SYNAPTIC TARGET SELECTIVITY AND INPUT OF GABAERGIC BASKET AND BISTRATIFIED INTERNEURONS IN THE CA1 AREA OF THE RAT HIPPOCAMPUS

To assess the position of interneurons in the hippocampal network, fas t spiking cells were recorded intracellularly in vitro and filled with biocytin. Sixteen non-principal cells were selected on the basis of 1 ) cell bodies located in the pyramidal layer and in the middle of the slice, 2) extensive labeling of their axons, and 3) a branching patter n of the axon indicating that they were not axo-axonic cells. Examinat ion of their efferent synapses (n = 400) demonstrated that the cells m ade synapses on cell bodies, dendritic shafts, spines, and axon initia l segments (AIS), Statistical analysis of the distribution of differen t postsynaptic elements, together with published data (n = 288) for 12 similar cells, showed that the interneurons were heterogeneous with r egard to the frequency of synapses given to different parts of pyramid al cells. When the cells were grouped according to whether they had le ss or more than 40% somatic synaptic targets, each population appeared homogeneous. The population (n = 19) innervating a high proportion of somata (53 +/- 10%, SD) corresponds to basket cells. They also form s ynapses with proximal dendrites (44 +/- 12%) and rarely with AISs and spines. One well-filled basket cell had 8,859 boutons within the slice , covering an area of 0.331 mm(2) of pyramidal layer tangentially and containing 7,150 pyramidal cells, 933 (13%) of which were calculated t o be innervated, assuming that each pyramidal cell received nine to te n synapses. It was extrapolated that the intact axon probably had abou t 10,800 boutons innervating 1,140 pyramids. The proportion of innerva ted pyramidal cells decreased from 28% in the middle to 4% at the edge of the axonal field. The other group of neurons, the bistratified cel ls (n = 9), showed a preference for dendritic shafts (79 +/- 8%) and s pines (17 +/- 8%) as synaptic targets, rarely terminating on somata (4 +/- 8%). Their axonal field was significantly larger (1,250 +/- 180 m u m) in the medio-lateral direction than that of basket cells (760 +/- 130 mu m). The axon terminals of bistratified cells were smaller than those of basket cells. Furthermore, in contrast to bistratified cells , basket cells had a significant proportion of dendrites in stratum la cunosum-moleculare suggesting a direct entorhinal input. The results d efine two distinct types of GABAergic neuron innervating pyramidal cel ls in a spatially segregated manner and predict different functions fo r the two inputs. The perisomatic termination of basket cells is suite d for the synchronization of a subset of pyramidal cells that they sel ect from the population within their axonal field, whereas the termina tion of bistratified cells in conjunction with Schaffer collateral/com missural terminals may govern the timing of CA3 input and/or voltage-d ependent conductances in the dendrites. (C) 1996 Wiley-Liss, Inc.