Target-specific regulation of synaptic amplitudes in the neocortex

J Neurosci. 2005 Jan 26;25(4):1024-33. doi: 10.1523/JNEUROSCI.3951-04.2005.

Abstract

In layers 2/3 in the rat visual cortex, glutamatergic synapses, between pyramidal neurons and GABAergic interneurons, show target-specific depression or facilitation. To study the mechanisms regulating these short-term synaptic modifications, we recorded from synaptically connected pyramidal neurons (presynaptic) and multipolar or bitufted interneurons (postsynaptic). Evoked AMPA receptor (AMPAR)- or NMDA receptor (NMDAR)-mediated EPSCs were pharmacologically isolated at these pyramidal-to-interneuron synapses while altering release probability (P(r)) by changing the extracellular Ca2+ concentration ([Ca2+]o). At the pyramidal-to-multipolar synapse, which shows paired-pulse depression, elevation of [Ca2+]o from physiological concentrations (2 mm) to 3 mm increased the amplitude of the initial AMPAR-mediated EPSC and enhanced paired-pulse depression. In contrast, the initial NMDAR-mediated EPSC did not change in amplitude with raised P(r) nor was paired-pulse depression altered. This lack of an increase of NMDAR-mediated currents is not a result of Ca2+-dependent effects on the NMDAR. Rather, at the pyramidal-to-multipolar synapse, raised P(r) increases the transient glutamate concentration at individual release sites, possibly reflecting multivesicular release. In contrast, at the pyramidal-to-bitufted synapse, which shows facilitation, AMPAR- and NMDAR-meditated EPSCs showed parallel increases in response to raised P(r). Thus, our results reveal differential recruitment of AMPA and NMDARs at depressing and facilitating synapses in layers 2/3 of the cortex and suggest that the mechanisms regulating dynamic aspects of synaptic transmission are target specific.

Publication types

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

MeSH terms

  • Animals
  • Calcium / physiology
  • Dipeptides / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • In Vitro Techniques
  • Interneurons / physiology
  • Neocortex / physiology*
  • Neuronal Plasticity / physiology
  • Pyramidal Cells / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / physiology
  • Receptors, Glutamate / physiology*
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Synapses / drug effects
  • Synapses / physiology*
  • Synaptic Vesicles / physiology
  • Visual Cortex / physiology

Substances

  • Dipeptides
  • Receptors, AMPA
  • Receptors, Glutamate
  • Receptors, N-Methyl-D-Aspartate
  • gamma-glutamylglycine
  • Calcium