Learning increases intrinsic excitability of hippocampal interneurons

J Neurosci. 2013 Mar 27;33(13):5499-506. doi: 10.1523/JNEUROSCI.4068-12.2013.

Abstract

Learning-related intrinsic excitability changes of pyramidal neurons via modulation of the postburst afterhyperpolarization (AHP) have been repeatedly demonstrated in multiple brain regions (especially the hippocampus), after a variety of learning tasks, and in multiple species. While exciting and important, the changes in pyramidal neurons are only a part of the neural circuitry involved in successful learning. For a more complete picture of the dynamic learning-related changes in the neural network, changes in inhibitory circuitry must also be systematically examined and characterized. Here we show in young adult rats and mice that learning the hippocampus-dependent trace eyeblink conditioning task induces enhanced inhibition onto CA1 pyramidal neurons mediated, in part, by an increase in intrinsic excitability of somatostatin-positive inhibitory neurons (SOMs). Furthermore, both CA1 pyramidal and SOM interneurons shared a common cellular mechanism (reduction in SK channel-mediated AHP) that led to the learning-induced increased intrinsic excitability.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / physiology*
  • Analysis of Variance
  • Animals
  • Conditioning, Eyelid / physiology*
  • Electric Stimulation
  • Electromyography
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology*
  • GABA Antagonists / pharmacology
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology*
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • Interneurons / physiology*
  • Male
  • Mice
  • Mice, Transgenic
  • Morpholines / pharmacology
  • Pyridazines / pharmacology
  • Rats
  • Sodium Channel Blockers / pharmacology
  • Somatostatin / metabolism
  • Tetrodotoxin / pharmacology

Substances

  • (+)-(S)-5,5-dimethylmorpholinyl-2-acetic acid
  • GABA Antagonists
  • Morpholines
  • Pyridazines
  • Sodium Channel Blockers
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Tetrodotoxin
  • Somatostatin
  • gabazine