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Neuroendocrine suppression of female courtship in a wild passerine: corticotropin-releasing factor and endogenous opioids.

During emergencies in their natural environments, vertebrates initiate coping mechanisms that redirect behavior away from nonessential activities and towards survival. Reproductive behaviors are suppressed. Evidence from field studies on passerine birds shows that this inhibition may not depend on the suppression of gonadal sex steroids, since during the breeding season they remain elevated despite activation of the stress response. We hypothesize that an alternate, central mechanism mediates the inhibition of reproductive behavior during stress in passerines. In this study, we tested the intracerebroventricular effects of endogenous opioids and corticotropin-releasing factor (CRF), neuropeptides implicated in the stress response, on courtship behavior in wild-caught female white-crowned sparrows. Beta-endorphin (beta-EN) significantly inhibited copulation solicitation, an estrogen-dependent courtship display, 30 min after treatment. Naloxone, an opioid antagonist, enhanced the behavior. CRF caused a suppression of solicitation that was reversible by pretreatment with naloxone, suggesting an intermediary role for endogenous opioids in CRF-induced suppression of courtship. The effects of beta-EN and CRF on solicitation appear to be independent of any general effects on locomotor activity. These results support our hypothesis that stress neuropeptides orchestrate coping behaviors in wild birds.

Adaptation, Psychological

Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster.

The medial nucleus of the amygdala is important for the neural control of reproductive behavior in the adult male Syrian hamster. Two types of signals are essential for this behavior, chemosensory stimuli and gonadal steroids; these signals appear to be received in different parts of the medial nucleus. The anterior region receives input from olfactory and vomeronasal systems, both of which are required for this behavior, whereas the posterior region receives gonadal hormone inputs. Behavioral studies have also suggested a functional differentiation of these two areas; electrolytic lesions of the anterior, but not the posterior, part eliminates normal sexual behavior. In this study, the efferent projections of the anterior and posterior divisions of the medial nucleus of the amygdala in the Syrian hamster were analyzed throughout the forebrain after injections of the anterograde neuronal tracer, Phaseolus vulgaris-leucoagglutinin. Neurons of the anterior, but not the posterior, medial nucleus, were found to project to numerous olfactory bulb projection areas and to the ventral striatopallidal complex. Within areas of the chemosensory circuitry that control reproductive behavior, the anterior region of the medial nucleus projects to the intermediate part of the posterior bed nucleus of the stria terminalis and the lateral part of the medial preoptic area, whereas the posterior region of the medial nucleus projects to the medial parts of these areas. Differences in targets were also observed in the ventromedial nucleus of the hypothalamus where the anterior region projects to the core while the posterior part projects to the shell of this nucleus. Furthermore, reciprocal projections between the anterior and posterior regions of the medial nucleus were observed. Taken together, these studies support the hypothesis that the anterior and posterior regions of the medial amygdaloid nucleus provide substantially different contributions to the control of reproductive behaviors.

Amygdala

Androgenic regulation of hypothalamic aromatase activity in prepubertal and postpubertal male golden hamsters.

Doses of testosterone that fully activate male reproductive behavior in castrated adult male hamsters fail to elicit mounting and intromissions in prepubertal castrates, even when circulating levels of testosterone are equivalent in the two age groups. We hypothesize that this differential responsiveness to testosterone is mediated at least in part by the efficacy with which testosterone in the hypothalamus is aromatized to estradiol, an important hormone mediating male sexual behavior. Therefore, hypothalamic aromatase activity, as measured by the conversion of [3H]testosterone to [3H]estradiol in tissue homogenates, was assessed in four separate experiments: 1) intact prepubertal and adult male golden hamsters, 2 and 3) castrated adult or prepubertal males that received either a 0- or 2.5-mg dose of testosterone, and 4) castrated adult and prepubertal males treated with the 2.5-mg dose oftestosterone. These studies demonstrate that hypothalamic aromatase activity is significantly higher in adult males compared with prepubertal males, and that hypothalamic aromatase activity is increased by testosterone to the same extent in both the adult and prepubertal male hamster. Therefore, the failure of testosterone-treated castrated prepubertal male hamsters to engage in the full suite of male reproductive behaviors is not due to the inability of testosterone to be converted into estradiol in the hypothalamus. Differences in the ability of testosterone to increase aromatase activity in other brain regions, or differences in the action of testosterone and/or estradiol on other cellular processes must account for the inability of testosterone to facilitate male reproductive behavior in juvenile males.

