Electrical activity of neurons in the ventrolateral septum and bed nuclei of the stria terminalis in suckled rats: Statistical analysis gives evidence for sensitivity to oxytocin and for relation to the milk-ejection reflex

Abstract

Our previous results obtained by lesioning or stimulating the ventrolateral part of the lateral septum and the bed nuclei of the stria terminalis suggested that this area is involved in the control of milk ejection pattern in rats. The present study was undertaken with the aim of testing ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons as a putative link of the neuronal network controlling the bursting activity of oxytocin neurons in suckled lactating rats (anaesthetized with urethane). Ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons were recorded simultaneously with hypothalamic oxytocin neurons in either the paraventricular or supraoptic nucleus in rats with ( N = 26) or without ( N = 29) periodic milk ejections. Analysis of their firing pattern enabled differentiation of two subgroups: type I, characterized by numerous high frequency spikes, often grouped in clusters; and type II with very few or no high frequency clusters of spikes. The probability density function of the interspike intervals of both patterns could be modelled using a mixture of two log-normal distributions, the parameters of which differed significantly. The presence or absence of milk ejections did not influence the overall mean level of activity (2.0 ± 0.5 and 1.9 ± 0.4 spikes/s, respectively). However, the characteristics of the type I firing pattern were affected by the presence of the milk-ejection reflex. The average level of activity was not always constant and 16/55 ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons displayed cyclical activity (from 0.6 ± 0.2 to 4.0 ± 0.5 spikes/s) both in the presence ( N = 8) and absence ( N = 8) of the milk-ejection reflex. In five of eight neurons recorded during milk-ejection reflex, the cycles in firing were clearly correlated with the bursting of oxytocin neurons. These five neurons exhibited the type I firing pattern. The three remaining neurons and the eight neurons recorded in the absence of milk-ejection reflex displayed the type II firing pattern. Oxytocin (1–2 ng = 0.45−0.9 mU) was injected into the third ventricle (i.c.v.) in order to examine the possible involvement of ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons in the facilitatory effect of oxytocin on the reflex. Oxytocin caused an excitation of 13/47 ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons independent of whether the reflex was facilitated by oxytocin ( N = 6) or not ( N = 7). In the former case, the increase in firing rate occurred before facilitation of the reflex. Most of the oxytocin-sensitive neurons (10/13) had the type I firing pattern, the characteristics of which were variably affected by oxytocin. The positions of 18 neurons were histologically localized in the ventrolateral part of the lateral septum-bed nuclei of the stria terminalis by iontophoretic deposition of a dye. The location of 10 of these neurons was further correlated with oxytocin-binding sites using autoradiography. The majority of these neurons (including both oxytocin-sensitive and -insensitive neurons) were located in regions expressing oxytocin-binding sites. In conclusion, there exists a population of ventrolateral part of the lateral septum-bed nuclei of the stria terminalis neurons displaying numerous high frequency spikes (type I firing pattern) which exhibits a strong correlation with milk ejection-related bursting activity of hypothalamic oxytocin neurons, and/or which are sensitive to oxytocin. It is suggested that these neurons might be involved as an element of a neuronal network mediating the central effects of oxytocin on the milk-ejection reflex.