Functional and anatomical variations in retinorecipient brain areas in Arvicanthis niloticus and Rattus norvegicus: implications for the circadian and masking systems

ABSTRACT

Daily rhythms in light exposure influence the expression of behavior by entraining circadian rhythms and through its acute effects on behavior (i.e., masking). Importantly, these effects of light are dependent on the temporal niche of the organism; for diurnal organisms, light increases activity, whereas for nocturnal organisms, the opposite is true. Here we examined the functional and morphological differences between diurnal and nocturnal rodents in retinorecipient brain regions using Nile grass rats (Arvicanthis niloticus) and Sprague-Dawley (SD) rats (Rattus norvegicus), respectively. We established the presence of circadian rhythmicity in cFOS activation in retinorecipient brain regions in nocturnal and diurnal rodents housed in constant dark conditions to highlight different patterns between the temporal niches. We then assessed masking effects by comparing cFOS activation in constant darkness (DD) to that in a 12:12 light/dark (LD) cycle, confirming light responsiveness of these regions during times when masking occurs in nature. The intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPN) exhibited significant variation among time points in DD of both species, but their expression profiles were not identical, as SD rats had very low expression levels for most timepoints. Light presentation in LD conditions induced clear rhythms in the IGL of SD rats but eliminated them in grass rats. Additionally, grass rats were the only species to demonstrate daily rhythms in LD for the habenula and showed a strong response to light in the superior colliculus. Structurally, we also analyzed the volumes of the visual brain regions using anatomical MRI, and we observed a significant increase in the relative size of several visual regions within diurnal grass rats, including the lateral geniculate nucleus, superior colliculus, and optic tract. Altogether, our results suggest that diurnal grass rats devote greater proportions of brain volume to visual regions than nocturnal rodents, and cFOS activation in these brain regions is dependent on temporal niche and lighting conditions.

KEYWORDS:

• Diurnality
• visual system
• circadian
• light exposure
• magnetic resonance imaging

Acknowledgments

AJG was supported by a National Institutes of Health (NIH) Ruth L. Kirschstein National Research Service Award (NRSA) from the National Institute of Neurological Disorders and Stroke (NINDS) (F32 NS083360). We also thank the Hope College Psychology Department for their support of this project, and the Hope College Division of Social Sciences for providing startup funds to AJG. This work was also supported by a National Institutes of Mental Health grant (R01 MH53433) and a National Science Foundation grant (IOS 1051919). EMS and DDSM were supported by the National Cancer Institute grant (R21 CA185163). We would like to acknowledge Dr. Laura Smale for her input on experimental design and editing of the manuscript, and Dr. Tony Nunez for tissue collection.

Disclosure of Interest

The authors report no conflict of interest.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, [AJG], upon reasonable request.

Supplementary Materials

Supplemental data for this article can be accessed here.

Additional information

Funding

This work was supported by the Division of Integrative Organismal Systems [IOS 1051919]; National Cancer Institute [R21 CA185163]; National Institute of Mental Health [R01 MH53433]; National Institute of Neurological Disorders and Stroke [F32 NS083360].