Ryanodine Receptor Activation Induces Long-Term Plasticity of Spine Calcium Dynamics
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 s...
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| Published in | PLoS biology Vol. 13; no. 6; p. e1002181 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.06.2015
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1002181 |
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| Abstract | 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. |
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| AbstractList | 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 Ca
2+
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.
A combination of two-photon calcium imaging, electrophysiology, and modelling shows how ryanodine receptors (a type of intracellular calcium channel) generate a signalling nanodomain within individual dendritic spines, enabling compartmentalized plasticity of calcium dynamics.
Experiences change neuronal circuits, and these circuit changes outlast the initial experiences. This means that, in neurons, the fast electrical activity encoding experiences needs to be transduced into longer-lived biochemical and structural changes. A key mediator between these two timescales of neuronal activity is the Ca
2+
ion. Ca
2+
serves both as an electric charge carrier mediating fast voltage changes at the membrane and as a second messenger activating intracellular signalling cascades. Even within the spatial confines of dendritic spines, the specialized domains of dendrites that receive synaptic connections, Ca
2+
encodes a versatile array of specific functions. In this study, we first demonstrate that voltage-gated Ca
2+
channels and ryanodine receptors, intracellular channels located on the membrane of the endoplasmic reticulum through which Ca
2+
can be released into the cytosol, are electrochemically coupled in single dendritic spines. We identify how ryanodine receptors induce enhancement of the Ca
2+
influx, mediated by the opening of voltage-gated Ca
2+
channels, induced by action potentials in a compartmentalized, spine-specific manner. Within the femtoliter volume of a single spine, specificity of this route of Ca
2+
-signalling is achieved by a signalling nanodomain centred on the ryanodine receptor. Our work stresses the role of the ryanodine receptor not only as an ion channel releasing Ca
2+
from the endoplasmic reticulum but also as a macromolecular complex generating specificity of Ca
2+
-signalling within the spatial constraints of a single spine. 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. 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. |
| Author | Johenning, Friedrich W. Rüdiger, Sten Pannasch, Ulrike Rückl, Martin Schmitz, Dietmar Theis, Anne-Kathrin |
| AuthorAffiliation | 2 Berlin Institute of Health (BIH), Berlin, Germany 6 DZNE- German Center for Neurodegenerative Diseases, Berlin, Germany The Salk Institute for Biological Studies, UNITED STATES 3 Institute of Physics, Humboldt Universität, Berlin, Germany 1 Neuroscience Research Center, Charité-Universitätsmedizin, Berlin, Germany 5 Cluster of Excellence ‘NeuroCure’, Charité-Universitätsmedizin, Berlin, Germany 4 Bernstein Center for Computational Neuroscience, Berlin, Germany |
| AuthorAffiliation_xml | – name: 1 Neuroscience Research Center, Charité-Universitätsmedizin, Berlin, Germany – name: 4 Bernstein Center for Computational Neuroscience, Berlin, Germany – name: The Salk Institute for Biological Studies, UNITED STATES – name: 5 Cluster of Excellence ‘NeuroCure’, Charité-Universitätsmedizin, Berlin, Germany – name: 6 DZNE- German Center for Neurodegenerative Diseases, Berlin, Germany – name: 3 Institute of Physics, Humboldt Universität, Berlin, Germany – name: 2 Berlin Institute of Health (BIH), Berlin, Germany |
