{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,4]],"date-time":"2026-06-04T23:51:04Z","timestamp":1780617064128,"version":"3.54.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1012429","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T00:00:00Z","timestamp":1727049600000}}],"reference-count":132,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2024,9,11]],"date-time":"2024-09-11T00:00:00Z","timestamp":1726012800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["227420"],"award-info":[{"award-number":["227420"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100023233","name":"National Institute for Health and Care Research Applied Research Collaboration Oxford and Thames Valley","doi-asserted-by":"publisher","award":["NIHR203316"],"award-info":[{"award-number":["NIHR203316"]}],"id":[{"id":"10.13039\/501100023233","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002425","name":"Brazilian Government","doi-asserted-by":"crossref","award":["CAPES\/PRINT 88887.583995\/2020-00"],"award-info":[{"award-number":["CAPES\/PRINT 88887.583995\/2020-00"]}],"id":[{"id":"10.13039\/501100002425","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Dutch Ministry of Education (OCW) via the Dutch Research Council","award":["DBI2 project (024.005.022, Gravitation)"],"award-info":[{"award-number":["DBI2 project (024.005.022, Gravitation)"]}]},{"name":"Wellcome Trust Discovery Award","award":["227420"],"award-info":[{"award-number":["227420"]}]},{"name":"NIHR Oxford Health Biomedical Research Centre","award":["NIHR203316"],"award-info":[{"award-number":["NIHR203316"]}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>The field of computer vision has long drawn inspiration from neuroscientific studies of the human and non-human primate visual system. The development of convolutional neural networks (CNNs), for example, was informed by the properties of simple and complex cells in early visual cortex. However, the computational relevance of oscillatory dynamics experimentally observed in the visual system are typically not considered in artificial neural networks (ANNs). Computational models of neocortical dynamics, on the other hand, rarely take inspiration from computer vision. Here, we combine methods from computational neuroscience and machine learning to implement multiplexing in a simple ANN using oscillatory dynamics. We first trained the network to classify individually presented letters. Post-training, we added temporal dynamics to the hidden layer, introducing refraction in the hidden units as well as pulsed inhibition mimicking neuronal alpha oscillations. Without these dynamics, the trained network correctly classified individual letters but produced a mixed output when presented with two letters simultaneously, indicating a bottleneck problem. When introducing refraction and oscillatory inhibition, the output nodes corresponding to the two stimuli activate sequentially, ordered along the phase of the inhibitory oscillations. Our model implements the idea that inhibitory oscillations segregate competing inputs in time. The results of our simulations pave the way for applications in deeper network architectures and more complicated machine learning problems.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1012429","type":"journal-article","created":{"date-parts":[[2024,9,11]],"date-time":"2024-09-11T13:38:51Z","timestamp":1726061931000},"page":"e1012429","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Oscillations in an artificial neural network convert competing inputs into a temporal code"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7887-3395","authenticated-orcid":true,"given":"Katharina","family":"Duecker","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marco","family":"Idiart","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcel","family":"van Gerven","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ole","family":"Jensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,9,11]]},"reference":[{"key":"pcbi.1012429.ref001","volume-title":"Convolutional networks for images, speech, and time-series","author":"Y LeCun","year":"1995"},{"key":"pcbi.1012429.ref002","first-page":"1","volume-title":"Advances in Neural Information Processing Systems","author":"A Krizhevsky","year":"2012"},{"key":"pcbi.1012429.ref003","doi-asserted-by":"crossref","first-page":"e7068349","DOI":"10.1155\/2018\/7068349","article-title":"Deep learning for computer vision: a brief review","volume":"2018","author":"A Voulodimos","year":"2018","journal-title":"Computational Intelligence and Neuroscience"},{"key":"pcbi.1012429.ref004","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.neuroimage.2016.03.063","article-title":"Dynamics of scene representations in the human brain revealed by magnetoencephalography and deep neural networks","volume":"153","author":"RM Cichy","year":"2017","journal-title":"NeuroImage"},{"issue":"1","key":"pcbi.1012429.ref005","doi-asserted-by":"crossref","first-page":"27755","DOI":"10.1038\/srep27755","article-title":"Comparison of deep neural networks to spatio-temporal cortical dynamics of human visual