Reproductive Neuroendocrine Pathways of Social Behavior (original) (raw)
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Social Regulation of Gonadotropin-Releasing Hormone
Journal of Experimental Biology, 2002
In vertebrates, gonadotropin-releasing hormone (GnRH) delivered by hypothalamic neurons to the pituitary gland, regulates reproduction through release of pituitary gonadotropins that regulate gonadal function (Cattanach et al., 1977; Mason et al., 1986; Sherwood, 1987). In ...
2006
The availability of tools for probing the genome and proteome more efficiently has allowed for the rapid discovery of novel genes and peptides that play important, previously uncharacterized roles in neuroendocrine regulation. In this review, the role of a class of neuropeptides containing the C-terminal Arg-Phe-NH 2 (RFamide) in regulating the reproductive axis will be highlighted. Neuropeptides containing the C-terminal Phe-Met-Arg-Phe-NH 2 (FMRFamide) were first identified as cardioregulatory elements in the bi-valve mollusk Macrocallista nimbosa. During the past two decades, numerous studies have shown the presence of structurally similar peptides sharing the RFamide motif across taxa. In vertebrates, RFamide peptides have pronounced influences on opiatergic regulation and neuroendocrine function. Two key peptides in this family are emerging as important regulators of the reproductive axis, kisspeptin and gonadotropin-inhibitory hormone (GnIH). Kisspeptin acts as the accelerator, directly driving gonadotropin-releasing hormone (GnRH) neurons, whereas GnIH acts as the restraint. Recent evidence suggests that both peptides play a role in mediating the negative feedback effects of sex steroids. This review presents the hypothesis that these peptides share complementary roles by responding to internal and external stimuli with opposing actions to precisely regulate the reproductive axis.
Hormonal and neurotransmitter regulation of GnRH gene expression and related reproductive behaviors
Behavior Genetics, 1996
Gonadotropin-releasing hormone (GnRH), having a highly conserved structure across mammalian species, plays a pivotal role in the control of the neuroendocrine events and the inherent sexual behaviors essential for reproductive function. Recent advances in molecular genetic technology have contributed greatly to the investigation of several aspects of GnRH physiology, particularly steroid hormone and neurotransmitter regulation of GnRH gene expression. Behavioral studies have focused on the actions of GnRH in steroid-sensitive brain regions to understand better its role in the facilitation of mating behavior. To date, however, there are no published reports which directly correlate GnRH gene expression and reproductive behavior. The intent of this article is to review the current understanding of the way in which changes in GnRH gene expression, and modifications of GnRH neuronal activity, may ultimately influence reproductive behavior.
The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone
Integrative and Comparative Biology, 2008
Synopsis Gonadotropin-releasing hormone (GnRH) controls the reproductive physiology and behavior of vertebrates by stimulating synthesis and release of gonadotropin from the pituitary gland. In 2000, another hypothalamic neuropeptide, gonadotropin-inhibitory hormone (GnIH), was discovered in quail and found to be an inhibiting factor for gonadotropin release. GnIH homologs are present in the brains of vertebrates, including birds, mammals, amphibians, and fish. These peptides, categorized as RF amide-related peptides (RFRPs), possess a characteristic LPXRF-amide (X ¼ L or Q) motif at their C-termini. GnIH/RFRP precursor mRNA encodes a polypeptide that is possibly cleaved into three mature peptides in birds and two in mammals. The names of these peptides are GnIH, GnIH-related peptide-1 (GnIH-RP-1) and GnIH-RP-2 in birds, and RFRP-1 and RFRP-3 in mammals. GnIH/RFRP is synthesized in neurons of the paraventricular nucleus of the hypothalamus in birds and the dorsomedial hypothalamic area in mammals. GnIH neurons project to the median eminence, thus providing a functional neuroanatomical infrastructure to regulate anterior pituitary function. In quail, GnIH inhibits gonadal activity by decreasing synthesis and release of gonadotropin. The widespread distribution of GnIH/RFRP immunoreactive fibers in all animals tested suggests various actions within the brain. In accordance, GnIH/RFRP receptor mRNA is also expressed widely in the brain and the pituitary. GnIH/RFRP immunoreactive axon terminals are in probable contact with GnRH neurons in birds and mammals, and we recently demonstrated expression of GnIH receptor mRNA in GnRH-I and GnRH-II neurons in European starlings. Thus, GnIH/RFRP may also inhibit gonadotropin synthesis and release by inhibiting GnRH neurons in addition to having direct actions on the pituitary gland. Intracerebroventricular administration of GnIH/RFRP further inhibits reproductive behaviors in songbirds and rodents, possibly via direct actions on the GnRH system. The expression of GnIH/RFRP is regulated by melatonin which is an internal indicator of day length in vertebrates. Stress stimuli also regulate the expression of GnIH/RFRP in songbirds and rodents. Accordingly, GnIH/RFRP may serve as a transducer of environmental information and social interactions into endogenous physiology and behavior of the animal. Recently, it was shown that GnIH/RFRP and its receptor are also expressed in the gonads of birds, rodents and primates. In sum, the existing data suggest that GnIH/RFRP is an important mediator of reproductive function acting at the level of the brain, pituitary, and the gonad in birds and mammals.
