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Y-F Wang, H Negoro, and K Honda

Abstract

Unilateral knife cuts were performed in the midbrain of lactating rats and the activities of oxytocin neurones were recorded extracellularly from the supraoptic nuclei (SON) in order to investigate the location of the neural mechanism responsible for the synchronization of milk-ejection bursts of oxytocin neurones in different magnocellular nuclei of the hypothalamus. The lesions involved the mesencephalic lateral tegmentum, the intermedial tegmentum and the central grey. Ninety-six SON neurones were antidromically activated by neurohypophyseal stimulation and were also identified as oxytocin neurones, which included 17 pair-recorded neurones. First, the response of oxytocin neurones recorded from the unilateral SON to bilateral or unilateral suckling was tested. During bilateral suckling, not only the oxytocin neurones recorded from the SON on the intact side (n=34) but also those recorded from the SON on the lesioned side (n=58) displayed milk-ejection bursts. When only the nipples ipsilateral to the lesion were suckled (ipsilateral suckling), bursts were induced in most of the oxytocin neurones on the intact (83·3%, n=12) and lesioned side (88·9%, n=27). In contrast, none of the oxytocin neurones (n=37) produced bursts and none of the rats tested (n=23) showed milk ejections during contralateral suckling. Secondly, some characteristics of the bursts of pair-recorded neurones during bilateral suckling and their response to different modes of suckling were investigated. When oxytocin neurones on both sides displayed milk-ejection bursts, they were always well synchronized but the mean burst amplitude of the neurones on the lesioned side (55·6 ±4·9 spikes, n=43) was significantly (P<0·05) lower than that of the neurones on the intact side (65·7 ±5·6 spikes, n=43). Late-recruited neurones were observed in 6 pairs of oxytocin neurones, and these mainly occurred in the neurones on the lesioned side (5/6). In 5 pair-recorded oxytocin neurones, bursts could also be induced synchronously by ipsilateral suckling but not by contralateral suckling. Thus it is very likely that the major mechanism synchronizing the milk-ejection bursts of oxytocin neurones in the bilateral SON is located in the region rostral to the midbrain.

Journal of Endocrinology (1995) 144, 463–470

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H. NEGORO, S. VISESSUWAN, and R. C. HOLLAND

SUMMARY

Spontaneous firing rates were determined from extracellular recordings made from 878 antidromically identified units in the paraventricular nucleus (PVN) during the reproductive cycle of the female rat and in analytical experiments. In the latter, rats were ovariectomized and subsequently received either no treatment or oestrogen and/or progesterone. Among rats at metoestrus, dioestrus, mid-pregnancy and in ovariectomized progesterone-treated groups there was no significant difference in the firing rates. However, they were significantly lower than the rates recorded during pro-oestrus, oestrus, full-term pregnancy, the day of parturition, during lactation and in ovariectomized, oestrogen-treated rats. In spayed rats the mean firing rate was significantly lower than at pro-oestrus, oestrus, fullterm pregnancy, the 24 h period after parturition, during lactation and after oestrogen treatment. When progesterone was given subcutaneously to oestrogenized rats, the PVN activity, increased by oestrogen, was significantly depressed 4 h after administration. By 8 h the firing rate had completely recovered.

The frequency distribution of the firing rates in pro-oestrus and oestrus showed an approximately normal distribution while those in metoestrus and dioestrus and mid-pregnancy had a Poisson distribution. At full term there were two peaks: one in the range of 3–5 spikes/s and the other less than one spike/s. The distribution was approximately normal on the day of parturition and subsequently the pattern became irregular. In ovariectomized rats and those treated with progesterone it was of a Poisson type while there was a distinct shift to higher frequencies after oestrogen treatment.

The mean absolute refractory period, measured for each unit, varied and appears to be dependent on hormonal conditions. It was short in oestrus and long in dioestrus and mid-pregnancy. Oestrogen treatment significantly shortened the absolute refractory period of ovariectomized rats.

