Spine Calcium Transients Induced by Synaptically-Evoked Action Potentials Can Predict Synapse Location and Establish Synaptic Democracy
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{"title"=>"Spine calcium transients induced by synaptically-evoked action potentials can predict synapse location and establish synaptic democracy", "type"=>"journal", "authors"=>[{"first_name"=>"David C.", "last_name"=>"Sterratt", "scopus_author_id"=>"6602952618"}, {"first_name"=>"Martine R.", "last_name"=>"Groen", "scopus_author_id"=>"37047196600"}, {"first_name"=>"Rhiannon M.", "last_name"=>"Meredith", "scopus_author_id"=>"7006667790"}, {"first_name"=>"Arjen", "last_name"=>"van Ooyen", "scopus_author_id"=>"56207446800"}], "year"=>2012, "source"=>"PLoS Computational Biology", "identifiers"=>{"sgr"=>"84864071361", "doi"=>"10.1371/journal.pcbi.1002545", "issn"=>"1553734X", "pui"=>"365284177", "isbn"=>"10.1371/journal.pcbi.1002545", "pmid"=>"22719238", "scopus"=>"2-s2.0-84864071361"}, "id"=>"8235e544-f497-37d0-aaff-8f80ae04e020", "abstract"=>"CA1 pyramidal neurons receive hundreds of synaptic inputs at different distances from the soma. Distance-dependent synaptic scaling enables distal and proximal synapses to influence the somatic membrane equally, a phenomenon called \"synaptic democracy\". How this is established is unclear. The backpropagating action potential (BAP) is hypothesised to provide distance-dependent information to synapses, allowing synaptic strengths to scale accordingly. Experimental measurements show that a BAP evoked by current injection at the soma causes calcium currents in the apical shaft whose amplitudes decay with distance from the soma. However, in vivo action potentials are not induced by somatic current injection but by synaptic inputs along the dendrites, which creates a different excitable state of the dendrites. Due to technical limitations, it is not possible to study experimentally whether distance information can also be provided by synaptically-evoked BAPs. Therefore we adapted a realistic morphological and electrophysiological model to measure BAP-induced voltage and calcium signals in spines after Schaffer collateral synapse stimulation. We show that peak calcium concentration is highly correlated with soma-synapse distance under a number of physiologically-realistic suprathreshold stimulation regimes and for a range of dendritic morphologies. Peak calcium levels also predicted the attenuation of the EPSP across the dendritic tree. Furthermore, we show that peak calcium can be used to set up a synaptic democracy in a homeostatic manner, whereby synapses regulate their synaptic strength on the basis of the difference between peak calcium and a uniform target value. We conclude that information derived from synaptically-generated BAPs can indicate synapse location and can subsequently be utilised to implement a synaptic democracy.", "link"=>"http://www.mendeley.com/research/spine-calcium-transients-induced-synapticallyevoked-action-potentials-predict-synapse-location-estab", "reader_count"=>65, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>20, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>20, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Engineering"=>6, "Unspecified"=>4, "Mathematics"=>3, "Agricultural and Biological Sciences"=>32, "Medicine and Dentistry"=>2, "Neuroscience"=>14, "Philosophy"=>1, "Physics and Astronomy"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>6}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>14}, "Physics and Astronomy"=>{"Physics and Astronomy"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Mathematics"=>{"Mathematics"=>3}, "Unspecified"=>{"Unspecified"=>4}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Greece"=>1, "Japan"=>2, "United Kingdom"=>2, "Switzerland"=>2, "Portugal"=>1, "Germany"=>3, "Spain"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/624109"], "description"=>"<p><b>A</b>, Relationship between path distance to soma and EPSP attenuation. Coloured circles indicate selected spines (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2</a>). <b>B–G</b>, Peak, integral and delay-to-peak voltage and calcium signals as correlates for EPSP attenuation. <i>R</i><sup>2</sup> values indicated for each fit.