{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T10:24:01Z","timestamp":1767176641393,"version":"build-2238731810"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1009521","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,10,27]],"date-time":"2021-10-27T00:00:00Z","timestamp":1635292800000}}],"reference-count":87,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2021,10,15]],"date-time":"2021-10-15T00:00:00Z","timestamp":1634256000000},"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"],"abstract":"<jats:p>Inhibitory interneurons shape the spiking characteristics and computational properties of cortical networks. Interneuron subtypes can precisely regulate cortical function but the roles of interneuron subtypes for promoting different regimes of cortical activity remains unclear. Therefore, we investigated the impact of fast spiking and non-fast spiking interneuron subtypes on cortical activity using a network model with connectivity and synaptic properties constrained by experimental data. We found that network properties were more sensitive to modulation of the fast spiking population, with reductions of fast spiking excitability generating strong spike correlations and network oscillations. Paradoxically, reduced fast spiking excitability produced a reduction of global excitation-inhibition balance and features of an inhibition stabilised network, in which firing rates were driven by the activity of excitatory neurons within the network. Further analysis revealed that the synaptic interactions and biophysical features associated with fast spiking interneurons, in particular their rapid intrinsic response properties and short synaptic latency, enabled this state transition by enhancing gain within the excitatory population. Therefore, fast spiking interneurons may be uniquely positioned to control the strength of recurrent excitatory connectivity and the transition to an inhibition stabilised regime. Overall, our results suggest that interneuron subtypes can exert selective control over excitatory gain allowing for differential modulation of global network state.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1009521","type":"journal-article","created":{"date-parts":[[2021,10,15]],"date-time":"2021-10-15T14:47:38Z","timestamp":1634309258000},"page":"e1009521","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["State transitions through inhibitory interneurons in a cortical network model"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0033-8197","authenticated-orcid":true,"given":"Alexander","family":"Bryson","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4580-841X","authenticated-orcid":true,"given":"Samuel F.","family":"Berkovic","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4960-6375","authenticated-orcid":true,"given":"Steven","family":"Petrou","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5497-7234","authenticated-orcid":true,"given":"David B.","family":"Grayden","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2021,10,15]]},"reference":[{"key":"pcbi.1009521.ref001","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.conb.2019.09.008","article-title":"Functional flexibility in cortical circuits","volume":"58","author":"JA Cardin","year":"2019","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1009521.ref002","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/j.tins.2018.07.015","article-title":"Inhibitory Interneurons Regulate Temporal Precision and Correlations in Cortical Circuits","volume":"41","author":"JA Cardin","year":"2018","journal-title":"Trends Neurosci"},{"key":"pcbi.1009521.ref003","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.neuron.2016.06.033","article-title":"GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits","author":"R Tremblay","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1009521.ref004","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms2056","article-title":"Evidence of an inhibitory restraint of seizure activity in humans.","volume":"3","author":"CA Schevon","year":"2012","journal-title":"Nat Commun."},{"key":"pcbi.1009521.ref005","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1126\/science.274.5293.1724","article-title":"Chaos in neuronal networks with balanced excitatory and inhibitory activity","volume":"274","author":"C Van Vreeswijk","year":"1996","journal-title":"Science (80-)."},{"key":"pcbi.1009521.ref006","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1038\/nature12983","article-title":"Interneuron cell types are fit to function","volume":"505","author":"A Kepecs","year":"2014","journal-title":"Nature"},{"key":"pcbi.1009521.ref007","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1126\/science.1179850","article-title":"The asynchronous state in cortical circuits","volume":"327","author":"A Renart","year":"2010","journal-title":"Science (80-)."