Unitary IPSPs Evoked by Interneurons at the Stratum Radiatum-Stratum Lacunosum-Moleculare Border in the CA1 Area of the Rat Hippocampus in Vitro

J Physiol. 1998 Feb 1;506 ( Pt 3)(Pt 3):755-73. doi: 10.1111/j.1469-7793.1998.755bv.x.

Abstract

1. Hippocampal non-principal neurons at the stratum radiatum-stratum lacunosum-moleculare border (R-LM interneurons) of the CA1 area may constitute several cell classes and have been implicated in the generation of GABAergic unitary IPSPs. Using biocytin-filled electrodes we recorded R-LM interneurons intracellularly in vitro and determined their postsynaptic effects in concomitantly recorded pyramidal cells. 2. Light microscopic analysis revealed four populations of R-LM interneurons with distinct axons: (1) basket cells (n = 4) with axons predominantly ramifying in the pyramidal cell layer; (2) Schaffer collateral/commissural pathway-associated interneurons (n = 10) stratifying in stratum radiatum and, to a lesser extent, stratum oriens; (3) perforant pathway-associated interneurons (n = 6) innervating the perforant path termination zone in stratum lacunosum-moleculare of the CA1 area as well as equivalent portions of the dentate gyrus and subiculum; and (4) neurogliaform interneurons (n = 2) characterized by their dense, compact axonal and dendritic arbour. 3. Random electron microscopic sampling of synaptic targets revealed a preponderance of pyramidal neurons as postsynaptic elements. Basket cells had a synaptic target preference for somata and proximal dendrites, whereas the remainder of R-LM interneurons innervated dendritic shafts and spines. The axon of dendrite-targeting cells formed up to six putative contacts with individual postsynatpic pyramidal cells. 4. Anatomically recovered R-LM interneurons (n = 22) had a mean resting membrane potential of -56.7 +/- 3.6 mV, a membrane time constant of 12.9 +/- 7.7 ms and an input resistance of 86.4 +/- 29.2 M omega. Depolarizing current pulses generally elicited overshooting action potentials (70.8 +/- 6.9 mV) which had a mean duration, when measured at half-amplitude, of 0.7 +/- 0.1 ms. In response to prolonged (> 200 ms) depolarizing current pulses all R-LM interneurons displayed (a varying degree of) spike frequency adaptation. 5. Basket cells, Schaffer-associated and neurogliaform interneurons elicited small-amplitude (< 2 mV), short-latency IPSPs in postsynaptic pyramids (n = 5, 13 and 1, respectively). Those interactions in which an effect was elicited with the repetitive activation of the presynaptic neuron (n = 13) showed a substantial degree of postsynaptic response summation. Unitary IPSPs had fast kinetics and, whenever tested (n = 5; 1 basket cell and 4 Schaffer-associated interneurons), were abolished by the GABAA receptor antagonist bicuculline. 6. Thus, R-LM interneurons comprise several distinct populations which evoke fast GABAA receptor mediated IPSPs. The domain-specific innervation of postsynaptic pyramidal cells suggests functionally diverse effects on the integration of afferent information in functionally non-equivalent compartments of pyramidal cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Axons / physiology
  • Axons / ultrastructure
  • Electric Stimulation
  • Electrophysiology
  • Excitatory Postsynaptic Potentials / physiology*
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Hippocampus / ultrastructure
  • In Vitro Techniques
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Membrane Potentials / physiology
  • Microscopy, Electron
  • Neuroglia / physiology
  • Neuroglia / ultrastructure
  • Patch-Clamp Techniques
  • Rats
  • Rats, Wistar
  • Synapses / physiology
  • Synapses / ultrastructure