Circadian Photoreception: From Phototransduction to Behaviour

Abstract

Environmental light is detected by three classes of ocular photoreceptor, the rods and cones of the outer retina and photosensitive retinal ganglion cells (pRGCs) that utilise the photopigment melanopsin. In addition to their endogenous photosensitivity, pRGCs receive indirect inputs from the rods and cones. The primary role of the rods and cones is to collect light information for the construction of a visual image, whilst the pRGCs send direct projections to many regions of the brain to regulate nonimage-forming responses to light, including the entrainment of circadian rhythms. The master circadian pacemaker of mammals resides within the suprachiasmatic nuclei (SCN), and light information is transmitted from the pRGCs via their axonal projections which form the retinohypothalamic tract. Neurones within the SCN respond to retinal illumination with changes in electrical activity showing characteristic fast-transient components at the light transitions and a sustained response throughout light exposure. Until recently it was assumed that the fast-transient responses were driven by the rods and/or cones, via their inputs to the pRGCs, whilst the sustained responses to light were mediated by melanopsin. However, more recent studies show that both transient and sustained responses can be generated in the absence of melanopsin, suggesting a significant level of functional redundancy between photoreceptor classes. Although SCN electrical activity appears normal in melanopsin-deficient mice, these animals show attenuated light-induced phase-shifting response in behavioural activity. Collectively these findings raise intriguing questions about how different classes of retinal photoreceptor interact to encode nonimage-forming responses to light and suggest that recordings of multiunit activity at the level of the SCN do not entirely mirror the effects of light on circadian behaviour.