object recognition reveals hierarchical correspondence","volume":"6","author":"RM Cichy","year":"2016","journal-title":"Scientific Reports"},{"issue":"27","key":"pcbi.1012429.ref006","doi-asserted-by":"crossref","first-page":"10005","DOI":"10.1523\/JNEUROSCI.5023-14.2015","article-title":"Deep neural networks reveal a gradient in the complexity of neural representations across the ventral stream","volume":"35","author":"U G\u00fc\u00e7l\u00fc","year":"2015","journal-title":"Journal of Neuroscience"},{"key":"pcbi.1012429.ref007","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"},{"key":"pcbi.1012429.ref008","article-title":"Multi-scale hierarchical neural network models that bridge from single neurons in the primate primary visual cortex to object recognition behavior","author":"T Marques","year":"2021","journal-title":"bioRxiv"},{"key":"pcbi.1012429.ref009","first-page":"407007","article-title":"Brain-Score: Which Artificial Neural Network for Object Recognition is most Brain-Like?","author":"M Schrimpf","year":"2020","journal-title":"bioRxiv"},{"issue":"23","key":"pcbi.1012429.ref010","doi-asserted-by":"crossref","first-page":"8619","DOI":"10.1073\/pnas.1403112111","article-title":"Performance-optimized hierarchical models predict neural responses in higher visual cortex","volume":"111","author":"DLK Yamins","year":"2014","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"3","key":"pcbi.1012429.ref011","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1038\/nn.4244","article-title":"Using goal-driven deep learning models to understand sensory cortex","volume":"19","author":"DLK Yamins","year":"2016","journal-title":"Nature Neuroscience"},{"key":"pcbi.1012429.ref012","article-title":"A biology-inspired recurrent oscillator network for computations in high-dimensional state space","author":"F Effenberger","year":"2022","journal-title":"bioRxiv"},{"issue":"42","key":"pcbi.1012429.ref013","doi-asserted-by":"crossref","first-page":"eabd4205","DOI":"10.1126\/sciadv.abd4205","article-title":"Incorporating intrinsic suppression in deep neural networks captures dynamics of adaptation in neurophysiology and perception","volume":"6","author":"K Vinken","year":"2020","journal-title":"Science Advances"},{"key":"pcbi.1012429.ref014","article-title":"Phase of firing does not reflect temporal order in sequence memory of humans and recurrent neural networks","author":"S Liebe","year":"2022","journal-title":"bioRxiv"},{"issue":"6","key":"pcbi.1012429.ref015","doi-asserted-by":"crossref","first-page":"3554","DOI":"10.1152\/jn.00535.2009","article-title":"Quantitative analysis and biophysically realistic neural modeling of the MEG mu rhythm: Rhythmogenesis and modulation of sensory-evoked responses","volume":"102","author":"SR Jones","year":"2009","journal-title":"Journal of Neurophysiology"},{"issue":"4","key":"pcbi.1012429.ref016","first-page":"668","article-title":"Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception","volume":"32","author":"RG Law","year":"2021","journal-title":"Cerebral Cortex"},{"issue":"45","key":"pcbi.1012429.ref017","doi-asserted-by":"crossref","first-page":"18553","DOI":"10.1073\/pnas.1215385109","article-title":"Thalamic model of awake alpha oscillations and implications for stimulus processing","volume":"109","author":"S Vijayan","year":"2012","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1012429.ref018","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1038\/s42003-020-0947-8","article-title":"Layer 4 pyramidal neuron dendritic bursting underlies a post-stimulus visual cortical alpha rhythm","volume":"3","author":"RD Traub","year":"2020","journal-title":"Communications Biology"},{"issue":"5203","key":"pcbi.1012429.ref019","doi-asserted-by":"crossref","first-page":"1512","DOI":"10.1126\/science.7878473","article-title":"Storage of 7 +\/- 2 short-term memories in oscillatory subcycles","volume":"267","author":"JE Lisman","year":"1995","journal-title":"Science"},{"issue":"2","key":"pcbi.1012429.ref020","doi-asserted-by":"crossref","first-page":"e0296217","DOI":"10.1371\/journal.pone.0296217","article-title":"Mechanistic role of alpha oscillations in a computational model of working memory","volume":"19","author":"G Soroka","year":"2024","journal-title":"PLOS ONE"},{"issue":"46","key":"pcbi.1012429.ref021","doi-asserted-by":"crossref","first-page":"18023","DOI":"10.1073\/pnas.0809511105","article-title":"Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model","volume":"105","author":"C B\u00f6rgers","year":"2008","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"4","key":"pcbi.1012429.ref022","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1093\/brain\/57.4.355","article-title":"The Berger Rhythm: Potential Changes from the Occipital Lobes in Man","volume":"57","author":"ED Adrian","year":"1934","journal-title":"Brain"},{"issue":"1","key":"pcbi.1012429.ref023","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\u00fcr Psychiatrie und Nervenkrankheiten"},{"issue":"3","key":"pcbi.1012429.ref024","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1016\/j.neuron.2012.01.010","article-title":"How does the