Axon-sparing lesion of the preoptic area enhances receptivity and diminishes proceptivity among components of female rat sexual behavior

Hoshina, Y; Takeo, Teruko; Nakano, Kyoko; Sato, Tatsusuke; Sakuma, Yasuo

doi:10.1016/0166-4328(94)90160-0

Cited by 132 publications

(69 citation statements)

References 39 publications

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“…Within the POA, implants of estradiol promote sexual behaviors in male mice (22,47,48). In female mice, lesions of the POA decrease proceptivity and increase receptivity in female mice, whereas electrical stimulation of the MPA led to persistent decreases in lordosis (49,50) without interfering with proceptivity (50). Microinjection of galanin bilaterally to the POA stimulates lordosis after EB priming, suggesting that an inhibitory tone on the MPA is necessary for lordosis to proceed (51).…”

Section: Discussionmentioning

confidence: 99%

siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice

Ribeiro

Musatov

Shteyler

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The medial preoptic area has been shown to be intricately involved in many behaviors, including locomotion, sexual behavior, maternal care, and aggression. The gene encoding estrogen receptor-α (ERα) protein is expressed in preoptic area neurons, and a very dense immunoreactive field of ERα is found in the preoptic region. ERα knockout animals show deficits in maternal care and sexual behavior and fail to exhibit increases in these behaviors in response to systemic estradiol treatment. In the present study, we used viralvector mediated RNA interference to silence ERα expression specifically in the preoptic area of female mice and measured a variety of behaviors, including social and sexual aggression, maternal care, and arousal activity. Suppression of ERα in the preoptic area almost completely abolished maternal care, significantly increasing the latency to pup retrieval and significantly reducing the time the moms spent nursing and licking the pups. Strikingly, maternal aggression toward a male intruder was not different between control and preoptic ERα-silenced mice, demonstrating the remarkably specific role of ERα in these neurons. Reduction of ERα expression in preoptic neurons significantly decreased sexual behavior in female mice and increased aggression toward both sexual partners and male intruders in a seminatural environment. Estrogen-dependent increases in arousal, measured by home cage activity, were not mediated by ERα expression in the preoptic neurons we targeted, as ERα-suppressed mice had increases similar to control mice. Thus, we have established that a specific gene in a specific group of neurons is required for a crucially important natural behavior.ating back to the 1970s, the preoptic region has been implicated in a variety of complex, natural, biologically crucial behaviors, ranging from sexual behavior to locomotion to maternal care. These roles for the preoptic region were first demonstrated using lesion studies; for instance, radiofrequency, electrolytic, and cytotoxic lesions of the medial preoptic area (MPA) were shown to disrupt many components of maternal care (1-6). Likewise, electrolytic lesions (7-9), chemical lesions (9-11), or knife-cuts disrupting preoptic afferents (12,13) all severely impair or abolish male sexual behavior, whereas electrical stimulation of this region enhances male copulatory behaviors (14). Additionally, c-Fos expression, a marker of neuronal activation, is significantly increased in the preoptic region following copulatory behaviors (15). With respect to locomotor activity, there is ample evidence demonstrating that electrical or chemical stimulation of preoptic neurons enhances locomotor activity in rats (16)(17)(18)(19).Given the importance of the preoptic region in mediating these complex biologically relevant hormone-dependent behaviors, the next step was to establish the cytochemical make-up of these populations of neurons. Before immunocytochemical techniques were routinely used, placement of hormone extracts was used to delineate the hormone and...

