Spreading Depression Sends Microglia on Lévy Flights
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{"title"=>"Spreading depression sends microglia on lévy flights", "type"=>"journal", "authors"=>[{"first_name"=>"Yelena Y.", "last_name"=>"Grinberg", "scopus_author_id"=>"22134470200"}, {"first_name"=>"John G.", "last_name"=>"Milton", "scopus_author_id"=>"7102435949"}, {"first_name"=>"Richard P.", "last_name"=>"Kraig", "scopus_author_id"=>"7006946498"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-79955618364", "doi"=>"10.1371/journal.pone.0019294", "pui"=>"361702830", "issn"=>"19326203", "pmid"=>"21541289", "isbn"=>"0011-3891", "sgr"=>"79955618364"}, "id"=>"0313c819-ca16-3332-9ad7-66be489d2475", "abstract"=>"Spreading depression (SD) is thought to cause migraine aura, and perhaps migraine, and includes a transient loss of synaptic activity preceded and followed by increased neuronal excitability. Activated microglia influence neuronal activity and play an important role in homeostatic synaptic scaling via release of cytokines. Furthermore, enhanced neuronal function activates microglia to not only secrete cytokines but also to increase the motility of their branches, with somata remaining stationary. While SD also increases the release of cytokines from microglia, the effects on microglial movement from its synaptic activity fluctuations are unknown. Accordingly, we used time-lapse imaging of rat hippocampal slice cultures to probe for microglial movement associated with SD. We observed that in uninjured brain whole microglial cells moved. The movements were well described by the type of Lévy flight known to be associated with an optimal search pattern. Hours after SD, when synaptic activity rose, microglial cell movement was significantly increased. To test how synaptic activity influenced microglial movement, we enhanced neuronal activity with chemical long-term potentiation or LPS and abolished it with TTX. We found that microglial movement was significantly decreased by enhanced neuronal activity and significantly increased by activity blockade. Finally, application of glutamate and ATP to mimic restoration of synaptic activity in the presence of TTX stopped microglial movement that was otherwise seen with TTX. Thus, synaptic activity retains microglial cells in place and an absence of synaptic activity sends them off to influence wider expanses of brain. Perhaps increased microglial movements after SD are a long-lasting, and thus maladaptive, response in which these cells increase neuronal activity via contact or paracrine signaling, which results in increased susceptibility of larger brain areas to SD. If true, then targeting mechanisms that retard activity-dependent microglial Lévy flights may be a novel means to reduce susceptibility to migraine.", "link"=>"http://www.mendeley.com/research/spreading-depression-sends-microglia-l%C3%A9vy-flights", "reader_count"=>6, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>3, "Medicine and Dentistry"=>2, "Neuroscience"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}}, "reader_count_by_country"=>{"United States"=>1, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/391830", "https://ndownloader.figshare.com/files/391847", "https://ndownloader.figshare.com/files/391857", "https://ndownloader.figshare.com/files/391874", "https://ndownloader.figshare.com/files/391892", "https://ndownloader.figshare.com/files/391918"], "description"=>"<div><p>Spreading depression (SD) is thought to cause migraine aura, and perhaps migraine, and includes a transient loss of synaptic activity preceded and followed by increased neuronal excitability. Activated microglia influence neuronal activity and play an important role in homeostatic synaptic scaling via release of cytokines. Furthermore, enhanced neuronal function activates microglia to not only secrete cytokines but also to increase the motility of their branches, with somata remaining stationary. While SD also increases the release of cytokines from microglia, the effects on microglial movement from its synaptic activity fluctuations are unknown. Accordingly, we used time-lapse imaging of rat hippocampal slice cultures to probe for microglial movement associated with SD. We observed that in uninjured brain whole microglial cells moved. The movements were well described by the type of Lévy flight known to be associated with an optimal search pattern. Hours after SD, when synaptic activity rose, microglial cell movement was significantly increased. To test how synaptic activity influenced microglial movement, we enhanced neuronal activity with chemical long-term potentiation or LPS and abolished it with TTX. We found that microglial movement was significantly decreased by enhanced neuronal activity and significantly increased by activity blockade. Finally, application of glutamate and ATP to mimic restoration of synaptic activity in the presence of TTX stopped microglial movement that was otherwise seen with TTX. Thus, synaptic activity retains microglial cells in place and an absence of synaptic activity sends them off to influence wider expanses of brain. Perhaps increased microglial movements after SD are a long-lasting, and thus maladaptive, response in which these cells increase neuronal activity via contact or paracrine signaling, which results in increased susceptibility of larger brain areas to SD. If true, then targeting mechanisms that retard activity-dependent microglial Lévy flights may be a novel means to reduce susceptibility to migraine.