The Daily Melatonin Pattern in Djungarian Hamsters Depends on the Circadian Phenotype

Abstract

Djungarian hamsters (Phodopus sungorus) bred at the Institute of Halle reveal three different circadian phenotypes. The wild type (WT) shows normal locomotor activity patterns, whereas in hamsters of the DAO (delayed activity onset) type, the activity onset is continuously delayed. Since the activity offset in those hamsters remains coupled to “light-on,” the activity time becomes compressed. Hamsters of the AR (arrhythmic) type are episodically active throughout the 24 h. Previous studies showed that a disturbed interaction of the circadian system with the light-dark (LD) cycle contributes to the phenomenon observed in DAO hamsters. To gain better insight into the underlying mechanisms, the authors investigated the daily melatonin rhythm, as it is a reliable marker of the circadian clock. Hamsters were kept individually under standardized laboratory conditions (LD 14:10, T = 22°C ± 2°C, food and water ad libitum). WT, DAO (with exactly 5 h delay of activity onset), and AR hamsters were used for pineal melatonin and urinary 6-sulfatoxymelatonin (aMT6s) measurement. Pineal melatonin content was determined at 3 time points: 4 h after “light-off” [D + 4], 1 h before “light-on” [L − 1], and 1 h after “light-on” [L + 1]). The 24-h profile of melatonin secretion was investigated by transferring the animals to metabolic cages for 27 h to collect urine at 3-h intervals for aMT6s analysis. WT hamsters showed high pineal melatonin content during the dark time (D + 4, L − 1), which significantly decreased at the beginning of the light period (L + 1). In contrast, DAO hamsters displayed low melatonin levels during the part of the dark period when animals were still resting (D + 4). At the end of the dark period (L − 1), melatonin content increased significantly and declined again when light was switched on (L + 1). AR hamsters showed low melatonin levels, comparable to daytime values, at all 3 time points. The results were confirmed by aMT6s data. WT hamsters showed a marked circadian pattern of aMT6s excretion. The concentration started to increase 3 h after “light-off” and reached daytime values 5 h after “light-on.” In DAO hamsters, in contrast, aMT6s excretion started about 6 h later and reached significantly lower levels compared to WT hamsters. In AR animals, aMT6s excretion was low at all times. The results clearly indicate the rhythm of melatonin secretion in DAO hamsters is delayed in accord with their delayed activity onset, whereas AR hamsters display no melatonin rhythm at all. Since the regulatory pathways for the rhythms of locomotor activity and melatonin synthesis (which are downstream from the suprachiasmatic nucleus [SCN]) are different but obviously convey the same signal, we conclude that the origin of the phenomenon observed in DAO hamsters must be located upstream of the SCN, or in the SCN itself. (Author correspondence: [email protected])

Keywords:

• Arrhythmic activity pattern
• Circadian rhythm
• Djungarian hamster
• Daily melatonin rhythm
• Disturbed photic entrainment

ACKNOWLEDGMENTS

The authors of the study are thankful to Kerstin Waegner, Birgit Gebhardt, and Christiane Calgari for technical advice, Jim Waterhouse for critical reading of the manuscript, and to three anonymous referees for helpful comments. The aMT6s investigations was funded by the Ethologische Gesellschaft e. V.

Declaration of Interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.