{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T21:08:16Z","timestamp":1772226496343,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1009196","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,7,22]],"date-time":"2021-07-22T00:00:00Z","timestamp":1626912000000}}],"reference-count":88,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2021,7,12]],"date-time":"2021-07-12T00:00:00Z","timestamp":1626048000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100001391","name":"Whitehall Foundation","doi-asserted-by":"publisher","award":["17-12-114"],"award-info":[{"award-number":["17-12-114"]}],"id":[{"id":"10.13039\/100001391","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1429500"],"award-info":[{"award-number":["1429500"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1513779"],"award-info":[{"award-number":["1513779"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"name":"lilly endowment, inc."}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>The directionality of network information flow dictates how networks process information. A central component of information processing in both biological and artificial neural networks is their ability to perform synergistic integration\u2013a type of computation. We established previously that synergistic integration varies directly with the strength of feedforward information flow. However, the relationships between both recurrent and feedback information flow and synergistic integration remain unknown. To address this, we analyzed the spiking activity of hundreds of neurons in organotypic cultures of mouse cortex. We asked how empirically observed synergistic integration\u2013determined from partial information decomposition\u2013varied with local functional network structure that was categorized into motifs with varying recurrent and feedback information flow. We found that synergistic integration was elevated in motifs with greater recurrent information flow beyond that expected from the local feedforward information flow. Feedback information flow was interrelated with feedforward information flow and was associated with decreased synergistic integration. Our results indicate that synergistic integration is distinctly influenced by the directionality of local information flow.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1009196","type":"journal-article","created":{"date-parts":[[2021,7,12]],"date-time":"2021-07-12T17:40:25Z","timestamp":1626111625000},"page":"e1009196","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":34,"title":["Partial information decomposition reveals that synergistic neural integration is greater downstream of recurrent information flow in organotypic cortical cultures"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2894-7138","authenticated-orcid":true,"given":"Samantha P.","family":"Sherrill","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7127-4418","authenticated-orcid":true,"given":"Nicholas M.","family":"Timme","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2368-1366","authenticated-orcid":true,"given":"John M.","family":"Beggs","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7006-4112","authenticated-orcid":true,"given":"Ehren L.","family":"Newman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2021,7,12]]},"reference":[{"issue":"1","key":"pcbi.1009196.ref001","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1093\/cercor\/13.1.53","article-title":"Closed-loop neuronal computations: focus on vibrissa somatosensation in rat","volume":"13","author":"E Ahissar","year":"2003","journal-title":"Cerebral Cortex"},{"issue":"1","key":"pcbi.1009196.ref002","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0167-7012(00)00201-3","article-title":"Artificial neural networks: fundamentals, computing, design, and application","volume":"43","author":"IA Basheer","year":"2000","journal-title":"Journal of microbiological methods"},{"key":"pcbi.1009196.ref003","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1146\/annurev-vision-082114-035447","article-title":"Deep neural networks: a new framework for modeling biological vision and brain information processing","volume":"1","author":"N Kriegeskorte","year":"2015","journal-title":"Annual review of vision science"},{"issue":"11","key":"pcbi.1009196.ref004","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/S0166-2236(00)01657-X","article-title":"The distinct modes of vision offered by feedforward and recurrent processing","volume":"23","author":"VA Lamme","year":"2000","journal-title":"Trends in neurosciences"},{"issue":"1","key":"pcbi.1009196.ref005","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1523\/JNEUROSCI.3789-11.2012","article-title":"Strong recurrent networks compute the orientation tuning of surround modulation in the primate primary visual cortex","volume":"32","author":"S Shushruth","year":"2012","journal-title":"Journal of Neuroscience"},{"issue":"2","key":"pcbi.1009196.ref006","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1162\/netn_a_00069","article-title":"Computation is concentrated in rich clubs of local cortical networks","volume":"3","author":"SP Faber","year":"2019","journal-title":"Network Neuroscience"},{"key":"pcbi.1009196.ref007","unstructured":"Williams PL, Beer RD. Generalized measures of information transfer. arXiv preprint arXiv:1102.1507. 