},{"key":"pcbi.1009521.ref008","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1023\/A:1008925309027","article-title":"Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons","author":"N. Brunel","year":"2000","journal-title":"J Comput Neurosci"},{"key":"pcbi.1009521.ref009","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1523\/JNEUROSCI.4637-10.2011","article-title":"Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches","volume":"31","author":"WL Shew","year":"2011","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref010","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1038\/nn.2105","article-title":"Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities","author":"M Okun","year":"2008","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref011","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1038\/nn.4243","article-title":"Efficient codes and balanced networks","author":"S Den\u00e8ve","year":"2016","journal-title":"Nature Neuroscience"},{"key":"pcbi.1009521.ref012","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1038\/nature13321","article-title":"Scanziani M. Equalizing excitation-inhibition ratios across visual cortical neurons","author":"M Xue","year":"2014","journal-title":"Nature"},{"key":"pcbi.1009521.ref013","doi-asserted-by":"crossref","first-page":"15760","DOI":"10.1523\/JNEUROSCI.3874-10.2010","article-title":"Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition","volume":"30","author":"J Kremkow","year":"2010","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref014","doi-asserted-by":"crossref","first-page":"4382","DOI":"10.1523\/JNEUROSCI.17-11-04382.1997","article-title":"Paradoxical effects of external modulation of inhibitory interneurons","volume":"17","author":"V. Tsodyks M","year":"1997","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref015","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/s41583-020-00390-z","article-title":"Inhibitory stabilization and cortical computation.","volume":"22","author":"S Sadeh","year":"2021","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1009521.ref016","article-title":"Inhibition stabilization is a widespread property of cortical networks.","author":"A Sanzeni","year":"2020","journal-title":"Elife"},{"key":"pcbi.1009521.ref017","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1016\/j.neuron.2009.03.028","article-title":"Inhibitory stabilization of the cortical network underlies visual surround suppression","volume":"62","author":"H Ozeki","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1009521.ref018","article-title":"Spatiotemporal constraints on optogenetic inactivation in cortical circuits.","volume":"8","author":"N Li","year":"2019","journal-title":"Elife"},{"key":"pcbi.1009521.ref019","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1038\/nrn2402","article-title":"Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex","volume":"9","author":"G a Ascoli","year":"2008","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1009521.ref020","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1038\/nrn1519","article-title":"Interneurons of the neocortical inhibitory system.","volume":"5","author":"H Markram","year":"2004","journal-title":"Nat Rev Neurosci."},{"key":"pcbi.1009521.ref021","doi-asserted-by":"crossref","first-page":"1310","DOI":"10.1093\/cercor\/bhh092","article-title":"Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex","volume":"14","author":"M Toledo-Rodriguez","year":"2004","journal-title":"Cereb Cortex"},{"key":"pcbi.1009521.ref022","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1038\/nn.4619","article-title":"Functions and dysfunctions of neocortical inhibitory neuron subtypes","author":"R Hattori","year":"2017","journal-title":"Nature Neuroscience"},{"key":"pcbi.1009521.ref023","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1126\/science.281.5379.985","article-title":"Cholinergic switching within neocortical inhibitory networks","volume":"281","author":"Z Xiang","year":"1998","journal-title":"Science (80-)."},{"key":"pcbi.1009521.ref024","article-title":"Serotonin enhances excitability and gamma frequency temporal integration in mouse prefrontal fast-spiking interneurons.","author":"JC Athilingam","year":"2017","journal-title":"Elife"},{"key":"pcbi.1009521.ref025","doi-asserted-by":"crossref","first-page":"3192","DOI":"10.1073\/pnas.1906369117","article-title":"GABA-mediated tonic inhibition differentially modulates gain in functional subtypes of cortical interneurons","volume":"117","author":"A Bryson","year":"2020","journal-title":"Proc Natl Acad Sci"},{"key":"pcbi.1009521.ref026","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":"pcbi.1009521.ref027","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1038\/nn.3917","article-title":"The neocortical circuit: Themes and variations","volume":"18","author":"KD Harris","year":"2015","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref028","article-title":"Microcircuits of excitatory and inhibitory neurons in layer 2\/3 of mouse barrel cortex","author":"M Avermann","year":"2012","journal-title":"J Neurophysiol"},{"key":"pcbi.1009521.ref029","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1016\/j.neuron.2011.02.025","article-title":"Dense inhibitory connectivity in neocortex","volume":"69","author":"E