</p> </div>", "links"=>[], "tags"=>["spreading", "sends", "microglia", "flights"], "article_id"=>137388, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.s001", "https://dx.doi.org/10.1371/journal.pone.0019294.s002", "https://dx.doi.org/10.1371/journal.pone.0019294.s003", "https://dx.doi.org/10.1371/journal.pone.0019294.s004", "https://dx.doi.org/10.1371/journal.pone.0019294.s005", "https://dx.doi.org/10.1371/journal.pone.0019294.s006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Spreading_Depression_Sends_Microglia_on_L_vy_Flights/137388", "title"=>"Spreading Depression Sends Microglia on Lévy Flights", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-04-26 02:03:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/780613"], "description"=>"<p>(<b>A</b>) Slice electrophysiological responsiveness was first verified by eliciting standard CA3 field potentials evoked by dentate gyrus bipolar electrical stimulation. Record shows typical CA3 evoked field potential with downward deflection from CA3 action potential and upward deflection, the “inverted” excitatory post-synaptic potential, recorded at the pyramidal neuron cell body area. (<b>B</b>) Spreading depression (SD) was elicited every ∼9 min for 1 hour by dentate gyrus bipolar electrical stimulation and confirmed via the stereotypic large negative DC potential change in the extracellular space. Small deflections in baseline record reflect spontaneous neuronal activity, which after the stimulus pulse for SD (first large vertical deflections in record) was followed by increased spontaneous activity (evident as increased baseline deflections). The latter led to the massive DC change of SD and thinning of the DC line (consistent with electrical silence).</p>", "links"=>[], "tags"=>["occurs", "transient", "synaptic"], "article_id"=>450988, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spreading_depression_occurs_with_a_transient_loss_of_synaptic_activity_/450988", "title"=>"Spreading depression occurs with a transient loss of synaptic activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:16:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/780832"], "description"=>"<p>(<b>A</b>) For cytoarchitectural reference, we show hippocampal principal neuron architecture using anti-NeuN immunostaining to illustrate the CA3 pyramidal neuron area. Microglia were immunolabeled specifically with CD11b to visualize their morphology under control conditions (<b>B</b>) and after 3 hour exposure to isolectin GS-IB<sub>4</sub> (<b>C</b>). In both microglial exemplary images, the cells (arrows) show a ramified morphology without evidence of activation (i.e., short and thick branches or change to ameboid cellular shape). Cal bars, 500 µm (<b>A</b>) 50 µm (<b>B</b> and <b>C</b>).</p>", "links"=>[], "tags"=>["microglial", "morphology", "was", "altered", "isolectin"], "article_id"=>451199, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hippocampal_slice_microglial_morphology_was_not_altered_by_exposure_to_isolectin_GS_IB_4_/451199", "title"=>"Hippocampal slice microglial morphology was not altered by exposure to isolectin GS-IB<sub>4</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:19:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/780948"], "description"=>"<p>Slice cultures were screened for vitality via the fluorescent dead-cell marker Sytox Green immediately before and after imaging. The dotted large arc outlines the pyramidal neuron layer and the smaller arc outlines the dentate gyrus. (<b>A</b>) An exemplary image acquired before filming showed no evidence of cell death. (<b>B</b>) Similarly, no evidence of cell death was seen after filming. These pre- and post-imaging Sytox pictures correspond to the control movie used for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019294#pone-0019294-g004\" target=\"_blank\"><b>Figure 4</b></a> and <b>Supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0019294#pone.0019294.s001\" target=\"_blank\">Video S1</a></b>.</p>", "links"=>[], "tags"=>["procedures", "did"], "article_id"=>451318, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Imaging_procedures_did_not_result_in_cell_death_/451318", "title"=>"Imaging procedures did not result in cell death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:21:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/781090"], "description"=>"<p>(<b>A</b>) Control movie frame with white lines showing paths of microglia (1–5) that moved ≥50 µm. (<b>B</b>) Cell #1 (<b>A</b>) path enlarged to show movement beginning at upper right and ending at lower left, yellow bars mark 2 and 4 hours. Orange dashed lines encircle regions with multiple small steps compared to occasional long steps, suggestive of a Lévy flight pattern. (<b>C</b>) Control microglial cell Δ velocity (<i>n</i> = 18 cells; 6462 Δ's) showed a Lévy power law distribution with exponent α = 0.9 and scale factor γ = 0.3 (black line). The red line shows a Gaussian distribution (α = 2; variance = 0.5). (<b>D</b>) Realization of a Lévy flight constructed using the distribution (<b>C</b>) determined from the full population of moving microglia (top) qualitatively reproduced the same intermittent behavior of an exemplary long-distance moving microglial cell (bottom). Cal bars, 50 µm (<b>A</b>) and 10 µm (<b>B</b>).