2011 Feb 8. Available from: https:\/\/arxiv.org\/abs\/1102.1507"},{"issue":"5","key":"pcbi.1009196.ref008","doi-asserted-by":"crossref","first-page":"e1004858","DOI":"10.1371\/journal.pcbi.1004858","article-title":"High-degree neurons feed cortical computations","volume":"12","author":"NM Timme","year":"2016","journal-title":"PLoS computational biology"},{"key":"pcbi.1009196.ref009","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.bandc.2015.09.004","article-title":"Partial information decomposition as a unified approach to the specification of neural goal functions","volume":"112","author":"M Wibral","year":"2017","journal-title":"Brain and cognition"},{"key":"pcbi.1009196.ref010","first-page":"1","article-title":"Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically-relevant timescales","volume":"2020","author":"SP Sherrill","journal-title":"Network Neuroscience"},{"issue":"9","key":"pcbi.1009196.ref011","doi-asserted-by":"crossref","first-page":"494","DOI":"10.3390\/e19090494","article-title":"Quantifying information modification in developing neural networks via partial information decomposition","volume":"19","author":"M Wibral","year":"2017","journal-title":"Entropy"},{"issue":"5226","key":"pcbi.1009196.ref012","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1126\/science.7638624","article-title":"Recurrent excitation in neocortical circuits","volume":"269","author":"RJ Douglas","year":"1995","journal-title":"Science"},{"issue":"13","key":"pcbi.1009196.ref013","doi-asserted-by":"crossref","first-page":"R496","DOI":"10.1016\/j.cub.2007.04.024","article-title":"Recurrent neuronal circuits in the neocortex","volume":"17","author":"RJ Douglas","year":"2007","journal-title":"Current biology"},{"issue":"8","key":"pcbi.1009196.ref014","doi-asserted-by":"crossref","first-page":"2554","DOI":"10.1073\/pnas.79.8.2554","article-title":"Neural networks and physical systems with emergent collective computational abilities","volume":"79","author":"JJ Hopfield","year":"1982","journal-title":"Proceedings of the national academy of sciences"},{"issue":"6","key":"pcbi.1009196.ref015","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1016\/j.conb.2005.10.002","article-title":"Place cells, spatial maps and the population code for memory","volume":"15","author":"S Leutgeb","year":"2005","journal-title":"Current opinion in neurobiology"},{"issue":"2","key":"pcbi.1009196.ref016","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.neuron.2013.11.017","article-title":"CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation","volume":"81","author":"JP Neunuebel","year":"2014","journal-title":"Neuron"},{"issue":"11","key":"pcbi.1009196.ref017","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1101\/lm.631207","article-title":"An attractor network in the hippocampus: theory and neurophysiology","volume":"14","author":"ET Rolls","year":"2007","journal-title":"Learning & memory"},{"key":"pcbi.1009196.ref018","doi-asserted-by":"crossref","first-page":"74","DOI":"10.3389\/fnsys.2013.00074","article-title":"The mechanisms for pattern completion and pattern separation in the hippocampus","volume":"7","author":"E Rolls","year":"2013","journal-title":"Frontiers in systems neuroscience"},{"issue":"35","key":"pcbi.1009196.ref019","doi-asserted-by":"crossref","first-page":"8835","DOI":"10.1073\/pnas.1719397115","article-title":"Recurrent computations for visual pattern completion","volume":"115","author":"H Tang","year":"2018","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"2\u20134","key":"pcbi.1009196.ref020","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/S0167-2789(97)00107-3","article-title":"Time for retrieval in recurrent associative memories","volume":"107","author":"A Treves","year":"1997","journal-title":"Physica D: Nonlinear Phenomena"},{"issue":"1","key":"pcbi.1009196.ref021","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.neuron.2005.11.026","article-title":"Dynamic shape synthesis in posterior inferotemporal cortex","volume":"49","author":"SL Brincat","year":"2006","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1009196.ref022","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1167\/13.10.1","article-title":"Representational dynamics of object vision: the first 1000 ms","volume":"13","author":"T Carlson","year":"2013","journal-title":"Journal of vision"},{"issue":"3","key":"pcbi.1009196.ref023","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/nn.3635","article-title":"Resolving human object recognition in space and time","volume":"17","author":"RM Cichy","year":"2014","journal-title":"Nature