Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network

J Neurophysiol. 2005 Aug;94(2):1509-18. doi: 10.1152/jn.00957.2004. Epub 2005 Apr 27.

Abstract

The oriens-lacunosum moleculare (O-LM) subtype of interneuron is a key component in the formation of the theta rhythm (8-12 Hz) in the hippocampus. It is known that the CA1 region of the hippocampus can produce theta rhythms in vitro with all ionotropic excitation blocked, but the mechanisms by which this rhythmicity happens were previously unknown. Here we present a model suggesting that individual O-LM cells, by themselves, are capable of producing a single-cell theta-frequency firing, but coupled O-LM cells are not capable of producing a coherent population theta. By including in the model fast-spiking (FS) interneurons, which give rise to IPSPs that decay faster than those of the O-LM cells, coherent theta rhythms are produced. The inhibition to O-LM cells from the FS cells synchronizes the O-LM cells, but only when the FS cells themselves fire at a theta frequency. Reciprocal connections from the O-LM cells to the FS cells serve to parse the FS cell firing into theta bursts, which can then synchronize the O-LM cells. A component of the model O-LM cell critical to the synchronization mechanism is the hyperpolarization-activated h-current. The model can robustly reproduce relative phases of theta frequency activity in O-LM and FS cells.

Publication types

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

MeSH terms

  • Animals
  • Computer Simulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Hippocampus / cytology*
  • In Vitro Techniques
  • Interneurons / classification
  • Interneurons / physiology*
  • Interneurons / radiation effects
  • Ion Channels / physiology
  • Membrane Potentials / physiology
  • Membrane Potentials / radiation effects
  • Methoxyhydroxyphenylglycol / analogs & derivatives
  • Methoxyhydroxyphenylglycol / pharmacology
  • Neural Inhibition / physiology*
  • Neural Inhibition / radiation effects
  • Neural Networks, Computer*
  • Patch-Clamp Techniques / methods
  • Periodicity
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Wistar
  • Synaptic Transmission / physiology
  • Synaptic Transmission / radiation effects
  • Theta Rhythm*

Substances

  • Excitatory Amino Acid Antagonists
  • Ion Channels
  • Quinoxalines
  • 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline
  • Methoxyhydroxyphenylglycol
  • 3,4-dihydroxyphenylglycol