Synaptic cross talk between perisomatic-targeting interneuron classes expressing cholecystokinin and parvalbumin in hippocampus

J Neurosci. 2009 Apr 1;29(13):4140-54. doi: 10.1523/JNEUROSCI.5264-08.2009.

Abstract

Cholescystokinin (CCK)- or parvalbumin (PV)-containing interneurons are the major perisomatic-targeting interneurons in the cerebral cortex, including hippocampus, and are thought to form mutually exclusive networks. We used several techniques to test the alternative hypothesis that CCK and PV cells are coupled by chemical synapses. Triple immunofluorescence confocal microscopy revealed numerous axosomatic, axodendritic, and axoaxonic contacts stained for CCK, PV, and the presynaptic marker synaptophysin. The existence of mutual CCK and PV synapses was supported by dual EM immunolabeling. Paired whole-cell recordings detected unitary GABA(A)ergic synaptic transmission between identified CCK and PV cells, and single CCK cells could transiently inhibit action potential firing of synaptically coupled PV cells. We conclude that the major hippocampal perisomatic-targeting interneurons communicate synaptically. This communication should affect neuronal network activity, including neuronal oscillations, in which the CCK and PV cells have well established roles. The prevalence of CCK and PV networks in other brain regions suggests that internetwork interactions could be generally important.

Publication types

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

MeSH terms

  • Acetylcholine / pharmacology
  • Action Potentials / drug effects
  • Animals
  • Axons / physiology
  • Axons / ultrastructure
  • Biophysics
  • Cholecystokinin / metabolism*
  • Electric Stimulation / methods
  • Hippocampus / cytology*
  • Hippocampus / metabolism*
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / physiology
  • Interneurons / classification
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Lysine / analogs & derivatives
  • Lysine / metabolism
  • Male
  • Microscopy, Immunoelectron / methods
  • Neural Inhibition / drug effects
  • Parvalbumins / metabolism*
  • Patch-Clamp Techniques / methods
  • Rats
  • Rats, Sprague-Dawley
  • Synapses / classification
  • Synapses / physiology*
  • Synapses / ultrastructure
  • Synaptophysin / metabolism
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Parvalbumins
  • Synaptophysin
  • gamma-Aminobutyric Acid
  • Cholecystokinin
  • biocytin
  • Lysine
  • Acetylcholine