Synapse Geometry and Receptor Dynamics Modulate Synaptic Strength
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{"title"=>"Synapse geometry and receptor dynamics modulate synaptic strength", "type"=>"journal", "authors"=>[{"first_name"=>"Dominik", "last_name"=>"Freche", "scopus_author_id"=>"52263537400"}, {"first_name"=>"Ulrike", "last_name"=>"Pannasch", "scopus_author_id"=>"8632332900"}, {"first_name"=>"Nathalie", "last_name"=>"Rouach", "scopus_author_id"=>"6603232765"}, {"first_name"=>"David", "last_name"=>"Holcman", "scopus_author_id"=>"6701643334"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80053450670", "sgr"=>"80053450670", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pmid"=>"21984900", "doi"=>"10.1371/journal.pone.0025122", "pui"=>"362681587"}, "id"=>"bb3fba50-ba11-31de-a750-2f50fa2e5eee", "abstract"=>"Synaptic transmission relies on several processes, such as the location of a released vesicle, the number and type of receptors, trafficking between the postsynaptic density (PSD) and extrasynaptic compartment, as well as the synapse organization. To study the impact of these parameters on excitatory synaptic transmission, we present a computational model for the fast AMPA-receptor mediated synaptic current. We show that in addition to the vesicular release probability, due to variations in their release locations and the AMPAR distribution, the postsynaptic current amplitude has a large variance, making a synapse an intrinsic unreliable device. We use our model to examine our experimental data recorded from CA1 mice hippocampal slices to study the differences between mEPSC and evoked EPSC variance. The synaptic current but not the coefficient of variation is maximal when the active zone where vesicles are released is apposed to the PSD. Moreover, we find that for certain type of synapses, receptor trafficking can affect the magnitude of synaptic depression. Finally, we demonstrate that perisynaptic microdomains located outside the PSD impacts synaptic transmission by regulating the number of desensitized receptors and their trafficking to the PSD. We conclude that geometrical modifications, reorganization of the PSD or perisynaptic microdomains modulate synaptic strength, as the mechanisms underlying long-term plasticity.", "link"=>"http://www.mendeley.com/research/synapse-geometry-receptor-dynamics-modulate-synaptic-strength", "reader_count"=>71, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>24, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>1, "Student > Master"=>8, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>24, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>1, "Student > Master"=>8, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Mathematics"=>1, "Agricultural and Biological Sciences"=>41, "Medicine and Dentistry"=>3, "Neuroscience"=>10, "Physics and Astronomy"=>5, "Computer Science"=>5}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>10}, "Physics and Astronomy"=>{"Physics and Astronomy"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>41}, "Computer Science"=>{"Computer Science"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>2, "Japan"=>1, "United Kingdom"=>1, "Israel"=>1, "Germany"=>2}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/368169"], "description"=>"<div><p>Synaptic transmission relies on several processes, such as the location of a released vesicle, the number and type of receptors, trafficking between the postsynaptic density (PSD) and extrasynaptic compartment, as well as the synapse organization. To study the impact of these parameters on excitatory synaptic transmission, we present a computational model for the fast AMPA-receptor mediated synaptic current. We show that in addition to the vesicular release probability, due to variations in their release locations and the AMPAR distribution, the postsynaptic current amplitude has a large variance, making a synapse an intrinsic unreliable device. We use our model to examine our experimental data recorded from CA1 mice hippocampal slices to study the differences between mEPSC and evoked EPSC variance. The synaptic current but not the coefficient of variation is maximal when the active zone where vesicles are released is apposed to the PSD. Moreover, we find that for certain type of synapses, receptor trafficking can affect the magnitude of synaptic depression. Finally, we demonstrate that perisynaptic microdomains located outside the PSD impacts synaptic transmission by regulating the number of desensitized receptors and their trafficking to the PSD. We conclude that geometrical modifications, reorganization of the PSD or perisynaptic microdomains modulate synaptic strength, as the mechanisms underlying long-term plasticity.</p> </div>", "links"=>[], "tags"=>["synapse", "geometry", "receptor", "modulate", "synaptic"], "article_id"=>132736, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122", "stats"=>{"downloads"=>14, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Synapse_Geometry_and_Receptor_Dynamics_Modulate_Synaptic_Strength/132736", "title"=>"Synapse Geometry and Receptor Dynamics Modulate Synaptic Strength", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:45:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/729808"], "description"=>"<p>Default values of the simulation parameters (unless explicitly stated otherwise).