Central sites mediating reproductive responses to melatonin in juvenile male Siberian hamsters

doi:10.1016/0006-8993(92)90172-6

Brain Research

Volume 598, Issues 1–2, 11 December 1992, Pages 98-106

https://doi.org/10.1016/0006-8993(92)90172-6 Get rights and content

Abstract

Juvenile male Siberian hamsters received infusions of varying doses of melatonin (MEL), or saline vehicle, via microdialysis probes implanted in brain regions which have previously been shown to contain MEL receptors. Daily infusions were 10 h in length and occurred during exposure to constant light on days 22–34 of age. All animals were sacrificed on day 35 and paired testis weights recorded prior to preparation of the brain tissue for histological evaluation of the infusion site. Some animals were also blood-sampled prior to sacrifice for determination of circulating levels of prolactin (PRL). Saline infusions did not have a significant effect upon gonadal maturation, regardless of the infusion site, when compared with unoperated control animals reared under similar photoperiod conditions. In contrast, animals which received infusions of 75 pg MEL into the suprachiasmatic nucleus (SCN), paraventricular nucleus of the thalamus, or nucleus reuniens regions, showed a marked inhibition of gonadal growth. Infusions of this dose of MEL into various other neural regions (e.g. lateral hypothalamus, ventromedial nucleus of the hypothalamus, paraventricular nucleus of the hypothalamus) did not result in decreased testis weights at the time of sacrifice. Daily administration of 20 pg MEL inhibited gonadal maturation and resulted in decreased circulating PRL levels only when infused into the SCN region. For animals receiving the 7.5 pg dose, infusions into the midline thalamic nuclei were not successful in inhibiting testis growth, and infusions in the SCN region had only a marginal effect. These results indicate that endogenous MEL may influence at least one seasonal response in this species, i.e. reproductive responses to photoperiod, by acting at some or all of these central MEL binding sites.

References (50)

BrownM.H. et al.
Evidence that neurons of the paraventricular nucleus of the hypothalamus with projections to the spinal cord are sensitive to the toxic effects of N-methylaspartic acid
Neurosci. Lett.
(1987)
CarlsonL.L. et al.
Melatonin receptors and signal transduction during development in Siberian hamsters (Phodopus sungorus)
Dev. Brain Res.
(1991)
CassoneV.M. et al.
Entrainment of rat circadian rhythms by daily injection of melatonin depends upon the hypothalamic suprachiasmatic nucleus
Physiol. Behav.
(1986)
HastingsM.H.
Neuroendocrine rhythms
Pharmac. Ther.
(1991)
HastingsM.H. et al.
Intra-hypothalamic melatonin blocks photoperiodic responsiveness in the male Syrian hamster
Neuroscience
(1988)
KleinD.C. et al.
Pineal N-acetyltransferase and hydroxyindole-O-methyltransferase: control by the retinohypothalamic tract and the suprachiasmatic nucleus
Brain Res.
(1979)
LehmanM.N. et al.
Role of the hypothalamic paraventricular nucleus in neuroendocrine responses to daylength in the Golden hamster
Brain Res.
(1984)
MasonR. et al.
The electrophysiological effects of melatonin and a putative melatonin antagonist (N-acetyltryptamine) on rat suprachiasmatic neurones in vitro
Neurosci. Lett.
(1988)
MasonR. et al.
Neurophysiological responses to melatonin in the SCN of short-day sensitive and refractory hamster
Brain Res.
(1990)
McArthurA.J. et al.
Melatonin directly resets the rat suprachiasmatic circadian clock in vitro
Brain Res.
(1991)

PickardG.E. et al.

The hypothalamic paraventricular nucleus mediates the photoperiodic control of reproduction but not effects of light on the circadian rhythm of activity

Neurosci. Lett.

(1983)

ShibataS. et al.

Effects of melatonin on neuronal activity in the rat suprachiasmatic nucleus in vitro

Neurosci. Lett.

(1989)

VanecekJ. et al.

Short days induce changes in specific melatonin binding in hamster median eminence and anterior pituitary

Brain Res.

(1989)

VanecekJ. et al.

Hypothalamic melatonin receptor sites revealed by autoradiography

Brain Res.

(1987)

BartnessT.J. et al.

SCN lesions block responses to systemic melatonin infusions in Siberian hamsters

Am. J. Physiol.

(1991)

BerriaM. et al.

Lesions to the anterior hypothalamus prevent the melatonin-induced lengthening of delayed implantation

Endocrinology

(1989)

BittmanE.L. et al.

Suprachiasmatic and paraventricular control of photoperiodism in Siberian hamsters

Am. J. Physiol.

(1991)

BittmanE.L. et al.

Influences of the paraventricular and suprachiasmatic nuclei and olfactory bulbs on melatonin responses in the golden hamster

Biol. Reprod.

(1989)

BittmanE.L. et al.

Testicular responses to melatonin are altered by lesions of the suprachiasmatic nuclei in Golden hamsters

Biol. Reprod.

(1979)

BittmanE.L. et al.

