{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T10:26:45Z","timestamp":1767176805493,"version":"build-2238731810"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1013661","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T00:00:00Z","timestamp":1762992000000}}],"reference-count":89,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2025,11,6]],"date-time":"2025-11-06T00:00:00Z","timestamp":1762387200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["MOP-119498"],"award-info":[{"award-number":["MOP-119498"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000156","name":"Fonds de Recherche du Qu\u00c3\u00a9bec - Sant\u00c3\u00a9","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000156","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Neurons in the early visual cortex respond selectively to multiple features of visual stimuli, but they respond inconsistently to repeated presentation of the same visual stimulus. Such trial-to-trial response variabilities are often treated as random noise and addressed by simple trial-averaging to obtain the stimulus-driven response. However, response variability may primarily be caused by non-sensory factors, particularly by variations in cortical state. Here we recorded and analyzed neuronal spiking activity in response to natural images from areas 17 and 18 of cats, along with local population neuronal signals, i.e., local field potentials (LFPs) and multi-unit activity (MUA). Single neurons showed highly varying degrees of trial-to-trial response variability, even when recorded simultaneously. We used a variability ratio (VR) measure to quantify the trial-wise differences in neural responses, and two cortical state indicative measures, a global fluctuation index (GFI) calculated using MUA, and a synchrony index (SI) calculated from LFP signals. We propose a compact convolutional neural network model with parallel pathways, to capture the stimulus-driven activity and the cortical state-driven response variabilities. The stimulus-driven pathway is comprised of a spatiotemporal filter, a parametric rectifier and a Gaussian map, and the cortical state-driven pathway contains temporal filters for MUA and LFPs. The model parameters are fit to best predict each neuron\u2019s spiking activity. We further evaluated the improvements in estimated receptive fields of neurons when incorporating cortical state-related information in our system identification model. The fitted model performed with a significantly higher accuracy in predicting neural responses as well as qualitative improvements in the estimated receptive fields compared to a basic model with a stimulus-driven pathway alone. The neurons with higher response variability benefited more from the cortical state-driven pathway compared to less variable neurons. These results show that different neurons may differ greatly in their variability and in the degree of their relationship to indicators of cortical state fluctuations.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1013661","type":"journal-article","created":{"date-parts":[[2025,11,6]],"date-time":"2025-11-06T23:02:01Z","timestamp":1762470121000},"page":"e1013661","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Cortical state contributions to neuronal response variability in the early visual cortex: A system identification approach"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8135-2088","authenticated-orcid":true,"given":"Jinani","family":"Sooriyaarachchi","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8017-1886","authenticated-orcid":true,"given":"Chang\u2019an A.","family":"Zhan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9988-3936","authenticated-orcid":true,"given":"Curtis L.","family":"Baker Jr","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2025,11,6]]},"reference":[{"issue":"9","key":"pcbi.1013661.ref001","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.0020264","article-title":"Amplification of trial-to-trial response variability by neurons in visual cortex","volume":"2","author":"M Carandini","year":"2004","journal-title":"PLoS Biol"},{"issue":"8","key":"pcbi.1013661.ref002","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1016\/0042-6989(83)90200-6","article-title":"The statistical reliability of signals in single neurons in cat and monkey visual cortex","volume":"23","author":"DJ Tolhurst","year":"1983","journal-title":"Vision Res"},{"issue":"2","key":"pcbi.1013661.ref003","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1007\/BF00275002","article-title":"The response variability of striate cortical neurons in the behaving monkey","volume":"77","author":"R Vogels","year":"1989","journal-title":"Exp Brain Res"},{"issue":"5","key":"pcbi.1013661.ref004","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/nrn1888","article-title":"Neural correlations, population