Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus

Abstract

To assess the position of interneurons in the hippocampal network, fast 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 pattern of the axon indicating that they were not axo‐axonic cells. Examination of their efferent synapses (n = 400) demonstrated that the cells made synapses on cell bodies, dendritic shafts, spines, and axon initial segments (AIS). Statistical analysis of the distribution of different postsynaptic elements, together with published data (n = 288) for 12 similar cells, showed that the interneurons were heterogeneous with regard to the frequency of synapses given to different parts of pyramidal cells. When the cells were grouped according to whether they had less 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 synapses 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 mm2 of pyramidal layer tangentially and containing 7,150 pyramidal cells, 933 (13%) of which were calculated to be innervated, assuming that each pyramidal cell received nine to ten synapses. It was extrapolated that the intact axon probably had about 10,800 boutons innervating 1,140 pyramids. The proportion of innervated pyramidal cells decreased from 28% in the middle to 4% at the edge of the axonal field. The other group of neurons, the bistratified cells (n = 9), showed a preference for dendritic shafts (79 ± 8%) and spines (17 ± 8%) as synaptic targets, rarely terminating on somata (4 ± 8%). Their axonal field was significantly larger (1,250 ± 180 μm) in the medio‐lateral direction than that of basket cells (760 ± 130 μm). 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 lacunosum‐moleculare suggesting a direct entorhinal input. The results define two distinct types of GABAergic neuron innervating pyramidal cells in a spatially segregated manner and predict different functions for the two inputs. The perisomatic termination of basket cells is suited for the synchronization of a subset of pyramidal cells that they select from the population within their axonal field, whereas the termination of bistratified cells in conjunction with Schaffer collateral/commissural terminals may govern the timing of CA3 input and/or voltage‐dependent conductances in the dendrites. © 1996 Wiley‐Liss, Inc.

GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus

“…In the tissue derived from tumor-induced epileptic tissue (in which the GABA release experiments have been done), we found that almost one-third of the CB1-positive cells were negative for CCK. In contrast, the absolute number and size of the boutons may vary widely across different interneuron types, 12,16,30 which likely correlates with the amount of released GABA, and may also explain the discrepancy between the quantitative data of the anatomical and pharmacological experiments.…”

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…18,37,86,102 This connectivity feature allows synchronous inhibition of a multitude of pyramidal cells; the estimated numbers range from several hundred up to 2,500 cells. 85,103,104 Together with the dendritictargeting interneurons, the pattern of convergence and divergence in hippocampal network connectivity thus reflects the intense feed-forward and feedback control of principal cells by GABAergic inhibition. 17,37,101,105,106 Importantly, PV þ basket cells and axo-axonic cells strongly increase their spiking rate during specific oscillating network states of the hippocampus, especially during theta-, gamma-, and ripple oscillations.…”

Synaptic Communication among Hippocampal Interneurons: Properties of Spontaneous IPSCs in Morphologically Identified Cells

“…Recent in vitro and in vivo studies using intracellular labeling methods have identified several hippocampal CA1 interneuron types and have classified them according to their input and output features (Buhl et al, 1994;McBain et al, 1994;Sik et al, 1995;Freund and Buzsáki, 1996;Halasy et al, 1996;Maccaferri and McBain, 1996). Numerous physiological recordings were obtained from interneurons in this hippocampal subfield, but only two groups of dendritic inhibitory cells, namely bistratified cells and O-LM cells (Buhl et al, 1994;McBain et al, 1994;Sik et al, 1995;Halasy et al, 1996), have been morphologically characterized in detail.…”

“…Numerous physiological recordings were obtained from interneurons in this hippocampal subfield, but only two groups of dendritic inhibitory cells, namely bistratified cells and O-LM cells (Buhl et al, 1994;McBain et al, 1994;Sik et al, 1995;Halasy et al, 1996), have been morphologically characterized in detail. These cell types have been confirmed in our study as well.…”