Comparative transcriptomics across photoperiod in the Siberian hamster and Japanese quail brains

Seasonal morphological brain plasticity plays a key role in driving adaptive behavioural responses. Structural changes in the brain including the hippocampus and amygdala (nucleus taeniae in birds), across photoperiods are thought to underlie seasonal shifts in emotional state. For humans, this includes manifestations of short photoperiod seasonal affective disorder (SAD). While morphological brain changes are well documented, the associated transcriptomic dynamics remain poorly understood. Here, we examined the transcriptomes of the hippocampus and amygdala or nucleus taeniae in two highly photoperiodic species, the Siberian hamster (Phodopus sungorus) and the Japanese quail (Coturnix japonica), to identify transcriptomic changes underpinning seasonal shifts in emotional state. Hamsters and quail exhibited robust physiological changes between long and short photoperiod treatment. Under short photoperiod, hamsters displayed anxiety-like behaviour (increased grooming) in the open field test, consistent with a SAD-like phenotype. Transcriptomic analysis of the amygdala in hamsters identified 76 significantly differentially expressed (DE) transcripts (including transthyretin, TTR) and prolactin receptor, PRLR as differentially expressed, but not significantly. In the quail nucleus taeniae, we found 54 DE transcripts (including tenascin-C, TNC). In the hamster hippocampus, 14 DE transcripts were found, including mahogunin ring finger-1 (MGRN1), and 31 in the quail hippocampus, including eyes absent-2 (Eya2). These findings provide novel insights into the transcriptomic mechanisms underpinning seasonal affective states and suggest conserved roles for prolactin and thyroid hormone signalling in mediating seasonal changes in physiology and affective behaviour, particularly in the Siberian hamster. Oxford Nanopore RNA-sequencing files for hippocampus and amygdala brain tissue for Japanese quail and Siberian hamsters held under a long (16L:8D) or short (8L:16D) photoperiod (day length). Adult male Japanese quail (Coturnix japonica) were maintained in photoperiodic, temperature-controlled rooms (390 (l) x 400 (w) x 250 (h) cm) at 27 °C and 39 % relative humidity (at the National Avian research Facility (NARF) Roslin Institute, The University of Edinburgh. Rooms were illuminated by Aquaforce Pro/AQFPRO S LED 4300 - 840, providing 25 - 30 lux at floor level. The quail were kept in pens with wooden frames and wire mesh walls (175 (l) x 128 (w) x 195 (h) cm) containing deep litter (wooden shavings, Stevenson Brothers Avonbridge, U.K.) and furniture (wooden logs, boxes, and perches) enrichment. Food (quail breeder diet; Target Feeds U.K.) and water was provided ad libitum and was replenished daily. Male quail (n = 12) were held on a long photoperiod (18L:6D), for 6 weeks and either remained on 18L:6D (n = 5) or were transferred to a short photoperiod (6L:18D, n = 6) for 4 weeks. Adult male Siberian hamsters (Phodopus sungorus), were singly housed in polypropylene cages in the Veterinary Research facility at the University of Glasgow (PPL PP5701950). Hamsters were provided with rodent chow (SDS [BK001]) and cool tap water ad libitum, as well as cotton wool and cardboard tubes for enrichment and housing. The hamsters (n=12) were either housed in long photoperiod (16L:8D, n = 6) or initially housed in long photoperiod then transferred to short photoperiod (8L:16D, n = 6) for 12 weeks. Hamsters were age-matched where possible, to between 9 and 14 months at the time of collection, to account for age effects on photoperiod manipulation. After 12 weeks, animals were killed using cervical dislocation, and whole brains were collected onto dry ice.