coding and computation","volume":"7","author":"BB Averbeck","year":"2006","journal-title":"Nat Rev Neurosci"},{"issue":"6485","key":"pcbi.1013661.ref005","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1038\/370140a0","article-title":"Correlated neuronal discharge rate and its implications for psychophysical performance","volume":"370","author":"E Zohary","year":"1994","journal-title":"Nature"},{"issue":"5216","key":"pcbi.1013661.ref006","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1126\/science.7770778","article-title":"Reliability of spike timing in neocortical neurons","volume":"268","author":"ZF Mainen","year":"1995","journal-title":"Science"},{"issue":"9","key":"pcbi.1013661.ref007","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1038\/nrn3084","article-title":"Cortical state and attention","volume":"12","author":"KD Harris","year":"2011","journal-title":"Nat Rev Neurosci"},{"issue":"14","key":"pcbi.1013661.ref008","doi-asserted-by":"crossref","first-page":"4121","DOI":"10.1523\/JNEUROSCI.2502-15.2016","article-title":"Inferring Cortical Variability from Local Field Potentials","volume":"36","author":"Y Cui","year":"2016","journal-title":"J Neurosci"},{"issue":"3","key":"pcbi.1013661.ref009","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/s10827-009-0208-9","article-title":"Local field potentials indicate network state and account for neuronal response variability","volume":"29","author":"RC Kelly","year":"2010","journal-title":"J Comput Neurosci"},{"issue":"5283","key":"pcbi.1013661.ref010","doi-asserted-by":"crossref","first-page":"1868","DOI":"10.1126\/science.273.5283.1868","article-title":"Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses","volume":"273","author":"A Arieli","year":"1996","journal-title":"Science"},{"issue":"1","key":"pcbi.1013661.ref011","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1007\/BF01797193","article-title":"\u00dcber das Elektrenkephalogramm des Menschen","volume":"87","author":"H Berger","year":"1929","journal-title":"Archiv f Psychiatrie"},{"issue":"3","key":"pcbi.1013661.ref012","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1152\/physrev.00032.2011","article-title":"Control of sleep and wakefulness","volume":"92","author":"RE Brown","year":"2012","journal-title":"Physiol Rev"},{"key":"pcbi.1013661.ref013","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.eng.2021.11.013","article-title":"Progress of Brain Network Studies on Anesthesia and Consciousness: Framework and Clinical Applications","volume":"20","author":"J Liu","year":"2023","journal-title":"Engineering"},{"issue":"7","key":"pcbi.1013661.ref014","doi-asserted-by":"crossref","first-page":"3608","DOI":"10.3390\/ijms23073608","article-title":"A Comparison of Brain-State Dynamics across Common Anesthetic Agents in Male Sprague-Dawley Rats","volume":"23","author":"R Ward-Flanagan","year":"2022","journal-title":"Int J Mol Sci"},{"issue":"2","key":"pcbi.1013661.ref015","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.neuron.2014.09.033","article-title":"Pupil fluctuations track fast switching of cortical states during quiet wakefulness","volume":"84","author":"J Reimer","year":"2014","journal-title":"Neuron"},{"issue":"5831","key":"pcbi.1013661.ref016","doi-asserted-by":"crossref","first-page":"1612","DOI":"10.1126\/science.1139140","article-title":"Neural mechanisms of visual attention: how top-down feedback highlights relevant locations","volume":"316","author":"YB Saalmann","year":"2007","journal-title":"Science"},{"issue":"9","key":"pcbi.1013661.ref017","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1038\/nn.3785","article-title":"Sharp emergence of feature-selective sustained activity along the dorsal visual pathway","volume":"17","author":"D Mendoza-Halliday","year":"2014","journal-title":"Nat Neurosci"},{"issue":"6","key":"pcbi.1013661.ref018","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1016\/j.neuron.2011.02.040","article-title":"Effects and mechanisms of wakefulness on local cortical networks","volume":"69","author":"CM Constantinople","year":"2011","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1013661.ref019","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.neuron.2015.03.028","article-title":"Arousal and locomotion make distinct contributions to cortical activity patterns and visual encoding","volume":"86","author":"M Vinck","year":"2015","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1013661.ref020","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1038\/s41593-019-0502-4","article-title":"Single-trial neural dynamics are dominated by richly varied movements","volume":"22","author":"S Musall","year":"2019","journal-title":"Nat Neurosci"},{"issue":"6437","key":"pcbi.1013661.ref021","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1126\/science.aav7893","article-title":"Spontaneous