brain solve visual object recognition?","volume":"73","author":"JJ DiCarlo","year":"2012","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1012429.ref025","first-page":"1","article-title":"Distributed hierarchical processing in the primate cerebral cortex","volume":"1","author":"DJ Felleman","year":"1991","journal-title":"Cerebral Cortex (New York, NY: 1991)"},{"issue":"1456","key":"pcbi.1012429.ref026","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1098\/rstb.2005.1629","article-title":"Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics","volume":"360","author":"R Gattass","year":"2005","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"issue":"1","key":"pcbi.1012429.ref027","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":"The Journal of Physiology"},{"issue":"12","key":"pcbi.1012429.ref028","first-page":"1182","article-title":"Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex","volume":"11","author":"AT Smith","year":"2001","journal-title":"Cerebral Cortex (New York, NY: 1991)"},{"key":"pcbi.1012429.ref029","doi-asserted-by":"crossref","DOI":"10.1037\/10037-000","volume-title":"Perception and communication","author":"DE Broadbent","year":"1958"},{"issue":"46","key":"pcbi.1012429.ref030","doi-asserted-by":"crossref","first-page":"10577","DOI":"10.1523\/JNEUROSCI.3726-05.2005","article-title":"Do we know what the early visual system does?","volume":"25","author":"M Carandini","year":"2005","journal-title":"Journal of Neuroscience"},{"issue":"8","key":"pcbi.1012429.ref031","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.tics.2007.06.010","article-title":"Untangling invariant object recognition","volume":"11","author":"JJ DiCarlo","year":"2007","journal-title":"Trends in Cognitive Sciences"},{"issue":"1","key":"pcbi.1012429.ref032","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/0166-2236(92)90344-8","article-title":"Separate visual pathways for perception and action","volume":"15","author":"MA Goodale","year":"1992","journal-title":"Trends in Neurosciences"},{"issue":"3","key":"pcbi.1012429.ref033","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.neuropsychologia.2007.10.005","article-title":"Two visual systems re-viewed","volume":"46","author":"AD Milner","year":"2008","journal-title":"Neuropsychologia"},{"issue":"2","key":"pcbi.1012429.ref034","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/0959-4388(94)90066-3","article-title":"\u2018What\u2019 and\u2019where\u2019 in the human brain","volume":"4","author":"LG Ungerleider","year":"1994","journal-title":"Current Opinion in Neurobiology"},{"issue":"3","key":"pcbi.1012429.ref035","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.neuron.2012.03.033","article-title":"Attentional modulations related to spatial gating but not to allocation of limited resources in primate V1","volume":"74","author":"Y Chen","year":"2012","journal-title":"Neuron"},{"issue":"6","key":"pcbi.1012429.ref036","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1167\/17.6.19","article-title":"Evidence for unlimited capacity processing of simple features in visual cortex","volume":"17","author":"AL White","year":"2017","journal-title":"Journal of Vision"},{"issue":"20","key":"pcbi.1012429.ref037","doi-asserted-by":"crossref","first-page":"10087","DOI":"10.1073\/pnas.1822137116","article-title":"Parallel spatial channels converge at a bottleneck in anterior word-selective cortex","volume":"116","author":"AL White","year":"2019","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1012429.ref038","volume-title":"Prentice-Hall series in experimental psychology","author":"D Kahneman","year":"1973"},{"issue":"3","key":"pcbi.1012429.ref039","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1167\/jov.21.3.15","article-title":"Is there a serial bottleneck in visual object recognition?","volume":"21","author":"DV Popovkina","year":"2021","journal-title":"Journal of Vision"},{"issue":"2","key":"pcbi.1012429.ref040","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1038\/nrn3668","article-title":"Oscillatory multiplexing of population codes for selective communication in the mammalian brain","volume":"15","author":"TE Akam","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"issue":"1","key":"pcbi.1012429.ref041","doi-asserted-by":"crossref","first-page":"2715","DOI":"10.1038\/s41467-018-05121-8","article-title":"Single neurons may encode simultaneous stimuli by switching between activity patterns","volume":"9","author":"VC Caruso","year":"2018","journal-title":"Nature Communications"},{"key":"pcbi.1012429.ref042","article-title":"Neurons in Primate Visual Cortex Alternate between responses to multiple stimuli in their receptive field","volume":"10","author":"K Li","year":"2016","journal-title":"Frontiers in Computational Neuroscience"},{"issue":"3","key":"pcbi.1012429.ref043","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.tics.2015.01.002","article-title":"Neural population coding: combining insights from microscopic and mass signals","volume":"19","author":"S Panzeri","year":"2015","journal-title":"Trends in Cognitive