{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,16]],"date-time":"2026-04-16T04:21:41Z","timestamp":1776313301112,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1008533","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,12,29]],"date-time":"2020-12-29T00:00:00Z","timestamp":1609200000000}}],"reference-count":85,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2020,12,15]],"date-time":"2020-12-15T00:00:00Z","timestamp":1607990400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Excellence Initiative I-Site Paris Seine","award":["ANR-16-IDEX-008"],"award-info":[{"award-number":["ANR-16-IDEX-008"]}]},{"name":"Labex MME-DII","award":["ANR-11-LBX-0023-01"],"award-info":[{"award-number":["ANR-11-LBX-0023-01"]}]},{"name":"ANR Project ERMUNDY","award":["ANR-18-CE37-0014"],"award-info":[{"award-number":["ANR-18-CE37-0014"]}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>\n                    A synaptic theory of Working Memory (WM) has been developed in the last decade as a possible alternative to the persistent spiking paradigm. In this context, we have developed a neural mass model able to reproduce exactly the dynamics of heterogeneous spiking neural networks encompassing realistic cellular mechanisms for short-term synaptic plasticity. This population model reproduces the macroscopic dynamics of the network in terms of the firing rate and the mean membrane potential. The latter quantity allows us to gain insight of the Local Field Potential and electroencephalographic signals measured during WM tasks to characterize the brain activity. More specifically synaptic facilitation and depression integrate each other to efficiently mimic WM operations via either synaptic reactivation or persistent activity. Memory access and loading are related to stimulus-locked transient oscillations followed by a steady-state activity in the\n                    <jats:italic>\u03b2<\/jats:italic>\n                    -\n                    <jats:italic>\u03b3<\/jats:italic>\n                    band, thus resembling what is observed in the cortex during vibrotactile stimuli in humans and object recognition in monkeys. Memory juggling and competition emerge already by loading only two items. However more items can be stored in WM by considering neural architectures composed of multiple excitatory populations and a common inhibitory pool. Memory capacity depends strongly on the presentation rate of the items and it maximizes for an optimal frequency range. In particular we provide an analytic expression for the maximal memory capacity. Furthermore, the mean membrane potential turns out to be a suitable proxy to measure the memory load, analogously to event driven potentials in experiments on humans. Finally we show that the\n                    <jats:italic>\u03b3<\/jats:italic>\n                    power increases with the number of loaded items, as reported in many experiments, while\n                    <jats:italic>\u03b8<\/jats:italic>\n                    and\n                    <jats:italic>\u03b2<\/jats:italic>\n                    power reveal non monotonic behaviours. In particular,\n                    <jats:italic>\u03b2<\/jats:italic>\n                    and\n                    <jats:italic>\u03b3<\/jats:italic>\n                    rhythms are crucially sustained by the inhibitory activity, while the\n                    <jats:italic>\u03b8<\/jats:italic>\n                    rhythm is controlled by excitatory synapses.\n                  <\/jats:p>","DOI":"10.1371\/journal.pcbi.1008533","type":"journal-article","created":{"date-parts":[[2020,12,15]],"date-time":"2020-12-15T14:50:26Z","timestamp":1608043826000},"page":"e1008533","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":54,"title":["Exact neural mass model for synaptic-based working memory"],"prefix":"10.1371","volume":"16","author":[{"given":"Halgurd","family":"Taher","sequence":"first","affiliation":[]},{"given":"Alessandro","family":"Torcini","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8272-3493","authenticated-orcid":true,"given":"Simona","family":"Olmi","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2020,12,15]]},"reference":[{"issue":"1","key":"pcbi.1008533.ref001","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1037\/0033-295X.99.1.122","article-title":"A capacity theory of comprehension: individual differences in working memory","volume":"99","author":"MA Just","year":"1992","journal-title":"Psychological review"},{"issue":"3","key":"pcbi.1008533.ref002","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/0896-6273(95)90304-6","article-title":"Cellular basis of working memory","volume":"14","author":"PS Goldman-Rakic","year":"1995","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1008533.ref003","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1037\/0096-3445.128.3.309","article-title":"Working memory, short-term memory, and general fluid intelligence: a latent-variable approach","volume":"128","author":"RW Engle","year":"1999","journal-title":"Journal of experimental psychology: General"},{"key":"pcbi.1008533.ref004","volume-title":"Memory in the cerebral cortex: An empirical approach to neural networks in the human and nonhuman primate","author":"JM