Editorial: Reproductive Neuroendocrinology and Social Behavior (original) (raw)
Related papers
Reproductive Neuroendocrine Pathways of Social Behavior
Frontiers in endocrinology, 2016
Social behaviors are key components of reproduction, because they are essential for successful fertilization. Social behaviors, such as courtship, mating, and aggression, are strongly associated with sex steroids, such as testosterone, estradiol, and progesterone. Secretion of sex steroids from the gonads is regulated by the hypothalamus-pituitary-gonadal (HPG) axis in vertebrates. Gonadotropin-releasing hormone (GnRH) is a pivotal hypothalamic neuropeptide that stimulates gonadotropin release from the pituitary. In recent years, the role of neuropeptides containing the C-terminal Arg-Phe-NH2 (RFamide peptides) has been emphasized in vertebrate reproduction. In particular, two key RFamide peptides, kisspeptin and gonadotropin-inhibitory hormone (GnIH), emerged as critical accelerator and suppressor of gonadotropin secretion. Kisspeptin stimulates GnRH release by directly acting on GnRH neurons, whereas GnIH inhibits gonadotropin release by inhibiting kisspeptin, GnRH neurons, or pit...
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
Variation in reproductive capacity is common across the lives of all animals. In vertebrates, hypothalamic neurons that secrete GnRH are a primary mediator of such reproductive plasticity. Since social interactions suppress gonadal maturity in the Afri- can cichlid fish, Astatotilapia (Haplochromis) burtoni, we inves- tigated whether the electrical properties of GnRH neurons were also socially regulated. Adult A. burtoni males are either terri- torial (T) and reproductively active or nonterritorial (NT) and reproductively regressed, depending upon their social environ- ment. We compared the basic electrical properties of hypotha- lamic GnRH neurons from T and NT males using whole-cell elec- trophysiology in vitro. GnRH neurons were spontaneously active and exhibited several different activity patterns. A small fraction of neurons exhibited episodic activity patterns, which have been described in GnRH neurons from mammals. The type of activity pattern and spontaneous firing rate did ...
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.
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 ...
Social Signals Regulate Gonadotropin-Releasing Hormone Neurons in the Green Treefrog
Brain, Behavior and Evolution, 2005
Animals coordinate their physiological state with external cues to appropriately time reproduction. These external cues exert effects through influences on the gonadotropin-releasing hormone neurons (GnRH), at the apex of the hypothalamus-pituitary-gonad (HPG) axis. In green treefrogs, mating calls are important regulators of reproductive behavior and physiology. Reception of mating calls causes an increase in androgen levels, and androgens promote the production of mating calls, demonstrating a mutual influence between the communication and endocrine systems. In order to investigate the central nervous system correlates of social regulation of the HPG axis in green treefrogs, we exposed males to a mating chorus or a control stimulus (tones), counted the resulting number of septo-preoptic GnRH-immunoreactive cells (GnRH-ir), and measured changes in plasma androgens. We found that reception of the mating chorus caused an increase in the number of GnRH-ir cells. As previously shown, we also found that the reception of the mating chorus resulted in higher androgen levels, suggesting that the higher GnRH-ir cell number represents increased GnRH production and release. We suggest that mating calls are an important supplementary cue that promotes GnRH production and release within the context of GnRH regulation by seasonal cues. Previous studies have proposed a neuroanatomical link between the anuran auditory system and GnRH neurons. Our results demonstrate a functional role for this proposed sensory-endocrine circuit, and show for the first time an influence of acoustic signals on GnRH neurons.
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.
Hypothalamic inhibition of socio-sexual behaviour by increasing neuroestrogen synthesis
Nature Communications, 2014
Gonadotropin-inhibitory hormone (GnIH) is a hypothalamic neuropeptide that inhibits gonadotropin secretion and socio-sexual behaviours. Oestrogen (neuroestrogen) synthesized in the brain from androgen by aromatase regulates male socio-sexual behaviours. Here we show that GnIH directly activates aromatase and increases neuroestrogen synthesis in the preoptic area (POA) and inhibits socio-sexual behaviours of male quail. Aromatase activity and neuroestrogen concentration in the POA are low in the morning when the birds are active, but neuroestrogen synthesis gradually increases until the evening when the birds become inactive. Centrally administered GnIH in the morning increases neuroestrogen synthesis in the POA and decreases socio-sexual behaviours. Centrally administered 17b-oestradiol at higher doses also inhibits socio-sexual behaviours in the morning. These results suggest that GnIH inhibits male socio-sexual behaviours by increasing neuroestrogen synthesis beyond its optimum concentration for the expression of socio-sexual behaviours. This is the first demonstration of any hypothalamic neuropeptide that directly regulates neuroestrogen synthesis.
Endocrine Journal
After the discovery of GnRH, GnRH neurons have been considered to represent the final common pathway for the neural control of reproduction. There is now compelling data in mammals that two populations of kisspeptin neurons constitute two different systems to control the episodic and surge release of GnRH/LH for the control of different aspects of reproduction, follicular development and ovulation. However, accumulating evidence indicates that kisspeptin neurons in nonmammalian species do not serve as a regulator of reproduction, and the non-mammalian species are believed to show only surge release of GnRH to trigger ovulation. Therefore, the GnRH neurons in non-mammalian species may offer simpler models for the study of their functions in neuroendocrine regulation of reproduction, especially ovulation. Our research group has taken advantage of many unique technical advantages of small fish brain for the study of anatomy and physiology of GnRH neurons, which underlie regular ovulatory cycles during the breeding season. Here, recent advances in multidisciplinary study of GnRH neurons are reviewed, with a focus on studies using small teleost fish models.