Sciences"},{"issue":"3","key":"pcbi.1012429.ref044","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.tins.2009.12.001","article-title":"Sensory neural codes using multiplexed temporal scales","volume":"33","author":"S Panzeri","year":"2010","journal-title":"Trends in Neurosciences"},{"issue":"6","key":"pcbi.1012429.ref045","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/S0959-4388(97)80142-0","article-title":"Population coding and behavioral choice","volume":"7","author":"WB Kristan","year":"1997","journal-title":"Current Opinion in Neurobiology"},{"issue":"3","key":"pcbi.1012429.ref046","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1002\/hipo.450030307","article-title":"Phase relationship between hippocampal place units and the EEG theta rhythm","volume":"3","author":"J O\u2019Keefe","year":"1993","journal-title":"Hippocampus"},{"issue":"2","key":"pcbi.1012429.ref047","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K","article-title":"Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences","volume":"6","author":"WE Skaggs","year":"1996","journal-title":"Hippocampus"},{"issue":"6","key":"pcbi.1012429.ref048","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1016\/j.neuron.2013.03.007","article-title":"The theta-gamma neural code","volume":"77","author":"JE Lisman","year":"2013","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1012429.ref049","doi-asserted-by":"crossref","first-page":"2602","DOI":"10.1152\/jn.2000.83.5.2602","article-title":"Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding","volume":"83","author":"O Jensen","year":"2000","journal-title":"Journal of Neurophysiology"},{"issue":"2","key":"pcbi.1012429.ref050","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1101\/lm.3.2-3.279","article-title":"Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells","volume":"3","author":"O Jensen","year":"1996","journal-title":"Learning & Memory (Cold Spring Harbor, NY)"},{"issue":"7368","key":"pcbi.1012429.ref051","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/nature10439","article-title":"Theta-paced flickering between place-cell maps in the hippocampus","volume":"478","author":"K Jezek","year":"2011","journal-title":"Nature"},{"key":"pcbi.1012429.ref052","doi-asserted-by":"crossref","DOI":"10.3389\/fnhum.2010.00186","article-title":"Shaping functional architecture by oscillatory alpha activity: Gating by inhibition","volume":"4","author":"O Jensen","year":"2010","journal-title":"Frontiers in Human Neuroscience"},{"issue":"1","key":"pcbi.1012429.ref053","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.brainresrev.2006.06.003","article-title":"EEG alpha oscillations: The inhibition\u2013timing hypothesis","volume":"53","author":"W Klimesch","year":"2007","journal-title":"Brain Research Reviews"},{"issue":"48","key":"pcbi.1012429.ref054","doi-asserted-by":"crossref","first-page":"19377","DOI":"10.1073\/pnas.1117190108","article-title":"\u03b1-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking","volume":"108","author":"S Haegens","year":"2011","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1012429.ref055","doi-asserted-by":"crossref","first-page":"118746","DOI":"10.1016\/j.neuroimage.2021.118746","article-title":"Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability","volume":"247","author":"L Iemi","year":"2022","journal-title":"NeuroImage"},{"issue":"4","key":"pcbi.1012429.ref056","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.tics.2012.03.002","article-title":"An oscillatory mechanism for prioritizing salient unattended stimuli","volume":"16","author":"O Jensen","year":"2012","journal-title":"Trends in Cognitive Sciences"},{"key":"pcbi.1012429.ref057","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/978-3-642-33045-2_17","article-title":"Human brain oscillations: From physiological mechanisms to analysis and cognition","volume-title":"Magnetoencephalography","author":"O Jensen","year":"2014"},{"issue":"12","key":"pcbi.1012429.ref058","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/j.tics.2021.08.008","article-title":"An oscillatory pipelining mechanism supporting previewing during visual exploration and reading","volume":"25","author":"O Jensen","year":"2021","journal-title":"Trends in Cognitive Sciences"},{"issue":"7","key":"pcbi.1012429.ref059","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.tins.2014.04.001","article-title":"Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing","volume":"37","author":"O Jensen","year":"2014","journal-title":"Trends in Neurosciences"},{"issue":"11","key":"pcbi.1012429.ref060","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1167\/9.11.18","article-title":"Attentive and pre-attentive aspects of figural processing","volume":"9","author":"LG Appelbaum","year":"2009","journal-title":"Journal of Vision"},{"issue":"6","key":"pcbi.1012429.ref061","doi-asserted-by":"crossref","first-page":"3501","DOI":"10.1073\/pnas.0337630100","article-title":"The power of human brain magnetoencephalographic signals can be modulated up or down by changes in an attentive visual task","volume":"100","author":"Y