Ovarian steroids and sexual interaction alter oxytocinergic content and distribution in the basal forebrain

Caldwell, Jack D.; Jirikowski, Gustav F.; Greer, E.Rosalie; Stumpf, Walter E.; Pedersen, Cort A.

doi:10.1016/0006-8993(88)90882-7

Cited by 80 publications

(46 citation statements)

References 40 publications

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“…In contrast, in the caudal PeV, estrogen treatments significantly reduced the levels of OXT mRNA. The in situ hybridization technique verified the location of OXTproducing cells as suggested previously by immunocytochemical studies (6,7). The shifts in OXT mRNA levels seen with estrogen treatments suggest that in .ritu hybridization is useful not only as a marker for OXT synthesizing cells but also in detecting changes in OXT synthesis with steroid condition at the cellular level.…”

Section: Discussionsupporting

confidence: 78%

“…Jirikowski et al (6,7). In the present study these regions had positively hybridized cells with low grain densities.…”

Section: Discussionsupporting

confidence: 59%

“…The POA and AH are important for steroid mediation of maternal (24) and sexual behaviors (25,26). Evidence that OXT infusions into the MPOA enhance female sexual receptivity (1 1, 12) and that mating alters levels of immunoreactive OXT in the MPOA (7,12) increases interest in how estrogen controls OXT physiology in the POA. Cells in the rostra1 LSN have processes extending into the septum (6) suggesting central projection sites.…”

Section: Discussionmentioning

confidence: 99%

“…PeV oxytocinergic neurons send their processes parallel to the ependymal wall of the third ventricle. Both of these areas show changes in OXT distribution between the sexes and after mating (7,27). With the importance of OXT and the POA in reproductive behavior it is perhaps not surprising the degree to which preoptic OXT production is responsive to estrogen.…”

Section: Discussionmentioning

confidence: 99%

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Estrogen Alters Oxytocin mRNA Levels in the Preoptic Area

Caldwell

Brooks

Jirikowski

et al. 1989

J Neuroendocrinology

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Estrogen has numerous effects on immunoreactive levels of oxytocin (OXT) centrally, particularly in the preoptic lateral subcommissural nucleus (LSN). In this study in situ hybridization of a 38-base oligodeoxyribonucleotide (38mer) complementary to OXT mRNA revealed that estrogen treatment altered the pattern of OXT production in the rostral LSN and the more caudal anterior commissural nucleus. Rats were injected with 20 pg estradiol benzoate or sesame oil vehicle im 4 and 5 days after ovariectomy. On the sixth day all animals were perfused with paraformaldehyde-glutaraldehyde and their brains sectioned to 10 pm thickness in a -10 "C cryostat. Coronal brain sections were taken from four parallel levels of the preoptic-anterior hypothalamic area. These sections were mounted and hybridized insifu to a [1'25]-labeled 38mer for 16 h at 37 "C. Washed and dried slides were processed for autoradiography and analyzed with a light microscope. The effect of estrogen on OXT production differed between the rostral and caudal sections in both the LSN and periventricular (PeV) areas. Estrogen significantly increased OXT mRNA levels in LSN cells while decreasing hybridization in the anterior commissural nucleus cells. Changes in frequency patterns in the PeV paralleled those in the LSN with a significant drop of hybridization in the caudal PeV. Neurons hybridizing 38mer probe were also found in several other areas including the ventral medial preoptic area, lateral hypothalamus, bed nucleus of the stria terminalis and the nucleus triangularis septi. OXT mRNA levels were affected by estrogen treatments and this effect differed between the preoptic area and anterior hypothalamus. The sensitivity of LSN oxytocinergic cells to estrogen has implications for estrogen-sensitive OXT-enhanced reproductive behaviorsThe ovarian steroid estrogen influences oxytocin (OXT) physiology in the CNS. Estrogen treatments increase OXT release from Ihe posterior pituitary (1) and increase firing of oxytocinergic neurons in the paraventricular nucleus (PVN) (2). Levels of immunoreactive OXT in the PVN vary with estrous state in ways {hat suggest estrogen's influence (3). OXT immunoreactive levels :tho increase in the PVN and supraoptic nucleus (SON) peripar-I um as estrogen levels increase, while OXT levels in more rostral synthesis sites are decreasing (4).The preoptic area (POA) sites of OXT synthesis are particularly sensitive to estrogen influence. Estrogen implants increased OXT immunoreactive content in the POA (5). Short-term treatment with silastic implants of estradiol increased the number of OXT i~nmunostained cells in the periventricular (PeV) and dorsolateral I' OA as well as in several other sites (6). The collection of oxytocinergic cells ventrolateral of the anterior commissure in the dorsolateral POA and overlapping the septohypothalamic nucleus and bed nucleus of the stria terminalis (BnST) has been called the lateral subcommissural nucleus (LSN) (6, 7). Oxytocinergic cells in the LSN showed increased immunostaining after s...