| Author_xml | – sequence: 1 givenname: Friedrich W. surname: Johenning fullname: Johenning, Friedrich W. – sequence: 2 givenname: Anne-Kathrin surname: Theis fullname: Theis, Anne-Kathrin – sequence: 3 givenname: Ulrike surname: Pannasch fullname: Pannasch, Ulrike – sequence: 4 givenname: Martin surname: Rückl fullname: Rückl, Martin – sequence: 5 givenname: Sten surname: Rüdiger fullname: Rüdiger, Sten – sequence: 6 givenname: Dietmar surname: Schmitz fullname: Schmitz, Dietmar |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26098891$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1038/25547 10.1371/journal.pbio.1000190 10.1038/nature11554 10.1113/jphysiol.2005.098947 10.1038/35036035 10.1073/pnas.1210735110 10.1073/pnas.0605412104 10.1523/JNEUROSCI.5847-08.2009 10.1146/annurev-neuro-062111-150455 10.1152/physrev.00012.2013 10.1093/cercor/bhs315 10.1016/j.neuron.2004.11.016 10.1016/j.neuron.2005.01.003 10.1113/jphysiol.2009.184960 10.1038/25541 10.1038/35046076 10.1073/pnas.0905110106 10.1152/jn.2002.88.3.1270 10.1007/s00607-008-0003-x 10.1016/j.conb.2007.04.003 10.1073/pnas.1013580108 10.1093/cvr/cvr143 10.1523/JNEUROSCI.20-05-01791.2000 10.1146/annurev.biochem.76.053105.094237 10.1007/s00607-008-0004-9 10.1038/nrn3168 10.1093/cercor/bhs320 10.1155/2010/108190 10.1016/S0021-9258(19)85166-9 10.1016/j.pbiomolbio.2004.06.009 10.1523/JNEUROSCI.2474-10.2010 10.1146/annurev.ne.17.030194.002013 10.1371/journal.pcbi.1003965 10.1073/pnas.0608755103 10.1016/j.neuron.2010.12.009 10.1038/375682a0 10.1073/pnas.062510599 10.1523/JNEUROSCI.4561-10.2011 10.1016/j.cell.2012.06.052 10.1038/351751a0 10.1038/nn.3496 10.1126/science.1114816 10.1073/pnas.241516898 10.1152/jn.00422.2013 10.1016/j.neuron.2008.08.020 10.1038/sj.bjp.0704988 10.1016/S0006-3495(96)79272-X 10.1523/JNEUROSCI.1677-04.2004 10.1523/JNEUROSCI.2702-08.2008 10.1523/JNEUROSCI.5881-08.2009 10.1016/S0896-6273(02)00573-1 10.1038/nn1112 10.1096/fasebj.14.2.290 10.1038/81781 10.1523/JNEUROSCI.0573-09.2009 10.1038/nn1449 10.1111/j.1469-7793.1997.013bl.x 10.1016/j.neuron.2007.05.026 10.1016/S0031-6997(24)01313-9 10.1016/S0896-6273(00)80683-2 10.1016/S0896-6273(00)81125-3 10.1523/JNEUROSCI.19-11-04325.1999 10.1016/S0006-3495(02)75149-7 |
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| Copyright | 2015 Johenning et al 2015 Johenning et al 2015 Public Library of Science. 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: Johenning FW, Theis A-K, Pannasch U, Rückl M, Rüdiger S, Schmitz D (2015) Ryanodine Receptor Activation Induces Long-Term Plasticity of Spine Calcium Dynamics. PLoS Biol 13(6): e1002181. doi:10.1371/journal.pbio.1002181 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: FWJ AKT UP MR SR DS. Performed the experiments: FWJ AKT UP. Analyzed the data: FWJ AKT MR. Contributed reagents/materials/analysis tools: MR SR. Wrote the paper: FWJ AKT UP MR SR DS. The authors have declared that no competing interests exist. |
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| References | BL Bloodgood (ref37) 2009; 7 I Llano (ref26) 2000; 3 HR Ramay (ref64) 2011; 91 WN Ross (ref27) 2012; 13 LM Palmer (ref43) 2009; 29 W Zhao (ref52) 2000; 14 AM Stranahan (ref57) 2010; 2010 N Emptage (ref9) 1999; 22 JL Plotkin (ref15) 2013; 110 EA Finch (ref7) 1998; 396 T Hayama (ref50) 2013; 16 M Blatt (ref60) 2008; 82 A Lorincz (ref22) 2007; 104 JR Chalifoux (ref32) 2011; 31 Q Li (ref54) 2014; 24 I Goussakov (ref56) 2010; 30 A Grunditz (ref36) 2008; 28 H Ozaki (ref28) 2002; 137 P Beed (ref58) 2010; 68 K Holthoff (ref42) 2010; 588 J Kim (ref33) 2007; 54 R Yuste (ref6) 1995; 375 S Manita (ref18) 2009; 29 VM Sandler (ref24) 1999; 19 T Nakamura (ref13) 1999; 24 JL Sutko (ref20) 1997; 49 AJGD Holtmaat (ref59) 2005; 45 CR Raymond (ref11) 2005; 570 TM Hoogland (ref30) 2004; 24 KM Harris (ref3) 1994; 17 X Liu (ref55) 2012; 150 N Holbro (ref12) 2009; 106 EA Sobie (ref63) 2002; 83 UV Nägerl (ref41) 2004; 44 HK Kato (ref47) 