Fino","year":"2011","journal-title":"Neuron"},{"key":"pcbi.1009521.ref030","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.cell.2015.09.029","article-title":"Reconstruction and Simulation of Neocortical Microcircuitry","volume":"163","author":"H Markram","year":"2015","journal-title":"Cell"},{"key":"pcbi.1009521.ref031","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1371\/journal.pcbi.1002133","article-title":"Effective Stimuli for Constructing Reliable Neuron Models.","volume":"7","author":"S Druckmann","year":"2011","journal-title":"PLOS Comput Biol"},{"key":"pcbi.1009521.ref032","doi-asserted-by":"crossref","first-page":"e1002107","DOI":"10.1371\/journal.pcbi.1002107","article-title":"Models of neocortical layer 5b pyramidal cells capturing a wide range of dendritic and perisomatic active properties.","volume":"7","author":"E Hay","year":"2011","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1009521.ref033","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1109\/TNN.2003.820440","article-title":"Simple model of spiking neurons","volume":"14","author":"EM Izhikevich","year":"2003","journal-title":"IEEE Trans Neural Networks"},{"key":"pcbi.1009521.ref034","unstructured":"Lytton WW, Dura-Bernal S. NEURON implementation of Izhikevich artificial neuron model. Includes modifications for use with conductance-change synapses in a biophysical model cell (personal communication, N.T. Carnevale; see comments in Izh.mod and discussion at https:\/\/www.neuron. 2004. Available: https:\/\/www.modeldb.yale.edu\/39948"},{"key":"pcbi.1009521.ref035","doi-asserted-by":"crossref","DOI":"10.1113\/jphysiol.2001.012959","article-title":"Synaptic connections between layer 4 spiny neurone-layer 2\/3 pyramidal cell pairs in juvenile rat barrel cortex: Physiology and anatomy of interlaminar signalling within a cortical column","volume":"538","author":"D Feldmeyer","year":"2002","journal-title":"J Physiol"},{"key":"pcbi.1009521.ref036","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.0707853104","article-title":"Modeling a layer 4-to-layer 2\/3 module of a single column in rat neocortex: Interweaving in vitro and in vivo experimental observations","volume":"104","author":"L Sarid","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1009521.ref037","doi-asserted-by":"crossref","DOI":"10.1113\/jphysiol.1995.sp020521","article-title":"Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons","volume":"482","author":"N Spruston","year":"1995","journal-title":"J Physiol"},{"key":"pcbi.1009521.ref038","doi-asserted-by":"crossref","DOI":"10.1038\/1092","article-title":"Target-cell-specific facilitation and depression in neocortical circuits","volume":"1","author":"A Reyes","year":"1998","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref039","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":"pcbi.1009521.ref040","doi-asserted-by":"crossref","DOI":"10.1093\/cercor\/bhx276","article-title":"Segregated excitatoryinhibitory recurrent subnetworks in layer 5 of the rat frontal cortex","volume":"27","author":"M Morishima","year":"2017","journal-title":"Cereb Cortex"},{"key":"pcbi.1009521.ref041","article-title":"Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex","volume":"32","author":"RB Levy","year":"2012","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref042","doi-asserted-by":"crossref","first-page":"e1006781","DOI":"10.1371\/journal.pcbi.1006781","article-title":"Leveraging heterogeneity for neural computation with fading memory in layer 2\/3 cortical microcircuits.","volume":"15","author":"R Duarte","year":"2019","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1009521.ref043","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1113\/jphysiol.2003.044784","article-title":"Pyramidal cell communication within local networks in layer 2\/3 of rat neocortex","volume":"551","author":"C Holmgren","year":"2003","journal-title":"J Physiol"},{"key":"pcbi.1009521.ref044","article-title":"Synaptic Computation and Sensory Processing in Neocortical Layer 2\/3","volume":"78","author":"CCH Petersen","year":"2013","journal-title":"Neuron"},{"key":"pcbi.1009521.ref045","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1113\/jphysiol.2011.219576","article-title":"Intrinsic morphological diversity of thick-tufted layer 5 pyramidal neurons ensures robust and invariant properties of in silico synaptic connections","volume":"590","author":"S Ramaswamy","year":"2012","journal-title":"J Physiol"},{"key":"pcbi.1009521.ref046","first-page":"7","article-title":"Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs","author":"G Di Cristo","year":"2004","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref047","doi-asserted-by":"crossref","DOI":"10.3389\/fncir.2016.00027","article-title":"The diversity of cortical inhibitory synapses.","volume":"10","author":"Y Kubota","year":"2016","journal-title":"Front Neural Circuits."