{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,22]],"date-time":"2026-03-22T01:09:53Z","timestamp":1774141793725,"version":"3.50.1"},"reference-count":74,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2015,7,15]],"date-time":"2015-07-15T00:00:00Z","timestamp":1436918400000},"content-version":"vor","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.1004196","type":"journal-article","created":{"date-parts":[[2015,7,15]],"date-time":"2015-07-15T20:10:23Z","timestamp":1436991023000},"page":"e1004196","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":52,"title":["Emergence of Slow-Switching Assemblies in Structured Neuronal Networks"],"prefix":"10.1371","volume":"11","author":[{"given":"Michael T.","family":"Schaub","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yazan N.","family":"Billeh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Costas A.","family":"Anastassiou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christof","family":"Koch","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mauricio","family":"Barahona","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2015,7,15]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1038\/nn1233","article-title":"Large-scale recording of neuronal ensembles","volume":"7","author":"G Buzsaki","year":"2004","journal-title":"Nature Neuroscience"},{"key":"ref2","article-title":"Multiplexed, High Density Electrophysiology with Nanofabricated Neural Probes","volume":"6","author":"J Du","year":"2011","journal-title":"PLoS ONE"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1038\/nmeth.2434","article-title":"Whole-brain functional imaging at cellular resolution using light-sheet microscopy","volume":"10","author":"MB Ahrens","year":"2013","journal-title":"Nature Methods"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/j.neuron.2010.09.023","article-title":"Neural Syntax: Cell Assemblies, Synapsembles, and Readers","volume":"68","author":"G Buzsaki","year":"2010","journal-title":"Neuron"},{"key":"ref5","article-title":"The Organization of Behavior","author":"DO Hebb","year":"1949"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1038\/nrn1669","article-title":"Neural signatures of cell assembly organization","volume":"6","author":"K Harris","year":"2005","journal-title":"Nature Reviews Neuroscience"},{"key":"ref7","first-page":"507","article-title":"Highly nonrandom features of synaptic connectivity in local cortical circuits","volume":"3","author":"S Song","year":"2005","journal-title":"Plos Biology"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"5419","DOI":"10.1073\/pnas.1016051108","article-title":"A synaptic organizing principle for cortical neuronal groups","volume":"108","author":"R Perin","year":"2011","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1038\/nature03252","article-title":"Excitatory cortical neurons form fine-scale functional networks","volume":"433","author":"Y Yoshimura","year":"2005","journal-title":"Nature"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"3862","DOI":"10.1523\/JNEUROSCI.5795-10.2011","article-title":"Cell Diversity and Connection Specificity between Callosal Projection Neurons in the Frontal Cortex","volume":"31","author":"T Otsuka","year":"2011","journal-title":"Journal of Neuroscience"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1038\/nature09880","article-title":"Functional specificity of local synaptic connections in neocortical networks","volume":"473","author":"H Ko","year":"2011","journal-title":"Nature"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nature12654","article-title":"Cortical connectivity and sensory coding","volume":"503","author":"KD Harris","year":"2013","journal-title":"Nature"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.neuron.2008.12.020","article-title":"The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex","volume":"61","author":"S Lefort","year":"2009","journal-title":"Neuron"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1016\/j.neuron.2010.11.029","article-title":"An Embedded Subnetwork of Highly Active Neurons in the Neocortex","volume":"68","author":"L Yassin","year":"2010","journal-title":"Neuron"},{"key":"ref15","article-title":"Functional Clusters, Hubs, and Communities in the Cortical Micro- connectome","author":"M Shimono","year":"2014","journal-title":"Cerebral Cortex"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"16193","DOI":"10.1073\/pnas.1303813110","article-title":"Hierarchical excitatory synaptic connectivity in mouse olfactory cortex","volume":"110","author":"MJ McGinley","year":"2013","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1016\/S0896-6273(00)81209-X","article-title":"Olfactory functions are mediated by parallel and hierarchical processing","volume":"26","author":"I