</p>", "links"=>[], "tags"=>["moved", "distances"], "article_id"=>451459, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microglia_moved_long_distances_in_a_L_233_vy_flight_pattern_/451459", "title"=>"Microglia moved long distances in a Lévy flight pattern.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:24:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/781268"], "description"=>"<p>(<b>A</b>) Control slice cultures showed typical spontaneous (not shown) and evoked (<i>i</i>) CA3 area field potentials. Slices exposed to lipopolysaccharide (LPS) or chemical long-term potentiation (cLTP) showed increased synaptic activity that included CA3 area bursting (<i>ii</i>) and electrographic seizures (<i>iii</i>). Slices exposed to tetrodotoxin (TTX) showed no spontaneous or evoked synaptic activity (<i>iv</i>). Time calibration bars are 25 msec (<i>iv</i>) and 25 sec (<i>v</i>). (<b>B</b>) Microglial movement was quantified by tracking the cells that moved ≥50 µm from their position of origin. Specific microglial cell counts were 1.44±0.43 for control (<i>n</i> = 16 movies; range: 1–5 cells/movie), 0.06±0.06 for LPS (<i>n</i> = 16 movies; range: 0–1 cells/movie), 0.38±0.15 for cLTP (<i>n</i> = 16 movies; range: 0–2 cells/movie), and 8.40±1.89 for TTX (<i>n</i> = 5 movies; 3–13 cells/movie). Values are mean ± SEM. Data was statistically tested (see text) using cell counts transformed by √(<i>n</i>+1) with significance (P<0.05; “*”) shown here for illustration. (<b>C</b>) Microglial movement after TTX exposure also showed a Lévy power law distribution (red dots; <i>n</i> = 42 cells; 15,523 Δ's). The Lévy distribution of control cells (orange dots) is included for comparison, to show that the distributions appear very similar.</p>", "links"=>[], "tags"=>["long-distance", "was", "inversely", "proportional", "neuronal"], "article_id"=>451638, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microglial_long_distance_movement_was_inversely_proportional_to_neuronal_activity_/451638", "title"=>"Microglial long-distance movement was inversely proportional to neuronal activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:27:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/781392"], "description"=>"<p>(<b>A</b>) Microglial movement was recorded 7–13 hours after induction of spreading depression (SD) and microglial cell movement was quantified as with the other conditions, by tracking the cells that moved ≥50 µm from their position of origin. Specific microglial cell counts for SD movies (<i>n</i> = 5) were 0–16 cells per movie with a mean ± SEM of 7.60±2.86 cells/movie. Cell counts were 1.44±0.43 for control (<i>n</i> = 16 movies; range: 1–5 cells/movie). Values are mean ± SEM. Data was statistically tested (see text) using cell counts transformed by √(<i>n</i>+1) with significance (P<0.05; “*”) shown here for illustration. (<b>B</b>) Exemplary records of field potential responses to single paired pulse inhibition (PPI) show increased excitability following SD. Before SD (upper record) the second evoked response is decreased, consistent with fast GABAergic inhibition. The latter is not evident with PPI responses evoked 9 hours after SD (bottom record).</p>", "links"=>[], "tags"=>["increases", "spreading"], "article_id"=>451767, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microglial_migration_increases_long_after_the_electrical_silence_associated_with_spreading_depression_/451767", "title"=>"Microglial migration increases long after the electrical silence associated with spreading depression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:29:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/781523"], "description"=>"<p>(<b>A</b>) We added ATP and glutamate to hippocampal cultures in TTX and observed that this paradigm abrogated the increased microglial movement normally seen with TTX alone. Data was statistically tested (see text) using cell counts transformed by √(<i>n</i>+1) with significance (P<0.05; “*”) shown here for illustration. (<b>B</b>) Cartoon schematic shows how paracrine signals (e.g. glutamate or ATP) released from neurons with synaptic activity (black) may signal microglial cells to remain stationary (top) where they can respond with release of neuronal activity modulators (e.g. TNF-α [green]). In contrast, reduced neuronal activity may allow for the “release” of microglial cells to wander (bottom), thus allowing them to affect larger expanses of brain.</p>", "links"=>[], "tags"=>["interactive", "paracrine", "microglial"], "article_id"=>451897, "categories"=>["Neuroscience", "Immunology"], "users"=>["Yelena Y. Grinberg", "John G. Milton", "Richard P. Kraig"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0019294.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_of_potential_interactive_paracrine_basis_of_microglial_cell_movement_/451897", "title"=>"Schematic of potential interactive paracrine basis of microglial cell movement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-26 00:31:37"}

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