High Speed Two-Photon Imaging of Calcium Dynamics in Dendritic Spines: Consequences for Spine Calcium Kinetics and Buffer Capacity

Hdl Handle:
http://hdl.handle.net/10675.2/537
Title:
High Speed Two-Photon Imaging of Calcium Dynamics in Dendritic Spines: Consequences for Spine Calcium Kinetics and Buffer Capacity
Authors:
Cornelisse, L. Niels; van Elburg, Ronald A. J.; Meredith, Rhiannon M.; Yuste, Rafael; Mansvelder, Huibert D.
Abstract:
Rapid calcium concentration changes in postsynaptic structures are crucial for synaptic plasticity. Thus far, the determinants of postsynaptic calcium dynamics have been studied predominantly based on the decay kinetics of calcium transients. Calcium rise times in spines in response to single action potentials (AP) are almost never measured due to technical limitations, but they could be crucial for synaptic plasticity. With high-speed, precisely-targeted, two-photon point imaging we measured both calcium rise and decay kinetics in spines and secondary dendrites in neocortical pyramidal neurons. We found that both rise and decay kinetics of changes in calcium-indicator fluorescence are about twice as fast in spines. During AP trains, spine calcium changes follow each AP, but not in dendrites. Apart from the higher surface-to-volume ratio (SVR), we observed that neocortical dendritic spines have a markedly smaller endogenous buffer capacity with respect to their parental dendrites. Calcium influx time course and calcium extrusion rate were both in the same range for spines and dendrites when fitted with a dynamic multi-compartment model that included calcium binding kinetics and diffusion. In a subsequent analysis we used this model to investigate which parameters are critical determinants in spine calcium dynamics. The model confirmed the experimental findings: a higher SVR is not sufficient by itself to explain the faster rise time kinetics in spines, but only when paired with a lower buffer capacity in spines. Simulations at zero calcium-dye conditions show that calmodulin is more efficiently activated in spines, which indicates that spine morphology and buffering conditions in neocortical spines favor synaptic plasticity.
Editors:
Mei, Lin
Citation:
PLoS ONE. 2007 Oct 24; 2(10):e1073
Issue Date:
24-Oct-2007
URI:
http://hdl.handle.net/10675.2/537
DOI:
10.1371/journal.pone.0001073
PubMed ID:
17957255
PubMed Central ID:
PMC2034355
Type:
Article
ISSN:
1932-6203
Appears in Collections:
Department of Neurology: Faculty Research and Presentations

Full metadata record

DC FieldValue Language
dc.contributor.authorCornelisse, L. Nielsen_US
dc.contributor.authorvan Elburg, Ronald A. J.en_US
dc.contributor.authorMeredith, Rhiannon M.en_US
dc.contributor.authorYuste, Rafaelen_US
dc.contributor.authorMansvelder, Huibert D.en_US
dc.contributor.editorMei, Lin-
dc.date.accessioned2012-10-26T16:26:34Z-
dc.date.available2012-10-26T16:26:34Z-
dc.date.issued2007-10-24en_US
dc.identifier.citationPLoS ONE. 2007 Oct 24; 2(10):e1073en_US
dc.identifier.issn1932-6203en_US
dc.identifier.pmid17957255en_US
dc.identifier.doi10.1371/journal.pone.0001073en_US
dc.identifier.urihttp://hdl.handle.net/10675.2/537-
dc.description.abstractRapid calcium concentration changes in postsynaptic structures are crucial for synaptic plasticity. Thus far, the determinants of postsynaptic calcium dynamics have been studied predominantly based on the decay kinetics of calcium transients. Calcium rise times in spines in response to single action potentials (AP) are almost never measured due to technical limitations, but they could be crucial for synaptic plasticity. With high-speed, precisely-targeted, two-photon point imaging we measured both calcium rise and decay kinetics in spines and secondary dendrites in neocortical pyramidal neurons. We found that both rise and decay kinetics of changes in calcium-indicator fluorescence are about twice as fast in spines. During AP trains, spine calcium changes follow each AP, but not in dendrites. Apart from the higher surface-to-volume ratio (SVR), we observed that neocortical dendritic spines have a markedly smaller endogenous buffer capacity with respect to their parental dendrites. Calcium influx time course and calcium extrusion rate were both in the same range for spines and dendrites when fitted with a dynamic multi-compartment model that included calcium binding kinetics and diffusion. In a subsequent analysis we used this model to investigate which parameters are critical determinants in spine calcium dynamics. The model confirmed the experimental findings: a higher SVR is not sufficient by itself to explain the faster rise time kinetics in spines, but only when paired with a lower buffer capacity in spines. Simulations at zero calcium-dye conditions show that calmodulin is more efficiently activated in spines, which indicates that spine morphology and buffering conditions in neocortical spines favor synaptic plasticity.en_US
dc.rightsCornelisse et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.en_US
dc.subjectResearch Articleen_US
dc.subjectBiochemistry/Cell Signaling and Trafficking Structuresen_US
dc.subjectBiochemistry/Theory and Simulationen_US
dc.subjectBiophysics/Cell Signaling and Trafficking Structuresen_US
dc.subjectBiophysics/Theory and Simulationen_US
dc.subjectCell Biology/Neuronal and Glial Cell Biologyen_US
dc.subjectCell Biology/Neuronal Signaling Mechanismsen_US
dc.subjectComputational Biology/Computational Neuroscienceen_US
dc.subjectNeuroscience/Neuronal and Glial Cell Biologyen_US
dc.subjectNeuroscience/Neuronal Signaling Mechanismsen_US
dc.subjectNeuroscience/Theoretical Neuroscienceen_US
dc.titleHigh Speed Two-Photon Imaging of Calcium Dynamics in Dendritic Spines: Consequences for Spine Calcium Kinetics and Buffer Capacityen_US
dc.typeArticleen_US
dc.identifier.pmcidPMC2034355en_US
dc.contributor.corporatenameDepartment of Neurology-
dc.contributor.corporatenameCollege of Graduate Studies-
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