</p>", "links"=>[], "tags"=>["biophysics", "neuroscience", "mathematics"], "article_id"=>400164, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.t001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simulation_parameters_/400164", "title"=>"Simulation parameters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-10-03 00:02:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/729456"], "description"=>"<p>(A) For a PSD (diameter 200 nm with 100 AMPARs marked blue at time 0) and an outside reservoir (diameter 400 nm with 300 AMPARs marked pink at time 0), the time course of AMPAR exchange by receptor diffusion () is shown. Within 50 ms the two AMPAR populations (blue and pink lines) are equilibrate to 75%, while the average number of AMPARs on the PSD remains constant. Error bars: variance, light colors: sample trajectories. (B) The time course of exchange is shown for a PSD with partially impenetrable boundary. Despite placing 10 equally-spaced barriers (indicated in the inset by the dashed circle) covering 0 (blue) to 90% (green) of the total PSD boundary, the mean number of receptors (red) inside the PSD does not change. (C, E, G) Stimulation with two consecutive pulses (frequency ranging from 20 Hz–0.4 Hz), each leading to the release of 1 vesicle in the center of the AZ in either presence or absence of AMPAR diffusion. The paired-pulse ratio (PPR) is shown at the maximal number of open AMPARs for the JS (C), MN (E) and RL model (G). The effect of AMPAR diffusion on the PPR was maximal for 20 ms. (D, F, H) During 10 pulses of a 20 Hz pulse train, the number of diffusing (green) and immobile (red) open AMPARs decays, while the number of desensitized AMPARs increases (dashed).</p>", "links"=>[], "tags"=>["receptor", "trafficking", "synaptic"], "article_id"=>399814, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_receptor_trafficking_on_synaptic_transmission_/399814", "title"=>"Effect of receptor trafficking on synaptic transmission.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:43:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/729588"], "description"=>"<p>A spike train at a single synaptic connection can lead to strong postsynaptic depression. The normalized distributions of the maximal number of open AMPARs (for the MN scheme) per pulse at a single participating synapse are shown for different stimulation intensities. Insets: averaged spike-to-spike time course of AMPAR openings. During a single simulated Poissonian spike train, one vesicle was released per pulse where the release sites were 1) clustered at the AZ center (red), 2) uniformly distributed over PSD (blue), 3) uniformly distributed over the cleft (green). Enlarging the AMPAR reservoir from intra-cleft only (A–C) to an additional extra-cleft one of fourfold size (D–F) increases the averaged synaptic response.</p>", "links"=>[], "tags"=>["postsynaptic", "spike", "decorrelation", "reservoir"], "article_id"=>399944, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g007", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recovery_from_postsynaptic_depression_by_spike_decorrelation_and_reservoir_enlargement_/399944", "title"=>"Recovery from postsynaptic depression by spike decorrelation and reservoir enlargement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:45:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/729110"], "description"=>"<p>(A) Plot of the glutamate density in the extrasynaptic space for various times after vesicular release. Glial distance is 40 nm and transporter density is 5,000. (B, C) Clearance time and spreading distance is shown for various glial sheath distances from 10 nm to 100 nm and transporter densities from 2,500 to 5,000 to 10,000.</p>", "links"=>[], "tags"=>["extracellular"], "article_id"=>399466, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g003", "stats"=>{"downloads"=>5, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glutamate_dynamics_in_the_extracellular_space_/399466", "title"=>"Glutamate dynamics in the extracellular space.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:37:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/729019"], "description"=>"<p>(A) Schematic representation of the synapse: cleft height  = 20 nm, denotes the distance of vesicle release from cleft center,  = 40 nm is the distance from the glial sheath to the cleft exit, glial transporter density  = 5,000, cleft radius  = 200 nm, 130 AMPARs are uniformly distributed on the postsynaptic terminal. The vesicle release sites were uniformly distributed on presynaptic terminal inside the cleft. (B, C) Impact of variation of release site relative to the receptor location on the number of open AMPARs (B) and glutamate concentration in the cleft (C): Release site distance was varied in steps of 10 nm from the edge (200 nm, green) to the center (0 nm, red) of the AZ. (D, E) Doubling from 5,000 to 10,000 has little influence on peak open AMPAR numbers (D) and on glutamate molecules (E), but accelerates the time course of receptor closing. (F) Changing  = 20 nm, 40 nm, 100 nm affects the maximal number of open AMPARs (simultaneously released vesicles: from 1 to 7, is 5,000 (solid) or 10,000 (dashed)). Transporters maximally influence transmission for small and low number of released vesicles. (G) Increasing from 10 nm to 40 nm decreases the number of open AMPARs. (H) Influence of glial cells on synaptic transmission: Glutamate molecules re-entering the cleft after hitting the glial cell (no transporters,  = 0), for  = 20 nm to 60 nm.</p>", "links"=>[], "tags"=>["biophysics", "neuroscience", "mathematics"], "article_id"=>399374, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_the_cleft_/399374", "title"=>"Dynamics of the cleft.