2009; 29 BL Sabatini (ref1) 2002; 33 DR Laver (ref19) 1996; 71 O Garaschuk (ref16) 1997; 502 MT Harnett (ref38) 2012; 491 C Sala (ref14) 2014; 94 J Waters (ref46) 2005; 87 TJ Ngo-Anh (ref34) 2005; 8 R Araya (ref45) 2006; 103 BL Bloodgood (ref4) 2007; 17 Y Kovalchuk (ref10) 2000; 20 R Zalk (ref51) 2007; 76 BL Bloodgood (ref35) 2005; 310 SM Dudek (ref49) 2002; 99 MJ Berridge (ref2) 2000; 1 M Rückl (ref62) 2015; 11 MJ Higley (ref5) 2008; 59 H Takechi (ref8) 1998; 396 AT Gulledge (ref39) 2012; 7 PS McPherson (ref25) 1993; 268 YF Lu (ref17) 2002; 88 GG Du (ref21) 2001; 98 BL Sabatini (ref31) 2000; 408 R Yasuda (ref29) 2003; 6 R Yuste (ref40) 2013; 36 P Bastian (ref61) 2008; 82 R Yasuda (ref23) 2004; 219 MA Popovic (ref44) 2014; 24 T Adasme (ref53) 2011; 108 I Bezprozvanny (ref65) 1991; 351 O Bukalo (ref48) 2013; 110 |
| References_xml | – volume: 396 start-page: 757 issue: 6713 year: 1998 ident: ref8 article-title: A new class of synaptic response involving calcium release in dendritic spines publication-title: Nature doi: 10.1038/25547 – volume: 7 start-page: e1000190 issue: 9 year: 2009 ident: ref37 article-title: Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines publication-title: PLoS Biol doi: 10.1371/journal.pbio.1000190 – volume: 491 start-page: 599 issue: 7425 year: 2012 ident: ref38 article-title: Synaptic amplification by dendritic spines enhances input cooperativity publication-title: Nature doi: 10.1038/nature11554 – volume: 570 start-page: 97 issue: 1 year: 2005 ident: ref11 article-title: Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus publication-title: The Journal of Physiology doi: 10.1113/jphysiol.2005.098947 – volume: 1 start-page: 11 issue: 1 year: 2000 ident: ref2 article-title: The versatility and universality of calcium signalling publication-title: Nat Rev Mol Cell Biol doi: 10.1038/35036035 – volume: 110 start-page: 5175 issue: 13 year: 2013 ident: ref48 article-title: Synaptic plasticity by antidromic firing during hippocampal network oscillations publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.1210735110 – volume: 104 start-page: 1033 issue: 3 year: 2007 ident: ref22 article-title: Differential distribution of NCX1 contributes to spine-dendrite compartmentalization in CA1 pyramidal cells publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0605412104 – volume: 29 start-page: 6897 issue: 21 year: 2009 ident: ref43 article-title: Membrane potential changes in dendritic spines during action potentials and synaptic input publication-title: J Neurosci doi: 10.1523/JNEUROSCI.5847-08.2009 – volume: 36 start-page: 429 issue: 1 year: 2013 ident: ref40 article-title: Electrical Compartmentalization in Dendritic Spines publication-title: Annu Rev Neurosci doi: 10.1146/annurev-neuro-062111-150455 – volume: 219 start-page: l5 year: 2004 ident: ref23 article-title: Imaging calcium concentration dynamics in small neuronal compartments publication-title: Sci STKE – volume: 94 start-page: 141 issue: 1 year: 2014 ident: ref14 article-title: Dendritic spines: the locus of structural and functional plasticity publication-title: Physiological Reviews doi: 10.1152/physrev.00012.2013 – volume: 24 start-page: 353 issue: 2 year: 2014 ident: ref54 article-title: Making Synapses Strong: Metaplasticity Prolongs Associativity of Long-Term Memory by Switching Synaptic Tag Mechanisms publication-title: Cerebral Cortex doi: 10.1093/cercor/bhs315 – volume: 44 start-page: 759 issue: 5 year: 2004 ident: ref41 article-title: Bidirectional Activity-Dependent Morphological Plasticity in Hippocampal Neurons publication-title: Neuron doi: 10.1016/j.neuron.2004.11.016 – volume: 7 start-page: e36007 issue: 4 year: 2012 ident: ref39 article-title: Electrical Advantages of Dendritic Spines. Mansvelder HD, editor – volume: 45 start-page: 279 issue: 2 year: 2005 ident: ref59 article-title: Transient and Persistent Dendritic