Location-Dependent Excitatory Synaptic Interactions in Pyramidal Neuron Dendrites
Publication Date
July 19, 2012
Journal
PLOS Computational Biology
Authors
Bardia F. Behabadi, Alon Polsky, Monika Jadi, Jackie Schiller, et al
Volume
8
Issue
7
Pages
e1002599
DOI
https://dx.plos.org/10.1371/journal.pcbi.1002599
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1002599
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22829759
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3400572
Europe PMC
http://europepmc.org/abstract/MED/22829759
Web of Science
000306842200023
Scopus
84864043775
Mendeley
http://www.mendeley.com/research/locationdependent-excitatory-synaptic-interactions-pyramidal-neuron-dendrites
Events
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/316716"], "description"=>"<div><p>Neocortical pyramidal neurons (PNs) receive thousands of excitatory synaptic contacts on their basal dendrites. Some act as classical driver inputs while others are thought to modulate PN responses based on sensory or behavioral context, but the biophysical mechanisms that mediate classical-contextual interactions in these dendrites remain poorly understood. We hypothesized that if two excitatory pathways bias their synaptic projections towards proximal vs. distal ends of the basal branches, the very different local spike thresholds and attenuation factors for inputs near and far from the soma might provide the basis for a classical-contextual functional asymmetry. Supporting this possibility, we found both in compartmental models and electrophysiological recordings in brain slices that the responses of basal dendrites to spatially separated inputs are indeed strongly asymmetric. Distal excitation lowers the local spike threshold for more proximal inputs, while having little effect on peak responses at the soma. In contrast, proximal excitation lowers the threshold, but also substantially increases the gain of distally-driven responses. Our findings support the view that PN basal dendrites possess significant analog computing capabilities, and suggest that the diverse forms of nonlinear response modulation seen in the neocortex, including uni-modal, cross-modal, and attentional effects, could depend in part on pathway-specific biases in the spatial distribution of excitatory synaptic contacts onto PN basal dendritic arbors.</p> </div>", "links"=>[], "tags"=>["location-dependent", "excitatory", "synaptic", "interactions", "pyramidal", "neuron", "dendrites"], "article_id"=>122490, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Location_Dependent_Excitatory_Synaptic_Interactions_in_Pyramidal_Neuron_Dendrites/122490", "title"=>"Location-Dependent Excitatory Synaptic Interactions in Pyramidal Neuron Dendrites", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-07-19 00:41:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/605781"], "description"=>"<p>Conceptual curve families illustrate: <b><i>A,</i></b> pure threshold-lowering, <b><i>B,</i></b> pure gain-boosting, and <b><i>C,</i></b> mixed modulatory effects.</p>", "links"=>[], "tags"=>["excitatory", "driver-modulator"], "article_id"=>276273, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_spectrum_of_possible_excitatory_driver_modulator_classical_contextual_interactions_/276273", "title"=>"A spectrum of possible excitatory driver-modulator (classical-contextual) interactions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:44:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/605846"], "description"=>"<p><b><i>A,</i></b> Experimental setup. Whole-cell recordings were performed from the soma of a layer 5 pyramidal neuron. The cell was loaded with OGB-1 (200 µM) and was visualized using fluorescence confocal microscopy. Purple “clouds” denote sites of glutamate uncaging. <b><i>B,</i></b> Somatic responses to increasing stimulus intensity using UV laser focal uncaging of glutamate 60 µm from the soma. Black dashed trace shows extrapolated response based on linear fit to series of subthreshold response peaks. Ratio of actual to extrapolated response at local spike threshold defines the “Nonlinearity Relative to Linear Extrapolation” (NRLE) ratio (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#s4\" target=\"_blank\">Materials and Methods</a>). <b><i>C,</i></b> Same as (<b><i>B</i></b>), but for stimulus site 160 µm from soma. <b><i>D,</i></b> NRLE values at proximal and distal sites were equivalent (∼3) under control conditions, and were reduced to equivalent values (<1) by NMDA channel blockers APV and MK-801. Bars indicate mean ±SD. <b><i>E,</i></b> Model responses at soma to increasing stimulus intensity (# of synapses) at 70 µm. <b><i>F,</i></b> Same as (<b><i>E</i></b>) but for stimulus at 160 µm. <b><i>G,</i></b> As in the experimental data, model NRLE values under control and NMDA block conditions were nearly constant along the proximal-distal axis. Error bars indicate SD across four different dendritic branches in the model, highlighted in the inset in (<b><i>E</i></b>). <b><i>H,</i></b> Red data are same as in (<b><i>G</i></b>). When the NMDA-AMPA ratio is made uniformly higher or lower over the length of the dendrite (magenta and cyan dashed lines, respectively), the NRLE measure roughly follows suit (magenta and cyan points). Similarly, if the NMDA-AMPA ratio increases or decreases linearly along the length of the dendrite (diagonal green and blue dashed lines, respectively), the NRLE ratio also varies roughly linearly (green and blue points).