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

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 2x2 factorial design experiment to
test the effects of short photoperiod (4h:20h 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
showed disrupted activity and sleep patterns but maintained robust diel
rhythms and similar subjective day lengths as controls in neutral
photoperiods. 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.