Dehydration-induced modulation of kappa-opioid inhibition of vasopressin neurone activity

V. Scott, V. R. Bishop, G. Leng, C. H. Brown

Research output: Contribution to journalArticlepeer-review

Abstract

Dehydration increases vasopressin (antidiuretic hormone) secretion from the posterior pituitary gland to reduce water loss in the urine. Vasopressin secretion is determined by action potential firing in vasopressin neurones, which can exhibit continuous, phasic (alternating periods of activity and silence), or irregular activity. Autocrine kappa-opioid inhibition contributes to the generation of activity patterning of vasopressin neurones under basal conditions and so we used in vivo extracellular single unit recording to test the hypothesis that changes in autocrine kappa-opioid inhibition drive changes in activity patterning of vasopressin neurones during dehydration. Dehydration increased the firing rate of rat vasopressin neurones displaying continuous activity (from 7.1 +/- 0.5 to 9.0 +/- 0.6 spikes s-1) and phasic activity (from 4.2 +/- 0.7 to 7.8 +/- 0.9 spikes s-1), but not those displaying irregular activity. The dehydration-induced increase in phasic activity was via an increase in intraburst firing rate. The selective kappa-opioid receptor antagonist nor-binaltorphimine increased the firing rate of phasic neurones in non-dehydrated rats (from 3.4 +/- 0.8 to 5.3 +/- 0.6 spikes s-1) and dehydrated rats (from 6.4 +/- 0.5 to 9.1 +/- 1.2 spikes s-1), indicating that kappa-opioid feedback inhibition of phasic bursts is maintained during dehydration. In a separate series of experiments, prodynorphin mRNA expression was increased in vasopressin neurones of hyperosmotic rats, compared to hypo-osmotic rats. Hence, it appears that dynorphin expression in vasopressin neurones undergoes dynamic changes in proportion to the required secretion of vasopressin so that, even under stimulated conditions, autocrine feedback inhibition of vasopressin neurones prevents over-excitation.
Original languageEnglish
Pages (from-to)5679-5689
Number of pages11
JournalJournal of Physiology
Volume587
Issue number23
DOIs
Publication statusPublished - Dec 2009

Keywords

  • Action Potentials/drug effects
  • Animals
  • Cholecystokinin/pharmacology
  • Dehydration/physiopathology
  • Electrophysiology
  • Enkephalins/biosynthesis
  • Enkephalins/genetics
  • Female
  • Hypernatremia/physiopathology
  • Hyponatremia/physiopathology
  • Immunohistochemistry
  • In Situ Hybridization
  • Naltrexone/analogs & derivatives
  • Naltrexone/pharmacology
  • Narcotic Antagonists/pharmacology
  • Neurons/drug effects
  • Neurons/physiology
  • Oxytocin/pharmacology
  • Oxytocin/physiology
  • Protein Precursors/biosynthesis
  • Protein Precursors/genetics
  • RNA, Messenger/biosynthesis
  • RNA, Messenger/genetics
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Opioid, kappa/antagonists & inhibitors
  • Receptors, Opioid, kappa/physiology
  • Vasopressins/physiology

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