Hypothalamic Serotonin Lesions Unmask Hormone Responsiveness of Lordosis Behavior in Adult Male Rats

Moreines, Judith; Kelton, M M; Luine, Victoria N.; Pfaff, Donald W.; McEwen, Bruce S.

doi:10.1159/000124949

Cited by 29 publications

(12 citation statements)

References 29 publications

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“…We previously hypothesized that 5-HT fibers contribute to the suppression of the lordosis response in males. This postulate is consistent with numerous studies showing that lesions within the VMNvl can restore lordosis behavior in male rats (Kakeyama and Yamanouchi, 1994; Moreines et al, 1988). In PPT exposed females, however, even though 5-HT levels appear to be elevated to male-typical levels, we found no concomitant decrease in female sexual behavior indicating that other neurotransmitters may be involved in abrogating this response.…”

Section: Discussionsupporting

confidence: 92%

The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat

et al. 2011

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Now under intense scrutiny, due to its endocrine disrupting properties, the potential threat the plastics component bisphenol-a (BPA) poses to human health remains unclear. Found in a multitude of polycarbonate plastics, food and beverage containers, and medical equipment, BPA is thought to bind to estrogen receptors (ERs), thereby interfering with estrogen-dependent processes. Our lab has previously shown that exposure to BPA (50mg/kg bw or 50μg/kg bw) during the neonatal critical period is associated with advancement of puberty, early reproductive senescence and ovarian malformations in female Long-Evans rats. Here, using neural tissue obtained from the same animals, we explored the impact of neonatal BPA exposure on the development of sexually dimorphic hypothalamic regions critical for female reproductive physiology and behavior. Endpoints included quantification of oxytocin-immunoreactive neurons (OT-ir) in the paraventricular nucleus (PVN), serotonin (5-HT-ir) fiber density in the ventrolateral subdivision of the ventromedial nucleus (VMNvl) as well as ERα-ir neuron number in the medial preoptic area (MPOA), the VMNvl, and the arcuate nucleus (ARC). Both doses of BPA increased the number of OT-ir neurons within the PVN, but no significant effects were seen on 5-HT-ir fiber density or ERα-ir neuron number in any of the areas analyzed. In addition to hypothalamic development, we also assessed female sex behavior and body weight. No effect of BPA on sexual receptivity or proceptive behavior in females was observed. Females treated with BPA, however, weighed significantly more than control females by postnatal day 99. This effect of BPA on weight is critical because alterations in metabolism, are frequently associated with reproductive dysfunction. Collectively, the results of this and our prior study indicate that the impact of neonatal BPA exposure within the female rat hypothalamus is region specific and support the hypothesis that developmental BPA exposure may adversely affect reproductive development in females.

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Section: Discussionsupporting

confidence: 92%

The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat

et al. 2011

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“…The 5-H T|a ago nist, 8 -O H -D P A T , has been shown to inhibit female sex behavior and enhance male sexual behavior [26], Sex dif ferences have also been found following 5,7-DHT-induced denervation. Intrahypothalamic 5,7-D H T injec tion increased dendritic spine density in the V M N o f both sexes but was further enhanced by E in females only [7], In addition, 5,7-DHT-induced lordosis in male rats re quires different hormonal priming than that of female rats and the lordosis quotient in male rats is always lower than female rats [18,27].…”

Section: Discussionmentioning

confidence: 83%

Effect of 5,7-Dihydroxytryptamine, Ovariectomy and Gonadal Steroids on Serotonin Receptor Binding in Rat Brain

et al. 1994

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Quantitative autoradiography was used to assess alterations in serotonin (5-HT) receptor binding in the hypothalamus and hippocampus following denervation with 5, 7-dihydroxytryptamine (5, 7-DHT), ovariectomy (OVX) and gonadal steroid manipulation. Seven days after 5, 7-DHT injection, 5-HT_1a receptor density was significantly increased in the ventromedial hypothalamic nucleus (VMN) of intact but not OVX femaled rats. Under these conditions 5-HT_1b receptor density was unchanged in any brain region examined and 5-HT transporter binding was decreased in all 5, 7-DHT injected animals. In addition, there was a significant interaction between OVX and 5, 7-DHT for both the 5-HT_1a receptor and the 5-HT transporter in the VMN, such that OVX inhibited the 5, 7-DHT-induced increase in 5-HT_1a receptors and attenuated the 5, 7-DHT-induced decrease in 5-HT transporter binding. In a separate experiment the effect of gonadal steroid manipulation on 5-HT receptor binding was assessed. In female OVX rats, 5-HT_1a receptor density was unchanged by estrogen or estrogen and progesterone administration. In male rats, castration significantly decreased 5-HT_1a receptor density in the medial preoptic area. Estrogen and progesterone administration to female OVX rats increased the density of 5-HT_1b receptors in the VMN, as compared to estrogen alone. The relationship of these results to the role of 5-HT in mediating lordosis behavior is discussed.