</p>", "links"=>[], "tags"=>["calcium", "backpropagation", "correlates", "epsp"], "article_id"=>294601, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peak_spine_calcium_following_backpropagation_strongly_correlates_with_EPSP_attenuation_/294601", "title"=>"Peak spine calcium following backpropagation strongly correlates with EPSP attenuation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:16:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/623946"], "description"=>"<p>Colours indicate spine locations shown in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2</a>. <b>A–H</b>, Asynchronous inputs (240 synapses): In each of 100 simulations, the cell was presented with synaptic inputs whose activation times were randomly drawn from a 10 ms window. <b>A</b>, <b>E</b>, Example voltage and calcium traces of spines indicated in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2A</a>. <b>B–D</b>, <b>F–H</b>, Peak, integral, and delay-to-peak voltage and calcium changes at all asynchronously-activated spines across the dendritic tree plotted against path distance. <b>I–P</b>, Subthreshold inputs (170 synapses): <b>I</b>, <b>M</b>, Synaptically-stimulated changes in voltage and calcium at selected spines (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2</a>); <b>J–L</b>, <b>N–P</b>, Peak, integral and delay-to-peak voltage and calcium changes in spines following subthreshold stimulation plotted against path distance.</p>", "links"=>[], "tags"=>["asynchronous", "inputs", "subthreshold"], "article_id"=>294440, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_asynchronous_inputs_and_subthreshold_inputs_on_features_tested_/294440", "title"=>"The effect of asynchronous inputs and subthreshold inputs on features tested.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:14:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/623873"], "description"=>"<p>Three different CA1 morphology reconstructions used to test robustness of our simulations. <b>A</b>, <i>left panel</i>. CA1 morphology redrawn from data provided in Poirazi et al. (2003) and used in the other figures of this paper. <b>B</b>, <b>C</b>, <i>left panels</i>. Two different CA1 neurons filled with biocytin, processed and reconstructed in Neurolucida. Neurons came from hippocampal slice preparations of P28–42 rats. The axon is the same for all cells, taken from Poirazi et al. (2003). Scale bars 100 µm. <b>A–C</b>, <i>right panels</i>. Peak calcium concentration correlated with dendritic distance from soma for each neuronal reconstruction, with corresponding <i>R</i><sup>2</sup> values given.</p>", "links"=>[], "tags"=>["robust", "morphological"], "article_id"=>294374, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_model_is_robust_to_morphological_variations_/294374", "title"=>"The model is robust to morphological variations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:12:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/624167"], "description"=>"<p><b>A–F</b>, Peak, integral and delay-to-peak voltage and calcium signals correlated with for path distance. Coloured circles indicate selected spines (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2</a>). <i>R</i><sup>2</sup> values indicated for each fit.</p>", "links"=>[], "tags"=>["calcium", "correlated", "synapses", "scaled", "synaptic"], "article_id"=>294659, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g007", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peak_calcium_is_less_correlated_with_distance_once_synapses_are_scaled_according_to_synaptic_democracy_/294659", "title"=>"Peak calcium is less correlated with distance once synapses are scaled according to synaptic democracy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:17:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/624247"], "description"=>"<p><b>A</b>, Schematic showing the homeostatic regulation of synaptic strength, defined as AMPA conductance, by peak calcium. <b>B</b>, Peak calcium in spines during the time-lapse homeostatic simulation. Synapses are colour-coded and grouped according to distance. The black dotted line indicates the target level. <b>C</b>, Synaptic strength stabilises during a simulation run of 500 trials. As in B, synapses are grouped and colour-coded according to distance. <b>D</b>, Synaptic strength at the beginning (black crosses) and at the end of the scaling simulation (closed circles) plotted against distance. Black circles indicate the apical shaft, grey circles the oblique dendrites. <b>E</b>, EPSP amplitude at the soma of individual synapses plotted against distance at the start of the simulation. <b>F</b>, EPSP amplitude at the soma of individual synapses plotted against distance at the end of the simulation.