Synapse-Level Determination of Action Potential Duration by K+ Channel Clustering in Axons

• Published in: Neuron (Cambridge, Mass.) Mass.), 2016-07, Vol.91 (2), p.370-383
• Main Authors: Rowan, Matthew J.M., DelCanto, Gina, Yu, Jianqing J., Kamasawa, Naomi, Christie, Jason M.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Axons - physiology; Cerebellum - physiology; Colleges & universities; Interneurons - physiology; Lasers; Mice, Inbred C57BL; Microscopy; Morphology; Neurosciences; Patch-Clamp Techniques - methods; Plasmids; Potassium Channels - physiology; Presynaptic Terminals - physiology; Rodents; Simulation; Synapses - physiology; Synaptic Transmission - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2016.05.035

In axons, an action potential (AP) is thought to be broadcast as an unwavering binary pulse over its arbor, driving neurotransmission uniformly at release sites. Yet by recording from axons of cerebellar stellate cell (SC) interneurons, we show that AP width varies between presynaptic bouton sites, even within the same axon branch. The varicose geometry of SC boutons alone does not impose differences in spike duration. Rather, axonal patching revealed heterogeneous peak conductance densities of currents mediated mainly by fast-activating Kv3-type potassium channels, with clustered hotspots at boutons and restricted expression at adjoining shafts. Blockade of Kv channels at individual boutons indicates that currents immediately local to a release site direct spike repolarization at that location. Thus, the clustered arrangement and variable expression density of Kv3 channels at boutons are key determinants underlying compartmentalized control of AP width in a near synapse-by-synapse manner, multiplying the signaling capacity of these structures. •Spike duration varies between presynaptic boutons within an individual SC axon•The varicose geometry of presynaptic boutons does not alter spike duration•Fast-activating K+ channels are clustered at boutons and restricted from shafts•AP duration is determined by Kv3 channels immediately local to an individual bouton Rowan et al. find that APs are not uniformly represented across the axon arbor of SCs. Rather, spike duration is subject to local variation, determined at individual release sites, by clustering of fast-activating K+ channels, thus contributing to release heterogeneity.