neuroscience"},{"issue":"10","key":"pcbi.1009196.ref024","doi-asserted-by":"crossref","first-page":"3602","DOI":"10.1093\/cercor\/bhu203","article-title":"Predicting the time course of individual objects with MEG","volume":"25","author":"A Clarke","year":"2015","journal-title":"Cerebral Cortex"},{"issue":"6005","key":"pcbi.1009196.ref025","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1126\/science.1194908","article-title":"Functional compartmentalization and viewpoint generalization within the macaque face-processing system","volume":"330","author":"WA Freiwald","year":"2010","journal-title":"Science"},{"issue":"6747","key":"pcbi.1009196.ref026","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1038\/23703","article-title":"Global and fine information coded by single neurons in the temporal visual cortex","volume":"400","author":"Y Sugase","year":"1999","journal-title":"Nature"},{"issue":"3","key":"pcbi.1009196.ref027","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1016\/j.neuron.2014.06.017","article-title":"Spatiotemporal dynamics underlying object completion in human ventral visual cortex","volume":"83","author":"H Tang","year":"2014","journal-title":"Neuron"},{"key":"pcbi.1009196.ref028","first-page":"677237","article-title":"Recurrent networks can recycle neural resources to flexibly trade speed for accuracy in visual recognition","volume":"1","author":"CJ Spoerer","year":"2020","journal-title":"BioRxiv"},{"issue":"6031","key":"pcbi.1009196.ref029","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1126\/science.1202043","article-title":"Preserved feedforward but impaired top-down processes in the vegetative state","volume":"332","author":"M Boly","year":"2011","journal-title":"Science"},{"issue":"9","key":"pcbi.1009196.ref030","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1038\/nn.4356","article-title":"Sensory and decision-related activity propagate in a cortical feedback loop during touch perception","volume":"19","author":"SE Kwon","year":"2016","journal-title":"Nature neuroscience"},{"issue":"5","key":"pcbi.1009196.ref031","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1016\/j.neuron.2015.05.006","article-title":"A top-down cortical circuit for accurate sensory perception","volume":"86","author":"S Manita","year":"2015","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1009196.ref032","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/nrn3476","article-title":"Top-down influences on visual processing","volume":"14","author":"CD Gilbert","year":"2013","journal-title":"Nature Reviews Neuroscience"},{"key":"pcbi.1009196.ref033","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3389\/fnsys.2019.00031","article-title":"The role of top-down modulation in shaping sensory processing across brain states: implications for consciousness","volume":"13","author":"T Sikkens","year":"2019","journal-title":"Frontiers in systems neuroscience"},{"issue":"3","key":"pcbi.1009196.ref034","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1017\/S0140525X12000477","article-title":"Whatever next? Predictive brains, situated agents, and the future of cognitive science","volume":"36","author":"A Clark","year":"2013","journal-title":"Behavioral and brain sciences"},{"issue":"4","key":"pcbi.1009196.ref035","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.neuron.2012.10.038","article-title":"Canonical microcircuits for predictive coding","volume":"76","author":"AM Bastos","year":"2012","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1009196.ref036","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/j.neuron.2007.05.019","article-title":"Brain states: top-down influences in sensory processing","volume":"54","author":"CD Gilbert","year":"2007","journal-title":"Neuron"},{"issue":"2\u20133","key":"pcbi.1009196.ref037","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/S0165-0173(99)00049-1","article-title":"Gating of information flow within the limbic system and the pathophysiology of schizophrenia","volume":"31","author":"AA Grace","year":"2000","journal-title":"Brain Research Reviews"},{"issue":"1","key":"pcbi.1009196.ref038","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms13276","article-title":"Random synaptic feedback weights support error backpropagation for deep learning","volume":"7","author":"TP Lillicrap","year":"2016","journal-title":"Nature communications"},{"issue":"19","key":"pcbi.1009196.ref039","doi-asserted-by":"crossref","first-page":"8504","DOI":"10.1523\/JNEUROSCI.5124-12.2013","article-title":"Corticocortical feedback contributes to surround suppression in V1 of the alert primate","volume":"33","author":"JJ Nassi","year":"2013","journal-title":"Journal of Neuroscience"},{"issue":"1","key":"pcbi.1009196.ref040","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-018-04500-5","article-title":"Top-down feedback controls spatial summation and response amplitude in primate visual cortex","volume":"9","author":"L Nurminen","year":"2018","journal-title":"Nature