},{"key":"pcbi.1009521.ref048","article-title":"Anatomy and physiology of the thick-tufted layer 5 pyramidal neuron","volume":"9233","author":"S Ramaswamy","year":"2015","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1009521.ref049","doi-asserted-by":"crossref","first-page":"5280","DOI":"10.1523\/JNEUROSCI.4652-06.2007","article-title":"Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex","volume":"27","author":"M Rudolph","year":"2007","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref050","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1038\/nn.3051","article-title":"Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex","volume":"15","author":"LJ Gentet","year":"2012","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref051","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.tins.2012.03.008","article-title":"Experimental evidence for sparse firing in the neocortex","volume":"35","author":"AL Barth","year":"2012","journal-title":"Trends Neurosci"},{"key":"pcbi.1009521.ref052","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1016\/j.neuron.2011.02.022","article-title":"Synaptic mechanisms underlying sparse coding of active touch","volume":"69","author":"S Crochet","year":"2011","journal-title":"Neuron"},{"key":"pcbi.1009521.ref053","first-page":"26","article-title":"NetpyNE, a tool for data-driven multiscale modeling of brain circuits","author":"S Dura-Bernal","year":"2019","journal-title":"Elife"},{"key":"pcbi.1009521.ref054","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1152\/jn.00732.2015","article-title":"Inhibitory stabilization and visual coding in cortical circuits with multiple interneuron subtypes","volume":"115","author":"A Litwin-Kumar","year":"2016","journal-title":"J Neurophysiol"},{"key":"pcbi.1009521.ref055","doi-asserted-by":"crossref","first-page":"B53","DOI":"10.1115\/1.1579454","article-title":"Simulating, Analyzing, and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students","volume":"56","author":"B Ermentrout","year":"2003","journal-title":"Appl Mech Rev"},{"key":"pcbi.1009521.ref056","article-title":"Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex","author":"JA D\u2019amour","year":"2015","journal-title":"Neuron"},{"key":"pcbi.1009521.ref057","article-title":"Precise excitation-inhibition balance controls gain and timing in the hippocampus.","author":"A Bhatia","year":"2019","journal-title":"Elife"},{"key":"pcbi.1009521.ref058","article-title":"What is the dynamical regime of cerebral cortex?","author":"Y Ahmadian","year":"2019","journal-title":"arXiv"},{"key":"pcbi.1009521.ref059","article-title":"Beyond Poisson: Increased Spike-Time Regularity across Primate Parietal Cortex","author":"G Maimon","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1009521.ref060","article-title":"The log-dynamic brain: How skewed distributions affect network operations.","author":"G Buzs\u00e1ki","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"key":"pcbi.1009521.ref061","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1523\/JNEUROSCI.13-01-00334.1993","article-title":"The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs","volume":"13","author":"WR Softky","year":"1993","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref062","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-27777-6_2","article-title":"Inhibitory cell types, circuits and receptive fields in mouse visual cortex.","author":"EM Callaway","year":"2016","journal-title":"Research and Perspectives in Neurosciences."},{"key":"pcbi.1009521.ref063","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.neuron.2011.12.013","article-title":"Parvalbumin-Expressing Interneurons Linearly Transform Cortical Responses to Visual Stimuli","volume":"73","author":"V. Atallah B","year":"2012","journal-title":"Neuron"},{"key":"pcbi.1009521.ref064","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1038\/nature12176","article-title":"Distinct behavioural and network correlates of two interneuron types in prefrontal cortex","volume":"498","author":"D Kvitsiani","year":"2013","journal-title":"Nature"},{"key":"pcbi.1009521.ref065","article-title":"Cortical interneurons that specialize in disinhibitory control","author":"HJ Pi","year":"2013","journal-title":"Nature"},{"key":"pcbi.1009521.ref066","article-title":"Assessing the Role of Inhibition in Stabilizing Neocortical Networks Requires Large-Scale Perturbation of the Inhibitory Population","author":"S Sadeh","year":"2017","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref067","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.neuron.2014.12.026","article-title":"The stabilized supralinear network: A unifying circuit motif underlying multi-input integration in sensory cortex","volume":"85","author":"DB Rubin","year":"2015","journal-title":"Neuron"},{"key":"pcbi.1009521.ref068","doi-asserted-by":"crossref","first-page":"5931","DOI":"10.1523\/JNEUROSCI.5753-10.2011","article-title":"GABAA inhibition controls response gain in visual cortex","volume":"31","author":"S Katzner","year":"2011","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref069","article-title":"Mechanisms underlying gain modulation in the cortex","author":"KA Ferguson","year":"2020","journal-title":"Nature Reviews Neuroscience"},{"key":"pcbi.1009521.ref070","article-title":"Impact of correlated synaptic input on output firing rate and variability in simple neuronal models","author":"E Salinas","year":"2000","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref071","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.neuron.2009.04.008","article-title":"Rapid Neocortical Dynamics: Cellular and Network Mechanisms","author":"B Haider","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1009521.ref072","article-title":"Selective modulation of cortical state during spatial attention","author":"TA Engel","year":"2016","journal-title":"Science (80-)."