Spines in the Neocortex In Vivo publication-title: Neuron doi: 10.1016/j.neuron.2005.01.003 – volume: 588 start-page: 1085 issue: Pt 7 year: 2010 ident: ref42 article-title: Rapid time course of action potentials in spines and remote dendrites of mouse visual cortex neurons publication-title: The Journal of Physiology doi: 10.1113/jphysiol.2009.184960 – volume: 396 start-page: 753 issue: 6713 year: 1998 ident: ref7 article-title: Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites publication-title: Nature doi: 10.1038/25541 – volume: 408 start-page: 589 issue: 6812 year: 2000 ident: ref31 article-title: Analysis of calcium channels in single spines using optical fluctuation analysis publication-title: Nature doi: 10.1038/35046076 – volume: 106 start-page: 15055 issue: 35 year: 2009 ident: ref12 article-title: Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0905110106 – volume: 88 start-page: 1270 issue: 3 year: 2002 ident: ref17 article-title: Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus publication-title: Journal of Neurophysiology doi: 10.1152/jn.2002.88.3.1270 – volume: 82 start-page: 103 year: 2008 ident: ref60 article-title: A generic grid interface for parallel and adaptive scientific computing. Part I: abstract framework publication-title: Computing doi: 10.1007/s00607-008-0003-x – volume: 17 start-page: 345 issue: 3 year: 2007 ident: ref4 article-title: Ca2+ signaling in dendritic spines publication-title: Current Opinion in Neurobiology doi: 10.1016/j.conb.2007.04.003 – volume: 108 start-page: 3029 issue: 7 year: 2011 ident: ref53 article-title: Involvement of ryanodine receptors in neurotrophin-induced hippocampal synaptic plasticity and spatial memory formation publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1013580108 – volume: 91 start-page: 598 issue: 4 year: 2011 ident: ref64 article-title: Recovery of cardiac calcium release is controlled by sarcoplasmic reticulum refilling and ryanodine receptor sensitivity publication-title: Cardiovasc Res doi: 10.1093/cvr/cvr143 – volume: 20 start-page: 1791 issue: 5 year: 2000 ident: ref10 article-title: NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons publication-title: J Neurosci doi: 10.1523/JNEUROSCI.20-05-01791.2000 – volume: 76 start-page: 367 issue: 1 year: 2007 ident: ref51 article-title: Modulation of the Ryanodine Receptor and Intracellular Calcium publication-title: Annu Rev Biochem doi: 10.1146/annurev.biochem.76.053105.094237 – volume: 82 start-page: 121 year: 2008 ident: ref61 article-title: A generic grid interface for parallel and adaptive scientific computing. Part II: Implementation and tests in DUNE publication-title: Computing doi: 10.1007/s00607-008-0004-9 – volume: 13 start-page: 157 issue: 3 year: 2012 ident: ref27 article-title: Understanding calcium waves and sparks in central neurons publication-title: Nat Rev Neurosci doi: 10.1038/nrn3168 – volume: 24 start-page: 385 issue: 2 year: 2014 ident: ref44 article-title: Cortical Dendritic Spine Heads Are Not Electrically Isolated by the Spine Neck from Membrane Potential Signals in Parent Dendrites publication-title: Cerebral Cortex doi: 10.1093/cercor/bhs320 – volume: 2010 start-page: 108190 year: 2010 ident: ref57 article-title: Selective Vulnerability of Neurons in Layer II of the Entorhinal Cortex during Aging and Alzheimer's Disease publication-title: Neural Plasticity doi: 10.1155/2010/108190 – volume: 268 start-page: 13765 issue: 19 year: 1993 ident: ref25 article-title: The ryanodine receptor/Ca2+ release channel publication-title: J Biol Chem doi: 10.1016/S0021-9258(19)85166-9 – volume: 87 start-page: 145 issue: 1 year: 2005 ident: ref46 article-title: Backpropagating action potentials in neurones: measurement, mechanisms and potential functions publication-title: Prog Biophys Mol Biol doi: 10.1016/j.pbiomolbio.2004.06.009 – volume: 30 start-page: 