</p>", "links"=>[], "tags"=>["dendritic", "spike-threshold"], "article_id"=>276339, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Location_independence_of_the_dendritic_spike_threshold_nonlinearity_/276339", "title"=>"Location independence of the dendritic spike-threshold nonlinearity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:45:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/605940"], "description"=>"<p><b><i>A,</i></b> Location pairs are indexed on outer x and y axes, and depicted by electrode icons in insets (number shown under electrodes is separation distance). Proximal and distal stimulus intensity is indexed on inner x and y axes, respectively, in each subplot. Striped lines in 3 subplots on main diagonal are shown in (<b><i>B</i></b>). <b><i>B,</i></b> Dendritic spike threshold and amplitude recorded at the soma increased markedly as electrodes approached soma. <b><i>C,</i></b> Superposition of curves normalized to first suprathreshold point shows nearly invariant basic shape of input-output curve. The normalization was a x,y-scaling of each curve such that the first suprathreshold data point was placed at the middle of the plot.</p>", "links"=>[], "tags"=>["predictions", "compartmental"], "article_id"=>276444, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proximal_distal_interactions_predictions_of_the_detailed_compartmental_model_/276444", "title"=>"Proximal-distal interactions: predictions of the detailed compartmental model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:47:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/606079"], "description"=>"<p><b><i>A,</i></b> Schematic proximal and distal ‘stimulating electrodes’ are shown activating one highlighted terminal basal dendrite. <b><i>B,</i></b> Peak somatic responses for inputs at 90 and 150 µm as illustrated in (<b><i>A</i></b>). Plot shares color bar with <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi-1002599-g003\" target=\"_blank\">Figure 3A</a>. <b><i>C,</i></b> 2-compartment circuit diagram with proximal and distal NMDA conductances. <b><i>D,</i></b> Time-invariant responses for 2-compartment model. Parameters were hand tuned to resemble (<b><i>C</i></b>): Axial, distal leak and proximal leak conductances were 2.5,0.25, and 4 A.U., respectively. NMDA peak conductance was 0.5 A.U. per synapse. Overall peak response in 2-compartment model was scaled to match overall peak in (<b><i>C</i></b>) (V<sub>soma</sub> = 15.2 mV). For details on 2-compartment model see Figure S1 in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi.1002599.s001\" target=\"_blank\">Text S1</a>.</p>", "links"=>[], "tags"=>["interactions", "time-invariant", "2-compartmental", "indistinguishable", "produced", "compartmental"], "article_id"=>276567, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proximal_distal_interactions_in_a_time_invariant_2_compartmental_model_are_nearly_indistinguishable_from_those_produced_by_the_detailed_compartmental_model_/276567", "title"=>"Proximal-distal interactions in a time-invariant 2-compartmental model are nearly indistinguishable from those produced by the detailed compartmental model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:49:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/606174"], "description"=>"<p><b><i>A,</i></b> Somatic responses evoked by 50 Hz double pulse stimulation with bipolar theta electrode at distal site (210 µm from the soma), including a clearly visible dendritic spike. <b><i>B,</i></b> Somatic responses to proximal input alone at 120 µm, evoked by laser flash photolysis of caged glutamate. <b><i>C,</i></b> Distally evoked responses in the presence of constant proximal modulation activated simultaneously; modulatory input alone is indicated by asterisked trace in (<b><i>B</i></b>). <b><i>D,</i></b> Summary plot: each successive curve corresponds to a higher proximal modulation. Modulator-alone peaks are given by y-intercepts. Triangle indicates just-suprathreshold response to distal input, also shown in (<b><i>E</i></b>). Circle marks just-suprathreshold response for the distal stimulus when the proximal bias was simultaneously just-subthreshold for its own spike. <b><i>E,</i></b> Same cell as (<b><i>D</i></b>), with proximal and distal roles reversed. Square and pentagon correspond to just sub- and just supra-threshold response peaks, respectively, also shown in (<b><i>D</i></b>). <b><i>F, G,</i></b> Combined results of 294 stimulus pairs in 6 cells (cell-by-cell results shown in Figure S2 in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi.1002599.s001\" target=\"_blank\">Text S1</a>). Inset, stimulus sites are indicated by black triangles (electrical stimulation) and purple clouds (laser uncaging), dendrite length in ball-and-stick cartoon is 275 µm. Blue case is same as in (<b><i>A</i></b><i>–</i><b><i>E</i></b>). Red case included TTX (1 µM) perfused from an electrode near the soma to prevent somatic spiking which would have masked the subthreshold integration process being studied. Grey and orange cases used electrical stimulation at proximal site instead of uncaging, and included CNQX (10 µM) in the bath to block AMPAR responses in order to prevent somatic spiking due to fast AMPA currents.</p>", "links"=>[], "tags"=>["physiology", "neuroscience"], "article_id"=>276671, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proximal_distal_interactions_experimental_results_/276671", "title"=>"Proximal-distal interactions: experimental results.