Aging

Prostaglandin induction of spawning behavior in Cichlasoma bimaculatum (Pisces cichlidae).

Prostaglandin (PG) stimulates female spawning behavior in goldfish and in some other teleosts in which female reproductive behaviors consist of postovulatory oviposition acts. This study examined the effects of PG on female sexual behavior in a teleost fish, Cichlasoma bimaculatum, in which female reproductive behaviors involve both preovulatory courtship and substrate cleaning behaviors, and post-ovulatory oviposition behavior. In females of established pairs, PGF2 alpha injection (5 micrograms, im) at any stage of the spawning cycle, or in the parental phase, rapidly induced substrate cleaning which soon merged into oviposition behavior (without egg release). These results support a role for PG in oviposition behavior of Cichlasoma. However, indomethacin (1 mg, ip), a PG synthesis inhibitor, did not block oviposition in ovulated females which had begun to spawn. Indomethacin may not have lowered PG levels sufficiently. Alternatively, as shown by J.J. Polder (1971, Neth. J. Zool. 21, 265), oviposition behavior may be induced or maintained by other factors associated with the spawning situation.

Animals

Daily variation of multiple behaviors in Aplysia fasciata: integration of feeding, reproduction, and locomotion.

Daily variations in feeding, reproductive behaviors, and activity level were examined under three conditions: (1) animals had access to food and mates; (2) there was access only to food; (3) neither food nor mates were present. Behaviors differed in amplitude of variations from their daily mean value. Egg-laying had the strongest tendency to be clustered. Amplitude of variations in courtship and swimming was larger than those of immobility, crawling, and feeding, while moving in place was the least clustered behavior. Changes in state affected the tendency to be clustered. When food and mates were present, amplitude of variations became progressively larger for immobility, moving in place, crawling, and swimming. Behaviors differed in the degree to which variations were patterned as a 1/day oscillation. Relatively little of the variability in crawling, moving in place, courtship, and egg-laying was due to a 1/day oscillation under any condition. By contrast, a large proportion of the variability of immobility, swimming, mating, and eating was modulated by a 1/day oscillation in at least one condition. The contribution of a 1/day oscillation to variability differed in the conditions examined. For immobility and swimming, when food and mates were present, the 1/day component of variability became smaller. By contrast, presence of mates led to an increase in the 1/day component of variability modulating feeding. Daily peaks of swimming and feeding were in phase with one another, and out of phase with mating and feeding. The ratio of locomotion to inactivity is constant, independent of change in external conditions. However, this ratio varied throughout the day. When food and mates were absent, variations of immobility and swimming were strongly related to variations in the inactivity ratio. When food and mates were added, this tendency decreased. The data suggest that daily variations in occurrence of behaviors can be accounted for by interactions between oscillators affecting Aplysia behavior and motivational variables. A 1/day oscillator has strong effects on mating, swimming, and immobility. The effect of the oscillator is modified by changes in motivational state.

Animals

Thyroid hormone and estrogen interact to regulate behavior.