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T. Higuchi, H. Negoro, and J. Arita

ABSTRACT

Prolactin, GH, TSH, adrenaline and noradrenaline responses to the stress of immobilization were compared between lactating and non-lactating dioestrous rats. The concentrations of GH in plasma were reduced to a similar degree by the immobilization of lactating and non-lactating rats, and TSH levels were unchanged in both groups. The increases in plasma concentrations of adrenaline and noradrenaline induced by stress were significantly smaller in lactating than in non-lactating rats. Immobilization caused a marked increase in prolactin levels in the plasma of non-lactating rats but no increase in lactating rats. These changes may help to save energy and maintain milk production during the period of lactation.

Journal of Endocrinology (1989) 122, 495–498

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H. NEGORO, S. VISESSUWAN, and R. C. HOLLAND

SUMMARY

Three hundred and seventy-seven neurones in the paraventricular nucleus (PVN) were antidromically identified in female rats during various stages of the reproductive cycle and in ovariectomized rats with or without oestrogen or progesterone pretreatment. The units were tested for their responses to vaginal distension and pinching of the foot. Unit responses to vaginal distension varied during the oestrous cycle, pregnancy and lactation. The percentages of PVN units recorded at each stage which increased their firing rate in response to vaginal distension were 64·1% in pro-oestrus, 56·7% in oestrus, 33·3% in metoestrus, 42·4% in dioestrus, 6·9% in mid-pregnancy (day 12) which was significantly lower than in any other stage or condition, 72·0% at full term, 55·5% immediately (<24 h) after parturition and 40·0% during lactation. Furthermore, when tested in mid-pregnancy, there was a period of interruption of spontaneous firing in 13·8% of PVN units during vaginal distension.

The percentage of units which increased their firing rate during vaginal distension in ovariectomized rats was 42·4% and in ovariectomized, oestrogen-treated rats was 69·2% and thus significantly higher. While the percentage in progesterone-treated rats (35·1%) was not significantly different from that in ovariectomized rats, it was significantly lower than in the oestrogen-treated group. In addition, 18·9% of the units had a period of interruption of spontaneous firing in response to vaginal distension constituting the only group besides the mid-pregnancy group in which this was observed.

Pinching the foot also excited PVN unit activity in some cases. It was more frequently evoked by pinching a foot contralateral to the PVN nucleus from which the recording was taken. The response to stimulation of the ipsilateral foot was weaker or absent. The responsiveness of PVN units to pinching varied throughout the reproductive cycle as well as in ovariectomized rats with or without treatment with oestrogen or progesterone. The pattern of variation was dissimilar from that observed after vaginal distension and the magnitude of variation was smaller. Interruption of spontaneous firing was observed in seven different groups.

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T. Higuchi, K. Honda, and H. Negoro

ABSTRACT

The influence of oestrogen on LH and oxytocin responses to immobilization stress, and the involvement of noradrenergic afferent neurones in these responses, was examined in ovariectomized rats with or without pretreatment with oestrogen or after noradrenergic transmitter blockade. Immobilization of the rats on a board in a supine position for 1 h brought about a rapid decrease in LH levels and an increase in oxytocin levels in the blood of ovariectomized rats. Oestradiol benzoate (20 μg) injected s.c. the day before immobilization, decreased basal LH levels but had no effect on basal oxytocin levels. Immobilization stress applied to oestrogen-treated rats induced a small but significant increase in LH concentrations and a rise in oxytocin concentrations similar to that in rats without oestrogen pretreatment. A dopamine-β-hydroxylase inhibitor or phenoxybenzamine (α-adrenoceptor blocker) injected into ovariectomized rats reduced basal LH levels and increased basal oxytocin levels in the blood. Immobilization stress induced an increase in LH levels in rats treated with dopamine-β-hydroxylase inhibitor, but had no effect in rats treated with phenoxybenzamine. Stress induced a larger increase in blood oxytocin levels in rats treated with either drug compared with that in control rats injected with vehicle. On the other hand, propranolol (β-adrenoceptor blocker) had no effect on basal or stress-induced changes in LH or oxytocin levels in the blood. These results indicate that the LH response to stress, which might be mediated through α-adrenergic neurones, depends on the circulating oestrogen or LH levels before the stress. In contrast, the oxytocin response to stress may not be mediated by noradrenergic neurones and may not be influenced by oestrogen.

