Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network

Mutual synaptic interactions between GABAergic interneurons are thought to be of critical importance for the generation of network oscillations and fo r temporal encoding of information in the hippocampus. However, the functio nal properties of synaptic transmission between hippocampal interneurons ar e largely unknown. We have made paired recordings from basket cells (BCs) i n the dentate gyrus of rat hippocampal slices, followed by correlated light and electron microscopical analysis. Unitary GABA(A) receptor-mediated IPS Cs at BC-BC synapses recorded at the soma showed a fast rise and decay, wit h a mean decay time constant of 2.5 +/- 0.2 msec (32 degreesC). Synaptic tr ansmission at BC-BC synapses showed paired-pulse depression (PPD) (32 +/- 5 % for 10 msec interpulse intervals) and multiple-pulse depression during re petitive stimulation. Detailed passive cable model simulations based on som atodendritic morphology and localization of synaptic contacts further indic ated that the conductance change at the postsynaptic site was even faster, decaying with a mean time constant of 1.8 +/- 0.6 msec. Sequential triple r ecordings revealed that the decay time course of IPSCs at BC-BC synapses wa s approximately twofold faster than that at BC-granule cell synapses, where as the extent of PPD was comparable. To examine the consequences of the fas t postsynaptic conductance change for the generation of oscillatory activit y, we developed a computational model of an interneuron network. The model showed robust oscillations at frequencies >60 Hz if the excitatory drive wa s sufficiently large. Thus the fast conductance change at interneuron-inter neuron synapses may promote the generation of high-frequency oscillations o bserved in the dentate gyrus in vivo.