behaviors drive multidimensional, brainwide activity","volume":"364","author":"C Stringer","year":"2019","journal-title":"Science"},{"issue":"7553","key":"pcbi.1013661.ref022","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nature14273","article-title":"Diverse coupling of neurons to populations in sensory cortex","volume":"521","author":"M Okun","year":"2015","journal-title":"Nature"},{"issue":"6","key":"pcbi.1013661.ref023","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1038\/nrn3241","article-title":"The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes","volume":"13","author":"G Buzs\u00e1ki","year":"2012","journal-title":"Nat Rev Neurosci"},{"issue":"5679","key":"pcbi.1013661.ref024","doi-asserted-by":"crossref","first-page":"1926","DOI":"10.1126\/science.1099745","article-title":"Neuronal oscillations in cortical networks","volume":"304","author":"G Buzs\u00e1ki","year":"2004","journal-title":"Science"},{"key":"pcbi.1013661.ref025","doi-asserted-by":"crossref","first-page":"53","DOI":"10.14196\/mjiri.31.53","article-title":"Changes of the brain\u2019s bioelectrical activity in cognition, consciousness, and some mental disorders","volume":"31","author":"M Roohi-Azizi","year":"2017","journal-title":"Med J Islam Repub Iran"},{"issue":"1","key":"pcbi.1013661.ref026","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1523\/JNEUROSCI.4994-13.2015","article-title":"Cortical state determines global variability and correlations in visual cortex","volume":"35","author":"ML Sch\u00f6lvinck","year":"2015","journal-title":"J Neurosci"},{"issue":"22","key":"pcbi.1013661.ref027","doi-asserted-by":"crossref","first-page":"9499","DOI":"10.1073\/pnas.0701104104","article-title":"Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field","volume":"104","author":"KM Armstrong","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"pcbi.1013661.ref028","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.neuron.2014.02.006","article-title":"State dependence of noise correlations in macaque primary visual cortex","volume":"82","author":"AS Ecker","year":"2014","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1013661.ref029","doi-asserted-by":"crossref","DOI":"10.1167\/8.10.2","article-title":"The effects of spatial attention in early human visual cortex are stimulus independent","volume":"8","author":"SO Murray","year":"2008","journal-title":"J Vis"},{"issue":"12","key":"pcbi.1013661.ref030","doi-asserted-by":"crossref","first-page":"2970","DOI":"10.1093\/cercor\/bhp070","article-title":"Additive effects of attention and stimulus contrast in primary visual cortex","volume":"19","author":"A Thiele","year":"2009","journal-title":"Cereb Cortex"},{"issue":"3","key":"pcbi.1013661.ref031","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.neuron.2015.06.035","article-title":"The Nature of Shared Cortical Variability","volume":"87","author":"I-C Lin","year":"2015","journal-title":"Neuron"},{"issue":"9","key":"pcbi.1013661.ref032","doi-asserted-by":"crossref","first-page":"3054","DOI":"10.1172\/JCI42161","article-title":"How cortical neurons help us see: visual recognition in the human brain","volume":"120","author":"J Blumberg","year":"2010","journal-title":"J Clin Invest"},{"key":"pcbi.1013661.ref033","doi-asserted-by":"crossref","unstructured":"Cohen MX. A data-driven method to identify frequency boundaries in multichannel electrophysiology data. bioRxiv, 2020.2007.2009.195784. 2020. https:\/\/doi.org\/10.1101\/2020.07.09.195784","DOI":"10.1101\/2020.07.09.195784"},{"issue":"5","key":"pcbi.1013661.ref034","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1012127","article-title":"Estimating receptive fields of simple and complex cells in early visual cortex: A convolutional neural network model with parameterized rectification","volume":"20","author":"P Nguyen","year":"2024","journal-title":"PLoS Comput Biol"},{"issue":"11","key":"pcbi.1013661.ref035","doi-asserted-by":"crossref","first-page":"1920","DOI":"10.1523\/JNEUROSCI.1220-22.2023","article-title":"Model-Based Approach Shows ON Pathway Afferents Elicit a Transient Decrease of V1 Responses","volume":"43","author":"D St-Amand","year":"2023","journal-title":"J Neurosci"},{"key":"pcbi.1013661.ref036","doi-asserted-by":"crossref","unstructured":"Pachitariu M, Steinmetz N, Kadir S, Carandini M, Kenneth DH. Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels. bioRxiv, 061481. 