Endogenous activation of supraoptic nucleus kappa-opioid receptors terminates spontaneous phasic bursts in rat magnocellular neurosecretory cells

Colin H Brown, Gareth Leng, Mike Ludwig, Charles W Bourque

Research output: Contribution to journalArticlepeer-review

Abstract

Phasic activity in magnocellular neurosecretory vasopressin cells is characterized by alternating periods of activity (bursts) and silence. During phasic bursts, action potentials (spikes) are superimposed on plateau potentials that are generated by summation of depolarizing after-potentials (DAPs). Burst termination is believed to result from autocrine feedback inhibition of plateau potentials by the kappa-opioid peptide, dynorphin, which is copackaged in vasopressin neurosecretory vesicles and exocytosed from vasopressin cell dendrites during phasic bursts. Here we tested this hypothesis, using intracellular recording in vitro to show that kappa-opioid receptor antagonist administration enhanced plateau potential amplitude to increase postspike excitability during spontaneous phasic activity. The antagonist also increased postburst DAP amplitude in vitro, indicating that endogenous dynorphin probably reduces plateau potential amplitude by inhibiting the DAP mechanism. However, the kappa-opioid receptor antagonist did not affect the slow depolarization that follows burst termination, suggesting that recovery from endogenous kappa-opioid inhibition does not contribute to the slow depolarization. We also show, by extracellular single-unit recording, that that there is a strong random element in the timing of burst initiation and termination in vivo. Administration of a kappa-opioid receptor antagonist eliminated the random element of burst termination but did not alter the timing of burst initiation. We conclude that dendritic dynorphin release terminates phasic bursts by reducing the amplitude of plateau potentials to reduce the probability of spike firing as bursts progress. By contrast, dendritic dynorphin release does not greatly influence the membrane potential between bursts and evidently does not influence the timing of burst initiation.

Original languageEnglish
Pages (from-to)3235-44
Number of pages10
JournalJournal of Neurophysiology
Volume95
Issue number5
DOIs
Publication statusPublished - May 2006

Keywords

  • Action Potentials
  • Animals
  • Electric Stimulation
  • In Vitro Techniques
  • Male
  • Naltrexone
  • Narcotic Antagonists
  • Neurons
  • Rats
  • Rats, Long-Evans
  • Receptors, Opioid, kappa
  • Statistics, Nonparametric
  • Supraoptic Nucleus
  • Time Factors
  • Vasopressins

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