{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T05:43:09Z","timestamp":1772170989499,"version":"3.50.1"},"reference-count":69,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2008,3,28]],"date-time":"2008-03-28T00:00:00Z","timestamp":1206662400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1000036","type":"journal-article","created":{"date-parts":[[2008,3,28]],"date-time":"2008-03-28T17:11:30Z","timestamp":1206724290000},"page":"e1000036","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":17,"title":["Electrotonic Signals along Intracellular Membranes May Interconnect Dendritic Spines and Nucleus"],"prefix":"10.1371","volume":"4","author":[{"given":"Isaac","family":"Shemer","sequence":"first","affiliation":[]},{"given":"Bj\u00f6rn","family":"Brinne","sequence":"additional","affiliation":[]},{"given":"Jesper","family":"Tegn\u00e9r","sequence":"additional","affiliation":[]},{"given":"Sten","family":"Grillner","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2008,3,28]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0896-6273(00)80026-4","article-title":"Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity.","volume":"16","author":"K Deisseroth","year":"1996","journal-title":"Neuron"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1038\/32448","article-title":"Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons.","volume":"392","author":"K Deisseroth","year":"1998","journal-title":"Nature"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/85109","article-title":"Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity.","volume":"4","author":"GE Hardingham","year":"2001","journal-title":"Nat Neurosci"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1038\/345718a0","article-title":"Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation.","volume":"345","author":"PK Dash","year":"1990","journal-title":"Nature"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/0092-8674(94)90399-9","article-title":"Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila.","volume":"79","author":"JC Yin","year":"1994","journal-title":"Cell"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1523\/JNEUROSCI.20-01-00266.2000","article-title":"Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials.","volume":"20","author":"PG Mermelstein","year":"2000","journal-title":"J Neurosci"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1126\/science.1063395","article-title":"Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway.","volume":"294","author":"RE Dolmetsch","year":"2001","journal-title":"Science"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"15342","DOI":"10.1073\/pnas.211563998","article-title":"Calmodulin priming: nuclear translocation of a calmodulin complex and the memory of prior neuronal activity.","volume":"98","author":"PG Mermelstein","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1002\/cne.903600112","article-title":"Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: II. Spine distributions.","volume":"360","author":"NJ Bannister","year":"1995","journal-title":"J Comp Neurol"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/S0306-4522(00)00584-4","article-title":"The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control.","volume":"102","author":"E Papp","year":"2001","journal-title":"Neuroscience"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/S0896-6273(02)00573-1","article-title":"The life cycle of Ca(2+) ions in dendritic spines.","volume":"33","author":"BL Sabatini","year":"2002","journal-title":"Neuron"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1126\/science.272.5262.716","article-title":"Direct measurement of coupling between dendritic spines and shafts.","volume":"272","author":"K Svoboda","year":"1996","journal-title":"Science"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/S0021-9258(19)86127-6","article-title":"The complete amino acid sequence of the Ca2+-dependent modulator protein (calmodulin) of bovine brain.","volume":"255","author":"DM Watterson","year":"1980","journal-title":"J Biol Chem"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"3056","DOI":"10.1523\/JNEUROSCI.10-09-03056.1990","article-title":"Dendritic transport: quantitative analysis of the time course of somatodendritic transport of recently synthesized RNA.","volume":"10","author":"L Davis","year":"1990","journal-title":"J Neurosci"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/j.neuron.2004.07.022","article-title":"Kinesin transports RNA: isolation and characterization of an RNA-transporting granule.","volume":"43","author":"Y Kanai","year":"2004","journal-title":"Neuron"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1113\/jphysiol.2002.020362","article-title":"Spatial segregation and interaction of calcium signalling mechanisms in rat hippocampal CA1 pyramidal neurons.","volume":"543","author":"T Nakamura","year":"2002","journal-title":"J Physiol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/S0166-2236(00)01787-2","article-title":"The endoplasmic reticulum: one continuous or several separate Ca(2+) stores?","volume":"24","author":"OH Petersen","year":"2001","journal-title":"Trends Neurosci"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1523\/JNEUROSCI.17-01-00190.1997","article-title":"Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat.","volume":"17","author":"J Spacek","year":"1997","journal-title":"J Neurosci"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1016\/S0092-8674(00)80281-0","article-title":"Calcium-induced restructuring of nuclear envelope and endoplasmic reticulum calcium stores.","volume":"89","author":"K Subramanian","year":"1997","journal-title":"Cell"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"7510","DOI":"10.1073\/pnas.91.16.7510","article-title":"Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons.","volume":"91","author":"M Terasaki","year":"1994","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0896-6273(00)80510-3","article-title":"Neuronal calcium signaling.","volume":"21","author":"MJ Berridge","year":"1998","journal-title":"Neuron"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"4636","DOI":"10.1523\/JNEUROSCI.13-11-04636.1993","article-title":"Three-dimensional