2016. https:\/\/doi.org\/10.1101\/061481","DOI":"10.1101\/061481"},{"issue":"10","key":"pcbi.1013661.ref037","doi-asserted-by":"crossref","first-page":"4046","DOI":"10.1523\/JNEUROSCI.19-10-04046.1999","article-title":"Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons","volume":"19","author":"GC DeAngelis","year":"1999","journal-title":"J Neurosci"},{"issue":"1","key":"pcbi.1013661.ref038","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1113\/jphysiol.1962.sp006837","article-title":"Receptive fields, binocular interaction and functional architecture in the cat\u2019s visual cortex","volume":"160","author":"DH Hubel","year":"1962","journal-title":"J Physiol"},{"issue":"4522","key":"pcbi.1013661.ref039","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1126\/science.7292014","article-title":"Spatial frequency columns in primary visual cortex","volume":"214","author":"RB Tootell","year":"1981","journal-title":"Science"},{"issue":"4","key":"pcbi.1013661.ref040","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1163\/156856897X00357","article-title":"The Psychophysics Toolbox","volume":"10","author":"DH Brainard","year":"1997","journal-title":"Spat Vis"},{"key":"pcbi.1013661.ref041","first-page":"1","article-title":"What\u2019s new in Psychtoolbox-3?","volume":"36","author":"M Kleiner","year":"2007","journal-title":"Perception"},{"issue":"4","key":"pcbi.1013661.ref042","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1163\/156856897X00366","article-title":"The VideoToolbox software for visual psychophysics: transforming numbers into movies","volume":"10","author":"DG Pelli","year":"1997","journal-title":"Spat Vis"},{"issue":"5","key":"pcbi.1013661.ref043","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1523\/JNEUROSCI.4661-12.2012","article-title":"Natural versus synthetic stimuli for estimating receptive field models: a comparison of predictive robustness","volume":"32","author":"V Talebi","year":"2012","journal-title":"J Neurosci"},{"issue":"12","key":"pcbi.1013661.ref044","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1068\/p5321","article-title":"A biologically inspired algorithm for the recovery of shading and reflectance images","volume":"33","author":"A Olmos","year":"2004","journal-title":"Perception"},{"key":"pcbi.1013661.ref045","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.jneumeth.2005.12.005","article-title":"Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities","volume":"154","author":"KH Pettersen","year":"2006","journal-title":"J Neurosci Methods"},{"issue":"11","key":"pcbi.1013661.ref046","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1038\/14731","article-title":"Information theory and neural coding","volume":"2","author":"A Borst","year":"1999","journal-title":"Nat Neurosci"},{"issue":"3","key":"pcbi.1013661.ref047","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/j.neuron.2007.07.013","article-title":"Adaptation to stimulus contrast and correlations during natural visual stimulation","volume":"55","author":"NA Lesica","year":"2007","journal-title":"Neuron"},{"issue":"4","key":"pcbi.1013661.ref048","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1002\/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C","article-title":"Measuring phase synchrony in brain signals","volume":"8","author":"J-P Lachaux","year":"1999","journal-title":"Hum Brain Mapp"},{"key":"pcbi.1013661.ref049","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s10827-010-0228-5","article-title":"Methods for predicting cortical UP and DOWN states from the phase of deep layer local field potentials","volume":"29","author":"AB Saleem","year":"2010","journal-title":"J Comput Neurosci"},{"issue":"6","key":"pcbi.1013661.ref050","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1038\/nn.3711","article-title":"Partitioning neuronal variability","volume":"17","author":"RLT Goris","year":"2014","journal-title":"Nat Neurosci"},{"issue":"1","key":"pcbi.1013661.ref051","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nrn3136","article-title":"Normalization as a canonical neural computation","volume":"13","author":"M Carandini","year":"2011","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1013661.ref052","article-title":"Tensorflow: Large-scale machine learning on heterogeneous distributed systems.","author":"M Abadi","year":"2016"},{"key":"pcbi.1013661.ref053","unstructured":"Chollet F, & Others. Keras: The Python Deep Learning library. 2018. Available from https:\/\/ui.adsabs.harvard.edu\/abs\/2018ascl.soft06022C"},{"key":"pcbi.1013661.ref054","author":"L McInnes","year":"2018"},{"issue":"10","key":"pcbi.1013661.ref055","doi-asserted-by":"crossref","DOI":"10.1088\/1742-5468\/2008\/10\/P10008","article-title":"Fast unfolding of communities in large networks","volume":"2008","author":"VD Blondel","year":"2008","journal-title":"J Stat Mech"},{"issue":"4","key":"pcbi.1013661.ref056","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1523\/JNEUROSCI.2120-16.2016","article-title":"Nonlinear Y-Like Receptive Fields in the Early Visual Cortex: An Intermediate Stage for Building Cue-Invariant Receptive Fields from Subcortical Y Cells","volume":"37","author":"A Gharat","year":"2017","journal-title":"J