Summary
To investigate the hypothesis that oxytocin may be released within the magnocellular nuclei in vivo, push-pull cannula perfusions were performed in anaesthetized lactating rats in one supraoptic nucleus of the hypothalamus while recording the intramammary pressure and/or the electrical activity of oxytocin cells in the contralateral supraoptic nucleus. Oxytocin content was measured in samples collected over 15 min, under various conditions: 1) with no stimulation; 2) during suckling and suckling-induced reflex milk ejections; 3) during electrical stimulation of the neurohypophysis by trains of pulses that mimicked oxytocin cell bursts; 4) under osmotic stimulation by i.p. injection of 2 ml of 1.5 M NaCl to evoke a tonic and sustained oxytocin release from the neurohypophysis. Oxytocin release within the supraoptic nucleus increased significantly during the milk ejection reflex and, to a lesser extent, during burst-like electrical stimulation of the neurohypophysis. In suckled rats, the increase started before the first reflex milk ejection occurred. There was no apparent correlation between the amount of oxytocin in the perfusates and the number of milk ejections and oxytocin cell bursts occurring during each perfusion period. The amount of oxytocin in the perfusates further increased during facilitation of the milk ejection reflex by intraventricular injections of oxytocin or its analogue, isotocin. When suckling failed to evoke the milk ejection reflex, there was no change in intra-supraoptic oxytocin release. There was also no change after osmotic stimulation. When the push-pull cannula was positioned outside the supraoptic nucleus, there was no increase in the amount of oxytocin during the three types of stimulation tested. These results provide evidence for an endogenous release of oxytocin within the magnocellular nuclei in lactating rats. It is suggested that the increase in such a release induced by suckling is likely to be a pre-requisite for the onset and the maintenance of the characteristic intermittent bursting electrical activity of oxytocin cells leading to milk ejections.
Article PDF
Similar content being viewed by others
References
Albe-Fessard D, Stutinsky F, Libouban S (1966) Atlas stéréotaxique du diencéphale du rat blanc. CNRS (eds) CNRS Paris
Belin V, Moos F (1986) Paired recordings from supraoptic and paraventricular oxytocin cells in suckled rats: recruitment and synchronization. J Physiol (Lond) 377:369–390
Brimble MJ, Dyball REJ (1977) Characterization of the responses of oxytocin- and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation. J Physiol (Lond) 271:253–271
Brimble MJ, Dyball REJ, Forsling ML (1978) Oxytocin release following osmotic activation of oxytocin neurones in the paraventricular and supraoptic nuclei. J Physiol (Lond) 278:69–78
Brinton RE, Wamsley JK, Gee kw], Wan YP, Yamamura HI (1984) (3H)Oxytocin binding sites in the rat brain demonstrated by quantitative light microscopic autoradiography. Eur J Pharmacol 102:365–367
Chapman C, Hatton GI, Ho YW, Mason WT, Robinson ICAF (1983) Release of oxytocin (OXT) and vasopressin (AVP) from slices of guinea-pig hypothalamus containing supraoptic (s.o.n.) or paraventricular (p.v.n.) nuclei. J Physiol (Lond) 343: 40P-41P
Demotes-Mainard J, Chauveau J, Rodriguez F, Vincent JD, Poulain DA (1986) Septal release of vasopressin in response to osmotic, hypovolemic and electrical stimulation in rats. Brain Res 381:314–321
Di Scala-Guenot D, Strosser MT, Richard Ph (1987) Electrical stimulations of perifused magnocellular nuclei in vitro elicit Ca2+-dependent, tetrodotoxin-insensitive release of oxytocin and vasopressin. Neurosci Lett 76:209–214
Freund-Mercier MJ, Richard Ph (1981) Excitatory effects of intraventricular injections of oxytocin on the milk ejection reflex in the rat. Neurosci Lett 23:193–198
Freund-Mercier MJ, Richard Ph (1982) L'ocytocine facteur possible du contrôle hypothalamique de l'activation périodique et synchrone des neurones ocytocinergiques pendant la tétée. CR Acad Sci (Paris) 294:497–500
