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 postsynaptic 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 Ohm. 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 GABA(A) receptor antagonist
bicuculline. 6. Thus, R-LM interneurons comprise several distinct populations which
evoke fast GABA(A) 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.