Neurosci"},{"issue":"7","key":"pcbi.1013661.ref057","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.tins.2007.04.006","article-title":"Are corticothalamic \u201cup\u201d states fragments of wakefulness?","volume":"30","author":"A Destexhe","year":"2007","journal-title":"Trends Neurosci"},{"issue":"6","key":"pcbi.1013661.ref058","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.4249\/scholarpedia.1410","article-title":"Up and down states","volume":"3","author":"C Wilson","year":"2008","journal-title":"Scholarpedia J"},{"key":"pcbi.1013661.ref059","doi-asserted-by":"crossref","first-page":"51","DOI":"10.3389\/fncom.2012.00051","article-title":"Parametric models to relate spike train and LFP dynamics with neural information processing","volume":"6","author":"A Banerjee","year":"2012","journal-title":"Front Comput Neurosci"},{"issue":"5","key":"pcbi.1013661.ref060","doi-asserted-by":"crossref","first-page":"1698","DOI":"10.1073\/pnas.86.5.1698","article-title":"Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex","volume":"86","author":"CM Gray","year":"1989","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"pcbi.1013661.ref061","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1152\/jn.00919.2004","article-title":"LFP power spectra in V1 cortex: the graded effect of stimulus contrast","volume":"94","author":"JA Henrie","year":"2005","journal-title":"J Neurophysiol"},{"issue":"1","key":"pcbi.1013661.ref062","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1152\/physrev.1985.65.1.37","article-title":"Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena","volume":"65","author":"U Mitzdorf","year":"1985","journal-title":"Physiol Rev"},{"issue":"41","key":"pcbi.1013661.ref063","doi-asserted-by":"crossref","first-page":"13739","DOI":"10.1523\/JNEUROSCI.0743-10.2010","article-title":"Comparisons of the dynamics of local field potential and multiunit activity signals in macaque visual cortex","volume":"30","author":"SP Burns","year":"2010","journal-title":"J Neurosci"},{"key":"pcbi.1013661.ref064","doi-asserted-by":"crossref","unstructured":"Spacek MA, Swindale NV. Cortical state and natural movie responses in cat visual cortex. bioRxiv, 031765. 2015. https:\/\/doi.org\/10.1101\/031765","DOI":"10.1101\/031765"},{"issue":"22","key":"pcbi.1013661.ref065","doi-asserted-by":"crossref","first-page":"5696","DOI":"10.1523\/JNEUROSCI.0009-08.2008","article-title":"Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information","volume":"28","author":"A Belitski","year":"2008","journal-title":"J Neurosci"},{"issue":"43","key":"pcbi.1013661.ref066","doi-asserted-by":"crossref","first-page":"13702","DOI":"10.1523\/JNEUROSCI.2844-09.2009","article-title":"Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex","volume":"29","author":"FA Khawaja","year":"2009","journal-title":"J Neurosci"},{"key":"pcbi.1013661.ref067","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2202-16-S1-P264","article-title":"Two different mechanisms alternate during cortical synchronized states","volume":"16","author":"E Munro","year":"2015","journal-title":"BMC Neurosci"},{"key":"pcbi.1013661.ref068","article-title":"A non-oscillatory, millisecond-scale embedding of brain state provides insight into behavior","author":"DF Parks","year":"2023","journal-title":"bioRxiv"},{"key":"pcbi.1013661.ref069","doi-asserted-by":"crossref","first-page":"1273627","DOI":"10.3389\/fnins.2023.1273627","article-title":"Local field potentials and single unit dynamics in motor cortex of unconstrained macaques during different behavioral states","volume":"17","author":"R Yun","year":"2023","journal-title":"Front Neurosci"},{"key":"pcbi.1013661.ref070","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.neuroscience.2020.11.043","article-title":"Differential Effect of Anesthesia on Visual Cortex Neurons with Diverse Population Coupling","volume":"458","author":"H Lee","year":"2021","journal-title":"Neuroscience"},{"key":"pcbi.1013661.ref071","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.07224","article-title":"Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state","volume":"4","author":"T Bellay","year":"2015","journal-title":"Elife"},{"issue":"9","key":"pcbi.1013661.ref072","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1038\/nrn915","article-title":"The cognitive neuroscience of sleep: neuronal systems, consciousness and learning","volume":"3","author":"JA Hobson","year":"2002","journal-title":"Nat Rev Neurosci"},{"issue":"44","key":"pcbi.1013661.ref073","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2204959119","article-title":"Hippocampal gamma and sharp wave\/ripples mediate bidirectional interactions with cortical networks during sleep","volume":"119","author":"R Pedrosa","year":"2022","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7206","key":"pcbi.1013661.ref074","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1038\/nature07150","article-title":"Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice","volume":"454","author":"JFA