12128 issue: 36 year: 2010 ident: ref56 article-title: NMDA-Mediated Ca2+ Influx Drives Aberrant Ryanodine Receptor Activation in Dendrites of Young Alzheimer's Disease Mice publication-title: J Neurosci doi: 10.1523/JNEUROSCI.2474-10.2010 – volume: 17 start-page: 341 year: 1994 ident: ref3 article-title: Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function publication-title: Annu Rev Neurosci doi: 10.1146/annurev.ne.17.030194.002013 – volume: 11 start-page: e1003965 issue: 1 year: 2015 ident: ref62 article-title: Modulation of Elementary Calcium Release Mediates a Transition from Puffs to Waves in an IP3R Cluster Model publication-title: PLoS Comp Biol doi: 10.1371/journal.pcbi.1003965 – volume: 103 start-page: 17961 issue: 47 year: 2006 ident: ref45 article-title: The spine neck filters membrane potentials publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0608755103 – volume: 68 start-page: 1059 issue: 6 year: 2010 ident: ref58 article-title: Analysis of excitatory microcircuitry in the medial entorhinal cortex reveals cell-type-specific differences publication-title: Neuron doi: 10.1016/j.neuron.2010.12.009 – volume: 375 start-page: 682 issue: 6533 year: 1995 ident: ref6 article-title: Dendritic spines as basic functional units of neuronal integration publication-title: Nature doi: 10.1038/375682a0 – volume: 99 start-page: 3962 issue: 6 year: 2002 ident: ref49 article-title: Somatic action potentials are sufficient for late-phase LTP-related cell signaling publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.062510599 – volume: 31 start-page: 4221 issue: 11 year: 2011 ident: ref32 article-title: GABAB receptor modulation of voltage-sensitive calcium channels in spines and dendrites publication-title: J Neurosci doi: 10.1523/JNEUROSCI.4561-10.2011 – volume: 150 start-page: 1055 issue: 5 year: 2012 ident: ref55 article-title: Role of Leaky Neuronal Ryanodine Receptors in Stress- Induced Cognitive Dysfunction publication-title: Cell doi: 10.1016/j.cell.2012.06.052 – volume: 351 start-page: 751 issue: 6329 year: 1991 ident: ref65 article-title: Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum publication-title: Nature doi: 10.1038/351751a0 – volume: 16 start-page: 1409 issue: 10 year: 2013 ident: ref50 article-title: GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling publication-title: Nat Neurosci doi: 10.1038/nn.3496 – volume: 310 start-page: 866 issue: 5749 year: 2005 ident: ref35 article-title: Neuronal activity regulates diffusion across the neck of dendritic spines publication-title: Science doi: 10.1126/science.1114816 – volume: 98 start-page: 13625 issue: 24 year: 2001 ident: ref21 article-title: Ryanodine sensitizes the cardiac Ca(2+) release channel (ryanodine receptor isoform 2) to Ca(2+) activation and dissociates as the channel is closed by Ca(2+) depletion publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.241516898 – volume: 110 start-page: 2325 issue: 10 year: 2013 ident: ref15 article-title: Regulation of dendritic calcium release in striatal spiny projection neurons publication-title: Journal of Neurophysiology doi: 10.1152/jn.00422.2013 – volume: 59 start-page: 902 issue: 6 year: 2008 ident: ref5 article-title: Calcium Signaling in Dendrites and Spines: Practical and Functional Considerations publication-title: Neuron doi: 10.1016/j.neuron.2008.08.020 – volume: 137 start-page: 1207 issue: 8 year: 2002 ident: ref28 article-title: Inhibitory mechanism of xestospongin-C on contraction and ion channels in the intestinal smooth muscle publication-title: British Journal of Pharmacology doi: 10.1038/sj.bjp.0704988 – volume: 71 start-page: 732 issue: 2 year: 1996 ident: ref19 article-title: Response of ryanodine receptor channels to Ca2+ steps produced by rapid solution exchange publication-title: Biophys J doi: 10.1016/S0006-3495(96)79272-X – volume: 24 start-page: 8416 