Distinct Local Circuits Between Neocortical Pyramidal Cells and Fast-Spiking Interneurons in Young Adult Rats

Abstract

Connections between layer V pyramidal cells and GABAergic fast-spiking interneurons (pyramidal-FS) were studied by paired recordings combined with morphological analyses in acute neocortical slices from 28- to 52-day-old rats. Pairs of spikes elicited in pyramidal cells at a stimulation rate of 0.2 Hz induced unitary excitatory postsynaptic currents (EPSCs) in FS interneurons that displayed facilitation (48%), depression (38.5%), or neither depression nor facilitation (13.5%). Analyses of the EPSC amplitude distributions indicate that depressing connections always showed multiple functional release sites. On the contrary, facilitating connections consisted either of one or several release sites. At a holding potential of −72 mV, the quantal size ( q) and the release probability ( p) of facilitating connections with a single release site were –21.9 ± 7.5 pA and 0.49 ± 0.19 (SD), respectively. The mean q and the estimated number of release sites ( n) at connections showing multiple sites were obtained by decreasing the release probability and did not differ between depressing and facilitating synapses (depressing connections: q = –15.3 ± 2.5 pA, n = 5.1 ± 3, facilitating connections: q = –23.9 ± 9.8 pA, n = 7.8 ± 5.4). However, the quantal content at facilitating synapses with multiple sites (1.9 ± 1.5) was significantly different from that at depressing connections (4.1 ± 3.9). Finally, quantitative morphological analyses revealed that most of the pyramidal cells displaying facilitation can be differentiated from those displaying depression by a more densely branched apical dendritic tree. Therefore two types of morphologically distinct pyramidal cells form excitatory connections with FS interneurons that differ in their short-term plasticity characteristics. Facilitating and depressing connections may provide a differential control of the temporal information processing of FS cells and thus finely regulate the inhibitory effect of these interneurons in neocortical networks of young adult rats.