Central melanopsin projections in the diurnal rodent, Arvicanthis niloticus.

Jennifer L Langel,Jens Hannibal,Gema Esquiva,Laura Smale

doi:10.3389/fnana.2015.00093

Abstract

The direct effects of photic stimuli on behavior are very different in diurnal and nocturnal species, as light stimulates an increase in activity in the former and a decrease in the latter. Studies of nocturnal mice have implicated a select population of retinal ganglion cells that are intrinsically photosensitive (ipRGCs) in mediation of these acute responses to light. ipRGCs are photosensitive due to the expression of the photopigment melanopsin; these cells use glutamate and pituitary adenylate cyclase-activating polypeptide (PACAP) as neurotransmitters. PACAP is useful for the study of central ipRGC projections because, in the retina, it is found exclusively within melanopsin cells. Little is known about the central projections of ipRGCs in diurnal species. Here, we first characterized these cells in the retina of the diurnal Nile grass rat using immunohistochemistry (IHC). The same basic subtypes of melanopsin cells that have been described in other mammals were present, but nearly 25% of them were displaced, primarily in its superior region. PACAP was present in 87.7% of all melanopsin cells, while 97.4% of PACAP cells contained melanopsin. We then investigated central projections of ipRGCs by examining the distribution of immunoreactive PACAP fibers in intact and enucleated animals. This revealed evidence that these cells project to the suprachiasmatic nucleus, lateral geniculate nucleus (LGN), pretectum, and superior colliculus. This distribution was confirmed with injections of cholera toxin subunit β coupled with Alexa Fluor 488 in one eye and Alexa Fluor 594 in the other, combined with IHC staining of PACAP. These studies also revealed that the ventral and dorsal LGN and the caudal olivary pretectal nucleus receive less innervation from ipRGCs than that reported in nocturnal rodents. Overall, these data suggest that although ipRGCs and their projections are very similar in diurnal and nocturnal rodents, they may not be identical.

Highlights

In mammals, light has a strong impact on daily activity rhythms by synchronizing an organism’s internal clock with rhythms in the external environment and through more acute effects on general activity
Melanopsin in the Nile Grass Rat Retina Melanopsin expression was examined in flat mount retinas from animal housed in a 12:12 LD cycle and from animals housed in constant darkness due to previous reports in rats showing a slight increase in melanopsin protein expression during prolonged periods in constant darkness (Hannibal et al, 2013)
Melanopsin was located mainly in the cell membrane of the soma and dendritic processes but in animals kept in constant darkness melanopsin was found in the membrane of axons projecting to the optic nerve (Figure 1)

Summary

Introduction

Light has a strong impact on daily activity rhythms by synchronizing an organism’s internal clock with rhythms in the external environment (i.e., light entrainment) and through more acute effects on general activity (a phenomenon known as masking). The neural pathways contributing to these differences are not well understood but they are likely to involve circuits that receive signals, directly or indirectly, from a subset of retinal ganglion cells that are intrinsically photosensitive (ipRGCs) These cells, which contain the photopigment melanopsin, are important for non-image-forming visual functions, such as entrainment, masking, melatonin suppression, and regulation of the pupillary light reflex (PLR). Cones, or melanopsin, masking still occurs (Mrosovsky et al, 2001; Panda et al, 2002), but removal of all three types of photoreceptors or ipRGCs eliminates masking and entrainment (Hattar et al, 2003; Panda et al, 2003; Goz et al, 2008; Guler et al, 2008; Hatori et al, 2008) It is clear, that ipRGCs play an essential role in transmission of photic signals that lead to a masking response in nocturnal mice. The question of whether this is the case in diurnal species is an open one, and differences along circuits that process signals from ipRGCs could theoretically contribute the differences in the acute effects of light on activity in day- and night-active animals

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Discussion

Conclusion