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Section: Discussionmentioning

confidence: 99%

siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice

Ribeiro

Musatov

Shteyler

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…MPO plays a gender-dependent role in reproductive behavior. In females, bilateral lesions of the MPO facilitate the occurrence of lordosis (Powers and Valenstein, 1972;Nance et al, 1977;Rodriguez-Sierra and Terasawa, 1979;Lisk and MacGregor, 1982;Hoshina et al, 1994); chemical or electrical stimulation of MPO suppresses it (Moss et al, 1974;Zasorin et al, 1975;Pfaff and Sakuma, 1979;Takeo et al, 1993). By contrast, in males MPO lesions completely abolish mounting, intromission, and ejaculation, whereas stimulation of this region induces copulation (Heimer and Larrson, 1966;Lisk, 1966;Malsbury et al, 1981;Hansen et al, 1982;Arendash and Gorski, 1983;Edwards and Einhorn, 1986).…”

Section: Reproductivementioning

confidence: 99%

“…Taken together, these results suggest that the MPO + PAG + RVM projection constitutes a functional pathway. This circuit may coordinately regulate neuroendocrine, motor, and autonomic adjustments necessary for the elaboration of sexual behaviors.Key words: reproduction; antinociception; cardiovascular regulation; brainstem; sexual behavior; immunohistochemistryThe medial preoptic area (h/[PO) is a sexually dimorphic structure Simerly et al, 1984;Bloch and Gorski, 1988) that plays a pivotal role in sexual behavior and neuroendocrine function (Lisk, 1966;Powers and Valenstein, 1972;Pfaff and Sakuma, 1979;Hansen et al, 1982;Arendash and Gorski, 1983;Kalra and Kalra, 1983;Docke et al, 1984;Sachs and Meisel, 1988;Simerly et al, 1990;DonCarlos et al, 1991;Takeo et al, 1993;Hoshina et al, 1994). We recently reported that MPO robustly innervates the midbrain periaqueductal gray (PAG) (Rizvi et al, 1992) and terminates in discrete, longitudinally organized columns running through the rostrocaudal axis of PAG.…”

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confidence: 99%

Medial preoptic area afferents to periaqueductal gray medullo-output neurons: a combined Fos and tract tracing study

et al. 1996

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We have shown recently that the medial preoptic area (MPO) robustly innervates discrete columns along the rostrocaudal axis of the midbrain periaqueductal gray (PAG). However, the location of PAG neurons responsive to MPO activation is not known. Anterograde tract tracing was used in combination with Fos immunohistochemistry to characterize the MPO -+ PAG pathway anatomically and ,functionally within the same animal. Focal electrical or chemical stimulation of MPO in anesthetized rats induced extensive Fos expression within the PAG compared with sham controls. Fos-positive neurons were organized as 2-3 longitudinal columns. The organization and location of these columns overlapped remarkably well with the distribution of fibers and terminals in PAG labeled by Phaseolus vulgaris leucoagglutinin (PHA-L) injected into the same MPO stimulation site. This indicates that MPO inputs may terminate on the soma or proximal dendrites of neurons exhibiting elevated Fos. A second series of experiments investigated whether MPO stimulation excited PAG neurons with descending projections to the medulla. Retrograde labeling of PAG neurons projecting to the medial and lateral regions of the rostroventral medulla (RVM) was combined with MPO-induced Fos expression. The results showed that a substantial population (3743%)of Fos-positive PAG neurons projected to the ventral medulla. This indicates that MPO stimulation engages PAG-medullary output neurons. Taken together, these results suggest that the MPO + PAG + RVM projection constitutes a functional pathway. This circuit may coordinately regulate neuroendocrine, motor, and autonomic adjustments necessary for the elaboration of sexual behaviors.Key words: reproduction; antinociception; cardiovascular regulation; brainstem; sexual behavior; immunohistochemistryThe medial preoptic area (h/[PO) is a sexually dimorphic structure Simerly et al., 1984;Bloch and Gorski, 1988) that plays a pivotal role in sexual behavior and neuroendocrine function (Lisk, 1966;Powers and Valenstein, 1972;Pfaff and Sakuma, 1979;Hansen et al., 1982;Arendash and Gorski, 1983;Kalra and Kalra, 1983;Docke et al., 1984;Sachs and Meisel, 1988;Simerly et al., 1990;DonCarlos et al., 1991;Takeo et al., 1993;Hoshina et al., 1994). We recently reported that MPO robustly innervates the midbrain periaqueductal gray (PAG) (Rizvi et al., 1992) and terminates in discrete, longitudinally organized columns running through the rostrocaudal axis of PAG.PAG plays a key role in antinociception (Reynolds, 1969;Liebeskind et al., 1973;Oliveras et al., 1974;Behbehani and Fields, 1979; Lovick, 3985;Morgan and Liebeskind, 1987;Reichling et al., 1988;Lovick, 1990), cardiovascular control (Lovick, 1985;Carrive et al., 1987;Carrive et al., 1988;Carrive et al., 1989a;Lovick, 1990;Verberne and Guyenet, 1992;Murphy et al., 1994a;Murphy et al., 1995), and many of the same neuroendocrine and reproductive functions as MPO (Pfaff and SchwartzGiblin, 1988;Ogawa et al., 1991;Shipley et al., 1995). PAG neurons involved in these functions also are ...

