Cited by 327Neuroendocrine regulation and behaviorHypothalamic control of reproductive hormonesNeuropeptides and Animal Physiology

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The milk-ejection reflex of the rat: a 20-to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release

WAKERLEY, J. B., LINCOLN, D. W.·1973·Journal of Endocrinology

DOI 10.1677/joe.0.0570477

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Abstract

SUMMARY Antidromically-identified paraventricular (PV) neurones were studied in the anaesthetized rat during milk ejection (ME) evoked by the natural stimulus provided by the suckling young. An intermittent pattern of ME was observed, though the ME interval was slightly longer (10–20 min) in the doe during unit recording than in unoperated or conscious animals (5–15 min). PV neurones displayed a steady background of spike discharge in both the non-lactating rat and lactating rat during suckling. The firing rates ranged from 0 to 9·4 spikes/s and were exponentially distributed with 32% of the units firing at <1 spike/s. Phasic patterns of discharge were seen in 18% of the units. Fifty-eight per cent of the PV units displayed a stereotyped and explosive acceleration in spike activity some 15–20 s before the rise in intramammary pressure at ME. The peak firing rate during this brief (2–4 s) response was in the range of 24–84 spikes/s. A prominent after-inhibition was then displayed by these responsive units, though this second component of the response was variable in duration (7–56 s). The electrical activity of the remaining units, including all the cells with phasic discharge, was not correlated with ME. There was no apparent change in the intensity of the suckling stimulus at the time of PV activation, i.e. 15–20 s before ME. Secondly, the activity of the PV neurones was not influenced by the rise in the intramammary pressure and the increased sucking of the pups at the time of ME. Simulation of an individual ME was obtained with both 1 mu. exogenous oxytocin, i.v., and electrical stimulation of the neurohypophysis (50 pulses/s for 4 s). The latencies to ME ranged from 7–14 s and 11–23 s, respectively. In conclusion, an explosive increase in the electrical activity of PV neurones precipitates the release of oxytocin at ME.