},{"key":"pcbi.1009521.ref073","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1038\/nn.3464","article-title":"Cellular mechanisms of brain state-dependent gain modulation in visual cortex","volume":"16","author":"PO Polack","year":"2013","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref074","article-title":"Cortical state and attention","author":"KD Harris","year":"2011","journal-title":"Nature Reviews Neuroscience"},{"key":"pcbi.1009521.ref075","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":"Nat Neurosci"},{"key":"pcbi.1009521.ref076","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1016\/S0896-6273(02)00820-6","article-title":"Gain Modulation from Background Synaptic Input","volume":"35","author":"FS Chance","year":"2002","journal-title":"Neuron"},{"key":"pcbi.1009521.ref077","doi-asserted-by":"crossref","first-page":"10388","DOI":"10.1523\/JNEUROSCI.23-32-10388.2003","article-title":"Barrages of synaptic activity control the gain and sensitivity of cortical neurons","volume":"23","author":"Y Shu","year":"2003","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref078","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1093\/cercor\/6.2.93","article-title":"A brief history of time (constants).","volume":"6","author":"C Koch","year":"1996","journal-title":"Cereb Cortex"},{"key":"pcbi.1009521.ref079","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1523\/JNEUROSCI.3735-11.2012","article-title":"Single neuron firing properties impact correlation-based population coding","volume":"32","author":"S Hong","year":"2012","journal-title":"J Neurosci"},{"key":"pcbi.1009521.ref080","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/s10827-009-0142-x","article-title":"Sensitivity of firing rate to input fluctuations depends on time scale separation between fast and slow variables in single neurons","volume":"27","author":"BN Lundstrom","year":"2009","journal-title":"J Comput Neurosci"},{"key":"pcbi.1009521.ref081","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1038\/nn.3488","article-title":"Tuned thalamic excitation is amplified by visual cortical circuits","volume":"16","author":"AD Lien","year":"2013","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref082","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/nature22324","article-title":"Maintenance of persistent activity in a frontal thalamocortical loop","volume":"545","author":"V. Guo Z","year":"2017","journal-title":"Nature"},{"key":"pcbi.1009521.ref083","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms2376","article-title":"On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy.","volume":"4","author":"E Krook-Magnuson","year":"2013","journal-title":"Nat Commun."},{"key":"pcbi.1009521.ref084","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1038\/nn.3950","article-title":"Microcircuits and their interactions in epilepsy: Is the focus out of focus?","volume":"18","author":"JT Paz","year":"2015","journal-title":"Nat Neurosci"},{"key":"pcbi.1009521.ref085","article-title":"Layer- and Cell-Specific Recruitment Dynamics during Epileptic Seizures In Vivo","author":"F Aeed","year":"2020","journal-title":"Ann Neurol"},{"key":"pcbi.1009521.ref086","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1038\/s41583-020-0262-x","article-title":"Macroscopic gradients of synaptic excitation and inhibition in the neocortex.","volume":"21","author":"XJ Wang","year":"2020","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1009521.ref087","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1038\/nrn2286","article-title":"Pyramidal neurons: dendritic structure and synaptic integration","volume":"9","author":"N. Spruston","year":"2008","journal-title":"Nat Rev Neurosci"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1009521","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,10,27]],"date-time":"2021-10-27T00:00:00Z","timestamp":1635292800000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1009521","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,27]],"date-time":"2021-10-27T13:43:34Z","timestamp":1635342214000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1009521"}},"subtitle":[],"editor":[{"given":"Lyle J.","family":"Graham","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2021,10,15]]},"references-count":87,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,10,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1009521","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,15]]}}}