Savic","year":"2000","journal-title":"Neuron"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/cercor\/1.1.1","article-title":"Distributed hierarchical processing in the primate cerebral cortex","volume":"1","author":"DJ Felleman","year":"1991","journal-title":"Cerebral Cortex"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.cub.2013.03.015","article-title":"Systematic Analysis of Neural Projections Reveals Clonal Composition of the Drosophila Brain","volume":"23","author":"M Ito","year":"2013","journal-title":"Current Biology"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/0006-8993(88)91499-0","article-title":"Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm","volume":"439","author":"C J Pavlides","year":"1988","journal-title":"Brain Research"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"11725","DOI":"10.1523\/JNEUROSCI.23-37-11725.2003","article-title":"Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough","volume":"23","author":"J Hyman","year":"2003","journal-title":"Journal of Neuroscience"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1038\/nn.3220","article-title":"Slow dynamics and high variability in balanced cortical networks with clustered connections","volume":"15","author":"A Litwin-Kumar","year":"2012","journal-title":"Nature Neuroscince"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1162\/089976698300017214","article-title":"Chaotic balanced state in a model of cortical circuits","volume":"10","author":"C van Vreeswijk","year":"1998","journal-title":"Neural Computation"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1007\/s11222-007-9033-z","article-title":"A tutorial on spectral clustering","volume":"17","author":"U von Luxburg","year":"2007","journal-title":"Statistics and Computing"},{"key":"ref25","unstructured":"Zhang X, Rao Nadakuditi R, Newman MEJ (2013) Spectra of random graphs with community structure and arbitrary degrees. URL <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/arxiv.org\/abs\/1310.0046v1\" xlink:type=\"simple\">http:\/\/arxiv.org\/abs\/1310.0046v1<\/ext-link>. arXiv:1310.0046."},{"key":"ref26","doi-asserted-by":"crossref","first-page":"012803","DOI":"10.1103\/PhysRevE.87.012803","article-title":"Spectra of random graphs with arbitrary expected degrees","volume":"87","author":"RR Nadakuditi","year":"2013","journal-title":"Physical Review E"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.neuron.2009.02.005","article-title":"Balanced Amplification: A New Mechanism of Selective Amplification of Neural Activity Patterns","volume":"61","author":"BK Murphy","year":"2009","journal-title":"Neuron"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"111","DOI":"10.2307\/1909285","article-title":"Aggregation of Variables in Dynamic Systems","volume":"29","author":"HA Simon","year":"1961","journal-title":"Econometrica"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"e2148","DOI":"10.1371\/journal.pone.0002148","article-title":"On How Network Architecture Determines the Dominant Patterns of Spontaneous Neural Activity","volume":"3","author":"RF Gal\u00e1n","year":"2008","journal-title":"PLoS ONE"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"12755","DOI":"10.1073\/pnas.0903215107","article-title":"Stability of graph communities across time scales","volume":"107","author":"JC Delvenne","year":"2010","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"e32210","DOI":"10.1371\/journal.pone.0032210","article-title":"Markov Dynamics as a Zooming Lens for Multiscale Community Detection: Non Clique-Like Communities and the Field-of-View Limit","volume":"7","author":"MT Schaub","year":"2012","journal-title":"PLoS ONE"},{"key":"ref32","first-page":"221","article-title":"Dynamics On and Of Complex Networks","volume":"Volume 2","author":"JC Delvenne","year":"2013"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.jneumeth.2014.08.011","article-title":"Revealing cell assemblies at multiple levels of granularity","volume":"236","author":"YN Billeh","year":"2014","journal-title":"Journal of Neuroscience Methods"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"188104","DOI":"10.1103\/PhysRevLett.97.188104","article-title":"Eigenvalue Spectra of Random Matrices for Neural Networks","volume":"97","author":"K Rajan","year":"2006","journal-title":"Physical Review Letters"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"1895","DOI":"10.1103\/PhysRevLett.60.1895","article-title":"Spectrum of Large Random Asymmetric Matrices","volume":"60","author":"HJ Sommers","year":"1988","journal-title":"Physical Review Letters"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.neuron.2008.12.012","article-title":"Memory without Feedback in a Neural Network","volume":"61","author":"MS Goldman","year":"2009","journal-title":"Neuron"},{"key":"ref37","doi-asserted-by":"crossref","DOI":"10.1515\/9780691213101","article-title":"Spectra and pseudospectra: