Permissive Effect of Centrally Administered Oxytocin on the Excitatory Response of Oxytocin Neurones to Ventral Tegmental Stimulation in the Suckled Lactating Rat

• Published in: Journal of neuroendocrinology 2000-09, Vol.12 (9), p.843-852
• Main Authors: Cosgrave, A. S., Richardson, C. M., Wakerley, J. B.
• Format: Article
• Language: English
• Subjects: Action Potentials; Animals; Electric Stimulation; Electrodes; excitatory responses; Female; i.c.v. oxytocin; Injections, Intraventricular; Kinetics; Lactation - physiology; mesencephalic ventral tegmentum; Milk Ejection - physiology; milk-ejection reflex; Neurons - physiology; Oxytocin - administration & dosage; Oxytocin - pharmacology; Oxytocin - physiology; oxytocin neurones; permissive effect; Rats; Rats, Wistar; Reproducibility of Results; Sucking Behavior
• ISSN: 0953-8194; 1365-2826
• DOI: 10.1046/j.1365-2826.2000.00531.x

The mesencephalic ventral tegmentum has been implicated in the milk‐ejection reflex and modulation of inputs from this region could provide a mechanism whereby central oxytocin facilitates synchronous bursting of oxytocin neurones during suckling. Experiments were therefore undertaken to investigate the effect of intracerebroventricular (i.c.v.) oxytocin on the response of oxytocin neurones to ventral tegmental stimulation. Oxytocin neurones were recorded in the supraoptic nucleus of urethane‐anaesthetized lactating rats during suckling, and their response to single shock stimulation of the ventral tegmentum was monitored using peri‐stimulus time‐interval histograms. Before i.c.v. oxytocin, oxytocin neurones were either unresponsive to ventral tegmental stimulation, or displayed a small inhibition. However, after administration of oxytocin (2.2 ng i.c.v.), seven out of eight neurones tested displayed a pronounced excitatory response (onset latency 78.4 ± 4.8 ms, duration 73.4 ± 8.3 ms). This permissive effect on the excitatory response was only observed in the presence of suckling, and followed the same time course as facilitation of the milk‐ejection reflex, being maximal immediately before each facilitated bursting response in the oxytocin neurones. The response to ventral tegmental stimulation remained unaltered after intraperitoneal administration of hypertonic saline to cause a generalized increase in the excitability of the oxytocin neurones. Moreover, i.c.v. oxytocin had no effect on the response of oxytocin neurones to stimulation of a descending input from the medial septum. In conclusion, administration of i.c.v. oxytocin has a selective permissive effect on the excitation of oxytocin neurones from the ventral tegmentum, and this supports previous in vitro studies suggesting that centrally released oxytocin may act as a modulator of afferent transmission to the magnocellular nuclei. This effect on the afferent excitation of oxytocin neurones may provide a mechanism whereby i.c.v. oxytocin facilitates suckling‐evoked bursting activity.