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:36:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/729720"], "description"=>"<p>(A) Synapse model in which clusters of AMPARs (a, b, c) are co-localized with release sites of vesicle fusion. (B) Reliable neuron-to-neuron communication can result from three signaling modes: spatial integration (over several synaptic contacts), time integration (over several bursts at a single synapse) or distributed signaling (at robust synaptic connections, see text.</p>", "links"=>[], "tags"=>["site-receptor", "alignment", "synaptic"], "article_id"=>400079, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g008", "stats"=>{"downloads"=>3, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_release_site_receptor_alignment_at_simple_and_multiple_synaptic_boutons_/400079", "title"=>"Summary of the release site-receptor alignment at simple and multiple synaptic boutons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 00:01:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/729337"], "description"=>"<p>(A–C) An equilibrated synapse (A) transits, by extrasynaptic AMPAR insertion (B), to a synapse with an increased number of PSD-based AMPARs (C). Insertion of receptors leads to a 27% increase in the number of open AMPARs (B). Translocation of these receptors to the PSD results in a further 23% increase (C). This transition can be viewed as a two-step process following LTP where at the beginning receptors are apposed to the presynaptic area but are not inside the PSD. (D–F) The distribution of the synaptic response corresponding to the synaptic settings of (A), (B), (C), where (D) corresponds to (A). Three different release site distributions were simulated: release at the the AZ center (red); release sites uniformly distributed over the AZ (blue); release sites uniformly distributed over the entire presynaptic terminal (green). The current variation is more reduced for release at the AZ center or for a small active zone compared to a uniform release. (Glial transporter density: 5,000.).</p>", "links"=>[], "tags"=>["ampar"], "article_id"=>399700, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increase_in_AMPAR_density_following_long_term_potentiation_/399700", "title"=>"Increase in AMPAR density following long term potentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:41:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/729183"], "description"=>"<p>Figures (A) to (F) show the mean (solid line) and variance (dashed) of the number of open AMPARs for different configurations of vesicle release sites and AMPARs: (A) for vesicle release sites and AMPARs uniformly distributed (UD) over AZ and PSD, respectively, (B) for UD release sites but AMPARs clustered at the PSD, (C) for release sites and AMPARs clustered at the AZ center and the PSD, respectively. In that case, the CV is divided by 10, while the mean number of peak open AMPARs increases from 15 to 20 to 35. (D–F) The number of AMPARs for different release distributions (red: release in the center of the AZ; blue: release sites UD over PSD; green: release sites UD over the presynaptic terminal). (G–I) The distributions of the number of peak open AMPARs, corresponding to the different release site and receptor localizations. (J) The coefficient of variation of AMPAR-mediated peak amplitudes of miniature EPSCs (n = 8) is larger compared to evoked EPSCs (n = 15, P0.01). Representative sample traces of AMPAR-EPSCs (Scale bar, 10 pA, 5 ms) and mEPSCs (Scale bar, 5 pA, 5 ms) are shown above the respective bars.</p>", "links"=>[], "tags"=>["synaptic", "alignment", "sites"], "article_id"=>399542, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_efficiency_of_synaptic_transmission_by_alignment_of_release_sites_and_receptors_/399542", "title"=>"Increased efficiency of synaptic transmission by alignment of release sites and receptors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:39:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/728898"], "description"=>"<p>(A) Sketch of an excitatory synapse consisting of the presynaptic terminal where vesicles are released, and the postsynaptic element where glutamate receptors are located. The synapse is surrounded by astroglial processes containing glutamate transporters (GLTs). Presynaptic vesicle fusion occurs at randomly selected locations, released glutamate (blue) diffuses in the cleft and binds to AMPARs (green) or GLTs (pink). AMPARs diffuse between the PSD, where they can attach to scaffolding molecules (orange) and the extrasynaptic regions, where they can undergo endocytosis (1) and exocytosis (2), maintaining the number of AMPARs at the post-synaptic terminal. (B) Two co-axial cylinders represent the pre- and postsynaptic terminal, forming a gap which represents the synaptic cleft. AMPARs (green) are distributed inside and outside the PSD. The trajectory of a glutamate molecule as illustrated by red, blue or green arrows corresponds to binding to AMPARs, GLTs or diffusing away from the cleft (at 500 nm), respectively.</p>", "links"=>[], "tags"=>["synapse"], "article_id"=>399252, "categories"=>["Mathematics", "Neuroscience", "Biophysics"], "users"=>["Dominik Freche", "Ulrike Pannasch", "Nathalie Rouach", "David Holcman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025122.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Representation_of_the_synapse_dynamics_/399252", "title"=>"Representation of the synapse dynamics.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-10-03 02:34:12"}

PMC Usage Stats | Further Information

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