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Section: Discussionsupporting

confidence: 78%

“…Jirikowski et al (6,7). In the present study these regions had positively hybridized cells with low grain densities.…”

Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Estrogen Alters Oxytocin mRNA Levels in the Preoptic Area

Caldwell

Brooks

Jirikowski

et al. 1989

J Neuroendocrinology

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“…In contrast, central OT release is known to be involved in several reproductive behaviors, including facilitation of the onset of sexual and maternal behavior (22). CS has been shown to alter OT receptor affinity and density in the medial preoptic area (9) and to increase the expression of c-Fos in OT neurons of the parvicellular paraventricular nucleus. These neurons release OT centrally and into the median eminence (38) and hence to the anterior pituitary through the long portal vessels, which very likely influences circadian PRL secretion.…”

Section: Discussionmentioning

confidence: 99%

Systemic oxytocin induces a prolactin secretory rhythm via the pelvic nerve in ovariectomized rats

Helena

Cristancho-Gordo

González-Iglesias

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Helena CV, Cristancho-Gordo R, Gonzalez-Iglesias AE, Tabak J, Bertram R, Freeman ME. Systemic oxytocin induces a prolactin secretory rhythm via the pelvic nerve in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 301: R676 -R681, 2011. First published June 15, 2011 doi:10.1152/ajpregu.00176.2011.-We have shown previously that an intravenous injection of oxytocin (OT) in ovariectomized (OVX) rats initiates a circadian rhythm of prolactin (PRL) secretion similar to that observed after cervical stimulation (CS). In this study, we investigated the pathway through which OT triggers the PRL rhythm. We first tested whether an intracerebroventricular injection of OT could trigger the PRL secretory rhythm. As it did not, we injected OT intravenously while an OT receptor antagonist was infused intravenously. This antagonist completely abolished the PRL surges, suggesting that a peripheral target of OT is necessary for triggering the PRL rhythm. We hypothesized that OT may induce PRL release, which would be transported into the brain and trigger the rhythm. In agreement with this, OT injection increased circulating PRL by 5 min. To test whether this acute increase in PRL release would induce the PRL rhythm, we compared the effect of intravenously administered thyrotropin-releasing hormone (TRH) and OT. Although TRH injection also increased PRL to a comparable level after 5 min, only OT-injected animals expressed the PRL secretory rhythm. Motivated by prior findings that bilateral resection of the pelvic nerve blocks CS-induced pseudopregnancy and OT-induced facilitation of lordosis, we then hypothesized that the OT signal may be transmitted through the pelvic nerve. In fact, OT injection failed to induce a PRL secretory rhythm in pelvic-neurectomized animals, suggesting that the integrity of the pelvic nerve is necessary for the systemic OT induction of the PRL secretory rhythm in OVX rats. oxytocin receptor; pseudopregnancy; lactotrophs MATING OR CERVICAL STIMULATION (CS) induces a circadian rhythm of prolactin (PRL) secretion in female rats, consisting of nocturnal (0300) and diurnal (1700) surges. The rhythm persists for 10 -12 days, which is about half the duration of pregnancy (19). As the rhythm in secretion continues for several days without additional stimuli, it has been suggested that a hypothalamic "memory" is activated by CS and acts to sustain the daily PRL surges (17). This rhythm can be produced in ovariectomized (OVX) rats, demonstrating that the memory does not require ovarian steroids (43). Despite these findings, the mechanism by which the memory is triggered is not understood.PRL secretion by lactotrophs is tonically inhibited by hypothalamic dopamine (DA) (3,11). Whereas the full generation of PRL surges requires a decrease in DA inhibition, the actions of one or more stimulating factors are also needed (16, 18). Several lines of evidence suggest that oxytocin (OT) may act as a PRL-releasing factor to induce PRL surges in several physiological paradigms (23, 39, 40), including mating. Beca...

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Estrogen influences on oxytocin mRNA expression in preoptic and anterior hypothalamic regions studied by in situ hybridization

Chung

McCabe

Pfaff

1991

J of Comparative Neurology

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Possible estrogen influences on oxytocin mRNA expression were studied in preoptic and anterior hypothalamic regions as might be important for behavioral as well as neuroendocrine controls. In situ hybridization for oxytocin mRNA determination was supported by immunocytochemical identification and was compared with vasopressin mRNA in situ hybridization. With these techniques, oxytocin-expressing neurons were identified in medial preoptic, anterior commissural, periventricular, paraventricular, supraoptic, and perifornical nuclei as well as the bed nucleus of the stria terminalis and intersupraopticoparaventricular (internuclear) islands. Distribution and number of oxytocin mRNA-containing neurons and oxytocin mRNA levels were compared between ovariectomized control rats given cholesterol implants and ovariectomized rats given short-term (2 days) or long-term (2 months) estradiol treatment (10% estradiol, subcutaneous silastic implants). Effectiveness of long-term estrogen treatment was confirmed behaviorally. While there was a trend in several cell groups for a larger number of oxytocin-mRNA-containing neurons to be observed following 2 days of estrogen treatment, this was not statistically significant. Moreover, additional oxytocin-mRNA containing cell groups were not seen after short or long estradiol treatment. With computer-aided analysis, mean pixels per oxytocin-mRNA expressing neuron (reflecting oxytocin mRNA content) were compared between groups: In the supraoptic nucleus and the anterior commissural nucleus, these were increased both by 2 days and 2 months of estradiol treatment. These differences may be important in modulating female reproductive behavior. Present findings also suggest that estradiol can affect the oxytocinergic system via an indirect route since the cell groups influenced here by estradiol do not contain estrogen receptors. Oxytocinergic neurons may serve as a good system to compare direct transcriptional with indirect effects of hormones.

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Ovarian steroids and sexual interaction alter oxytocinergic content and distribution in the basal forebrain

Cited by 80 publications

References 40 publications

Estrogen Alters Oxytocin mRNA Levels in the Preoptic Area

Estrogen Alters Oxytocin mRNA Levels in the Preoptic Area

Systemic oxytocin induces a prolactin secretory rhythm via the pelvic nerve in ovariectomized rats

Estrogen influences on oxytocin mRNA expression in preoptic and anterior hypothalamic regions studied by in situ hybridization

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