Poulet","year":"2008","journal-title":"Nature"},{"issue":"6","key":"pcbi.1013661.ref075","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1016\/j.neuron.2015.09.012","article-title":"Waking State: Rapid Variations Modulate Neural and Behavioral Responses","volume":"87","author":"MJ McGinley","year":"2015","journal-title":"Neuron"},{"key":"pcbi.1013661.ref076","doi-asserted-by":"crossref","first-page":"21","DOI":"10.3389\/fncir.2018.00021","article-title":"Neuromodulatory Correlates of Pupil Dilation","volume":"12","author":"RS Larsen","year":"2018","journal-title":"Front Neural Circuits"},{"issue":"1","key":"pcbi.1013661.ref077","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1152\/jn.00642.2010","article-title":"Removal of spurious correlations between spikes and local field potentials","volume":"105","author":"TP Zanos","year":"2011","journal-title":"J Neurophysiol"},{"issue":"7","key":"pcbi.1013661.ref078","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1038\/s41593-018-0171-8","article-title":"Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation","volume":"21","author":"B Pesaran","year":"2018","journal-title":"Nat Neurosci"},{"issue":"6","key":"pcbi.1013661.ref079","doi-asserted-by":"crossref","first-page":"3340","DOI":"10.1152\/jn.91365.2008","article-title":"High-amplitude positive spikes recorded extracellularly in cat visual cortex","volume":"102","author":"C Gold","year":"2009","journal-title":"J Neurophysiol"},{"key":"pcbi.1013661.ref080","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.jneumeth.2015.01.029","article-title":"ViSAPy: a Python tool for biophysics-based generation of virtual spiking activity for evaluation of spike-sorting algorithms","volume":"245","author":"E Hagen","year":"2015","journal-title":"J Neurosci Methods"},{"key":"pcbi.1013661.ref081"},{"issue":"3","key":"pcbi.1013661.ref082","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/S0896-6273(00)00072-6","article-title":"Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons","volume":"27","author":"P Kara","year":"2000","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1013661.ref083","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1152\/jn.1985.54.3.651","article-title":"Contrast gain control in the cat\u2019s visual system","volume":"54","author":"I Ohzawa","year":"1985","journal-title":"J Neurophysiol"},{"issue":"36","key":"pcbi.1013661.ref084","doi-asserted-by":"crossref","first-page":"12081","DOI":"10.1523\/JNEUROSCI.0211-14.2014","article-title":"Form-cue invariant second-order neuronal responses to contrast modulation in primate area V2","volume":"34","author":"G Li","year":"2014","journal-title":"J Neurosci"},{"key":"pcbi.1013661.ref085","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0079-6123(01)34013-X","article-title":"Processing of second-order stimuli in the visual cortex","volume":"134","author":"CL Baker","year":"2001","journal-title":"Prog Brain Res"},{"issue":"4","key":"pcbi.1013661.ref086","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1006897","article-title":"Deep convolutional models improve predictions of macaque V1 responses to natural images","volume":"15","author":"SA Cadena","year":"2019","journal-title":"PLoS Comput Biol"},{"issue":"1","key":"pcbi.1013661.ref087","doi-asserted-by":"crossref","first-page":"3791","DOI":"10.1038\/s41598-019-40535-4","article-title":"Characterisation of nonlinear receptive fields of visual neurons by convolutional neural network","volume":"9","author":"J Ukita","year":"2019","journal-title":"Sci Rep"},{"issue":"1","key":"pcbi.1013661.ref088","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s10827-018-0687-7","article-title":"Convolutional neural network models of V1 responses to complex patterns","volume":"46","author":"Y Zhang","year":"2019","journal-title":"J Comput Neurosci"},{"issue":"6707","key":"pcbi.1013661.ref089","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/24157","article-title":"State-dependent receptive-field restructuring in the visual cortex","volume":"396","author":"F W\u00f6rg\u00f6tter","year":"1998","journal-title":"Nature"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1013661","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T00:00:00Z","timestamp":1762992000000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013661","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T19:01:29Z","timestamp":1763060489000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013661"}},"subtitle":[],"editor":[{"given":"Fr\u00e9d\u00e9ric E.","family":"Theunissen","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2025,11,6]]},"references-count":89,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1013661","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,6]]}}}