Distribution of GABAergic synapses and their targets in the dentate gyrus of rat: a quantitative immunoelectron microscopic analysis.

The dentate gyrus has been shown to receive a laminated and target selective GABAergic input (Han et al., 1993; Halasy and Somogyi, 1993), but the numerical parameters of this innervation are not known. In order to establish the relative weight of GABAergic inputs to the dendritic versus somatic regions of granule cells the numerical density and proportion of GABA-immunopositive and immunonegative synaptic boutons and their postsynaptic targets were determined in the molecular and granule cell layers of the dentate gyrus using the postembedding immunogold method. The granule cell layer contained 9% of all synapses with the remaining 91% being in the molecular layer. Altogether 17% of all synaptic boutons were GABA-immunoreactive, and they formed either type 1 or type 2 synaptic junctions. About 88% of synaptic boutons in the granule cell layer and 7-8% in the molecular layer were GABA-positive. However, the numerical density (number of synapses per unit volume) of GABA-immunoreactive type 2 synapses was calculated to be only slightly less in the molecular layer than in the granule cell layer (100 x 10(6)/mm3 tissue in the granule cell layer and about 86 x 10(6)/mm3 in the molecular layer). In addition, GABA-positive type 1 synapses were found in lower number at the border region of the two layers. The mean volume of the molecular layer of the dentate gyrus in the Wistar rat was calculated to be nearly 4 times larger than the volume of the granule cell layer (West and Andersen, 1980). This means that 25-26% of all GABAergic type 2 synapses are located in the granule cell layer, and 74-75% in the molecular layer. The mean postsynaptic targets of the GABA-immunoreactive boutons in the granule cell layer were granule cell somata (46-60%), followed by dendritic shafts (26-29%), spines (up to 14%), and axon initial segments (7-9%). In the molecular layer the dominant postsynaptic targets of GABAergic synapses were dendritic shafts (63-72%), followed by dendritic spines (26-37%). About 2-3% of the targets of all GABA-immunoreactive synapses were GABA-immunoreactive dendritic shafts or somata. Up to 98% of all GABA-immunonegative synaptic boutons were found in the molecular layer, most of them terminating on dendritic spines. These results show that the dendritic region of the granule cells provides sites for GABAergic inhibition which in quantitative terms highly outnumber the somatic region in the dentate gyrus.