Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro

1. Inhibitory postsynaptic currents (IPSCs) evoked in CAI pyramidal cells ( n = 46) by identified interneurones (n = 43) located in str. oriens were re corded in order to compare their functional properties and to determine the effect of synapse location on the apparent IPXC kinetics as recorded using somatic voltage clamp at -70 mV and nearly symmetrical [Cl-]. 2. Five types of visualised presynaptic interneurone, oriens-lacunosum mole culare (O-LMC), basket (BC), axo-axonic (AAC), bistratified (BiC) and orien s-bistratified (O-BiC) cells, were distinguished by immunocytochemistry and /or synapse location using light and electron microscopy. 3. Somatostatin immunoreactive O-LMCs, innervating the most distal dendriti c shafts and spines, evoked the smallest amplitude (26 +/- 10 pA, S.E.M., n = 8) and slowest IPSCs (10-90% rise time, 6.2 +/- 0.6 ms; decay, 20.8 +/- 1.7 ms, n = 8), with no paired-pulse modulation of the second IPXC (93 +/- 4%) at 100 ms interspike interval. In contrast, parvalbumin-positive AACs e voked larger amplitude (308 +/- 103 pA, n = 7) and kinetically faster (rise time, 0.8 +/- 0.1 ms; decay 11.2 +/- 0.9 ms, n = 7) IPSCs showing paired-p ulse depression (to 68 +/- 5%, n = 6). Parvalbumin- or CCK-positive BCs (n = 9) terminating on soma/dendrites, BiCs (n = 4) and O-BiCs (n = 7) innerva ting dendrites evoked IPSCs with intermediate kinetic parameters. The prope rties of IPSCs and sensitivity to bicuculline indicated that they were medi ated by GABA(A) receptors. 4. In three cases, kinetically complex, multiphasic IPSCs, evoked by an act ion potential in the recorded basket cells, suggested that coupled interneu rones, possibly through electrotonic junctions, converged on the same posts ynaptic neurone. 5. The population of O-BiCs (4 of 4 somatostatin positive) characterised in this study had horizontal dendrites restricted to str. oriens/alveus and i nnervated stratum radiatum and oriens. Other BiCs had radial dendrites as d escribed earlier. The parameters of IPSCs evoked by BiCs and O-BiCs showed, the largest cell to cell variation, and a single interneurone could evoke b oth small and slow as well as large and relatively fast IPSCs. 6. The kinetic properties of the somatically recorded postsynaptic current are correlated with the innervated cell surface domain. A significant corre lation of rise and decay times for the overall population of unitary IPSCs suggests that electrotonic filtering of distal responses is a major factor for the location and cell type specific differences of unitary IPSCs, but m olecular heterogeneity of postsynaptic GABA(A) receptors may also contribut e to the observed kinetic differences. Furthermore, domain specific differe nces in the short-term plasticity of the postsynaptic response indicate a d ifferentiation of interneurones in activity-dependent responses.