Ryanodine Receptor Activation Induces Long-Term Plasticity of Spine Calcium Dynamics

• Published in: PLoS biology Vol. 13; no. 6; p. e1002181
• Main Authors: Johenning, Friedrich W., Theis, Anne-Kathrin, Pannasch, Ulrike, Rückl, Martin, Rüdiger, Sten, Schmitz, Dietmar
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.06.2015; Public Library of Science (PLoS)
• Subjects: Action Potentials; Animals; CA1 Region, Hippocampal - metabolism; Calcium; Calcium - metabolism; Data analysis; Dendritic Spines - metabolism; Endoplasmic reticulum; Entorhinal Cortex - metabolism; Experiments; Gene expression; Neuronal Plasticity; Patch-Clamp Techniques; Rats, Wistar; Rodents; Ryanodine Receptor Calcium Release Channel - metabolism; Signal processing
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.1002181

A key feature of signalling in dendritic spines is the synapse-specific transduction of short electrical signals into biochemical responses. Ca2+ 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) Ca2+ transients. These transients translate neuronal suprathreshold activation into intracellular biochemical events. Using a combination of electrophysiology, two-photon Ca2+ 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-Ca2+ transient. Spines regulate bAP Ca2+ influx independent of each other, as bAP-Ca2+ transient enhancement is compartmentalized and independent of the dendritic Ca2+ transient. Furthermore, this functional state change depends exclusively on bAPs travelling antidromically into dendrites and spines. Induction, but not expression, of bAP-Ca2+ transient enhancement is a spine-specific function of the RyR. We demonstrate that RyRs can form specific Ca2+ signalling nanodomains within single spines. Functionally, RyR mediated Ca2+ release in these nanodomains induces a new form of Ca2+ transient plasticity that constitutes a spine specific storage mechanism of neuronal suprathreshold activity patterns.