Enhanced Intrinsic Excitability in Basket Cells Maintains Excitatory-Inhibitory Balance in Hippocampal Circuits

The dynamics of inhibitory circuits in the cortex is thought to rely mainly on synaptic modifications. We challenge this view by showing that hippocampal parvalbumin-positive basket cells (PV-BCs) of the CA1 region express long-term (>30 min) potentiation of intrinsic neuronal excitability (LTP-IEPV-BC) upon brief repetitive stimulation of the Schaffer collaterals. LTP-IEPV-BC is induced by synaptic activation of metabotropic glutamate receptor subtype 5 (mGluR5) and mediated by the downregulation of Kv1 channel activity. LTP-IEPV-BC promotes spiking activity at the gamma frequency (∼35 Hz) and facilitates recruitment of PV-BCs to balance synaptic and intrinsic excitation in pyramidal neurons. In conclusion, activity-dependent modulation of intrinsic neuronal excitability in PV-BCs maintains excitatory-inhibitory balance and thus plays a major role in the dynamics of hippocampal circuits. ► The dynamics of inhibitory circuits is thought to rely on synaptic modifications ► Results show that basket cells express persistent increase in neuronal excitability ► This plasticity depends on mGluR5 and involves the regulation of Kv1 channels ► This plasticity facilitates recruitment of basket cells to balance excitation Campanac et al. show that stimulation of glutamatergic synapses induces long-lasting enhancement of intrinsic neuronal excitability in a subset of hippocampal inhibitory interneurons. This plasticity has important consequences in hippocampal circuits.