Differences in the refractory properties of two distinct inhibitory circuitries in field CA1 of the hippocampus

Brain Res. 1995 Dec 18;704(2):298-306. doi: 10.1016/0006-8993(95)01137-4.

Abstract

Extracellular reflections of IPSPs were examined in two distinct circuitries in field CA1 of the hippocampus. Stimulation in the stratum radiatum in the presence of AMPA receptor antagonists elicited positive potentials in the same stratum that were eliminated by picrotoxin, a blocker of GABAA receptors. Laminar profile analysis revealed that the response was maximal in the stratum radiatum at a point well distal to the pyramidal cell body layer and had a negative reflection in the stratum oriens. These field IPSPs presumably mediate the feedforward inhibition normally activated by the Schaffer-commissural projections to field CA1. Stimulation of the alveus produced an antidromic response followed by a much slower positive potential in recordings collected in the pyramidal cell layer. The latter response was suppressed by AMPA receptor antagonists or picrotoxin, as expected for disynaptic, recurrent (feedback) inhibition. The laminar profile for the feedback field IPSPs had its maximum near the pyramidal cell layer and its negative dipole in the stratum radiatum. Feedforward IPSPs were inhibited by about 50% if they were preceded within 200 ms by a priming pulse while feedback IPSPs were reduced by less than 20% under comparable conditions. The refractory effect was minimally dependent on stimulation intensity but was strongly affected by an antagonist of GABAB receptors. Attempts to modify IPSPs in the s. radiatum with long trains of low frequency stimulation or with theta-burst stimulation were not successful, suggesting that GABAergic synapses do not have the plasticities found in their glutamatergic counterparts. These results indicate that interneurons contacted by the extrinsic afferents of hippocampus form GABAergic synapses that differ in terms of spatial location and functional properties from the synapses generated by interneurons innervated by the recurrent collaterals of the pyramidal cells. The findings also suggest that repetitive afferent activity, while reducing the influence of dendritic IPSPs on excitatory input, will leave feedback suppression of cell spiking largely intact.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Electrophysiology
  • Excitatory Amino Acid Antagonists / pharmacology
  • GABA Antagonists / pharmacology
  • Hippocampus / physiology*
  • Long-Term Potentiation / physiology
  • Neural Inhibition / physiology*
  • Neuronal Plasticity / physiology
  • Picrotoxin / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • gamma-Aminobutyric Acid / physiology

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • Picrotoxin
  • gamma-Aminobutyric Acid
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-Amino-5-phosphonovalerate