Abstract
Intrinsically photosensitive retinal ganglion cells (ipRGCs) represent a new class of photoreceptors which support a variety of non-image forming physiological functions, such as circadian photoentrainment, pupillary light reflex and masking responses to light. In view of the recently proposed role of retinal inputs for the regulation of diurnal and nocturnal behavior, we performed the first deep analysis of the ipRGC system in a diurnal rodent model, Arvicanthis ansorgei , and compared the anatomical and physiological properties of ipRGCs with those of nocturnal mice. Based on somata location, stratification pattern and melanopsin expression, we identified two main ipRGC types in the retina of Arvicanthis : M1, constituting 74% of all ipRGCs and non-M1 (consisting mainly of the M2 type) constituting the following 25%. The displaced ipRGCs were rarely encountered. Phenotypical staining patterns of ganglion cell markers showed a preferential expression of Brn3 and neurofilaments in non-M1 ipRGCs. In general, the anatomical properties and molecular phenotyping of ipRGCs in Arvicanthis resemble ipRGCs of the mouse retina, however the percentage of M1 cells is considerably higher in the diurnal animal. Multi-electrode array recordings (MEA) identified in newborn retinas of Arvicanthis three response types of ipRGCs (type I, II and III) which are distinguished by their light sensitivity, response strength, latency and duration. Type I ipRGCs exhibited a high sensitivity to short light flashes and showed, contrary to mouse type I ipRGCs, robust light responses to 10 ms flashes. The morphological, molecular and physiological analysis reveals very few differences between mouse and Arvicanthis ipRGCs. These data imply that the influence of retinal inputs in defining the temporal niche could be related to a stronger cone input into ipRGCs in the cone-rich Arvicanthis retina, and to the higher sensitivity of type I ipRGCs and elevated proportion of M1 cells.
Highlights
In mammals, non-visual photoreception provides the most important time cue for synchronization of the master clock in the suprachiasmatic nuclei (SCN) with the solar day
The majority of intrinsically photosensitive retinal ganglion cells (ipRGCs) (2063 of 2787 ipRGCs; 74%) were strongly melanopsin-immunopositive with somata located in the ganglion cell layer (GCL) and arborizations in the outermost part of the inner plexiform layer (IPL) (OFF sublamina) (Figures 1 and 2)
In Arvicanthis, this population mainly expressed features of the M2 type, characterized by somata located in the GCL and dendrites branching in the innermost layer (ON sublamina) of the IPL (Figures 1 and 2)
Summary
Non-visual photoreception provides the most important time cue for synchronization of the master clock in the suprachiasmatic nuclei (SCN) with the solar day. Non-visual photoreception is governed by melanopsinexpressing, intrinsically photosensitive retinal ganglion cells (ipRGCs) encoding irradiance information used for photoentrainment [8,9]. Rod and cone signals, which contribute to the light response in the SCN and to circadian entrainment [10], act through activation of the ipRGCs [11,12]. In doubleknockout mice lacking the photopigment melanopsin and RPE65, a key protein used in retinal chromophore recycling, which retain only a small rod input, the phase of circadian activity rhythms with respect to the external light/dark cycle is reversed from nocturnal to diurnal entrainment [13]. A similar switch from nocturnal to diurnal activity was observed in wild-type mice under light/dark cycles with light intensities reduced to scotopic levels, suggesting that the state of photoreceptors can play an important role in determining phasing of activity in diurnal and nocturnal species [13,14]
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