Generation Of Circannual Rhythms Research Articles

Hypothesis

Circannual rhythms are innately timed long-term (tau ≈ 12 months) cycles of physiology and behavior, crucial for life in habitats ranging from the equator to the Poles. Here the authors propose that circannual rhythm generation depends on tissue-autonomous, reiterated cycles of cell division, functional differentiation, and cell death. They see the feedback control influencing localized stem cell niches as crucial to this cyclical histogenesis hypothesis. Analogous to multi-oscillator circadian organization, circannual rhythm generation occurs in multiple tissues with hypothalamic and pituitary sites serving as central pacemakers. Signals including day length, nutrition, and social factors can synchronize circannual rhythms through hormonal influences, notably via the thyroid and glucocorticoid axes, which have profound effects on histogenesis. The authors offer 4 arguments in support of this hypothesis: (1) Cyclical histogenesis is a prevalent process in seasonal remodeling of physiology. It operates over long time domains and exhibits tissue autonomy in its regulation. (2) Experiments in which selected peripheral endocrine signals are held constant indicate that circannual rhythms are not primarily the product of interacting hormonal feedback loops. (3) Hormones known to control cell proliferation, differentiation, and organogenesis profoundly affect circannual rhythm expression. (4) The convergence point between photoperiodic input pathways and circannual rhythm expression occurs in histogenic regions of the hypothalamus and pituitary. In this review, the authors discuss how testing this hypothesis will depend on the use of cellular/molecular tools and animal models borrowed from developmental biology and neural stem cell research.

Photoperiod as a proximate factor in control of seasonality in the subtropical male Tree Sparrow, Passer montanus

BackgroundMost species of birds exhibit well-defined seasonality in their various physiological and behavioral functions like reproduction, molt, bill color etc. such that they occur at the most appropriate time of the year. Day length has been shown to be a major source of temporal information regulating seasonal reproduction and associated events in a number of avian species. The present study aims to investigate the role of photoperiod in control of seasonal cycles in the subtropical male tree sparrow (Passer montanus) and to compare its responses at Shillong (Latitude 25°34'N, Longitude 91°53'E) with those exhibited by its conspecifics and related species at other latitudes.ResultsInitial experiment involving study of seasonal cycles revealed that the wild tree sparrows posses definite seasonal cycles of testicular volume, molt and bill color. These cycles were found remarkably linked to annual solar cycle suggesting the possibility of their photoperiodic control. To confirm this possibility in the next experiment, the photosensitive birds were exposed to three different light-dark regimes that were close to what they experience at this latitude: 9L/15D (close to shortest day length), 12L/12D (equinox day length) and 14L/10D (close to longest day length) for 18 months. Tree sparrows showed testicular growth followed by regression and development of photorefractoriness, molting and bill color changes only under long daily photoperiods (12 L and 14 L) but not under short daily photoperiod (9 L). Birds, under stimulatory photoperiods, did not show reinitiation of the above responses after the completion of initiation regression cycle even after their exposure to these photoperiods for 18 months. This precludes the possibility of circannual rhythm generation and suggests the involvement of photoperiodic mechanism in control of their seasonal cycles. Further, replacement of body and primary feathers progressed with gonadal regression only under long days suggesting that the two high energy demanding events of reproduction and molt are phased at two different times in the annual cycle of the bird and are photoperiodically regulated. Results of the final experiment involving exposure of photosensitive birds to a variety of photoperiodic treatments (9L/15D, 10L/14D, 11L/13D, 12L/12D, 14L/10D and 16L/8D) for 30 days suggested that the light falling for 11 h or more is important in inducing testicular growth and function in this species.ConclusionThese results clearly indicate that despite of small photofluctuation, subtropical tree sparrows are capable of fine discrimination of photoperiodic information and use day length as a proximate environmental factor to time their seasonal responses similar to their conspecifics and related species at other latitudes suggesting the conservation of photoperiodic control mechanism in them.

A Physiological Model of a Circannual Oscillator

Recent evidence based on studies in hypothalamo-pituitary disconnected Soay sheep suggests that the generation of circannual rhythms may be local to specific tissues or physiological systems. Now, the authors present a physiological model of a circannual rhythm generator centered in the pituitary gland based on the interaction between melatonin-responsive cells in the pars tuberalis that act to decode photoperiod, and lactotroph cells of the adjacent pars distalis that secrete prolactin. The model produces a self-sustained, circannual rhythm in endocrine output that the authors explore by mathematical modeling. The circannual oscillation requires a delayed negative feedback mechanism. The authors highlight specific features of the pituitary dynamics as a guide to future research on circannual rhythms.