Gonadotropin-releasing hormone signaling in behavioral plasticity
Current Opinion in Neurobiology, 2006
Sex and reproduction sculpt brain and behavior throughout life and evolution. In vertebrates, gonadotropin-releasing hormone (GnRH) is essential to these processes. Recent advances have uncovered novel regulatory mechanisms in GnRH signaling, such as the initiation of sexual maturation by kisspeptins. Yet despite our increasing molecular knowledge, we know very little about environmental influences on GnRH signaling and reproductive behavior. Alternative model systems have been crucial for understanding the plasticity of GnRH effects within an organismal context. For instance, GnRH signaling is under the control of seasonal cues in songbirds, whereas social signals regulate GnRH in cichlid fishes, with crucial consequences for reproduction and behavior. Analyzing cellular signaling cascades within an organismic context is essential for an integrative understanding of GnRH function.
Differential social regulation of two pituitary gonadotropin-releasing hormone receptors
Behavioural Brain Research, 2006
In many vertebrates, social interactions regulate reproductive capacity by altering the activity of the hypothalamic-pituitary-gonadal (HPG) axis. To better understand the mechanisms underlying social regulation of reproduction, we investigated the relationship between social status and one main component of the HPG axis: expression levels of gonadotropin-releasing hormone receptor (GnRH-R). Social interactions dictate reproductive capacity in the cichlid fish Astatotilapia burtoni. Reproductively active territory holders suppress the HPG axis of non-territorial males through repeated aggressive encounters. To determine whether the expression of GnRH-R is socially regulated, we quantified mRNA levels of two GnRH-R variants in the pituitaries and brains of territorial (T) and non-territorial (NT) A. burtoni males. We found that T males had significantly higher levels of pituitary GnRH-R1 mRNA than NT males. In contrast, GnRH-R2 mRNA levels in the pituitary did not vary with social status. Pituitaries from both T and NT males expressed significantly higher mRNA levels of GnRH-R1 than GnRH-R2. GnRH mRNA levels in the brain correlated positively with GnRH-R1 mRNA levels in the pituitary but did not correlate with pituitary GnRH-R2. Measurements of GnRH-R1 and GnRH-R2 mRNA levels across the whole brain revealed no social status differences. These results show that, in addition to the known effects of social status on other levels of the HPG axis, GnRH receptor in the pituitary is also a target of social regulation.
PeerJ, 2016
Recent work has led to the hypothesis that kisspeptin/neurokinin B/dynorphin (KNDy) neurons in the arcuate nucleus (ARC) play a key role in gonadotropin-releasing hormone (GnRH) pulse generation and gonadal steroid feedback, with kisspeptin driving GnRH release and neurokinin B and dynorphin acting as pulse start and stop signals, respectively. A separate cell group, expressing RFamide-related peptide-3 (RFRP-3) has been shown to be a primary inhibitor of GnRH release. Very little is known regarding these cell groups in the bovine. In this study, we examined the relative immunoreactivity of kisspeptin, dynorphin, and RFRP-3 and their possible connectivity to GnRH neurons in the hypothalami of periestrus and diestrus bovine. While GnRH and RFRP-3 immunoreactivity were unchanged, kisspeptin and dynorphin immunoreactivity levels varied in relation to plasma progesterone concentrations and estrous status. Animals with higher plasma progesterone concentrations in diestrus had lower kissp...