the behavior of nonnormal matrices and operators","author":"LN Trefethen","year":"2005"},{"key":"ref38","article-title":"Matrix Computations","author":"H Golub","year":"1996"},{"key":"ref39","doi-asserted-by":"crossref","unstructured":"Stewart GW (2001) Matrix Algorithms Volume 2: Eigensystems, volume 2. Siam.","DOI":"10.1137\/1.9780898718058"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1162\/NECO_a_00091","article-title":"Collective stability of networks of winner-take-all circuits","volume":"23","author":"U Rutishauser","year":"2011","journal-title":"Neural Computation"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1038\/30918","article-title":"Collective dynamics of \u2018small-world\u2019 networks","volume":"393","author":"DJ Watts","year":"1998","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/nrn2575","article-title":"Complex brain networks: graph theoretical analysis of structural and functional systems","volume":"10","author":"E Bullmore","year":"2009","journal-title":"Nature Reviews Neuroscience"},{"key":"ref43","doi-asserted-by":"crossref","DOI":"10.3389\/fnins.2010.00200","article-title":"Modular and hierarchically modular organization of brain networks","volume":"4","author":"D Meunier","year":"2010","journal-title":"Frontiers in Neuroscience"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"054101","DOI":"10.1103\/PhysRevLett.89.054101","article-title":"Synchronization in Small-World Systems","volume":"89","author":"M Barahona","year":"2002","journal-title":"Physical Review Letters"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1126\/science.286.5439.509","article-title":"Emergence of Scaling in Random Networks","volume":"286","author":"AL Barabsi","year":"1999","journal-title":"Science"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1126\/science.2315702","article-title":"Simulation of paleocortex performs hierarchical clustering","volume":"247","author":"J Ambrosingerson","year":"1990","journal-title":"Science"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1126\/science.1089662","article-title":"Communication in neuronal networks","volume":"301","author":"S Laughlin","year":"2003","journal-title":"Science"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"318326","DOI":"10.1038\/nature12983","article-title":"Interneuron cell types are fit to function","volume":"505","author":"A Kepecs","year":"2014","journal-title":"Nature"},{"key":"ref49","article-title":"Tasks for inhibitory interneurons in intact brain circuits","author":"L Roux","year":"2014","journal-title":"Neuropharmacology"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1016\/j.neuron.2007.02.012","article-title":"Disynaptic inhibition between neocortical pyramidal cells mediated by martinotti cells","volume":"53","author":"G Silberberg","year":"2007","journal-title":"Neuron"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.neuron.2012.11.004","article-title":"Neocortical Somatostatin-Expressing GABAergic Interneurons Disinhibit the Thalamorecipient Layer 4","volume":"77","author":"H Xu","year":"2013","journal-title":"Neuron"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1662","DOI":"10.1038\/nn.3544","article-title":"A disinhibitory circuit mediates motor integration in the somatosensory cortex","volume":"16","author":"S Lee","year":"2013","journal-title":"Nature Neuroscience"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1038\/nature12676","article-title":"Cortical interneurons that specialize in disinhibitory control","volume":"503","author":"HJ Pi","year":"2013","journal-title":"Nature"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1038\/nn.3446","article-title":"Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons","volume":"16","author":"CK Pfeffer","year":"2013","journal-title":"Nature Neuroscience"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1242\/jeb.017574","article-title":"Energy limitation as a selective pressure on the evolution of sensory systems","volume":"211","author":"JE Niven","year":"2008","journal-title":"Journal of Experimental Biology"},{"key":"ref56","doi-asserted-by":"crossref","DOI":"10.1103\/PhysRevLett.106.058101","article-title":"Predicting Criticality and Dynamic Range in Complex Networks: Effects of Topology","volume":"106","author":"DB Larremore","year":"2011","journal-title":"Physical Review Letters"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"11167","DOI":"10.1523\/JNEUROSCI.23-35-11167.2003","article-title":"Neuronal avalanches in neocortical circuits","volume":"23","author":"J Beggs","year":"2003","journal-title":"Journal of Neuroscience"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1038\/nature02078","article-title":"Spontaneously emerging cortical representations of visual attributes","volume":"425","author":"T