communications"},{"issue":"12","key":"pcbi.1009196.ref041","doi-asserted-by":"crossref","first-page":"e115764","DOI":"10.1371\/journal.pone.0115764","article-title":"Multiplex networks of cortical and hippocampal neurons revealed at different timescales","volume":"9","author":"N Timme","year":"2014","journal-title":"PloS one"},{"issue":"8","key":"pcbi.1009196.ref042","doi-asserted-by":"crossref","first-page":"e105324","DOI":"10.1371\/journal.pone.0105324","article-title":"Large-scale, high-resolution multielectrode-array recording depicts functional network differences of cortical and hippocampal cultures","volume":"9","author":"S Ito","year":"2014","journal-title":"PloS one"},{"issue":"1","key":"pcbi.1009196.ref043","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1523\/JNEUROSCI.11-01-00072.1991","article-title":"Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro","volume":"11","author":"A Mason","year":"1991","journal-title":"Journal of Neuroscience"},{"issue":"2","key":"pcbi.1009196.ref044","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1152\/jn.1994.71.2.437","article-title":"Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs","volume":"71","author":"HA Swadlow","year":"1994","journal-title":"Journal of neurophysiology"},{"issue":"5","key":"pcbi.1009196.ref045","doi-asserted-by":"crossref","first-page":"e1006153","DOI":"10.1371\/journal.pcbi.1006153","article-title":"Functional triplet motifs underlie accurate predictions of single-trial responses in populations of tuned and untuned V1 neurons","volume":"14","author":"JB Dechery","year":"2018","journal-title":"PLoS computational biology"},{"issue":"10","key":"pcbi.1009196.ref046","doi-asserted-by":"crossref","first-page":"3743","DOI":"10.1093\/cercor\/bhu252","article-title":"Functional clusters, hubs, and communities in the cortical microconnectome","volume":"25","author":"M Shimono","year":"2015","journal-title":"Cerebral Cortex"},{"issue":"2","key":"pcbi.1009196.ref047","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.neuron.2014.12.018","article-title":"Visual areas exert feedforward and feedback influences through distinct frequency channels","volume":"85","author":"AM Bastos","year":"2015","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1009196.ref048","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1113\/jphysiol.1959.sp006308","article-title":"Receptive fields of single neurones in the cat\u2019s striate cortex","volume":"148","author":"DH Hubel","year":"1959","journal-title":"The Journal of physiology"},{"issue":"4","key":"pcbi.1009196.ref049","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.conb.2004.07.007","article-title":"Sparse coding of sensory inputs","volume":"14","author":"BA Olshausen","year":"2004","journal-title":"Current opinion in neurobiology"},{"issue":"2","key":"pcbi.1009196.ref050","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1113\/jphysiol.1997.sp022031","article-title":"Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex","volume":"500","author":"H Markram","year":"1997","journal-title":"The Journal of physiology"},{"issue":"Apr","key":"pcbi.1009196.ref051","first-page":"1091","article-title":"Sparse activity and sparse connectivity in supervised learning","volume":"14","author":"M Thom","year":"2013","journal-title":"Journal of Machine Learning Research"},{"issue":"22","key":"pcbi.1009196.ref052","doi-asserted-by":"crossref","first-page":"5216","DOI":"10.1523\/JNEUROSCI.0540-04.2004","article-title":"Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures","volume":"24","author":"JM Beggs","year":"2004","journal-title":"Journal of neuroscience"},{"issue":"6282","key":"pcbi.1009196.ref053","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/346359a0","article-title":"Formation of target-specific neuronal projections in organotypic slice cultures from rat visual cortex","volume":"346","author":"J Bolz","year":"1990","journal-title":"Nature"},{"issue":"2","key":"pcbi.1009196.ref054","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1007\/BF00274981","article-title":"Cellular organization and development of slice cultures from rat visual cortex","volume":"77","author":"M Caeser","year":"1989","journal-title":"Experimental brain research"},{"issue":"7","key":"pcbi.1009196.ref055","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1002\/neu.480230702","article-title":"Formation and preservation of cortical layers in slice cultures","volume":"23","author":"M G\u00f6tz","year":"1992","journal-title":"Journal of neurobiology"},{"issue":"5670","key":"pcbi.1009196.ref056","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1126\/science.1093173","article-title":"Synfire chains and cortical songs: temporal modules of cortical activity","volume":"304","author":"Y Ikegaya","year":"2004","journal-title":"Science"},{"issue":"4","key":"pcbi.1009196.ref057","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1016\/S0306-4522(99)00009-3","article-title":"Patterns of spontaneous activity and morphology of interneuron types in organotypic cortex and thalamus\u2013cortex cultures","volume":"92","author":"O