</p>", "links"=>[], "tags"=>["established", "homeostatic", "rules", "calcium"], "article_id"=>294740, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g008", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_democracy_established_using_homeostatic_rules_based_on_peak_calcium_levels_/294740", "title"=>"Synaptic democracy established using homeostatic rules based on peak calcium levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:19:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/624355"], "description"=>"<p>The investigated synaptic stimulations are: BAP, BAP with asynchronous jitter, BAP with scaled synapses and subthreshold stimulation. The symbols +/− in the table indicate the direction of the correlation between the measured signals (calcium and voltage) and the features (peak response, integral and delay-to-peak) tested for distance-dependence from the soma and measured in the spines.</p>", "links"=>[], "tags"=>["directions", "correlations", "conditions", "synaptic"], "article_id"=>294845, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_R_2_values_and_directions_of_correlations_for_different_conditions_of_synaptic_stimulation_/294845", "title"=>"Summary of <i>R</i><sup>2</sup> values and directions of correlations for different conditions of synaptic stimulation.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-06-14 01:20:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/623778"], "description"=>"<p><b>A</b>, CA1 model neuron. Circles indicate spine head locations of example measurements highlighted in B–L. <b>B–F</b>, Measurements from the spine heads indicated by the corresponding colours in panel A, indicating membrane potential (<b>B</b>), calcium concentration (<b>C</b>), NMDA-mediated currents (<b>D</b>), AMPA-mediated currents (<b>E</b>) and R-type currents (<b>F</b>). The right-hand plots show the same data, but magnified around the time of the arrival of the BAP at the spines. <b>G–L</b>, Peak, integral and delay-to-peak voltage and calcium measurements are plotted as predictors for path distance. Black circles indicate apical shaft spines. <i>R</i><sup>2</sup> values are shown.</p>", "links"=>[], "tags"=>["induction", "bap", "displays", "distance-dependent", "voltage", "calcium", "changes", "dendritic"], "article_id"=>294265, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g002", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_induction_of_BAP_displays_distance_dependent_voltage_and_calcium_changes_across_the_dendritic_tree_/294265", "title"=>"Synaptic induction of BAP displays distance-dependent voltage and calcium changes across the dendritic tree.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:11:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/323966", "https://ndownloader.figshare.com/files/324056", "https://ndownloader.figshare.com/files/324116", "https://ndownloader.figshare.com/files/324170"], "description"=>"<div><p>CA1 pyramidal neurons receive hundreds of synaptic inputs at different distances from the soma. Distance-dependent synaptic scaling enables distal and proximal synapses to influence the somatic membrane equally, a phenomenon called “synaptic democracy”. How this is established is unclear. The backpropagating action potential (BAP) is hypothesised to provide distance-dependent information to synapses, allowing synaptic strengths to scale accordingly. Experimental measurements show that a BAP evoked by current injection at the soma causes calcium currents in the apical shaft whose amplitudes decay with distance from the soma. However, <em>in vivo</em> action potentials are not induced by somatic current injection but by synaptic inputs along the dendrites, which creates a different excitable state of the dendrites. Due to technical limitations, it is not possible to study experimentally whether distance information can also be provided by synaptically-evoked BAPs. Therefore we adapted a realistic morphological and electrophysiological model to measure BAP-induced voltage and calcium signals in spines after Schaffer collateral synapse stimulation. We show that peak calcium concentration is highly correlated with soma-synapse distance under a number of physiologically-realistic suprathreshold stimulation regimes and for a range of dendritic morphologies. Peak calcium levels also predicted the attenuation of the EPSP across the dendritic tree. Furthermore, we show that peak calcium can be used to set up a synaptic democracy in a homeostatic manner, whereby synapses regulate their synaptic strength on the basis of the difference between peak calcium and a uniform target value. We conclude that information derived from synaptically-generated BAPs can indicate synapse location and can subsequently be utilised to implement a synaptic democracy.