Kenet","year":"2003","journal-title":"Nature"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"3844","DOI":"10.1073\/pnas.92.9.3844","article-title":"Theory of orientation tuning in visual-cortex","volume":"92","author":"R Ben-Yishai","year":"1995","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"5448","DOI":"10.1523\/JNEUROSCI.15-08-05448.1995","article-title":"An emergent model of orientation selectivity in cat visual cortical simple cells","volume":"15","author":"D Somers","year":"1995","journal-title":"Journal of Neuroscience"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/86089","article-title":"Intracortical origin of visual maps","volume":"4","author":"U Ernst","year":"2001","journal-title":"Nature Neuroscience"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1523\/JNEUROSCI.4514-06.2007","article-title":"Metastability of active CA3 networks","volume":"27","author":"T Sasaki","year":"2007","journal-title":"Journal of Neuroscience"},{"key":"ref63","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms6319","article-title":"Formation and maintenance of neuronal assemblies through synaptic plasticity","volume":"5","author":"A Litwin-Kumar","year":"2014","journal-title":"Nature Communications"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1038\/nature01834","article-title":"Organization of cell assemblies in the hippocampus","volume":"424","author":"K Harris","year":"2003","journal-title":"Nature"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/nature04587","article-title":"Reverse replay of behavioural sequences in hippocampal place cells during the awake state","volume":"440","author":"D Foster","year":"2006","journal-title":"Nature"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"1950","DOI":"10.1126\/science.278.5345.1950","article-title":"Spike synchronization and rate modulation differentially involved in motor cortical function","volume":"278","author":"A Riehle","year":"1997","journal-title":"Science"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1038\/nature00974","article-title":"An ultra-sparse code underlies the generation of neural sequences in a songbird","volume":"419","author":"R Hahnloser","year":"2002","journal-title":"Nature"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.1152\/jn.00891.2005","article-title":"Spike-timing precision underlies the coding efficiency of auditory receptor neurons","volume":"95","author":"A Rokem","year":"2006","journal-title":"Journal of Neurophysiology"},{"key":"ref69","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1371\/journal.pbio.0060016","article-title":"Sparse representation of sounds in the unanesthetized auditory cortex","volume":"6","author":"T Hromadka","year":"2008","journal-title":"PLoS Biology"},{"key":"ref70","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/nrn3687","article-title":"The log-dynamic brain: how skewed distributions affect network operations","volume":"15","author":"G Buzsaki","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"key":"ref71","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nature13186","article-title":"A mesoscale connectome of the mouse brain","volume":"508","author":"SW Oh","year":"2014","journal-title":"Nature"},{"key":"ref72","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1038\/nn.2479","article-title":"Connectivity reflects coding: a model of voltage-based STDP with homeostasis","volume":"13","author":"C Clopath","year":"2010","journal-title":"Nature Neuroscience"},{"key":"ref73","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.neuron.2013.05.023","article-title":"A Biophysically Detailed Model of Neocortical Local Field Potentials Predicts the Critical Role of Active Membrane Currents","volume":"79","author":"MW Reimann","year":"2013","journal-title":"Neuron"},{"key":"ref74","doi-asserted-by":"crossref","first-page":"036113","DOI":"10.1103\/PhysRevE.71.036113","article-title":"Efficient generation of large random networks","volume":"71","author":"V Batagelj","year":"2005","journal-title":"Phys Rev E"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1005288","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2017,2,10]],"date-time":"2017-02-10T00:00:00Z","timestamp":1486684800000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1004196","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,18]],"date-time":"2022-05-18T04:15:53Z","timestamp":1652847353000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1004196"}},"subtitle":[],"editor":[{"given":"Danielle S","family":"Bassett","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2015,7,15]]},"references-count":74,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2015,7,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1004196","relation":{"correction":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1005288","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,7,15]]}}}