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Photorefractoriness in Mammals: Dissociating a Seasonal Timer from the Circadian-Based Photoperiod Response

Medical Research Council Human Reproductive Sciences Unit (G.A.L., H.A.), Edinburgh EH16 4TG, Scotland; and School of Biological Sciences (J.D.J., G.W., D.G.H.), University of Aberdeen, Aberdeen AB24 2TZ, Scotland, United Kingdom

Address all correspondence and requests for reprints to: Dr. Gerald A. Lincoln, The Queen’s Medical Research Instiute, 47 Little France Crescent, Edinburgh EH16 4TJ, Scotland, United Kingdom. E-mail: g.lincoln{at}hrsu.mrc.ac.uk.

In seasonal animals, prolonged exposure to constant photoperiod induces photorefractoriness, causing spontaneous reversion in physiology to that of the previous photoperiodic state. This study tested the hypothesis that the onset of photorefractoriness is correlated with a change in circadian expression of clock genes in the suprachiasmatic nucleus (circadian pacemaker) and the pars tuberalis (PT, a melatonin target tissue). Soay sheep were exposed to summer photoperiod (16-h light) for either 6 or 30 wk to produce a photostimulated and photorefractory physiology, and seasonal changes were tracked by measuring the long-term prolactin cycles. Animals were killed at 4-h intervals throughout 24 h. Contrary to the hypothesis, the 24-h rhythmic expression of clock genes (Rev-erb, Per1, Per2, Bmal1, Cry1) in the suprachiasmatic nucleus and PT reflected the ambient photoperiod/melatonin signal and not the changing physiology. Contrastingly, the PT expression of -glycoprotein hormone subunit (GSU) and ßTSH declined in photorefractory animals toward a short day-like endocrinology. We conclude that the generation of long-term endocrine cycles depends on the interaction between a circadian-based, melatonin-dependent timer that drives the initial photoperiodic response and a non-circadian-based timer that drives circannual rhythmicity in long-lived species. Under constant photoperiod the two timers can dissociate, leading to the apparent refractory state.

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