Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids

Nature. 2004 Sep 16;431(7006):312-6. doi: 10.1038/nature02913.

Abstract

Neocortical GABA-containing interneurons form complex functional networks responsible for feedforward and feedback inhibition and for the generation of cortical oscillations associated with several behavioural functions. We previously reported that fast-spiking (FS), but not low-threshold-spiking (LTS), neocortical interneurons from rats generate a fast and precise self-inhibition mediated by inhibitory autaptic transmission. Here we show that LTS cells possess a different form of self-inhibition. LTS, but not FS, interneurons undergo a prominent hyperpolarization mediated by an increased K+-channel conductance. This self-induced inhibition lasts for many minutes, is dependent on an increase in intracellular [Ca2+] and is blocked by the cannabinoid receptor antagonist AM251, indicating that it is mediated by the autocrine release of endogenous cannabinoids. Endocannabinoid-mediated slow self-inhibition represents a powerful and long-lasting mechanism that alters the intrinsic excitability of LTS neurons, which selectively target the major site of excitatory connections onto pyramidal neurons; that is, their dendrites. Thus, modulation of LTS networks after their sustained firing will lead to long-lasting changes of glutamate-mediated synaptic strength in pyramidal neurons, with consequences during normal and pathophysiological cortical network activities.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Signaling / drug effects
  • Cannabinoid Receptor Modulators / pharmacology*
  • Electrophysiology
  • Endocannabinoids*
  • In Vitro Techniques
  • Interneurons / drug effects*
  • Interneurons / physiology*
  • Membrane Potentials / drug effects
  • Neocortex / cytology*
  • Neocortex / drug effects
  • Neocortex / physiology
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / physiology
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Cannabinoid Receptor Modulators
  • Endocannabinoids
  • Calcium