Environmental perturbations that increase plasma thyroid hormone (T3) concentrations also profoundly affect female reproductive behavior and physiology. We explored whether these effects were mediated by interactions between T3 receptor (TR) and estrogen receptor (ER). This hypothesis was of interest because the half-site of a consensus T3 response element DNA sequence is identical to an ER response element (ERE), and TRs bind to a consensus ERE. Molecular data presented in the accompanying paper [Zhu, Y.-S., Yen, P.M., Chin, W.W.& Pfaff, D.W. (1996) Proc. Natl. Acad. Sci. USA 93, 12587-12592] demonstrate that TRs and ERs are both present in rat hypothalamic nuclear extracts and that both can bind to the promoter the hypothalamic gene preproenkephalin and that interations between liganded TRs and ERs affect preproenkephalin transcription. In this paper, we show that molecular interactions between TRs and ERs are sufficient to mediate environmental effects on estrogen-controlled reproductive behavior. Ovariectomized (OVX) rats treated with high doses of T3 showed significantly lower levels of lordosis behavior in response to estradiol benzoate (EB) compared with OVX females treated with EB alone. Conversely, thyroidectomized/OVX females treated with EB showed significantly greater levels of lordosis behavior compared with OVX females treated with EB, showing the effect of endogenous T3. Thyroid hormone interference with EB-induced behavior could not be explained by a reduction in plasma E2 concentrations or by a general reduction in responsiveness of EB-sensitive tissues. Moreover, numbers of hypothalamic ER-immunoreactive cells increased dramatically following T3 treatment. These data suggest that T3 may reduce EB-dependent sexual behavior through interactions between TR and ER in the nuclei of behaviorally relevant hypothalamic neurons, envisioning for the first time a functional consequence of interactions between two nuclear hormone receptors in brain. These results also open up the possibility of molecular interactions on DNA encoding environmental signals, a new field for the study of neuronal integration.

Animals

Thermal constraints on maternal behavior during reproduction in dwarf hamsters (Phodopus).

The chronic hyperthermia of lactating dwarf hamster (Phodopus) dams may constrain maternal behavior if contact with the litter further increases their body temperature, forcing the termination of nest bouts to dissipate the heat load. Changes in female body temperature and nest attendance in two species of dwarf hamster (P. campbelli and P. sungorus) were recorded each minute over the reproductive cycle. As the pups develop from naked poikilotherms to well-insulated thermoregulators, they function as heat sinks and heat sources. This role of pup development in maternal thermoregulation interacts with the dam's activity, primarily nocturnal wheel running, to produce a complex pattern of heating and cooling in each species. Contact with the pups is more constrained by maternal temperature during the inactive phase (day), and more constrained in P. campbelli than in P. sungorus. The interspecific difference in pup development or maternal thermoregulation is consistent with predictions based on biparental care, and a thermoregulatory role for the male in P. campbelli, but not in P. sungorus. These data suggest that environmental temperature and water availability are ecological variables that affect maternal thermoregulation, reproductive success, and the need for biparental care.

Acclimatization

Behavior and reproductive function of rat male offspring treated prenatally with 5-bromo-2'-deoxyuridine.

5-Bromo-2'-deoxyuridine (BrdU) was administered intraperitoneally to Sprague-Dawley rats at doses of 50 mg/kg/d on Days 9 through 15 and at 100 mg/kg/d on Days 16 through 20 of gestation. Dams were allowed to deliver naturally. Male offspring were subjected to a variety of pre- and postweaning behavioral tests: surface righting, negative geotaxis, open field test, Biel maze test, wheel cage test, and shuttlebox avoidance test. After puberty, masculine sexual behavior was observed. Male offspring of dams treated with BrdU on Days 9 through 15 of gestation showed an accelerated negative geotaxis reflex and increased ambulation and rearing in open field, while those of dams treated on Days 16 through 20 of gestation showed normal activity. Offspring of dams treated on Days 9 through 15 of gestation showed a higher activity level in the wheel cage than offspring of dams treated on Days 16 through 20 of gestation. In the Biel maze, offspring of dams treated on Days 9 through 15 of gestation showed impaired learning and memory. In the shuttlebox avoidance response, offspring of dams treated on Days 9 through 15 of gestation moved significantly more than offspring of dams treated on Days 16 through 20 of gestation. Masculine sexual behavior was markedly reduced in male offspring of dams treated on Days 9 through 15 of gestation. However, no significant differences between groups in blood pressure nor heart rate were noted. We conclude that male offspring of dams treated with BrdU on Days 9 through 15 of gestation are hyperactive without hypertension and that these offspring show an impairment of masculine sexual behavior, i.e., hyposexuality.

Analysis of Variance

Neuroanatomical distribution and variations across the reproductive cycle of aromatase activity and aromatase-immunoreactive cells in the pied flycatcher (Ficedula hypoleuca).

