Acetylcholine Facilitates a Depolarization-Induced Enhancement of Inhibition in Rat CA1 Pyramidal Neurons

Cereb Cortex. 2017 Jan 1;27(1):852-862. doi: 10.1093/cercor/bhv276.

Abstract

Cholinergic mechanisms in the hippocampus regulate forms of synaptic plasticity linked with cognition and spatial navigation, but the underlying mechanisms remain largely unknown. Here, in rat hippocampal CA1 pyramidal cells under blockade of ionotropic glutamate receptors, we report that a single acetylcholine pulse and repeated depolarization activated a robust and enduring postsynaptic depolarization-induced enhancement of inhibition (DEI) that masked a presynaptic depolarization-induced suppression of inhibition (DSI). Increased cytosolic Ca2+ and M1-muscarinic receptor activation caused the rise in voltage-sensitive α5βγ2-containing γ-aminobutyric acid type-A receptors that generated DEI. In summary, this muscarinic-mediated activity-dependent plasticity rapidly transfers depolarization effects on inhibition from presynaptic suppression or DSI to postsynaptic enhancement or DEI, a change potentially relevant in behavior.

Keywords: GABAA-LTP; GPCR activity; cytosolic Ca2+; negative feedback; α5βγ2-GABAARs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / metabolism*
  • Animals
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / metabolism*
  • Calcium / metabolism
  • Cytosol / drug effects
  • Cytosol / metabolism
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology*
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Patch-Clamp Techniques
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism*
  • Rats, Wistar
  • Receptor, Cannabinoid, CB1 / metabolism
  • Receptor, Muscarinic M1 / metabolism
  • Receptors, G-Protein-Coupled / metabolism
  • Receptors, GABA-A / metabolism
  • Tissue Culture Techniques

Substances

  • Cnr1 protein, rat
  • Receptor, Cannabinoid, CB1
  • Receptor, Muscarinic M1
  • Receptors, G-Protein-Coupled
  • Receptors, GABA-A
  • Acetylcholine
  • Calcium