Freund-Mercier MJ, Richard Ph (1984) Electrophysiological evidence for facilitatory control of oxytocin neurones by oxytocin during suckling in the rat. J Physiol (Lond) 352:447–466
Freund-Mercier MJ, Stoeckel ME, Dietl MM, Palacios JM, Richard Ph (1988) Quantitative autoradiographic mapping of neurohypophysial-hormone-binding sites in the rat forebrain and pituitary gland. I. Characterization of different types of binding sites and their distribution in the Long Evans strain. Neuroscience 26:261–272
Kendrick KM, Keverne EB, Baldwin BA, Sharman DF (1986) Cerebrospinal fluid levels of acetylcholinesterase, monoamines and oxytocin during labour, parturition, vaginocervical stimulation, lamb separation and suckling in sheep. Neuroendocrinology 44:149–156
Lincoln DW (1974) Does a mechanism of negative feedback determine the intermittent release of oxytocin during suckling? J Endocr 60:193–194
Mason WT, Leng G (1984) Complex action potential waveform recorded from supraoptic and paraventricular neurones of the rat: evidence for sodium and calcium spike components at different membrane sites. Exp Brain Res 56:135–143
Mason WT, Hatton GI, Ho YW, Chapman C, Robinson ICAF (1986) Central release of oxytocin, vasopressin and neurophysin by magnocellular neurone depolarization: evidence in slices of guinea-pig and rat hypothalamus. Neuroendocrinology 42:311–322
Mens WBJ, Witter A, Van Wimersma-Greidanus Tj B (1983) Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF), half-times of disappearance of these neuropeptides from CSF. Brain Res 262:143–149
Meyer C, Freund-Mercier MJ, Guerné Y, Richard Ph (1987) Relationship between oxytocin release and amplitude of oxytocin cell neurosecretory bursts during suckling in the rat. J Endocrinol 114:263–270
Moos F, Richard Ph (1989) Paraventricular and supraoptic bursting oxytocin cells in rat are locally regulated by oxytocin and functionally related, J Physiol (Lond) 408:1–18
Moos F, Freund-Mercier MJ, Guerné Y, Guerné JM, Stoeckel ME, Richard Ph (1984) Release of oxytocin and vasopressin by magnocellular nuclei in vitro: specific facilitatory effect of oxytocin on its own release. J Endocrinol 102:63–72
Morris M, Barnard RR Jr, Sain LE (1984) Osmotic mechanisms regulating cerebrospinal fluid vasopressin and oxytocin in the conscious rat. Neuroendocrinology 39:377–383
Moss RL, Dyball REJ, Cross BA (1972) Excitation of antidromically identified neurosecretory cells of the paraventricular nucleus by oxytocin applied ionophoretically. Exp Neurol 34:95–102
Pow DV, Morris JF (1988) Exocytotic release of oxytocin and vasopressin in the central nervous system. Ann Endocrinol 49:42N
Summerlee AJS (1981) Extracellular recordings from oxytocin neurones during the expulsive phase of birth in unanaesthetized rats. J Physiol (Lond) 321:1–9
Swaab DF, Nijveldt F, Pool CW (1975) Distribution of oxytocin and vasopressin in the rat supraoptic and paraventricular nucleus. J Endocrinol 67:461–462
Takeda S, Kuwabara Y, Mizuno M (1985) Effects of pregnancy and labor on oxytocin levels in human plasma and cerebrospinal fluid. Endocrinol Jp 32:875–880
Theodosis DT (1985) Oxytocin-immunoreactive terminals synapse on oxytocin neurones in the supraoptic nucleus. Nature 313:682–684
Wakerley JB, Lincoln DW (1973) The milk ejection reflex of the rat: a 20-to 40-fold acceleration in the firing of paraventricular neurones during the release of oxytocin. J Endocrinol 57:477–493
Yamashita H, Okuya S, Inenaga K, Kasai M, Uesugi S, Kannan H, Kaneko T (1987) Oxytocin predominently excites putative oxytocin neurons in the rat supraoptic nucleus in vitro. Brain Res 416:364–368
Zaidi SMA, Heller H (1974) Can neurohypophysial hormones cross the blood-cerebrospinal fluid barrier? J Endocrinol 60:195–196
Zhu PC, Thureson-Klein A, Klein RL (1986) Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: a possible mechanism for neuropeptide release. Neuroscience 19:43–54
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Moos, F., Poulain, D.A., Rodriguez, F. et al. Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp Brain Res 76, 593–602 (1989). https://doi.org/10.1007/BF00248916
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00248916