Journal of Neuroendocrinology, 2000
Gonadotropin-releasing hormone (GnRH) is the primary hypothalamic factor responsible for the control of gonadotropin secretion in vertebrates. However, within the last decade, two other hypothalamic neuropeptides have been found to play key roles in the control of reproductive functions: gonadotropin-inhibitory hormone (GnIH) and kisspeptin. In 2000, we discovered GnIH in the quail hypothalamus. GnIH inhibits gonadotropin synthesis and release in birds through actions on GnRH neurons and gonadotropes, mediated via GPR147. Subsequently, GnIH orthologs were identified in other vertebrate species from fish to humans. As in birds, mammalian and fish GnIH orthologs inhibit gonadotropin release, indicating a conserved role for this neuropeptide in the control of the hypothalamo-pituitary-gonadal (HPG) axis across species. Following the discovery of GnIH, kisspeptin, encoded by the KiSS-1 gene, was discovered in mammals. In contrast to GnIH, kisspeptin has a direct stimulatory effect on GnRH neurons via GPR54. GPR54 is also expressed in pituitary cells, but whether gonadotropes are targets for kisspeptin remains unresolved. The KiSS-1 gene is also highly conserved and has been identified in mammals, amphibians and fish. We have recently found a second isoform of KiSS-1, designated KiSS-2, in several vertebrates, but not birds, rodents or primates. In this review, we highlight the discovery, mechanisms of action, and functional significance of these two chief regulators of the reproductive axis.
Hormones and Behavior, 1996
Reproduction in vertebrates is regulated by internal sig-port is part of a series of experiments designed to elucinals such as hormone levels and by external signals such date how external and internal cues are integrated in as social interactions. In an African cichlid fish, Haplothe hypothalamus to regulate reproduction in a cichlid chromis burtoni, the effect of social interactions is evifish, Haplochromis burtoni (Fernald, 1994; Fernald, 1996). dent in the hypothalamo-pituitary-gonadal (HPG) axis of Reproduction is influenced by numerous environmales. Territorial males, characterized by aggressive mental factors, including photoperiod, temperature, and reproductive activity, have significantly larger hypofood availability and social interactions (reviewed in thalamic gonadotropin-releasing hormone (GnRH)-con-Wingfield and Kenagy, 1991). These diverse environtaining neurons and larger testes than nonterritorial mental cues must all be transduced by the nervous sysmales. Furthermore, a switch in the social status of an tem and ultimately act on the hypothalamo-pituitaryadult male causes a corresponding change in GnRH neugonadal (HPG) axis. However, different cues may act ron size and testis size. Here we show that the GnRH-containing neurons in at different sites of the HPG axis. For example, informathe hypothalamus of adult territorial males are also intion about the photoperiod appears to act on the hypofluenced by gonadal hormones. Castration of territorial thalamus, affecting neurons containing gonadotropinmales caused GnRH neurons to increase in size. This releasing hormone (GnRH) (Wingfield and Kenagy, neuronal hypertrophy in castrated animals was pre-1991). Secretion of GnRH regulates release of gonadovented either by testosterone (T) or 11-ketotestosterone tropin hormones (GtHs) from the pituitary, which in (KT) treatment. Estradiol (E2) treatment did not reduce turn stimulate gonadal growth and steroid hormone GnRH cell size in castrated animals. These results sugproduction. In contrast to photoperiod, temperature gest that androgens reduce the size of GnRH cells may not affect GnRH neurons and may instead act through negative feedback. Since E2 had no effect, anthrough other hypothalamo-pituitary axes to influence drogen influence on GnRH cell size appears to be indethe gonad (e.g., Wingfield et al., 1996). Social cues also pendent of aromatization. These data are consistent with the hypothesis that the setpoint for hypothalamic GnRH affect reproduction, but, depending on the species, it cell size is determined by social cues and that this setis unclear whether social cues affect GnRH neurons point is maintained by negative feedback from gonadal (Wingfield and Kenagy, 1991). Thus, all external cues androgens. ᭧ 1996 Academic Press, Inc. that influence reproduction have been found to act at the level of the HPG axis. Recent studies of an African cichlid fish, H. burtoni, have demonstrated that social status affects the HPG The ability of animals to integrate many environmenaxis of males. In H. burtoni, males are either territorial tal and internal signals to time reproduction approprior nonterritorial. Territorial males are dominant, agately has long been of interest (e.g., Lehrman, 1965). gressive, and reproductively active. In contrast, nonter-Only recently, however, have the techniques become ritorial males are less aggressive and do not reproduce available to pursue this question at the cellular and molecular levels of nervous system function. This re