visualization of the smooth endoplasmic reticulum in Purkinje cell dendrites.","volume":"13","author":"ME Martone","year":"1993","journal-title":"J Neurosci"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1085\/jgp.94.2.261","article-title":"K+-selective channel from sarcoplasmic reticulum of split lobster muscle fibers.","volume":"94","author":"JM Tang","year":"1989","journal-title":"J Gen Physiol"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1085\/jgp.72.6.775","article-title":"Nile blue fluorescence signals from cut single muscle fibers under voltage or current clamp conditions.","volume":"72","author":"J Vergara","year":"1978","journal-title":"J Gen Physiol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/BF00229243","article-title":"Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum.","volume":"55","author":"G Meissner","year":"1983","journal-title":"Mol Cell Biochem"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"2035","DOI":"10.1111\/j.1460-9568.2006.04733.x","article-title":"Non-fibrillar beta-amyloid abates spike-timing-dependent synaptic potentiation at excitatory synapses in layer 2\/3 of the neocortex by targeting postsynaptic AMPA receptors.","volume":"23","author":"I Shemer","year":"2006","journal-title":"Eur J Neurosci"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"11985","DOI":"10.1073\/pnas.93.21.11985","article-title":"Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells.","volume":"93","author":"M Rapp","year":"1996","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref28","first-page":"9","article-title":"Cable theory for dendritic neurons.","author":"W Rall","year":"1989"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"4631","DOI":"10.1016\/S0021-9258(17)30435-0","article-title":"Electrogenicity of Ca2+ transport catalyzed by the Ca2+-ATPase from sarcoplasmic reticulum.","volume":"253","author":"P Zimniak","year":"1978","journal-title":"J Biol Chem"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/S0896-6273(01)00402-0","article-title":"Stores not just for storage. intracellular calcium release and synaptic plasticity.","volume":"31","author":"CR Rose","year":"2001","journal-title":"Neuron"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0896-6273(00)80683-2","article-title":"Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines.","volume":"22","author":"N Emptage","year":"1999","journal-title":"Neuron"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"6961","DOI":"10.1523\/JNEUROSCI.17-18-06961.1997","article-title":"Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel.","volume":"17","author":"M Naraghi","year":"1997","journal-title":"J Neurosci"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/0143-4160(92)90046-U","article-title":"Buffering of calcium in the vicinity of a channel pore.","volume":"13","author":"MD Stern","year":"1992","journal-title":"Cell Calcium"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/S0896-6273(00)80983-6","article-title":"Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release.","volume":"20","author":"E Neher","year":"1998","journal-title":"Neuron"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/j.neuroscience.2005.11.038","article-title":"Density and morphology of dendritic spines in mouse neocortex.","volume":"138","author":"I Ballesteros-Yanez","year":"2006","journal-title":"Neuroscience"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"4613","DOI":"10.1523\/JNEUROSCI.14-08-04613.1994","article-title":"Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices.","volume":"14","author":"G Major","year":"1994","journal-title":"J Neurosci"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/S0079-6123(02)36012-6","article-title":"Spine distribution in cortical pyramidal cells: a common organizational principle across species.","volume":"136","author":"GN Elston","year":"2002","journal-title":"Prog Brain Res"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1038\/35104061","article-title":"Dendritic spines: structure, dynamics and regulation.","volume":"2","author":"H Hering","year":"2001","journal-title":"Nat Rev Neurosci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.ceb.2005.12.004","article-title":"The nuclear envelope: form and reformation.","volume":"18","author":"AJ Prunuske","year":"2006","journal-title":"Curr Opin Cell Biol"},{"key":"ref40","first-page":"25","article-title":"Linear cable theory.","author":"JJ Jack","year":"1975"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1111\/j.1469-7793.1999.00169.x","article-title":"Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single \u2018barrel\u2019 of developing rat somatosensory cortex.","volume":"521 (Part 1)","author":"D Feldmeyer","year":"1999","journal-title":"J Physiol"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/BF01870750","article-title":"A K+-selective, three-state channel from fragmented sarcoplasmic reticulum of frog leg muscle.","volume":"61","author":"PP Labarca","year":"1981","journal-title":"J Membr Biol"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/0143-4160(93)90002-N","article-title":"Reconstitution of a voltage-activated calcium conducting cation channel from brain microsomes.","volume":"14","author":"C Martin","year":"1993","journal-title":"Cell Calcium"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1038\/346374a0","article-title":"Voltage-dependent InsP3-insensitive calcium channels in membranes of pancreatic endoplasmic reticulum vesicles.","volume":"346","author":"A Schmid","year":"1990","journal-title":"Nature"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/S0006-3495(93)81100-7","article-title":"Voltage and temperature dependence of single K+ channels isolated from canine cardiac sarcoplasmic reticulum.","volume":"65","author":"WK Shen","year":"1993","journal-title":"Biophys J"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/BF00233541","article-title":"Characterization of a chloride channel reconstituted from cardiac sarcoplasmic reticulum.","volume":"147","author":"C Townsend","year":"1995","journal-title":"J Membr Biol"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"1505","DOI":"10.1126\/science.281.5382.1505","article-title":"CBP: a signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV.","volume":"281","author":"S Chawla","year":"1998","journal-title":"Science"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/S0143-4160(97)90085-3","article-title":"Effects of 1-methyladenine on nuclear Ca2+ transients and meiosis resumption in starfish oocytes are mimicked by the nuclear injection of inositol 1,4,5-trisphosphate and cADP-ribose.","volume":"22","author":"L Santella","year":"1997","journal-title":"Cell Calcium"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1074\/jbc.271.1.478","article-title":"Inositol 1,4,5-trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signaling by inositol 1,4,5-trisphosphate. Discrete distribution of inositol phosphate receptors to inner and outer nuclear membranes.","volume":"271","author":"JP Humbert","year":"1996","journal-title":"J Biol Chem"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"7166","DOI":"10.1093\/emboj\/16.23.7166","article-title":"Nuclear calcium signalling by individual cytoplasmic calcium puffs.","volume":"16","author":"P Lipp","year":"1997","journal-title":"EMBO J"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/0092-8674(95)90494-8","article-title":"ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope.","volume":"80","author":"OV Gerasimenko","year":"1995","journal-title":"Cell"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1835","DOI":"10.1126\/science.270.5243.1835","article-title":"Diffusion across the nuclear envelope inhibited by depletion of the nuclear Ca2+ store.","volume":"270","author":"L Stehno-Bittel","year":"1995","journal-title":"Science"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"3051","DOI":"10.1523\/JNEUROSCI.13-07-03051.1993","article-title":"Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain.","volume":"13","author":"AH Sharp","year":"1993","journal-title":"J Neurosci"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/S0022-5193(85)80233-2","article-title":"Model of calcium movements in the mammalian myocardium: interval-strength relationship.","volume":"113","author":"D Adler","year":"1985","journal-title":"J Theor Biol"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.ejheart.2005.05.011","article-title":"Cardiac contractility modulation by non-excitatory currents: Studies in isolated cardiac muscle.","volume":"8","author":"CB Brunckhorst","year":"2006","journal-title":"Eur J Heart Fail"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"1722","DOI":"10.1523\/JNEUROSCI.20-05-01722.2000","article-title":"Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization.","volume":"20","author":"A Majewska","year":"2000","journal-title":"J Neurosci"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"1682","DOI":"10.1073\/pnas.85.5.1682","article-title":"Activity-dependent accumulation of calcium in Purkinje cell dendritic spines.","volume":"85","author":"SB Andrews","year":"1988","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref58","first-page":"348","article-title":"Tissue anisotropy, the cardiac bidomain, and the virtual cathode.","author":"JP Wikswo Jr","year":"1995"},{"key":"ref59","first-page":"253","article-title":"Mechanisms for electrical stimulation of excitable tissue.","volume":"22","author":"BJ Roth","year":"1994","journal-title":"Crit Rev Biomed Eng"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"H2368","DOI":"10.1152\/ajpheart.00988.2002","article-title":"Nonlinear effects in subthreshold virtual electrode polarization.","volume":"284","author":"AT Sambelashvili","year":"2003","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1016\/S0006-3495(94)80846-X","article-title":"Virtual electrode effects in myocardial fibers.","volume":"66","author":"SB Knisley","year":"1994","journal-title":"Biophys J"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/0301-0082(92)90015-7","article-title":"The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs.","volume":"39","author":"J Defelipe","year":"1992","journal-title":"Prog Neurobiol"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/j.0953-816X.2003.03166.x","article-title":"Synaptology of the proximal segment of pyramidal cell basal dendrites.","volume":"19","author":"L Alonso-Nanclares","year":"2004","journal-title":"Eur J Neurosci"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/BF00341418","article-title":"Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components.","volume":"171","author":"J Spacek","year":"1985","journal-title":"Anat Embryol (Berl)"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1038\/nn835","article-title":"Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways.","volume":"5","author":"GE Hardingham","year":"2002","journal-title":"Nat Neurosci"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/S0896-6273(00)80343-8","article-title":"Giga-ohm seals on intracellular membranes: a technique for studying intracellular ion channels in intact cells.","volume":"19","author":"EA Jonas","year":"1997","journal-title":"Neuron"},{"key":"ref67","first-page":"195","article-title":"Model neurons II: Conductances and morphology.","author":"P Dayan","year":"2001"},{"key":"ref68","first-page":"25","article-title":"Linear Cable Theory.","author":"C Koch","year":"1999"},{"key":"ref69","first-page":"81","article-title":"A computational test of the requirements for conduction in demyelinated axons.","volume":"3","author":"M Hines","year":"1991","journal-title":"J Restor Neurol Neurosci"}],"container-title":["PLoS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1000036","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,6]],"date-time":"2021-09-06T14:05:18Z","timestamp":1630937118000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1000036"}},"subtitle":[],"editor":[{"given":"Karl J.","family":"Friston","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2008,3,28]]},"references-count":69,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2008,3,28]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1000036","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1112135.568117","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2008,3,28]]}}}