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“…In addition, 5-HT terminals in the VMN appear to tonically inhibit the expression of lordosis [2,3,6,24], More recently, 8-OH-DPAT, a 5-HTU agonist which in hibits lordosis when given peripherally [5,6], was shown to inhibit induction of lordosis on proestrus when applied intracranially to the VMN [4]. Consistent with this inhibitory influence on lordosis, progesterone administration to es tradiol benzoate (EB)-primed females, in doses sufficient to induce lordosis, is associated with decreased VMN 5-HT activity [7][8][9], The data obtained here are consistent with the results of these previous studies and suggest that 5-HT terminals in the VMN contribute to activation of lor dosis on proestrus through disinhibition.…”

Section: Serotonergic System and Lordosis Respondingmentioning

confidence: 99%

Serotonin, Catecholamines and Metabolites in Discrete Brain Areas in Relation to Lordotic Responding on Proestrus

Luine¹

1993

Neuroendocrinology

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Levels of serotonin (5-HT) and metabolite, 5-hydroxyindole-acetic acid (5-HIAA), dopamine and metabolites, dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA), and norepinephrine (NE) were measured in microdissected brain areas at 14.30 and 19.30 h on diestrus and proestrus in rats. Lordosis, sexual behavior, was exhibited only by proestrous females at 19.30 h. The content of monoamines and/or metabolites changed from afternoon to early evening of diestrus in a number of brain regions. On proestrus, during the time when females became sexually receptive, additional changes appeared and many diestrous changes were reversed or amplified. Proestrus-specific changes were found in areas provinding the descending circuit for regulation of lordosis, the medial preoptic nucleus (mPOA), ventromedial nucleus of the hypothalamus (VMN) and midbrain central gray (MCG), and in areas outside of endocrine control centers such as parietal cortex (Ctx) and dorsal raphe nucleus (DR). Thus, these data are consistent with previous studies showing functional changes in monoaminergic transmitters during the day/night cycle and during hormonal induction of neuroendocrine events. NE levels increased between 14.30 and 19.30 h on proestrus in most brain areas, ranging from 20% increases in mPOA and Ctx to a 220% increase in the DR. NE levels decreased on proestrus in the VMN. The direction of proestrous changes in NE were reversed in some, but not all of the areas, between the afternoon and evening of diestrus. Dopamine was detectable in all areas sampled, and the metabolites HVA and DOPAC were detectable in some but not all areas. In the mPOA, DOPAC increased 100% during proestrus but was unchanged during the same period on diestrus suggesting a facilitatory effect of dopamine on lordosis in this area. Dopamine terminals in the MCG may inhibit behavior since HVA increased 150% between 14.30 and 19.30 h on diestrus and decreased 40% during the same interval on proestrus. For the serotonergic system, 5-HIAA levels increased 45% in the mPOA and 200% in the MCG from the afternoon to evening of proestrus but did not change on diestrus. In the VMN, 5-HIAA increased 60% between 14.30 and 19.30 h on diestrus but did not change during the same time on proestrus. 5-HIAA also increased 580% in the DR nucleus and 70% in the Ctx during proestrus but not diestrus. These data are consistent with previous studies suggesting that 5-HT terminals regulate lordosis responding on proestrus through hormone-dependent modulations at both facilitatory and inhibitory sites. In the VMN, where 5-HT inhibits lordosis, gonadal hormones appear to decrease the availability of 5-HT, and in the mPOA and MCG, where 5-HT may facilitate lordosis, gonadal hormones appear to increase the availability of 5-HT.

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Hypothalamic Serotonin Lesions Unmask Hormone Responsiveness of Lordosis Behavior in Adult Male Rats

Cited by 29 publications

References 29 publications

The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat

The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat

Effect of 5,7-Dihydroxytryptamine, Ovariectomy and Gonadal Steroids on Serotonin Receptor Binding in Rat Brain

Serotonin, Catecholamines and Metabolites in Discrete Brain Areas in Relation to Lordotic Responding on Proestrus

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