Chen","year":"2003","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"4","key":"pcbi.1012429.ref062","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1016\/S0896-6273(00)80734-5","article-title":"Increased activity in human visual cortex during directed attention in the absence of visual stimulation","volume":"22","author":"S Kastner","year":"1999","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1012429.ref063","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1152\/jn.2000.83.3.1751","article-title":"Attention to both space and feature modulates neuronal responses in macaque area V4","volume":"83","author":"CJ McAdams","year":"2000","journal-title":"Journal of Neurophysiology"},{"issue":"4715","key":"pcbi.1012429.ref064","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1126\/science.4023713","article-title":"Selective attention gates visual processing in the extrastriate cortex","volume":"229","author":"J Moran","year":"1985","journal-title":"Science (New York, NY)"},{"issue":"4","key":"pcbi.1012429.ref065","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1152\/jn.1999.81.4.1783","article-title":"Effect of Spatial Attention on the Responses of Area MT Neurons","volume":"81","author":"E Seidemann","year":"1999","journal-title":"Journal of Neurophysiology"},{"issue":"6","key":"pcbi.1012429.ref066","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1038\/75797","article-title":"Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex","volume":"3","author":"J Anderson","year":"2000","journal-title":"Nature Neuroscience"},{"issue":"43","key":"pcbi.1012429.ref067","doi-asserted-by":"crossref","first-page":"15482","DOI":"10.1073\/pnas.0406343101","article-title":"Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks","volume":"101","author":"N Kopell","year":"2004","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pcbi.1012429.ref068","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/S0079-6123(08)61248-0","article-title":"Potassium currents in hippocampal pyramidal cells","volume":"83","author":"JF Storm","year":"1990","journal-title":"Progress in Brain Research"},{"issue":"8","key":"pcbi.1012429.ref069","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"},{"key":"pcbi.1012429.ref070","volume-title":"Deep Learning","author":"I Goodfellow","year":"2016"},{"key":"pcbi.1012429.ref071","unstructured":"Glorot X, Bengio Y. Understanding the difficulty of training deep feedforward neural networks. In: Proceedings of the Thirteenth International Conference on Artificial Intelligence and Statistics. JMLR Workshop and Conference Proceedings; 2010. p. 249\u2013256."},{"key":"pcbi.1012429.ref072","author":"DP Kingma","year":"2017","journal-title":"Adam. A Method for Stochastic Optimization"},{"issue":"3","key":"pcbi.1012429.ref073","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/j.neuron.2010.09.023","article-title":"Neural Syntax: Cell Assemblies, Synapsembles, and Readers","volume":"68","author":"G Buzs\u00e1ki","year":"2010","journal-title":"Neuron"},{"issue":"6948","key":"pcbi.1012429.ref074","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1038\/nature01834","article-title":"Organization of cell assemblies in the hippocampus","volume":"424","author":"KD Harris","year":"2003","journal-title":"Nature"},{"issue":"4","key":"pcbi.1012429.ref075","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1038\/nn.2276","article-title":"Gating multiple signals through detailed balance of excitation and inhibition in spiking networks","volume":"12","author":"TP Vogels","year":"2009","journal-title":"Nature Neuroscience"},{"issue":"5","key":"pcbi.1012429.ref076","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/S0301-0082(02)00004-7","article-title":"Channels underlying neuronal calcium-activated potassium currents","volume":"66","author":"P Sah","year":"2002","journal-title":"Progress in Neurobiology"},{"issue":"2","key":"pcbi.1012429.ref077","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1073\/pnas.76.2.986","article-title":"Intradendritic recordings from hippocampal neurons","volume":"76","author":"RK Wong","year":"1979","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"3","key":"pcbi.1012429.ref078","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/s41592-019-0686-2","article-title":"SciPy 1.0: fundamental algorithms for scientific computing in Python","volume":"17","author":"P Virtanen","year":"2020","journal-title":"Nature Methods"},{"issue":"3","key":"pcbi.1012429.ref079","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/j.neuron.2009.10.022","article-title":"Phase resetting as a mechanism for supramodal attentional control","volume":"64","author":"C Kayser","year":"2009","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1012429.ref080","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/j.neuron.2013.06.001","article-title":"Coding of Information in the Phase of Local Field Potentials within Human Medial Temporal Lobe","volume":"79","author":"BA Lopour","year":"2013","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1012429.ref081","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.cub.2008.02.023","article-title":"Phase-of-firing coding