The anatomical distribution and seasonal variations in aromatase activity and in the number of aromatase-immunoreactive cells were studied in the brain of free-living male pied flycatchers (Ficedula hypoleuca). A high aromatase activity was detected in the telencephalon and diencephalon but low to negligible levels were present in the optic lobes, cerebellum, and brain stem. In the diencephalon, most aromatase-immunoreactive cells were confined to three nuclei implicated in the control of reproductive behaviors: the medial preoptic nucleus, the nucleus of the stria terminalis, and the ventromedial nucleus of the hypothalamus. In the telencephalon, the immunopositive cells were clustered in the medial part of the neostriatum and in the hippocampus as previously described in another songbird species, the zebra finch. No immunoreactive cells could be observed in the song control nuclei. A marked drop in aromatase activity was detected in the anterior and posterior diencephalon in the early summer when the behavior of the birds had switched from defending a territory to helping the female in feeding the nestlings. This enzymatic change is presumably controlled by the drop in plasma testosterone levels observed at that stage of the reproductive cycle. No change in enzyme activity, however, was seen at that time in other brain areas. The number of aromatase-immunoreactive cells also decreased at that time in the caudal part of the medial preoptic nucleus but not in the ventromedial nucleus of the hypothalamus (an increase was even observed), suggesting that differential mechanisms control the enzyme concentration and enzyme activity in the hypothalamus. Taken together, these data suggest that changes in diencephalic aromatase activity contribute to the control of seasonal variations in reproductive behavior of male pied flycatchers but the role of the telencephalic aromatase in the control of behavior remains unclear at present.

Animals

Endocrine events associated with spawning behavior in the sea lamprey (Petromyzon marinus).

Levels of estradiol, progesterone, and testosterone were determined in plasma of sea lamprey (Petromyzon marinus) undergoing certain behaviors associated with spawning in natural and artificial stream environments. Significantly higher levels of estradiol, progesterone, and testosterone were found in males than in females. In the artificial spawning channel, levels of estradiol were significantly higher in females exhibiting resting and swimming behaviors than in fanning, nest building, and spawning behaviors. No significant correlation was found with either progesterone or testosterone levels and the various reproductive behaviors. The data presented are the first experimental evidence that suggest gonadal steroids may be correlated with certain reproductive behaviors in the sea lamprey.

Aggression

Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice.

PRL is an anterior pituitary hormone that, along with GH and PLs, forms a family of hormones that probably resulted from the duplication of an ancestral gene. The PRLR is also a member of a larger family, known as the cytokine class-1 receptor superfamily, which currently has more than 20 different members. PRLRs or binding sites are widely distributed throughout the body. In fact, it is difficult to find a tissue that does not express any PRLR mRNA or protein. In agreement with this wide distribution of receptors is the fact that now more than 300 separate actions of PRL have been reported in various vertebrates, including effects on water and salt balance, growth and development, endocrinology and metabolism, brain and behavior, reproduction, and immune regulation and protection. Clearly, a large proportion of these actions are directly or indirectly associated with the process of reproduction, including many behavioral effects. PRL is also becoming well known as an important regulator of immune function. A number of disease states, including the growth of different forms of cancer as well as various autoimmune diseases, appear to be related to an overproduction of PRL, which may act in an endocrine, autocrine, or paracrine manner, or via an increased sensitivity to the hormone. The first step in the mechanism of action of PRL is the binding to a cell surface receptor. The ligand binds in a two-step process in which site 1 on PRL binds to one receptor molecule, after which a second receptor molecule binds to site 2 on the hormone, forming a homodimer consisting of one molecule of PRL and two molecules of receptor. The PRLR contains no intrinsic tyrosine kinase cytoplasmic domain but associates with a cytoplasmic tyrosine kinase, JAK2. Dimerization of the receptor induces tyrosine phosphorylation and activation of the JAK kinase followed by phosphorylation of the receptor. Other receptor-associated kinases of the Src family have also been shown to be activated by PRL. One major pathway of signaling involves phosphorylation of cytoplasmic State proteins, which themselves dimerize and translocate to nucleus and bind to specific promoter elements on PRL-responsive genes. In addition, the Ras/Raf/MAP kinase pathway is also activated by PRL and may be involved in the proliferative effects of the hormone. Finally, a number of other potential mediators have been identified, including IRS-1, PI-3 kinase, SHP-2, PLC gamma, PKC, and intracellular Ca2+. The technique of gene targeting in mice has been used to develop the first experimental model in which the effect of the complete absence of any lactogen or PRL-mediated effects can be studied. Heterozygous (+/-) females show almost complete failure to lactate after the first, but not subsequent, pregnancies. Homozygous (-/-) females are infertile due to multiple reproductive abnormalities, including ovulation of premeiotic oocytes, reduced fertilization of oocytes, reduced preimplantation oocyte development, lack of embryo implantation, and the absence of pseudopregnancy. Twenty per cent of the homozygous males showed delayed fertility. Other phenotypes, including effects on the immune system and bone, are currently being examined. It is clear that there are multiple actions associated with PRL. It will be important to correlate known effects with local production of PRL to differentiate classic endocrine from autocrine/paracrine effects. The fact that extrapituitary PRL can, under some circumstances, compensate for pituitary PRL raises the interesting possibility that there may be effects of PRL other than those originally observed in hypophysectomized rats. The PRLR knockout mouse model should be an interesting system by which to look for effects activated only by PRL or other lactogenic hormones. On the other hand, many of the effects reported in this review may be shared with other hormones, cytokines, or growth factors and thus will be more difficult to study. (ABSTRACT TRUNCATED)