Circannual prolactin rhythms: calendar-like timer revealed in the pituitary gland

Although photoperiodic regulation of annual rhythms in reproduction and other functions has been well characterized, the basis for the endogenous generation of circannual rhythms during exposure to constant conditions has not been elucidated. Lincoln and colleagues have recently reported that circannual prolactin rhythms in rams persist after hypothalamo-pituitary disconnection, but not after pinealectomy. Does the pars tuberalis, the site of pituitary gland melatonin receptors, generate circannual rhythms and integrate photoperiodic signals mediated by melatonin?

Characterizing a Mammalian Circannual Pacemaker

Many species express endogenous cycles in physiology and behavior that allow anticipation of the seasons. The anatomical and cellular bases of these circannual rhythms have not been defined. Here, we provide strong evidence using an in vivo Soay sheep model that the circannual regulation of prolactin secretion, and its associated biology, derive from a pituitary-based timing mechanism. Circannual rhythm generation is seen as the product of the interaction between melatonin-regulated timer cells and adjacent prolactin-secreting cells, which together function as an intrapituitary "pacemaker-slave" timer system. These new insights open the way for a molecular analysis of long-term timing mechanisms.

Clock genes in calendar cells as the basis of annual timekeeping in mammals--a unifying hypothesis.

Melatonin-based photoperiod time-measurement and circannual rhythm generation are long-term time-keeping systems used to regulate seasonal cycles in physiology and behaviour in a wide range of mammals including man. We summarise recent evidence that temporal, melatonin-controlled expression of clock genes in specific calendar cells may provide a molecular mechanism for long-term timing. The agranular secretory cells of the pars tuberalis (PT) of the pituitary gland provide a model cell-type because they express a high density of melatonin (mt1) receptors and are implicated in photoperiod/circannual regulation of prolactin secretion and the associated seasonal biological responses. Studies of seasonal breeding hamsters and sheep indicate that circadian clock gene expression in the PT is modulated by photoperiod via the melatonin signal. In the Syrian and Siberian hamster PT, the high amplitude Per1 rhythm associated with dawn is suppressed under short photoperiods, an effect that is mimicked by melatonin treatment. More extensive studies in sheep show that many clock genes (e.g. Bmal1, Clock, Per1, Per2, Cry1 and Cry2) are expressed in the PT, and their expression oscillates through the 24-h light/darkness cycle in a temporal sequence distinct from that in the hypothalamic suprachiasmatic nucleus (central circadian pacemaker). Activation of Per1 occurs in the early light phase (dawn), while activation of Cry1 occurs in the dark phase (dusk), thus photoperiod-induced changes in the relative phase of Per and Cry gene expression acting through PER/CRY protein/protein interaction provide a potential mechanism for decoding the melatonin signal and generating a long-term photoperiodic response. The current challenge is to identify other calendar cells in the central nervous system regulating long-term cycles in reproduction, body weight and other seasonal characteristics and to establish whether clock genes provide a conserved molecular mechanism for long-term timekeeping.

Clock genes and the long-term regulation of prolactin secretion: evidence for a photoperiod/circannual timer in the pars tuberalis.

Prolactin secretion is regulated by photoperiod through changes in the 24-h melatonin profile and displays circannual rhythmicity under constant photoperiod. These two processes appear to occur principally within the pituitary gland, controlled by the pars tuberalis. This is evident because: (i) hypothalamic-pituitary disconnected (HPD) sheep show marked changes in prolactin secretion in response to switches in photoperiod and manipulations of melatonin, similar to brain-intact controls; (ii) HPD sheep also show photoperiod-specific, long-term cycles in prolactin secretion under constant long or short days, with the timing maintained even when prolactin secretion is blocked for 2-3 months; and (iii) pars tuberalis cells, but not lactotrophs, express high concentrations of melatonin (MT1) receptor, and exhibit a duration-sensitive, cAMP-dependant, inhibitory response to physiological concentrations of melatonin. This suggests the existence of an intrinsic, reversible photoperiod-circannual timer in pars tuberalis cells. A full complement of clock genes (Bmal1, Clock, Per1, Per2, Cry1 and Cry2) are expressed in the ovine pars tuberalis, and undergo 24-h cyclical expression as observed in a cell autonomous, circadian clock. Activation of Per genes occurs in the early day (melatonin off-set), while activation of Cry genes occurs in the early night (melatonin on-set). This temporal association is evident under both long and short days, thus the Per-Cry interval varies directly with photoperiod. Because, PER : CRY, protein : protein interactions affect stability, nuclear entry and gene transcription based on rodent data, the change in phasing of Per/Cry expression provides a potential mechanism for decoding the long day/short day melatonin signal. A speculative, but testable, extension of this hypothesis is that intrinsically regulated changes in the phase of Per/Cry rhythms, regulates both photorefractoriness and the generation of circannual rhythms in prolactin secretion.