The distribution of melatonin binding sites in neuroendocrine tissues of the ewe

Biol. Reprod.

(1990)

BonnefondC. et al.

Effects of timed melatonin infusions and lesions of the suprachiasmatic nuclei on prolactin and progesterone secretions in pregnant or psuedopregnant mink (Mustela vison)

J. Neuroendocrinol.

(1990)

BonnefondC. et al.

The hypothalamus and photoperiodic control of FSH secretion by melatonin in the male Syrian hamster

J. Endocrinol.

(1989)

BorerK.T. et al.

Hamster prolactin: physiological changes in blood and pituitary concentrations as measured by homologous radioimmunoassay

Neuroendocrinology

(1982)

CarterD.S. et al.

Antigonadal effects of timed melatonin infusions in pinealectomized male Djungarian hamsters (Phodopus sungorus): duration is the critical parameter

Endocrinology

(1983)

CarterD.S. et al.

Progonadal role of the pineal in the Djungarian hamster (Phodopus sungorus): mediation by melatonin

Endocrinology

(1983)

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Seasonal reproduction is a common adaptive strategy among mammals that allows for breeding to occur at times of the year when it is most advantageous for the subsequent survival and growth of offspring. A major mechanism responsible for seasonal reproduction is a striking increase in the responsiveness of gonadotropin-releasing hormone (GnRH) neurons to the negative feedback effects of estradiol. The neural and neuroendocrine circuitry responsible for mammalian seasonal reproduction has been primarily studied in three animal models: the sheep, and two species of hamsters. In this review, we first describe the afferent signals, neural circuitry and transmitters/peptides responsible for seasonal reproductive transitions in sheep, and then compare these mechanisms with those derived from studies in hamsters. The results suggest common principles as well as differences in the role of specific brain nuclei and neuropeptides, including that of kisspeptin cells of the hypothalamic arcuate nucleus, in regulating seasonal reproduction among mammals.
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Lesions of these brain regions also prevent photoinduced changes in reproductive physiology (Maywood and Hastings, 1995). Delivery of long-duration MEL infusions directly into the SCN, the thalamic paraventricular nuclei (PVt), or the nucleus reuniens nuclei (NRe) is sufficient to induce short-day-like changes in reproductive physiology (Dowell and Lynch, 1987; Hastings et al., 1988; Badura and Goldman, 1992; Freeman and Zucker, 2001). Insights into the dependence of photoperiodic time measurement on pineal MEL have been derived almost exclusively from studies of photoperiodic changes in reproductive physiology and adiposity (Bartness et al., 1993; Goldman, 2001).
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The thalamic paraventricular nucleus (PVT), by contrast, is necessary only for the body mass response (Purvis and Duncan, 1997). Several MEL binding/MEL1a-receptor mRNA expressing sites are also sufficient to trigger SD-like gonadal regression and decreases in body mass when MEL is applied site-specifically in a long SD-like duration including the SCN (Badura and Goldman, 1992; Leitner and Bartness, 2010), DMH (Leitner and Bartness, 2010), subZona Incerta (subZI; (Leitner and Bartness, 2010)) and the PVT (gonadal regression, not body mass decreases (Leitner and Bartness, 2010)). The advent of advanced DNA screening methods/tools sparked a new interest in the role of daylength in driving physiology and behavior.
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Central sites mediating reproductive responses to melatonin in juvenile male Siberian hamsters

Abstract

Neurosci. Lett.

Dev. Brain Res.

Physiol. Behav.

Pharmac. Ther.

Neuroscience

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

Brain Res.

Neurosci. Lett.

Neurosci. Lett.

Brain Res.

Brain Res.

SCN lesions block responses to systemic melatonin infusions in Siberian hamsters

Am. J. Physiol.

Lesions to the anterior hypothalamus prevent the melatonin-induced lengthening of delayed implantation

Endocrinology

Suprachiasmatic and paraventricular control of photoperiodism in Siberian hamsters

Am. J. Physiol.

Influences of the paraventricular and suprachiasmatic nuclei and olfactory bulbs on melatonin responses in the golden hamster

Biol. Reprod.

Testicular responses to melatonin are altered by lesions of the suprachiasmatic nuclei in Golden hamsters

Biol. Reprod.

The distribution of melatonin binding sites in neuroendocrine tissues of the ewe

Biol. Reprod.

Effects of timed melatonin infusions and lesions of the suprachiasmatic nuclei on prolactin and progesterone secretions in pregnant or psuedopregnant mink (Mustela vison)

J. Neuroendocrinol.

The hypothalamus and photoperiodic control of FSH secretion by melatonin in the male Syrian hamster

J. Endocrinol.

Hamster prolactin: physiological changes in blood and pituitary concentrations as measured by homologous radioimmunoassay

Neuroendocrinology

Antigonadal effects of timed melatonin infusions in pinealectomized male Djungarian hamsters (Phodopus sungorus): duration is the critical parameter

Endocrinology

Progonadal role of the pineal in the Djungarian hamster (Phodopus sungorus): mediation by melatonin

Endocrinology