of natural visual stimuli in primary visual cortex","volume":"18","author":"MA Montemurro","year":"2008","journal-title":"Current Biology"},{"issue":"10","key":"pcbi.1012429.ref082","doi-asserted-by":"crossref","DOI":"10.1016\/j.tics.2005.08.011","article-title":"A mechanism for cognitive dynamics: neuronal communication through neuronal coherence","volume":"9","author":"P Fries","year":"2005","journal-title":"Trends in cognitive sciences"},{"issue":"1","key":"pcbi.1012429.ref083","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.neuron.2015.09.034","article-title":"Rhythms for cognition: Communication Through Coherence","volume":"88","author":"P Fries","year":"2015","journal-title":"Neuron"},{"issue":"11","key":"pcbi.1012429.ref084","doi-asserted-by":"crossref","first-page":"e1002760","DOI":"10.1371\/journal.pcbi.1002760","article-title":"Efficient \u201ccommunication through coherence\u201d requires oscillations structured to minimize interference between signals","volume":"8","author":"TE Akam","year":"2012","journal-title":"PLoS computational biology"},{"issue":"10","key":"pcbi.1012429.ref085","doi-asserted-by":"crossref","first-page":"e1005162","DOI":"10.1371\/journal.pcbi.1005162","article-title":"Theta-gamma coding meets Communication-through-Coherence: Neuronal oscillatory multiplexing theories reconciled","volume":"12","author":"D McLelland","year":"2016","journal-title":"PLOS Computational Biology"},{"issue":"2","key":"pcbi.1012429.ref086","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0153-16.2017","article-title":"Communication between brain areas based on nested oscillations","volume":"4","author":"M Bonnefond","year":"2017","journal-title":"eNeuro"},{"issue":"2","key":"pcbi.1012429.ref087","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/0010-0285(92)90007-O","article-title":"The reviewing of object files: object-specific integration of information","volume":"24","author":"D Kahneman","year":"1992","journal-title":"Cognitive Psychology"},{"issue":"2","key":"pcbi.1012429.ref088","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.neuron.2020.01.032","article-title":"Combined phase-rate coding by persistently active neurons as a mechanism for maintaining multiple items in working memory in humans","volume":"106","author":"J Kami\u0144ski","year":"2020","journal-title":"Neuron"},{"issue":"7290","key":"pcbi.1012429.ref089","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1038\/nature08860","article-title":"Human memory strength is predicted by theta-frequency phase-locking of single neurons","volume":"464","author":"U Rutishauser","year":"2010","journal-title":"Nature"},{"key":"pcbi.1012429.ref090","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.conb.2014.11.001","article-title":"Communication through coherence with inter-areal delays","volume":"31","author":"AM Bastos","year":"2015","journal-title":"Current Opinion in Neurobiology"},{"issue":"5","key":"pcbi.1012429.ref091","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1016\/j.neuron.2012.06.037","article-title":"Attentional stimulus selection through selective synchronization between monkey visual areas","volume":"75","author":"CA Bosman","year":"2012","journal-title":"Neuron"},{"issue":"40","key":"pcbi.1012429.ref092","doi-asserted-by":"crossref","first-page":"14332","DOI":"10.1073\/pnas.1402773111","article-title":"Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex","volume":"111","author":"T van Kerkoerle","year":"2014","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"40","key":"pcbi.1012429.ref093","doi-asserted-by":"crossref","first-page":"9976","DOI":"10.1523\/JNEUROSCI.2699-08.2008","article-title":"Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques","volume":"28","author":"A Bollimunta","year":"2008","journal-title":"The Journal of Neuroscience: The Official Journal of the Society for Neuroscience"},{"issue":"13","key":"pcbi.1012429.ref094","doi-asserted-by":"crossref","first-page":"4935","DOI":"10.1523\/JNEUROSCI.5580-10.2011","article-title":"Neuronal mechanisms and attentional modulation of corticothalamic \u03b1 oscillations","volume":"31","author":"A Bollimunta","year":"2011","journal-title":"The Journal of Neuroscience: The Official Journal of the Society for Neuroscience"},{"key":"pcbi.1012429.ref095","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1093\/cercor\/bhv304","article-title":"Ongoing alpha activity in V1 regulates visually driven spiking responses","volume":"27","author":"K Dougherty","year":"2017","journal-title":"Cerebral Cortex"},{"issue":"2","key":"pcbi.1012429.ref096","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.neuron.2015.12.018","article-title":"Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas","volume":"89","author":"G Michalareas","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1012429.ref097","doi-asserted-by":"crossref","first-page":"2313","DOI":"10.1016\/j.cub.2012.10.020","article-title":"Layer-specific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex","volume":"22","author":"E Spaak","year":"2012","journal-title":"Current