Mechanisms underlying rule learning-induced enhancement of excitatory and inhibitory synaptic transmission

J Neurophysiol. 2012 Feb;107(4):1222-9. doi: 10.1152/jn.00356.2011. Epub 2011 Nov 30.

Abstract

Training rats to perform rapidly and efficiently in an olfactory discrimination task results in robust enhancement of excitatory and inhibitory synaptic connectivity in the rat piriform cortex, which is maintained for days after training. To explore the mechanisms by which such synaptic enhancement occurs, we recorded spontaneous miniature excitatory and inhibitory synaptic events in identified piriform cortex neurons from odor-trained, pseudo-trained, and naive rats. We show that olfactory discrimination learning induces profound enhancement in the averaged amplitude of AMPA receptor-mediated miniature synaptic events in piriform cortex pyramidal neurons. Such physiological modifications are apparent at least 4 days after learning completion and outlast learning-induced modifications in the number of spines on these neurons. Also, the averaged amplitude of GABA(A) receptor-mediated miniature inhibitory synaptic events was significantly enhanced following odor discrimination training. For both excitatory and inhibitory transmission, an increase in miniature postsynaptic current amplitude was evident in most of the recorded neurons; however, some neurons showed an exceptionally great increase in the amplitude of miniature events. For both excitatory and inhibitory transmission, the frequency of spontaneous synaptic events was not modified after learning. These results suggest that olfactory discrimination learning-induced enhancement of synaptic transmission in cortical neurons is mediated by postsynaptic modulation of AMPA receptor-dependent currents and balanced by long-lasting modulation of postsynaptic GABA(A) receptor-mediated currents.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • Analysis of Variance
  • Animals
  • Behavior, Animal
  • Bicuculline / pharmacology
  • Cerebral Cortex / cytology
  • Discrimination Learning / physiology*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • GABA Antagonists / pharmacology
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / physiology
  • Male
  • Neurons / physiology*
  • Olfactory Pathways / physiology*
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Smell / physiology*
  • Sodium Channel Blockers / pharmacology
  • Synaptic Transmission / physiology*
  • Tetrodotoxin / pharmacology

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Quinoxalines
  • Sodium Channel Blockers
  • Tetrodotoxin
  • FG 9041
  • 2-Amino-5-phosphonovalerate
  • Bicuculline