Cell type-specific, presynaptic LTP of inhibitory synapses on fast-spiking GABAergic neurons in the mouse visual cortex

J Neurosci. 2012 Sep 19;32(38):13189-99. doi: 10.1523/JNEUROSCI.1386-12.2012.

Abstract

Properties and plasticity of inhibitory synapses on fast-spiking (FS) GABAergic (FS-GABA) interneurons in layer II/III of the mouse visual cortex were examined in cortical slices by whole-cell recordings of IPSCs or IPSPs evoked by activation of presynaptic FS or non-FS GABAergic interneurons. Unitary IPSCs (uIPSCs) evoked by action potentials of FS-GABA neurons have shorter onset latency, faster rising slope, higher peak amplitude, and faster decay time than those evoked by action potentials of non-FS-GABA neurons. Tetanic activation of presynaptic FS-GABA neurons induced long-term potentiation (LTP) of uIPSCs, whereas that of presynaptic non-FS-GABA neurons did not induce LTP, indicating that long-term plasticity of inhibitory synapses on FS-GABA neurons is pathway specific. For further analysis of inhibitory synaptic plasticity, IPSPs evoked by electrical stimulation of an adjacent site in the cortex were recorded from FS-GABA neurons. Theta burst stimulation induced LTP of IPSPs in 12 of 14 FS-GABA neurons. The paired-pulse stimulation protocol and coefficient of variation analysis indicated that this form of LTP may be presynaptic in origin. Filling postsynaptic cells with a Ca(2+) chelator did not block the induction of LTP, suggesting no involvement of postsynaptic Ca(2+) rise. Also, this form of LTP was dependent neither on metabotropic glutamate receptors nor voltage-gated Ca(2+) channels of the L and T types. Further pharmacological analysis indicated that voltage-gated Ca(2+) channels other than the P/Q type, such as N and R types, were not involved in LTP, suggesting that P/Q-type channels are a candidate for factors inducing LTP of inhibitory synapses between FS-GABA neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / genetics
  • Action Potentials / physiology*
  • Animals
  • Animals, Newborn
  • Bicuculline / pharmacology
  • Biophysical Phenomena / drug effects
  • Biophysical Phenomena / genetics
  • Biophysics
  • Calcium / metabolism
  • Calcium Channel Blockers / pharmacology
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • GABA-A Receptor Antagonists / pharmacology
  • GABAergic Neurons / classification
  • GABAergic Neurons / drug effects
  • GABAergic Neurons / physiology*
  • Glutamate Decarboxylase / genetics
  • Green Fluorescent Proteins / genetics
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / genetics
  • Long-Term Synaptic Depression / drug effects
  • Long-Term Synaptic Depression / genetics
  • Long-Term Synaptic Depression / physiology*
  • Mefloquine / pharmacology
  • Mice
  • Mice, Transgenic
  • Neural Inhibition / drug effects
  • Neural Inhibition / genetics
  • Neural Inhibition / physiology*
  • Patch-Clamp Techniques
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology
  • Synapses / classification
  • Synapses / drug effects
  • Synapses / genetics
  • Synapses / physiology*
  • Time Factors
  • Vesicular Inhibitory Amino Acid Transport Proteins / genetics
  • Visual Cortex / cytology*

Substances

  • Calcium Channel Blockers
  • Excitatory Amino Acid Antagonists
  • GABA-A Receptor Antagonists
  • Vesicular Inhibitory Amino Acid Transport Proteins
  • Viaat protein, mouse
  • Green Fluorescent Proteins
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1
  • Calcium
  • Mefloquine
  • Bicuculline