Animals

Psychological factors affecting health after toxicological disasters.

Exposure to toxic substances in the environment is an ever more common event, that may cause physical as well as psychological harm. When an entire community is exposed, the term 'toxicological disaster' is used. The mere threat of such an event may be a source of stress, associated with changes in mental health, physical health, and changes in health-related behaviors. A review is presented of the literature about the effects of the stressful experience of toxicological disasters on health and health-related behaviors. Three questions are examined: (a) do toxicological disasters represent a specific type of stressor, different from other stressors?; (b) which stress-mediated health effects have been observed in the aftermath of toxicological disasters? and (c) is there evidence for a higher vulnerability in certain identifiable risk groups? On the basis of the available literature, it is concluded that toxicological disasters may have profound effects on subjective health, especially on symptom reporting, and on a number of psychophysiological parameters. Evidence for a substantial impact of disaster-related stress on either physical or psychiatric morbidity remains inconclusive. In this respect toxicological disasters do not appear to differ from other stressors. There is some evidence that toxicological disasters may have a more pronounced effect on health-related behaviors, especially on reproductive behavior (number of births and abortions). Women, and especially those who have young children to care for, appear to be more at risk for the observed health effects. The evidence for a higher vulnerability in other risk groups (e.g., former psychiatric patients remains inconclusive.

Adaptation, Psychological

The health of Navajo women: findings from the Navajo Health and Nutrition Survey, 1991-1992.

Cancer-screening behaviors, reproductive history, risk behaviors during pregnancy and chronic disease risk factors were examined in a representative sample of 566 Navajo women residing on the Navajo Reservation in 1991-1992. Among all women 15 y and older, 59% were overweight, 4% were current smokers, 10% currently used smokeless tobacco and 12% were anemic. Seventy-one percent of Navajo women aged 18 and older reported ever having had a Pap smear, but only 35% of women aged 50 and over reported ever having had a mammogram. Among parous women, the prevalence of having received no prenatal care for any pregnancy declined from 60% among women 60 and older to 13% among women 20-29 y of age, and the prevalence of ever having had a child born at home declined from 82 to 2%. These data suggest marked secular improvement in these pregnancy-related risk behaviors. However, data on cancer-screening behaviors indicate opportunities to improve health of Navajo women by increasing their use of mammography and Pap smear screening services.

Adolescent

Effect of transportation on sexual behavior of cats.

Transportation of an established feline colony approximately 1500 miles did not inhibit the resumption of behavioral reproductive cyclicity. Estrous behavior was observed as early as 18 days following shipment and mean duration of these first post-transfer estrous periods was normal. Relocation appeared to induce a synchronizing effect on behavioral cyclicity, since 76.2% and 42.9% of the population exhibited estrous onset during Days 18--31 and Days 24--26 respectively, following transport.

Animals