Opioids hyperpolarize beta-endorphin neurons via mu-receptor activation of a potassium conductance

Neuroendocrinology. 1990 Sep;52(3):268-75. doi: 10.1159/000125597.

Abstract

Intracellular recordings were made from hypothalamic arcuate (ARC) neurons with biocytin-filled electrodes under current- and voltage-clamp in slices prepared from ovariectomized guinea pigs which were pretreated with estradiol. Forty-three neurons were identified after linking the intracellular biocytin with streptavidin-FITC and subsequently were examined for beta-endorphin immunoreactivity. Ten of these neurons were immunoreactive for beta-endorphin. beta-Endorphin neurons displayed the following passive membrane properties: RMP:-56 +/- 2 mV; Rin: 439 +/- 66 M omega; tau: 17.5 +/- 2.4 ms; and often fired spontaneously (5.9 +/- 2.2 Hz). These membrane characteristics were not different from identified neurons in the ARC that were not immunoreactive for beta-endorphin. beta-Endorphin neurons exhibited instantaneous inward rectification and time-dependent rectification. The mu-opioid agonist Tyr-D-Ala-Gly-MePhe-Gly-ol (DAGO) decreased spontaneous firing, induced membrane hyperpolarization (12 +/- 2 mV; range 6-22 mV) and decreased the Rin (38 +/- 4%) of the beta-endorphin neurons. These effects of DAGO were blocked by the opioid antagonist naloxone (1 microM) and were not blocked by 1 microM TTX. DAGO-responsive cells were unaffected by either kappa- or delta-receptor opioid agonists. These results indicate that mu-receptors may be autoreceptors on ARC beta-endorphin neurons and that activation of opioid mu-receptors hyperpolarizes beta-endorphin neurons via an increase in K+ conductance. Therefore, opioid peptides may modulate opioid tone through an 'ultra-short loop' feedback control mechanism.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • Bacterial Proteins
  • Cell Membrane / physiology
  • Endorphins / pharmacology*
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)-
  • Enkephalins / pharmacology
  • Female
  • Fluorescein-5-isothiocyanate
  • Fluoresceins
  • Fluorescent Antibody Technique
  • Fluorescent Dyes
  • Guinea Pigs
  • Lysine / analogs & derivatives
  • Membrane Potentials / drug effects
  • Microscopy, Fluorescence
  • Naloxone / pharmacology
  • Neurons / drug effects
  • Neurons / physiology*
  • Potassium Channels / drug effects
  • Potassium Channels / physiology*
  • Receptors, Opioid / physiology*
  • Receptors, Opioid, mu
  • Streptavidin
  • Thiocyanates
  • beta-Endorphin / metabolism*

Substances

  • Bacterial Proteins
  • Endorphins
  • Enkephalins
  • Fluoresceins
  • Fluorescent Dyes
  • Potassium Channels
  • Receptors, Opioid
  • Receptors, Opioid, mu
  • Thiocyanates
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)-
  • Naloxone
  • beta-Endorphin
  • Streptavidin
  • biocytin
  • Fluorescein-5-isothiocyanate
  • Lysine