Biology"},{"issue":"12","key":"pcbi.1012429.ref098","doi-asserted-by":"crossref","first-page":"e3990","DOI":"10.1371\/journal.pone.0003990","article-title":"Gamma Power Is Phase-Locked to Posterior Alpha Activity","volume":"3","author":"D Osipova","year":"2008","journal-title":"PLOS ONE"},{"key":"pcbi.1012429.ref099","doi-asserted-by":"crossref","DOI":"10.3389\/fnhum.2010.00191","article-title":"Shifts in gamma phase\u2013amplitude xoupling frequency from theta to alpha over posterior cortex during visual tasks","volume":"4","author":"B Voytek","year":"2010","journal-title":"Frontiers in Human Neuroscience"},{"key":"pcbi.1012429.ref100","doi-asserted-by":"crossref","first-page":"e85035","DOI":"10.7554\/eLife.85035","article-title":"Distinct roles of forward and backward alpha-band waves in spatial visual attention","volume":"12","author":"A Alamia","year":"2023","journal-title":"eLife"},{"key":"pcbi.1012429.ref101","first-page":"1","article-title":"A traveling waves perspective on temporal binding","author":"A Alamia","year":"2023","journal-title":"Journal of Cognitive Neuroscience"},{"key":"pcbi.1012429.ref102","doi-asserted-by":"crossref","first-page":"120047","DOI":"10.1016\/j.neuroimage.2023.120047","article-title":"Perceptual echoes as travelling waves may arise from two discrete neuronal sources","volume":"272","author":"A Zhigalov","year":"2023","journal-title":"NeuroImage"},{"issue":"7834","key":"pcbi.1012429.ref103","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1038\/s41586-020-2802-y","article-title":"Spontaneous traveling cortical waves gate perception in behaving primates","volume":"587","author":"ZW Davis","year":"2020","journal-title":"Nature"},{"issue":"1","key":"pcbi.1012429.ref104","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s42003-022-03052-1","article-title":"Cortical neural dynamics unveil the rhythm of natural visual behavior in marmosets","volume":"5","author":"T Kaneko","year":"2022","journal-title":"Communications Biology"},{"issue":"5","key":"pcbi.1012429.ref105","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1016\/j.cub.2022.01.003","article-title":"Tuning alpha rhythms to shape conscious visual perception","volume":"32","author":"F Di Gregorio","year":"2022","journal-title":"Current Biology"},{"issue":"7","key":"pcbi.1012429.ref106","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1162\/jocn_a_01397","article-title":"Alpha oscillations and feedback processing in visual cortex for conscious perception","volume":"31","author":"T Ro","year":"2019","journal-title":"Journal of Cognitive Neuroscience"},{"key":"pcbi.1012429.ref107","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1146\/annurev-neuro-062012-170325","article-title":"Decoding neural representational spaces using multivariate pattern analysis","volume":"37","author":"JV Haxby","year":"2014","journal-title":"Annual Review of Neuroscience"},{"key":"pcbi.1012429.ref108","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1016\/j.neuroimage.2018.02.044","article-title":"Multivariate pattern analysis for MEG: A comparison of dissimilarity measures","volume":"173","author":"M Guggenmos","year":"2018","journal-title":"NeuroImage"},{"issue":"11","key":"pcbi.1012429.ref109","doi-asserted-by":"crossref","first-page":"3191","DOI":"10.1111\/ejn.15084","article-title":"Phasic modulation of visual representations during sustained attention","volume":"55","author":"MWJ van Es","year":"2022","journal-title":"European Journal of Neuroscience"},{"key":"pcbi.1012429.ref110","author":"International Brain Laboratory","year":"2023","journal-title":"A Brain-Wide Map of Neural Activity during Complex Behaviour"},{"issue":"6539","key":"pcbi.1012429.ref111","doi-asserted-by":"crossref","first-page":"eabf4588","DOI":"10.1126\/science.abf4588","article-title":"Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings","volume":"372","author":"NA Steinmetz","year":"2021","journal-title":"Science"},{"issue":"1","key":"pcbi.1012429.ref112","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/s41593-019-0550-9","article-title":"A large-scale standardized physiological survey reveals functional organization of the mouse visual cortex","volume":"23","author":"SEJ de Vries","year":"2020","journal-title":"Nature Neuroscience"},{"issue":"7852","key":"pcbi.1012429.ref113","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/s41586-020-03171-x","article-title":"Survey of spiking in the mouse visual system reveals functional hierarchy","volume":"592","author":"JH Siegle","year":"2021","journal-title":"Nature"},{"issue":"27","key":"pcbi.1012429.ref114","doi-asserted-by":"crossref","first-page":"eabe1833","DOI":"10.1126\/sciadv.abe1833","article-title":"The essential role of recurrent processing for Fig-ground perception in mice","volume":"7","author":"L Kirchberger","year":"2021","journal-title":"Science Advances"},{"issue":"1","key":"pcbi.1012429.ref115","doi-asserted-by":"crossref","first-page":"3736","DOI":"10.1038\/s41467-022-31407-z","article-title":"Rhythmic interactions between the mediodorsal thalamus and prefrontal cortex precede human visual perception","volume":"13","author":"BJ Griffiths","year":"2022","journal-title":"Nature