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Ryanodine receptor activation induces long-term plasticity of spine calcium dynamics

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Item Type:Article
Title:Ryanodine receptor activation induces long-term plasticity of spine calcium dynamics
Creators Name:Johenning, F.W. and Theis, A.K. and Pannasch, U. and Rückl, M. and Rüdiger, S. and Schmitz, D.
Abstract:A key feature of signalling in dendritic spines is the synapse-specific transduction of short electrical signals into biochemical responses. Ca(2+) is a major upstream effector in this transduction cascade, serving both as a depolarising electrical charge carrier at the membrane and an intracellular second messenger. Upon action potential firing, the majority of spines are subject to global back-propagating action potential (bAP) Ca(2+) transients. These transients translate neuronal suprathreshold activation into intracellular biochemical events. Using a combination of electrophysiology, two-photon Ca(2+) imaging, and modelling, we demonstrate that bAPs are electrochemically coupled to Ca2+ release from intracellular stores via ryanodine receptors (RyRs). We describe a new function mediated by spine RyRs: the activity-dependent long-term enhancement of the bAP-Ca(2+) transient. Spines regulate bAP Ca(2+) influx independent of each other, as bAP-Ca(2+) transient enhancement is compartmentalized and independent of the dendritic Ca(2+) transient. Furthermore, this functional state change depends exclusively on bAPs travelling antidromically into dendrites and spines. Induction, but not expression, of bAP-Ca(2+) transient enhancement is a spine-specific function of the RyR. We demonstrate that RyRs can form specific Ca(2+) signalling nanodomains within single spines. Functionally, RyR mediated Ca(2+) release in these nanodomains induces a new form of Ca(2+) transient plasticity that constitutes a spine specific storage mechanism of neuronal suprathreshold activity patterns.
Keywords:Action Potentials, Calcium, Dendritic Spines, Entorhinal Cortex, Hippocampal CA1 Region, Neuronal Plasticity, Patch-Clamp Techniques, Ryanodine Receptor Calcium Release Channel, Wistar Rats, Animals, Rats
Source:PLoS Biology
Publisher:Public Library of Science
Page Range:e1002181
Date:22 June 2015
Official Publication:https://doi.org/10.1371/journal.pbio.1002181
PubMed:View item in PubMed

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