issue: 39 year: 2004 ident: ref30 article-title: Facilitation of L-Type Ca2+ Channels in Dendritic Spines by Activation of 2 Adrenergic Receptors publication-title: J Neurosci doi: 10.1523/JNEUROSCI.1677-04.2004 – volume: 28 start-page: 13457 issue: 50 year: 2008 ident: ref36 article-title: Spine Neck Plasticity Controls Postsynaptic Calcium Signals through Electrical Compartmentalization publication-title: J Neurosci doi: 10.1523/JNEUROSCI.2702-08.2008 – volume: 29 start-page: 11153 issue: 36 year: 2009 ident: ref47 article-title: Non-Hebbian Synaptic Plasticity Induced by Repetitive Postsynaptic Action Potentials publication-title: J Neurosci doi: 10.1523/JNEUROSCI.5881-08.2009 – volume: 33 start-page: 439 issue: 3 year: 2002 ident: ref1 article-title: The life cycle of Ca(2+) ions in dendritic spines publication-title: Neuron doi: 10.1016/S0896-6273(02)00573-1 – volume: 6 start-page: 948 issue: 9 year: 2003 ident: ref29 article-title: Plasticity of calcium channels in dendritic spines publication-title: Nat Neurosci doi: 10.1038/nn1112 – volume: 14 start-page: 290 issue: 2 year: 2000 ident: ref52 article-title: Spatial learning induced changes in expression of the ryanodine type II receptor in the rat hippocampus publication-title: FASEB J doi: 10.1096/fasebj.14.2.290 – volume: 3 start-page: 1256 issue: 12 year: 2000 ident: ref26 article-title: Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients publication-title: Nat Neurosci doi: 10.1038/81781 – volume: 29 start-page: 7833 issue: 24 year: 2009 ident: ref18 article-title: Synaptic Activation and Membrane Potential Changes Modulate the Frequency of Spontaneous Elementary Ca2+ Release Events in the Dendrites of Pyramidal Neurons publication-title: J Neurosci doi: 10.1523/JNEUROSCI.0573-09.2009 – volume: 8 start-page: 642 issue: 5 year: 2005 ident: ref34 article-title: SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines publication-title: Nat Neurosci doi: 10.1038/nn1449 – volume: 502 start-page: 13 issue: 1 year: 1997 ident: ref16 article-title: Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones publication-title: The Journal of Physiology doi: 10.1111/j.1469-7793.1997.013bl.x – volume: 54 start-page: 933 issue: 6 year: 2007 ident: ref33 article-title: Regulation of Dendritic Excitability by Activity-Dependent Trafficking of the A-Type K+ Channel Subunit Kv4.2 in Hippocampal Neurons publication-title: Neuron doi: 10.1016/j.neuron.2007.05.026 – volume: 49 start-page: 53 issue: 1 year: 1997 ident: ref20 article-title: The pharmacology of ryanodine and related compounds publication-title: Pharmacol Rev doi: 10.1016/S0031-6997(24)01313-9 – volume: 22 start-page: 115 issue: 1 year: 1999 ident: ref9 article-title: Single synaptic events evoke NMDA receptor–mediated release of calcium from internal stores in hippocampal dendritic spines publication-title: Neuron doi: 10.1016/S0896-6273(00)80683-2 – volume: 24 start-page: 727 issue: 3 year: 1999 ident: ref13 article-title: Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials publication-title: Neuron doi: 10.1016/S0896-6273(00)81125-3 – volume: 19 start-page: 4325 issue: 11 year: 1999 ident: ref24 article-title: Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons publication-title: J Neurosci doi: 10.1523/JNEUROSCI.19-11-04325.1999 – volume: 83 start-page: 59 issue: 1 year: 2002 ident: ref63 article-title: Termination of cardiac Ca(2+) sparks: an investigative mathematical model of calcium-induced calcium release publication-title: Biophys J doi: 10.1016/S0006-3495(02)75149-7 |
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| SubjectTerms | 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 |
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| Title | Ryanodine Receptor Activation Induces Long-Term Plasticity of Spine Calcium Dynamics |
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