</p> </div>", "links"=>[], "tags"=>["calcium", "transients", "induced", "synaptically-evoked", "potentials", "synapse", "synaptic"], "article_id"=>123946, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002545.s001", "https://dx.doi.org/10.1371/journal.pcbi.1002545.s002", "https://dx.doi.org/10.1371/journal.pcbi.1002545.s003", "https://dx.doi.org/10.1371/journal.pcbi.1002545.s004"], "stats"=>{"downloads"=>10, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Spine_Calcium_Transients_Induced_by_Synaptically_Evoked_Action_Potentials_Can_Predict_Synapse_Location_and_Establish_Synaptic_Democracy/123946", "title"=>"Spine Calcium Transients Induced by Synaptically-Evoked Action Potentials Can Predict Synapse Location and Establish Synaptic Democracy", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-06-14 01:05:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/624035"], "description"=>"<p><b>A</b>, Relationship between peak voltage and soma-spine distance in a sample of branches in the CA1 model neuron. <b>B</b>, Relationship between voltage half-width and distance to the soma for same sample of branches shown in A. <b>C</b>, Relationship between voltage integral and distance to the soma for same sample of branches shown in A. <b>D</b>, <b>E</b>, <i>R</i><sup>2</sup> values for combinations of NMDA decay and calcium extrusion time constants for all spines, with and without R-type channels. # indicates an 80% decrease in NMDA decay and in calcium extrusion time constants that are used in all other figures in the manuscript. <b>F</b>, For 80% decrease in values (indicated # in E), relationship between soma-spine distance with peak voltage (<i>left panel</i>), voltage integral (<i>centre panel</i>) and peak calcium in spines (<i>right panel</i>). Correlations for peak voltage and voltage integral remain stable (compared with <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2G, H</a>) but the correlation with peak calcium concentration disappears (comparison with <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#pcbi-1002545-g002\" target=\"_blank\">Fig. 2J</a>).</p>", "links"=>[], "tags"=>["calcium", "conductance", "distance-dependent"], "article_id"=>294532, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_contribution_of_calcium_conductance_and_dynamics_to_distance_dependent_correlations_/294532", "title"=>"The contribution of calcium conductance and dynamics to distance-dependent correlations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:15:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/623671"], "description"=>"<p><b>A</b>, Two-photon compressed z-stack morphology of CA1 pyramidal neuron. Squares indicate line-scan measurement sites (scale bar 50 µm). <b>B</b>, Corresponding single BAP-induced fluorescence changes in the apical shaft. A double exponential is fitted to the fluorescence traces as described in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002545#s2\" target=\"_blank\">Materials and Methods</a>. Distances between the point measured and the soma are indicated, determined by tracing the fluorescence of Alexa 594 in 3D from the scanned region back to the soma. <b>C</b>, Peak calcium-induced fluorescence plotted against distance to soma. Mean ± S.E.M. shown. Multiple points are measured per cell. Fluorescence amplitude is plotted relative to the first measured data point at circa 100 µm, to show the distance-dependent decrease of amplitude corrected for the large amplitude variation between cells. <b>D</b>, CA1 pyramidal neuron morphology of the model (scale bar 100 µm). Circles indicate locations of recordings and points with corresponding colour in E–H similar to the experimental paradigm (A–C). <b>E</b>, <b>F</b>, Peak voltage and peak calcium levels in the apical shaft following a somatically-initiated BAP. <b>G</b>, <b>H</b>, Peak voltage and calcium levels versus distance from soma for all apical dendritic shaft locations. Note that distance to soma is measured in 3D along the dendrites, while panel D shows a 3D-compressed image.</p>", "links"=>[], "tags"=>["calcium", "induced", "somatic", "bap", "decays", "experiments"], "article_id"=>294162, "categories"=>["Neuroscience"], "users"=>["David C. Sterratt", "Martine R. Groen", "Rhiannon M. Meredith", "Arjen van Ooyen"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002545.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peak_calcium_induced_by_somatic_BAP_decays_with_distance_in_both_experiments_and_model_simulation_/294162", "title"=>"Peak calcium induced by somatic BAP decays with distance in both experiments and model simulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-14 01:09:22"}

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