Neural mechanisms controlling seasonal reproduction: principles derived from the sheep model and its comparison with hamsters - PubMed (original) (raw)

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Neural mechanisms controlling seasonal reproduction: principles derived from the sheep model and its comparison with hamsters

Peyton W Weems et al. Front Neuroendocrinol. 2015 Apr.

Abstract

Seasonal reproduction is a common adaptive strategy among mammals that allows for breeding to occur at times of the year when it is most advantageous for the subsequent survival and growth of offspring. A major mechanism responsible for seasonal reproduction is a striking increase in the responsiveness of gonadotropin-releasing hormone (GnRH) neurons to the negative feedback effects of estradiol. The neural and neuroendocrine circuitry responsible for mammalian seasonal reproduction has been primarily studied in three animal models: the sheep, and two species of hamsters. In this review, we first describe the afferent signals, neural circuitry and transmitters/peptides responsible for seasonal reproductive transitions in sheep, and then compare these mechanisms with those derived from studies in hamsters. The results suggest common principles as well as differences in the role of specific brain nuclei and neuropeptides, including that of kisspeptin cells of the hypothalamic arcuate nucleus, in regulating seasonal reproduction among mammals.

Keywords: Dopamine; GnRH; Kisspeptin; Neuroendocrine; Photoperiod; Seasonality; Thyroid hormone.

Copyright © 2014 Elsevier Inc. All rights reserved.

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Figures

Figure 1

Figure 1

Comparison of seasonal reproductive patterns in sheep and hamsters. Changes in fertility are controlled by variations in the duration of daylight throughout the year (top panel), but photoperiod has different effects in these species. Short days stimulate reproductive function in sheep, so all ewes have ovulatory cycles during the fall and winter, but become anovulatory in the spring and summer (middle panel). In contrast, reproductive activity in hamsters (illustrated as changes in size of the testes in the bottom panel) is stimulated by long days; thus hamsters are fertile in the spring and summer and reproductive inactive in the fall and winter.

Figure 2

Figure 2

Seasonal changes in number of ARC kisspeptin cells (A) and their inputs to GnRH neurons (B). A: The number of kisspeptin-immunoreactive (Kiss) neurons in the middle and caudal ARC is decreased during anestrous (* p<.001). Images show examples of sections through the caudal ARC immunostained for kisspeptin in ewes perfused during either the breeding season or anestrus. Ewes were ovariectomized and implanted with E2 (OVX+E) to control for seasonal variation in endogenous steroid levels. Note that the number of kisspeptin cells in the POA, another major kisspeptin population (76), does not change seasonally. Bar = 100 μm. B: The percentage of GnRH cells in the MBH that receive one or more kisspeptin (Kiss) close contacts was less in anestrous than in breeding season ewes (* p<.001); GnRH cells in the POA or anterior hypothalamic area (AHA) showed no significant seasonal differences. In addition, GnRH cells in the MBH and AHA had significantly fewer Kiss contacts per cell in anestrous than in the breeding season (data not shown). Images show examples of dual immunoperoxidase stained sections in which close contacts (e.g., arrows) are seen between kisspeptin terminals (blue-black) and GnRH somas (brown) in the MBH. Bar = 15 μm. (A and B modified from ref. 48)

Figure 3

Figure 3

Schematic depiction of the neural circuitry in the hypothalamus regulating seasonal control of estradiol (E2) negative feedback. E2 acts upon ER-alpha containing cells (blue) in the ventromedial preoptic area (POA) and retrochiasmatic area (RCh); these neurons, in turn, stimulate A15 dopamine cells (red) via glutamatergic inputs. A15 dopamine cells project caudally to the mediobasal hypothalamus (MBH) and inhibit GnRH cells (brown) either directly at the level of their terminals in the median eminence, and/or indirectly via kisspeptin (Kiss) cells (green) in the arcuate nucleus. Seasonal plasticity has been demonstrated at several sites in this circuitry including that of glutamatergic contacts onto A15 neurons (42); the dendritic morphology of dopaminergic A15 neurons (43); and the number of kisspeptin inputs to GnRH neurons in the MBH (48). Such morphological changes may result in a functional “reconnection” of this circuitry during anestrus, and underlie the ability of E2 to inhibit GnRH pulse frequency at this time of year. OCh = optic chiasm. (Modified from ref. 27).

Figure 4

Figure 4

Comparison of the neural systems mediating the effects of long days on GnRH secretion in sheep, Syrian and Siberian hamsters. Note that long days (LD PP) are inhibitory in sheep, but stimulatory in hamsters. In sheep and Syrian hamsters, changes in ARC kisspeptin play a central role in the photoperiodic control of GnRH release, but different afferent inputs are involved in these two species. In contrast, kisspeptin does not appear to be important for seasonal changes in GnRH secretion in Siberian hamsters; rather the increase in circulating testosterone drives the changes observed in kisspeptin expression. See text for further details.

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