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Items 101–200 of 326

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“OT-secreting cells demonstrate brief (2–4 s), synchronized high-frequency bursts (40–80 Hz) during reflex milk ejections (Wakerley and Lincoln 1973).”
Background
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Roberts, C. B., O’Boyle, M., & Suter, K. J. (2008) · Journal of Computational Neuroscience · doi:10.1007/s10827-008-0095-5 · Cited by 33
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“Because hormone secretion by neuroendocrine cells, such as vasopressin and oxytocin neurons, has long been linked with burst firing activities (Wakerley and Lincoln, 1973; Dutton and Dyball, 1979), we examined whether KA injection affected GnRH neuron firing patterns and/or burst properties.”
Background
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“Further, cells which showed high frequency bursts of action potentials 10-20 s preceding each milk-ejection caused by the suckling of pups were classified as oxytocinergic cells and the remaining cells which showed no change in their firing pattern in response to suckling stimuli were classified as vasopressinergic ce…”
Background
Heterologous Expression of the Kv3.1 Potassium Channel Eliminates Spike Broadening and the Induction of a Depolarizing Afterpotential in the Peptidergic Bag Cell Neurons
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“Similar mechanisms may underlie sustained changes in activity that have been observed in other neurons, such as the magnocellular neurons of the hypothalamus (Wakerley and Lincoln, 1973).”
Background
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“…of vasopressin neurons (Dreifuss et al., 1976); during suckling the type firing irregularly dramatically and synchronously discharged brief high-frequency bursts with a milk ejection following each burst, so these neurons were characterised as oxytocinergic (Wakerley and Lincoln, 1973; Figure 2).”
Background
Increases in Dendritic Bundling and Dye Coupling of Supraoptic Neurons after the Induction of Maternal Behaviora
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“…(Poulain & Wakerley, 1982; Renaud, 1987; Bourque & Renaud, 1990), while OT plays a key role in parturition, milk ejection and maternal behaviour (Wakerley & Lincoln, 1973; Poulain & Wakerley, 1982; Bourque & Renaud, 1990; Crowley & Armstrong, 1992; Luckman et al. 1994; Russell et al. 1995).”
Background
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Background
Electrical Stimulation of the Rat Periventricular Nucleus Influences the Activity of Hypothalamic Arcuate Neurones
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“The reflex was first described in the rat by Wakerley and Lincoln in 1973 [20]: when hungry pups suckle at the nipples of their mother, the magnocellular oxytocin cells in the hypothalamus discharge an intense burst of spikes every 5–10 min, resulting in an abrupt milk let-down.”
Background
Opposing effects of intracerebroventricularly injected norepinephrine on oxytocin and vasopressin neurons in the paraventricular nucleus of the rat
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“Furthermore, in principle, our strategy is applicable to many other mammalian species beyond mice and rats [8] for characterizing the neural activities of OT neurons during lactation.”
Background
Extrinsic and Intrinsic Modulatory Mechanisms Involved in Regulating the Electrical Activity of Supraoptic Neuronsa
Bourque, C. W., Oliet, S. H. R., KIRKPATRICK, K., et al. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb55581.x · Cited by 23
Amygdalar inputs to ADH-secreting supraoptic neurones in rats
Hamamura, M., Shibuki, K., & Yagi, K. (1982) · Experimental Brain Research · doi:10.1007/bf00238618 · Cited by 23
Temporal Patterns of Neural Activity and Their Relation to the Secretion of Posterior Pituitary Hormones1
Dreifuss, J. J., Tribollet, E., & Mühlethaler, M. (1981) · Biology of Reproduction · doi:10.1095/biolreprod24.1.51 · Cited by 23
The Matter of Facts
Leng, G., & Leng, R. (2020) · The MIT Press eBooks · doi:10.7551/mitpress/12228.001.0001 · Cited by 25
Dynamics of Oxytocin Secretion
LINCOLN, D. W. (1974) · Springer eBooks · doi:10.1007/978-3-662-12587-8_13 · Cited by 22
Self-citation
Lesions of Hypothalamic Mammillary Body Desynchronise Milk‐Ejection Bursts of Rat Bilateral Supraoptic Oxytocin Neurones
Wang, Y.-F., Negoro, H., & Higuchi, T. (2013) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.2012.02368.x · Cited by 20
Reduced Oxytocin Release from the Neural Lobe of Lactating Rats is Associated with Reduced Pituitary Content and does not Reflect Reduced Excitability of Oxytocin Neurons
Higuchi, T., Bicknell, R. J., & Leng, G. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00278.x · Cited by 21
The Nursing and Suckling Behaviour of Pigs. III. Behaviour When Milk Ejection is Elicited by Manual Stimulation of the Udder
Fraser, D. J. (1975) · British Veterinary Journal · doi:10.1016/s0007-1935(17)35237-5 · Cited by 21