J. Endocr. (1986) 110, 245–250

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T. Higuchi, K. Honda, T. Fukuoka, H. Negoro, and K. Wakabayashi

ABSTRACT

A highly sensitive and specific radioimmunoassay (RIA) for oxytocin was developed and used to measure oxytocin concentrations during both suckling and parturition in individual rats. In urethane-anaesthetized rats, the suckling stimuli, provided by ten pups, induced intermittent increases in intramammary pressure of about 10 mmHg. This was associated with a significant (P < 0·01) increase in serum oxytocin levels from 19·5 ± 4·5 (s.e.m., n = 9) to 49·1 ± 7·4 pmol/l (n = 9) in the samples taken within 30 s from the time of the peak in the pressure. These rises in serum oxytocin returned rapidly to the basal levels as expected from the short half-life (1·46 min) of oxytocin in general circulation.

On day 22 or 23 of gestation, serum oxytocin levels remained stable until 0–0·5 h before the first fetus was expelled. They then increased significantly (P < 0·01) from 27·6± 4·6 pmol/l (n = 19) in samples taken 0–0·5 h before to 45·1 ± 5·6 pmol/l in samples taken after the expulsion of the first fetus and gradually increased until the last fetus was expelled. Serum oxytocin concentrations then declined but remained higher than those observed before the first fetus had been born until at least 1–1·5 h after the expulsion of the last fetus. Thus, this oxytocin RIA revealed increased concentrations of the hormone in blood during both suckling and parturition in the rat.

J. Endocr. (1985) 105, 339–346

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T. Higuchi, Y. Tadokoro, K. Honda, and H. Negoro

ABSTRACT

A detailed secretory profile of oxytocin during suckling and parturition was determined in unanaesthetized freely moving rats. Ten pups were reunited with their mothers after 12–15 h of separation. Unless the milk-ejection reflex occurred, there was no difference in serum oxytocin levels before separation and during the suckling of either four or five, or nine or ten pups. Serum oxytocin levels increased abruptly by 50·1 ± 4·2 (s.e.m.) pmol/l (n = 9) at milk ejection, and declined rapidly with a half-life of about 1·5 min. The peak concentration of blood oxytocin at each milk ejection was independent of the previous suckling period; values from the first three milk-ejection reflexes following the introduction of the pups and those observed 3–5 h after introduction were similar. The process of parturition was monitored by recording intra-uterine pressure with a balloon implanted in the uterus. On day 22 or 23 of pregnancy, continuous and rhythmical contractions of the uterus occurred (onset of parturition), but serum levels of oxytocin (21·1 ± 1·9 pmol/l; n = 13) did not alter until the expulsive phase. During the expulsive phase, fetuses were delivered after fetus-expulsion reflexes which were recorded as sudden large increases in intra-uterine pressure. Basal levels of oxytocin in the blood increased during this phase (32·5 ± 4·4 pmol/l; n = 13) and, in addition, rose by about 15 pmol/l and declined slowly after fetus-expulsion reflexes. The increase, however, was quite different from that seen at milk-ejection reflexes.