Klostermann","year":"1999","journal-title":"Neuroscience"},{"issue":"4","key":"pcbi.1009196.ref058","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/0306-4522(95)00405-X","article-title":"Neural dynamics in cortex-striatum co-cultures\u2014II. Spatiotemporal characteristics of neuronal activity","volume":"70","author":"D Plenz","year":"1996","journal-title":"Neuroscience"},{"issue":"3","key":"pcbi.1009196.ref059","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1523\/JNEUROSCI.2177-15.2016","article-title":"Rich-club organization in effective connectivity among cortical neurons","volume":"36","author":"S Nigam","year":"2016","journal-title":"Journal of Neuroscience"},{"issue":"4","key":"pcbi.1009196.ref060","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 Buzs\u00e1ki","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"issue":"3","key":"pcbi.1009196.ref061","doi-asserted-by":"crossref","first-page":"e68","DOI":"10.1371\/journal.pbio.0030068","article-title":"Highly nonrandom features of synaptic connectivity in local cortical circuits","volume":"3","author":"S Song","year":"2005","journal-title":"PLoS Biol"},{"issue":"11","key":"pcbi.1009196.ref062","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.1109\/TBME.2004.827936","article-title":"Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks","volume":"51","author":"J van Pelt","year":"2004","journal-title":"IEEE Transactions on Biomedical Engineering"},{"key":"pcbi.1009196.ref063","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0079-6123(04)47013-7","article-title":"Dynamics and plasticity in developing neuronal networks in vitro","volume":"147","author":"J van Pelt","year":"2005","journal-title":"Progress in brain research"},{"issue":"02","key":"pcbi.1009196.ref064","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1142\/S0129065707000968","article-title":"Network dynamics and synchronous activity in cultured cortical neurons","volume":"17","author":"M Chiappalone","year":"2007","journal-title":"International journal of neural systems"},{"issue":"4","key":"pcbi.1009196.ref065","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.1016\/j.neuroscience.2008.03.050","article-title":"Self-organization and neuronal avalanches in networks of dissociated cortical neurons","volume":"153","author":"V Pasquale","year":"2008","journal-title":"Neuroscience"},{"issue":"3","key":"pcbi.1009196.ref066","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1177\/155005949903000305","article-title":"The burst-suppression electroencephalogram","volume":"30","author":"E Niedermeyer","year":"1999","journal-title":"Clinical Electroencephalography"},{"issue":"33","key":"pcbi.1009196.ref067","doi-asserted-by":"crossref","first-page":"8465","DOI":"10.1523\/JNEUROSCI.1627-06.2006","article-title":"Dynamics and effective topology underlying synchronization in networks of cortical neurons","volume":"26","author":"D Eytan","year":"2006","journal-title":"Journal of Neuroscience"},{"issue":"6087","key":"pcbi.1009196.ref068","doi-asserted-by":"crossref","first-page":"1454","DOI":"10.1126\/science.1217230","article-title":"Awake hippocampal sharp-wave ripples support spatial memory","volume":"336","author":"SP Jadhav","year":"2012","journal-title":"Science"},{"issue":"11","key":"pcbi.1009196.ref069","doi-asserted-by":"crossref","first-page":"1679","DOI":"10.1038\/nn.4119","article-title":"Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep","volume":"18","author":"BP Staresina","year":"2015","journal-title":"Nature neuroscience"},{"issue":"1","key":"pcbi.1009196.ref070","first-page":"1","volume":"9","author":"AS Powanwe","year":"2019","journal-title":"Determinants of Brain Rhythm Burst Statistics. Scientific Reports"},{"issue":"3","key":"pcbi.1009196.ref071","doi-asserted-by":"crossref","first-page":"031907","DOI":"10.1103\/PhysRevE.82.031907","article-title":"Observed network dynamics from altering the balance between excitatory and inhibitory neurons in cultured networks","volume":"82","author":"X Chen","year":"2010","journal-title":"Physical Review E"},{"issue":"10","key":"pcbi.1009196.ref072","doi-asserted-by":"crossref","first-page":"e75824","DOI":"10.1371\/journal.pone.0075824","article-title":"Network bursting dynamics in excitatory cortical neuron cultures results from the combination of different adaptive mechanism","volume":"8","author":"T Masquelier","year":"2013","journal-title":"PloS one"},{"issue":"3","key":"pcbi.1009196.ref073","doi-asserted-by":"crossref","first-page":"031018","DOI":"10.1103\/PhysRevX.8.031018","article-title":"Homeostatic plasticity and external input shape neural network dynamics","volume":"8","author":"J Zierenberg","year":"2018","journal-title":"Physical Review X."