Asynchronous presynaptic glutamate release enhances neuronal excitability during the post‐spike refractory period
Iremonger, K. J., & Bains, J. S. (2015) · The Journal of Physiology · doi:10.1113/jp271485 · Cited by 20
“AHPs have been shown to promote rhythmic spiking and enhance temporal precision during spike trains (Berry & Meister, 1998; Bennett et al. 2000; Wolfart et al. 2001; Hallworth et al. 2003; Vervaeke et al. 2006).”
Background
A Predictive, Quantitative Model of Spiking Activity and Stimulus-Secretion Coupling in Oxytocin Neurons
Maícas-Royo, J., Leng, G., & MacGregor, D. J. (2018) · Endocrinology · doi:10.1210/en.2017-03068 · Cited by 19
“This nonlinearity is marked: during a reflex milk ejection, oxytocin cells fire about 100 spikes in just 2 seconds (22), and during this burst, each spike releases, on average, about 100 times as much oxytocin as spikes that occur at the typical basal firing rate of 2 spikes/s (23).”
BackgroundInfluential
Acute increases in arterial blood pressure do not reduce plasma vasopressin levels stimulated by angiotensin II or hyperosmolality in rats
Stocker, S. D., Schiltz, J. C., & Sved, A. F. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00526.2003 · Cited by 20
“On the other hand, putative oxytocin (OT) neurons show intermittent bursts of activity immediately before milk ejection (59, 60), are excited by CCK (36), but are insensitive to increases in ABP (32, 35).”
Background
Endocrine Neurons
CROSS, B. A., Dyball, R. E. J., Dyer, R. G., et al. (1975) · Elsevier eBooks · doi:10.1016/b978-0-12-571131-9.50011-6 · Cited by 20
Self-citation
Oxytocin and vasopressin in the hippocampus
Zăgrean, A., Georgescu, I.-A., Ieșanu, M. I., Ionescu, R.-B., Haret, R. M., Panaitescu, A. M., & Zăgrean, L. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.002 · Cited by 20
Chronic vs. Acute Interactions between Supraoptic Oxytocin Neurons and Astrocytes during Lactation: Role of Glial Fibrillary Acidic Protein Plasticity
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“Parturition[57] and suckling[32] both activate OXT neuron bursts, which are temporally closely related to release of OXT[22], noradrenaline[51], and glutamate[24] in the hypothalamus.”
Background
Voltage‐ and Ca2+‐Dependent Burst Generation in Neuroendocrine Dahlgren Cells in the Teleost Platichthys flesus
Brierley, M. J., Bauer, C. S., Lu, W., Riccardi, D., BALMENT, R. J., & McCrohan, C. R. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01238.x · Cited by 19
Oxytocin and the Milk-Ejection Reflex
Robinson, I. C. A. F. (1986) · Current topics in neuroendocrinology · doi:10.1007/978-3-642-70414-7_6 · Cited by 18
Facilitation of milk ejection-related activation of oxytocin-secreting neurones by osmotic stimulation in the rat
Negoro, H., Honda, K., Uchide, K., et al. (1987) · Experimental Brain Research · doi:10.1007/bf00236303 · Cited by 18
“The oxytocin neurones were identified by their antidromic response to electrical stimulation of the neural lobe and by observation of a short high-frequency burst of action potentials some 12-20 s before reflex milk ejection (Wakerley and Lincoln 1973).”
Background
THE POSTERIOR PITUITARY GLAND
Chard, T. (1975) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1975.tb03308.x · Cited by 19
The afferent pathway for carotid body chemoreceptor input to the hypothalamic supraoptic nucleus in the rat
Harris, M. C., Ferguson, A. V., & Banks, D. (1984) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00670540 · Cited by 18
“One is a bursting or phasic discharge showing periods of discharge alternating with periods of silence, and the other a slow more or less regular discharge ( Wakerley and Lincoln 1973; Lincoln and Wakerley 1974).”
The antidromic compound action potential of the hypothalamo-neurohypophysial tract, a tool for assessing posterior pituitary activity in vivo
Baertschi, A. J., & Dreifuss, J.-J. (1979) · Brain Research · doi:10.1016/0006-8993(79)91048-5 · Cited by 18

Authors: WAKERLEY, J. B., & LINCOLN, D. W.
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 1973-06-01
Volume: 57
Issue: 3
Pages: 477-493
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1677/joe.0.0570477
OpenAlex: W2053881206
Cited by: 327
References: 0
Citations by year: 2026: 4 · 2025: 3 · 2024: 4 · 2023: 5 · 2022: 10 · 2021: 4 · 2020: 3 · 2019: 1 · 2018: 5 · 2017: 1 · 2016: 6 · 2015: 10 · 2014: 11 · 2013: 2 · 2012: 2
FWCI: 28.43
Type: journal article
Language: en
Open access: closed
Locations: Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: milk ejection reflex, oxytocin release, neuronal firing rate, suckling stimulus, intramammary pressure, lactation
MeSH terms: Action Potentials, Ethanol, Animals, Female, Hypothalamus, Lactation, Mammary Glands, Animal, Microelectrodes, Micromanipulation, Neurons, Oxytocin, Pituitary Gland, Pregnancy, Pressure, Reflex, Sucking Behavior, Urethane, Rats

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The milk-ejection reflex of the rat: a 20-to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release

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