SAD rats: Effects of short photoperiod and carbohydrate consumption on sleep, liver steatosis, and the gut microbiome in diurnal grass rats

ABSTRACT

Seasonal affective disorder (SAD) is a recurrent depression triggered by exposure to short photoperiods, with a subset of patients reporting hypersomnia, increased appetite, and carbohydrate craving. Dysfunction of the microbiota – gut – brain axis is frequently associated with depressive disorders, but its role in SAD is unknown. Nile grass rats (Arvicanthis niloticus) are potentially useful for exploring the pathophysiology of SAD, as they are diurnal and have been found to exhibit anhedonia and affective-like behavior in response to short photoperiods. Further, given grass rats have been found to spontaneously develop metabolic syndrome, they may be particularly susceptible to environmental triggers of metabolic dysbiosis. We conducted a 2 × 2 factorial design experiment to test the effects of short photoperiod (4 h:20 h Light:Dark (LD) vs. neutral 12:12 LD), access to a high concentration (8%) sucrose solution, and the interaction between the two, on activity, sleep, liver steatosis, and the gut microbiome of grass rats. We found that animals on short photoperiods maintained robust diel rhythms and similar subjective day lengths as controls in neutral photoperiods but showed disrupted activity and sleep patterns (i.e. a return to sleep after an initial bout of activity that occurs ~ 13 h before lights off). We found no evidence that photoperiod influenced sucrose consumption. By the end of the experiment, some grass rats were overweight and exhibited signs of non-alcoholic fatty liver disease (NAFLD) with micro- and macro-steatosis. However, neither photoperiod nor access to sucrose solution significantly affected the degree of liver steatosis. The gut microbiome of grass rats varied substantially among individuals, but most variation was attributable to parental effects and the microbiome was unaffected by photoperiod or access to sucrose. Our study indicates short photoperiod leads to disrupted activity and sleep in grass rats but does not impact sucrose consumption or exacerbate metabolic dysbiosis and NAFLD.

KEYWORDS:

• Photoperiod
• seasonal affective disorder
• metabolic dysbiosis
• non-alcoholic fatty liver disease

Acknowledgments

We would like to thank the Animal Care staff at the University of Alaska Fairbanks for their help with animal husbandry. We thank the Washington Animal Disease Diagnostic Laboratory at Washington State University for the liver stains. We thank Boaz Mohar for all the time he spent with liver imaging, and Kyle Dilliplaine of the Institute of Arctic Biology Genomics Core Lab for sequencing the microbiome samples.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

All the R code used to analyze data in this paper are available on github: https://github.com/ckdeal/Grass_Rats. Data used in this paper are available from Dryad: https://doi.org/10.5061/dryad.n2z34tn3g. Sequence data can be found at the following link: https://www.ncbi.nlm.nih.gov/sra/PRJNA1006454.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/07420528.2023.2288223.

Additional information

Funding

Financial support for this project was provided by the Alaska INBRE program; SM and KC were supported by the Biomedical Learning and Student Training (BLaST) program. Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Numbers [RL5GM118990] and [P20GM103395]. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.