Communications"},{"issue":"10","key":"pcbi.1012429.ref116","doi-asserted-by":"crossref","first-page":"e3000487","DOI":"10.1371\/journal.pbio.3000487","article-title":"Alpha oscillations and traveling waves: Signatures of predictive coding?","volume":"17","author":"A Alamia","year":"2019","journal-title":"PLOS Biology"},{"issue":"48","key":"pcbi.1012429.ref117","doi-asserted-by":"crossref","first-page":"18849","DOI":"10.1523\/JNEUROSCI.2455-13.2013","article-title":"Propagating neocortical gamma bursts are coordinated by traveling alpha waves","volume":"33","author":"A Bahramisharif","year":"2013","journal-title":"Journal of Neuroscience"},{"issue":"6","key":"pcbi.1012429.ref118","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1016\/j.neuron.2018.05.019","article-title":"Theta and alpha oscillations are traveling waves in the human neocortex","volume":"98","author":"H Zhang","year":"2018","journal-title":"Neuron"},{"issue":"12","key":"pcbi.1012429.ref119","doi-asserted-by":"crossref","first-page":"2743","DOI":"10.1162\/089976601317098510","article-title":"Information transfer between rhythmically coupled networks: Reading the hippocampal phase code","volume":"13","author":"O Jensen","year":"2001","journal-title":"Neural Computation"},{"issue":"5203","key":"pcbi.1012429.ref120","doi-asserted-by":"crossref","first-page":"1512","DOI":"10.1126\/science.7878473","article-title":"Storage of 7 +\/- 2 short-term memories in oscillatory subcycles","volume":"267","author":"JE Lisman","year":"1995","journal-title":"Science (New York, NY)"},{"issue":"6","key":"pcbi.1012429.ref121","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1068\/p3029","article-title":"Is it a bird? Is it a plane? Ultra-rapid visual categorisation of natural and artifactual objects","volume":"30","author":"R VanRullen","year":"2001","journal-title":"Perception"},{"key":"pcbi.1012429.ref122","unstructured":"Cohen G, Afshar S, Tapson J, van Schaik A. EMNIST: Extending MNIST to handwritten letters. In: 2017 International Joint Conference on Neural Networks (IJCNN); 2017. p. 2921\u20132926. Available from: https:\/\/ieeexplore.ieee.org\/abstract\/document\/7966217?casa_token=VYVpqIorsuMAAAAA:DUdROy9jm9Sstzh4r8C25IBSwKWxf5RYq-0uMcNUPhh8o4pgjBvBY9JBtWGCLirImhtzy_Wd."},{"issue":"11","key":"pcbi.1012429.ref123","doi-asserted-by":"crossref","first-page":"2278","DOI":"10.1109\/5.726791","article-title":"Gradient-based learning applied to document recognition","volume":"86","author":"Y LeCun","year":"1998","journal-title":"Proceedings of the IEEE"},{"key":"pcbi.1012429.ref124","author":"R Wu","year":"2015","journal-title":"Deep Image: Scaling up Image Recognition"},{"key":"pcbi.1012429.ref125","volume-title":"Deep learning with Python","author":"F Chollet","year":"2021"},{"issue":"4","key":"pcbi.1012429.ref126","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1162\/jocn_a_01819","article-title":"Leveraging spiking deep neural networks to understand the neural mechanisms underlying selective attention","volume":"34","author":"LKA S\u00f6rensen","year":"2022","journal-title":"Journal of Cognitive Neuroscience"},{"key":"pcbi.1012429.ref127","doi-asserted-by":"crossref","DOI":"10.3389\/fnins.2018.00987","article-title":"Sparse computation in adaptive spiking neural networks","volume":"12","author":"D Zambrano","year":"2019","journal-title":"Frontiers in Neuroscience"},{"key":"pcbi.1012429.ref128","volume-title":"An introductory course in computational neuroscience","author":"P Miller","year":"2018"},{"key":"pcbi.1012429.ref129","first-page":"1","volume-title":"Advances in Neural Information Processing Systems","author":"RTQ Chen","year":"2018"},{"issue":"11","key":"pcbi.1012429.ref130","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1038\/s42256-022-00556-7","article-title":"Closed-form continuous-time neural networks","volume":"4","author":"R Hasani","year":"2022","journal-title":"Nature Machine Intelligence"},{"key":"pcbi.1012429.ref131","author":"R Hasani","year":"2020","journal-title":"Liquid Time-constant Networks"},{"issue":"47","key":"pcbi.1012429.ref132","doi-asserted-by":"crossref","first-page":"23772","DOI":"10.1073\/pnas.1913092116","article-title":"The generation and propagation of the human alpha rhythm","volume":"116","author":"M Halgren","year":"2019","journal-title":"Proceedings of the National Academy of Sciences"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1012429","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T00:00:00Z","timestamp":1727049600000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012429","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T13:40:11Z","timestamp":1727098811000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012429"}},"subtitle":[],"editor":[{"given":"Stefano","family":"Panzeri","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,9,11]]},"references-count":132,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,9,11]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1012429","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.11.27.568876","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,11]]}}}