J. Endocr. (1986) 110, 251–256

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T. Higuchi, K. Uchide, K. Honda, and H. Negoro

ABSTRACT

Blood levels of oxytocin during parturition in pelvic-neurectomized rats were determined by radioimmuno-assay. Four out of 29 pelvic-neurectomized rats completed parturition within 23 days of pregnancy. These rats exhibited an increase in blood levels of oxytocin during parturition similar to those of sham-operated control rats, but delivery took longer and there was a higher percentage of still-births. The rise in blood levels of oxytocin was smaller in the 16 rats in which the first fetus was expelled but where delivery did not end within day 23 of gestation than that in sham-operated controls. Levels did not increase in the other nine rats which failed to deliver the first fetus within 23 days of pregnancy. They did, however, show signs indicating delivery, such as stretch movements, vaginal bleeding and/or excretion of mucus within 23 days of gestation. Oxytocin infusion (2 mu./min) for 2–4 h increased uterine contractions in the pelvic-neurectomized rats but failed to reduce the percentage of still-births or the duration of delivery. Immuno-neutralization of circulating oxytocin by anti-oxytocin serum in intact pregnant rats resulted in a significant but much smaller prolongation of the duration of delivery compared with that observed in pelvic-neurectomized rats. The rise in blood levels of oxytocin during pregnancy may be induced, at least in part, by the Ferguson reflex via the pelvic nerve and may thus facilitate the process of delivery. A shortage of oxytocin secretion may not, however, be the main cause of the dystocia in pelvic-neurectomized rats.

J. Endocr. (1986) 109,149–154

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T. Higuchi, K. Uchide, K. Honda, and H. Negoro

ABSTRACT

Developmental changes in levels of oxytocin in the blood and the pituitary gland and in oxytocin responses to oxytocin-releasing stimuli were investigated in the rat from the fetus close to term to the 40-day-old young adult. The oxytocin content of the pituitary gland rose gradually from fetuses of 21 days of gestation to 40-day-old rats. Pituitary oxytocin levels expressed in terms of body weight also increased up to day 25 after birth and declined slightly thereafter. In contrast, serum concentrations of oxytocin increased from day 21 of pregnancy up to day 5 after birth but were stable thereafter. Oxytocin levels in both blood and the pituitary gland were equal in 23-day-old fetuses and 1-day-old infants born on day 22 of pregnancy. There was no difference in serum and pituitary oxytocin levels in newborn pups and unborn littermates of day 22 or 23 of gestation. The i.p. injection of hypertonic saline induced a significant increase in serum oxytocin levels on day 5 and later, but no effect in the fetus on day 22 of gestation and in the 1-day-old infant. The responsiveness to the osmotic stimuli increased after 5 days of age. The i.p. injection of diethyl-dithiocarbamate, a noradrenaline synthesis inhibitor, or phenobarbitone was effective in raising blood oxytocin levels only in rats older than 10 and 20 days of age respectively. These findings, that a gradual increase in oxytocin levels in both blood and the pituitary gland without an apparent increase in its release and the absence of a pituitary response to oxytocin-releasing stimuli during the perinatal period, do not support a role for fetal oxytocin in the initiation of labour in the rat.

J. Endocr. (1985) 106, 311–316

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T. Higuchi, K. Honda, S. Takano, and H. Negoro

ABSTRACT

The release of oxytocin in response to an osmotic stimulus and immobilization stress was compared in lactating rats 8–12 days after delivery and in non-lactating rats. Intravenous injection of hypertonic saline or immobilization stress induced an increase in blood oxytocin levels in both lactating and non-lactating rats, but the increment in the former was significantly lower than that in the latter. The lower responsiveness of oxytocin release to stress in lactating rats was not altered by ovariectomy 2 days after parturition. Oxytocin release induced by electrical stimulation of the anteroventral third ventricle (an osmoreceptive area), paraventricular nucleus and neurohypophysis was significantly lower, to a similar extent, in lactating rats compared with non-lactating rats. These findings indicate that the structural reorganization reported in the hypothalamo-neurohypophysial system may not function to facilitate release of oxytocin in response to stress and osmotic stimulus in lactating rats. The reduced responsiveness of the release of oxytocin is independent of the influence of ovarian hormones, and may be due to the low ability of the oxytocin neurone itself to release oxytocin, and/or due to the activated inhibitory influence on the oxytocin neurone in the lactating rat.

J. Endocr. (1988) 116, 225–230