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Electrophysiology and distribution of oxytocin and vasopressin neurons in the hypothalamic paraventricular nucleus: a study in male and female rats

Abstract

Magnocellular neurosecretory cells (MNCs) clustered in the hypothalamic paraventricular nucleus (PVN) and supraoptic nucleus constitute a major source of oxytocin (OXT) and arginine vasopressin (AVP) peptides, and are among the best described peptidergic neurons in the brain. OXT and AVP are involved in a range of homeostatic processes, social behaviours, emotional processes, and learning. Notably, their actions can be sex-specific, and several sex differences in the anatomies of the OXT and AVP systems have been reported. Nonetheless, possible sex differences in the detailed distributions of MNCs and in their intrinsic electrical properties ex vivo have not been extensively examined. We addressed these issues utilizing immunostaining and patch-clamp ex vivo recordings. Here, we showed that Sprague-Dawley rat PVN AVP neurons are more numerous than OXT cells and that more neurons of both types are present in males. Furthermore, we identified several previously unreported differences between putative OXT and AVP MNC electrophysiology contributing to their partially unique profiles. Notably, elucidation of the highly specific action potential (AP) shapes, with AVP MNCs having a narrower AP and faster hyperpolarizing after-potential (HAP) kinetics than OXT MNCs, allowed unambiguous discrimination between OXT and AVP MNCs ex vivo for the first time. Moreover, the examined electrophysiological properties of male and female MNCs generally overlapped with the following exceptions: higher membrane resistance in male MNCs and HAP kinetics in putative OXT MNCs, which was slower in males. These reported observations constitute a thorough addition to the knowledge of MNC properties shaping their diverse physiological actions in both sexes.

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AK and AB conceived the project; AK, AB, PS, AG, AS, ZS, TB, GH, and ZR contributed to the data acquisition and interpretation of the results; AK performed, analysed, and interpreted the ex vivo electrophysiology data; PS and AS performed and analysed the ex vivo electrophysiology data; AK and AG performed the immunostaining and analysed and interpreted the resultant microscopy data; TB created the analysis tools; and AK and AB wrote the article. All authors provided comments and corrections and approved the final version of the manuscript.

Correspondence to Anna Blasiak.

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Kania, A., Sambak, P., Gugula, A. et al. Electrophysiology and distribution of oxytocin and vasopressin neurons in the hypothalamic paraventricular nucleus: a study in male and female rats. Brain Struct Funct 225, 285–304 (2020). https://doi.org/10.1007/s00429-019-01989-4

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Keywords

  • Paraventricular nucleus of the hypothalamus
  • Magnocellular neurosecretory cells
  • Oxytocin
  • Vasopressin
  • Sex differences
  • Electrophysiology