Structural plasticity in the hypothalamic supraoptic nucleus at lactation affects oxytocin-, but not vasopressin-secreting neurones

Abstract

Magnocellular neurones in the supraoptic nucleus of the hypothalamus are usually separated by neuropil and glial elements. In lactating animals, however, the surface membranes of many neurosecretory somata and dendrites are frequently in direct apposition, without any glial interposition. A significant number of such neurones are also bridged by the same presynaptic terminal (“double synapses”). As the supraoptic nucleus is composed of two types of neurosecretory cell, secreting either oxytocin or vasopressin, we carried out comparative quantitative analyses on identified supraoptic neurones of virgin and lactating rats to determine which neurones were affected by the structural changes and to what extent. The neurones were identified in: (i) normal and Brattleboro homozygote rats by electron microscopic immunocytochemistry (pre- and post-embedding procedures) using antisera raised against oxytocin, vasopressin and oxytocin-related neurophysin I, and (ii) in homozygous Brattleboro rats by their neuronal content of ≈170 nm neurosecretory granules. We report here that, in virgin animals under normal conditions, a small proportion of both types of neurone show neuronal appositions. At lactation, neuronal appositions are far more numerous and extensive, as are “double synapses”. These changes affect exclusively the oxytocinergic neurones. The increased appositions cannot result solely from glial retraction because the hypertrophied oxytocin cells have a greater absolute, though smaller proportional, coverage by glial processes than cells in the control animals. From the present observations, and those obtained in chronically dehydrated animals (see accompanying article), it is clear that the plastic changes in the supraoptic nucleus are closely related to the activity of its oxytocinergic neurones. During lactation, these structural modifications may serve to facilitate and maintain the characteristic synchronized electrical activity of these neurones at milk ejection. On a few occasions, we also found appositions between one oxytocinergic and one vasopressinergic neurone, which may account for the rare cases of electrophysiological interactions between the two types of cell.