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:51:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/606290"], "description"=>"<p><b><i>A, B,</i></b> Orthogonal views of 3D surface shown in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi-1002599-g004\" target=\"_blank\">Figure 4D</a> for the 2-compartment model. Curves are grouped into 4 categories (colors) based on modulation strength. Averages within each category are shown in bold. Gray curves in (<b><i>A</i></b>) were excluded from averaging, since corresponding experimental cases were not observed. <b><i>C, D,</i></b> Data from <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi-1002599-g005\" target=\"_blank\">Figure 5F,G</a> was scaled vertically and horizontally using fiducial points for each cell (triangle, square, pentagon, circle; see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#s4\" target=\"_blank\">Materials and Methods</a>) to allow comparison to model results despite different stimulus locations, efficacy, branch input resistances, etc.</p>", "links"=>[], "tags"=>["physiology", "neuroscience"], "article_id"=>276784, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_results_match_model_predictions_/276784", "title"=>"Experimental results match model predictions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:53:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/606426"], "description"=>"<p><b><i>A,B,</i></b> Somatic responses to 50 Hz independent Poisson inputs delivered to 3 (blue), 6 (green), and 9 (magenta) distal synapses centered at 190 µm in (<b><i>A</i></b>) and 17 (blue), 21 (green), and 25 (magenta) proximal synapses centered at 90 µm in (<b><i>B</i></b>). <b><i>C</i></b><i>,</i> Mean firing rates for distal drive with proximal modulation increasing from curve to curve (averages of 20 runs). Slope changes are accentuated by black bars centered at point of maximum slope. Colored squares correspond to traces in (<b><i>A</i></b><i>–</i><b><i>B</i></b>). <b><i>D,</i></b> Same as (<b><i>C</i></b>), but for proximal drive with distal modulation. Black bars accentuate left shifting of i-o curve. <b><i>E, F,</i></b> Similar input configuration to (<b><i>C</i></b><i>–</i><b><i>D</i></b>), but with proximal and distal inputs (same distances) on two different dendrites. Modulatory effect from both perspectives is linear, as evidenced by the nearly constant additive (vertical shifting) effect of either proximal or distal cross-branch modulation acting on the driver's input-output curves. <b><i>G,</i></b> Diagram illustrates driver-modulator interaction shown in (<b><i>C</i></b>). Proximal synapses when viewed as contextual modulators (left) lower the threshold θ and increase the gain α of the dendritic sigmoid nonlinearity. Distal synapses viewed as modulators (right) exert a left-shifting (threshold lowering) effect. Note diagrams are schematic representations of the modeling results; absolute and relative positions of the driver and modulator inputs in the schematics should not be given a literal spatial interpretation.</p>", "links"=>[], "tags"=>["predictions", "spike", "responses", "proximal-distal"], "article_id"=>276923, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_predictions_of_spike_rate_responses_also_show_strong_proximal_distal_asymmetry_/276923", "title"=>"Model predictions of spike rate responses also show strong proximal-distal asymmetry.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:55:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/606522"], "description"=>"<p><b><i>A,</i></b> L3 model morphology <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi.1002599-Mainen1\" target=\"_blank\">[89, see Materials and Methods for details]</a> with colored markers indicating one set of the locations of the 4 synapses evoking the responses shown in (<b><i>B</i></b>). <b><i>B,</i></b> Four synaptic inputs were placed on 100 sets of 4 randomly selected dendrites 50, 150, and 250 µm from the soma, evoking 4.6, 3.6, and 2.9 mV EPSPs on average. EPSP half width and risetime grew with distance from the soma. Error bars indicate s.d. of the mean across random dendritic sets. Compare to <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi-1002599-t001\" target=\"_blank\">Table 1</a> from Yoshimura et al. <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi.1002599-Yoshimura1\" target=\"_blank\">[47]</a> showing that EPSP half widths between modulatory� long-distance horizontal and vertical L4 “driver” inputs increased (34.5±19.9 vs. 53.0±28.1ms, p<0.05, t-test) as did EPSP rise times (3.9±2.5ms vs. 5±2.5ms, p<0.04, Wilcoxon rank-sum test, Figure 2B rise time data from Yoshimura et al. <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002599#pcbi.1002599-Yoshimura1\" target=\"_blank\">[47]</a> was digitized with Engauge Digitizer for statistical analysis in Matlab).</p>", "links"=>[], "tags"=>["time-course", "l3", "neuron", "suggests", "long-distance", "horizontal", "connections", "terminate", "proximally", "l4", "inputs"], "article_id"=>277006, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EPSP_time_course_analysis_of_L3_model_neuron_suggests_that_8220_modulatory_8221_long_distance_horizontal_connections_terminate_proximally_and_vertical_L4_8220_driver_8221_inputs_terminate_distally_/277006", "title"=>"EPSP time-course analysis of L3 model neuron suggests that “modulatory” long-distance horizontal connections terminate proximally and vertical L4 “driver” inputs terminate distally.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-19 01:56:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/606612"], "description"=>"<p>Model parameters.</p>", "links"=>[], "tags"=>["physiology", "neuroscience"], "article_id"=>277105, "categories"=>["Physiology", "Neuroscience"], "users"=>["Bardia F. Behabadi", "Alon Polsky", "Monika Jadi", "Jackie Schiller", "Bartlett W. Mel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002599.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_parameters_/277105", "title"=>"Model parameters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-07-19 01:58:25"}

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