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“…The present results emphasize that estrogen elicits lordosis reflex via excitation of efferent VMN neurons to the CG, whereas estrogen inhibits neurons in the preoptic and ventral tegmental continuum to exert the same behavioral effect [42][43][44]. Electrical stimulation of the VMN enhanced the reflex [10].…”

Section: Methodmentioning

confidence: 76%

Temporal Coincidence between the Excitation of Ventromedial Hypothalamic Efferents and the Induction of Lordosis Reflex in Ovariectomized Estrogen-Primed Rats.

1998

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Abstract. The temporal changes in excitability in ventromedial hypothalamic neurons which project to the midbrain central gray caused by chronic estrogen exposure were measured in ovariectomized rats. In 66 urethane-anesthetized animals which had either no capsule, or had a capsule containing estrogen implanted for 24 h, 48 h, 72 h or 96 h, 189 antidromic action potentials were recorded in the ventromedial hypothalamus (VMN) in response to stimulation of the midbrain central gray (CG). The antidromic activation threshold was lower in 40 recordings made from the VMN in the 72-h or 96-h group than in 67 from the no-treatment, 24-h or 48-h group. The decrease in the threshold coincided with the emergence of the lordosis reflex. In a separate cohort of ovariectomized rats, any absence of estrogen for 2-48 h before and during the measuring abolished the neuronal as well as the behavioral effects at 72 h. The results suggest that the lordosis reflex induced by estrogen alone depends on the excitation of VMN efferents to the CG. In addition, the indispensability of estrogen at the time of electrophysiological and behavioral evaluation indicates that a certain direct neural action of estrogen is involved in the behavioral activation. Implants of minute amounts of crystalline estradiol showed that the ventromedial nucleus of the hypothalamus (VMN) is the principal site for estrogen action to facilitate the lordosis reflex [9]. Stimulation and lesion studies have shown that the VMN facilitates the lordosis reflex via its descending projection to the midbrain central gray (CG) [10][11][12]. Estrogen-induced excitation of VMN neurons with axons to the CG in ovariectomized rats [13][14][15] corroborates the behavioral results. Experiments on neonatally gonadectomized males and neonatally androgenized females, in which the neural effects of estrogen in parallel with its behavioral capability to induce the lordosis reflex [16], provide additional evidence for the association of the neural effect of estrogen with facilitation of the lordosis reflex.In the present study we attempted to establish a

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Axon-sparing lesion of the preoptic area enhances receptivity and diminishes proceptivity among components of female rat sexual behavior

Cited by 132 publications

References 39 publications

siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice

siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice

Medial preoptic area afferents to periaqueductal gray medullo-output neurons: a combined Fos and tract tracing study

Temporal Coincidence between the Excitation of Ventromedial Hypothalamic Efferents and the Induction of Lordosis Reflex in Ovariectomized Estrogen-Primed Rats.

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