bistability does not necessarily define an opsin class and may have evolved more than once.