Dynamics of Action Potential Firing in Electrically Connected Striatal Fast-Spiking Interneurons

Front Cell Neurosci. 2013 Nov 14;7:209. doi: 10.3389/fncel.2013.00209. eCollection 2013.

Abstract

Fast-spiking interneurons (FSIs) play a central role in organizing the output of striatal neural circuits, yet functional interactions between these cells are still largely unknown. Here we investigated the interplay of action potential (AP) firing between electrically connected pairs of identified FSIs in mouse striatal slices. In addition to a loose coordination of firing activity mediated by membrane potential coupling, gap junctions (GJ) induced a frequency-dependent inhibition of spike discharge in coupled cells. At relatively low firing rates (2-20 Hz), some APs were tightly synchronized whereas others were inhibited. However, burst firing at intermediate frequencies (25-60 Hz) mostly induced spike inhibition, while at frequencies >50-60 Hz FSI pairs tended to synchronize. Spike silencing occurred even in the absence of GABAergic synapses or persisted after a complete block of GABAA receptors. Pharmacological suppression of presynaptic spike afterhyperpolarization (AHP) caused postsynaptic spikelets to become more prone to trigger spikes at near-threshold potentials, leading to a mostly synchronous firing activity. The complex pattern of functional coordination mediated by GJ endows FSIs with peculiar dynamic properties that may be critical in controlling striatal-dependent behavior.

Keywords: GABA; action potential; fast-spiking interneurons; gap junctions; striatum.