},{"issue":"3","key":"pcbi.1009196.ref074","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1093\/cercor\/bhx012","article-title":"In vivo spiking dynamics of intra-and extratelencephalic projection neurons in rat motor cortex","volume":"28","author":"A Saiki","year":"2018","journal-title":"Cerebral Cortex"},{"issue":"2","key":"pcbi.1009196.ref075","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.tics.2008.11.005","article-title":"Looking for cognition in the structure within the noise","volume":"13","author":"A Johnson","year":"2009","journal-title":"Trends in cognitive sciences"},{"issue":"4","key":"pcbi.1009196.ref076","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.tics.2010.01.008","article-title":"Two views of brain function","volume":"14","author":"ME Raichle","year":"2010","journal-title":"Trends in cognitive sciences"},{"key":"pcbi.1009196.ref077","doi-asserted-by":"crossref","first-page":"247","DOI":"10.3389\/fnhum.2016.00247","article-title":"New perspectives on spontaneous brain activity: dynamic networks and energy matter","volume":"10","author":"A Tozzi","year":"2016","journal-title":"Frontiers in human neuroscience"},{"issue":"5446","key":"pcbi.1009196.ref078","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1126\/science.286.5446.1943","article-title":"Linking spontaneous activity of single cortical neurons and the underlying functional architecture","volume":"286","author":"M Tsodyks","year":"1999","journal-title":"Science"},{"issue":"5","key":"pcbi.1009196.ref079","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/j.neuron.2005.09.015","article-title":"Development of precise maps in visual cortex requires patterned spontaneous activity in the retina","volume":"48","author":"J Cang","year":"2005","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1009196.ref080","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.brainres.2006.03.049","article-title":"Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development","volume":"1093","author":"M Chiappalone","year":"2006","journal-title":"Brain research"},{"issue":"4","key":"pcbi.1009196.ref081","doi-asserted-by":"crossref","first-page":"2161","DOI":"10.3390\/e16042161","article-title":"Quantifying unique information","volume":"16","author":"N Bertschinger","year":"2014","journal-title":"Entropy."},{"issue":"4","key":"pcbi.1009196.ref082","doi-asserted-by":"crossref","DOI":"10.3390\/e20040307","article-title":"Information decomposition of target effects from multi-source interactions: perspectives on previous, current and future work","volume":"20","author":"JT Lizier","year":"2018","journal-title":"Entropy"},{"issue":"9","key":"pcbi.1009196.ref083","doi-asserted-by":"crossref","first-page":"451","DOI":"10.3390\/e19090451","article-title":"Invariant components of synergy, redundancy, and unique information among three variables","volume":"19","author":"G Pica","year":"2017","journal-title":"Entropy"},{"issue":"1","key":"pcbi.1009196.ref084","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/s10827-010-0271-2","article-title":"Multivariate information-theoretic measures reveal directed information structure and task relevant changes in fMRI connectivity","volume":"30","author":"JT Lizier","year":"2011","journal-title":"Journal of computational neuroscience"},{"issue":"6","key":"pcbi.1009196.ref085","doi-asserted-by":"crossref","first-page":"066211","DOI":"10.1103\/PhysRevE.86.066211","article-title":"Expanding the transfer entropy to identify information circuits in complex systems","volume":"86","author":"S Stramaglia","year":"2012","journal-title":"Physical Review E"},{"issue":"4","key":"pcbi.1009196.ref086","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1109\/TNS.2004.832706","article-title":"What does the eye tell the brain?: Development of a system for the large-scale recording of retinal output activity","volume":"51","author":"AM Litke","year":"2004","journal-title":"IEEE Transactions on Nuclear Science"},{"issue":"2","key":"pcbi.1009196.ref087","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1103\/PhysRevLett.85.461","article-title":"Measuring information transfer","volume":"85","author":"T Schreiber","year":"2000","journal-title":"Physical review letters"},{"issue":"3","key":"pcbi.1009196.ref088","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1016\/j.neuroimage.2009.10.003","article-title":"Complex network measures of brain connectivity: uses and interpretations","volume":"52","author":"M Rubinov","year":"2010","journal-title":"Neuroimage"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1009196","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,7,22]],"date-time":"2021-07-22T00:00:00Z","timestamp":1626912000000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1009196","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,22]],"date-time":"2021-07-22T18:01:39Z","timestamp":1626976899000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1009196"}},"subtitle":[],"editor":[{"given":"Boris S.","family":"Gutkin","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2021,7,12]]},"references-count":88,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1009196","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1009196","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,12]]}}}