Fuster","year":"1999"},{"issue":"6984","key":"pcbi.1008533.ref005","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1038\/nature02447","article-title":"Neural activity predicts individual differences in visual working memory capacity","volume":"428","author":"EK Vogel","year":"2004","journal-title":"Nature"},{"key":"pcbi.1008533.ref006","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.cobeha.2014.08.001","article-title":"Multiple gates on working memory","volume":"1","author":"CH Chatham","year":"2015","journal-title":"Current opinion in behavioral sciences"},{"issue":"3997","key":"pcbi.1008533.ref007","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1126\/science.173.3997.652","article-title":"Neuron activity related to short-term memory","volume":"173","author":"JM Fuster","year":"1971","journal-title":"Science"},{"issue":"1","key":"pcbi.1008533.ref008","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1146\/annurev.neuro.24.1.167","article-title":"An integrative theory of prefrontal cortex function","volume":"24","author":"EK Miller","year":"2001","journal-title":"Annual review of neuroscience"},{"key":"pcbi.1008533.ref009","first-page":"173","article-title":"The role of prefrontal cortex in working memory: a mini review","volume":"9","author":"AH Lara","year":"2015","journal-title":"Frontiers in systems neuroscience"},{"issue":"2","key":"pcbi.1008533.ref010","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1152\/jn.1989.61.2.331","article-title":"Mnemonic coding of visual space in the monkey\u2019s dorsolateral prefrontal cortex","volume":"61","author":"S Funahashi","year":"1989","journal-title":"Journal of neurophysiology"},{"issue":"6735","key":"pcbi.1008533.ref011","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/20939","article-title":"Neuronal correlates of parametric working memory in the prefrontal cortex","volume":"399","author":"R Romo","year":"1999","journal-title":"Nature"},{"issue":"16","key":"pcbi.1008533.ref012","doi-asserted-by":"crossref","first-page":"5154","DOI":"10.1523\/JNEUROSCI.16-16-05154.1996","article-title":"Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque","volume":"16","author":"EK Miller","year":"1996","journal-title":"Journal of Neuroscience"},{"issue":"4","key":"pcbi.1008533.ref013","doi-asserted-by":"crossref","first-page":"209","DOI":"10.5709\/acp-0199-x","article-title":"Controlling working memory operations by selective gating: the roles of oscillations and synchrony","volume":"12","author":"M Dipoppa","year":"2016","journal-title":"Advances in cognitive psychology"},{"issue":"32","key":"pcbi.1008533.ref014","doi-asserted-by":"crossref","first-page":"7020","DOI":"10.1523\/JNEUROSCI.2486-17.2018","article-title":"Persistent spiking activity underlies working memory","volume":"38","author":"C Constantinidis","year":"2018","journal-title":"Journal of Neuroscience"},{"issue":"3","key":"pcbi.1008533.ref015","first-page":"237","article-title":"Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex","volume":"7","author":"DJ Amit","year":"1997","journal-title":"Cerebral cortex (New York, NY: 1991)"},{"issue":"9","key":"pcbi.1008533.ref016","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1093\/cercor\/10.9.910","article-title":"Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model","volume":"10","author":"A Compte","year":"2000","journal-title":"Cerebral cortex"},{"issue":"5712","key":"pcbi.1008533.ref017","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1126\/science.1104171","article-title":"Flexible control of mutual inhibition: a neural model of two-interval discrimination","volume":"307","author":"CK Machens","year":"2005","journal-title":"Science"},{"issue":"4","key":"pcbi.1008533.ref018","first-page":"374","article-title":"High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice","volume":"7","author":"A Gevins","year":"1997","journal-title":"Cerebral cortex (New York, NY: 1991)"},{"issue":"8","key":"pcbi.1008533.ref019","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1046\/j.1460-9568.2002.01975.x","article-title":"Frontal theta activity in humans increases with memory load in a working memory task","volume":"15","author":"O Jensen","year":"2002","journal-title":"European journal of Neuroscience"},{"issue":"11","key":"pcbi.1008533.ref020","doi-asserted-by":"crossref","first-page":"4244","DOI":"10.1523\/JNEUROSCI.18-11-04244.1998","article-title":"Induced \u03b3-band activity during the delay of a visual short-term memory task in humans","volume":"18","author":"C Tallon-Baudry","year":"1998","journal-title":"Journal of Neuroscience"},{"issue":"12","key":"pcbi.1008533.ref021","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1093\/cercor\/bhg084","article-title":"Gamma oscillations correlate with working memory load in humans","volume":"13","author":"MW Howard","year":"2003","journal-title":"Cerebral cortex"},{"issue":"8","key":"pcbi.1008533.ref022","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1038\/nn890","article-title":"Temporal structure in neuronal activity during working memory in macaque parietal cortex","volume":"5","author":"B Pesaran","year":"2002","journal-title":"Nature neuroscience"},{"issue":"2","key":"pcbi.1008533.ref023","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1523\/JNEUROSCI.3678-15.2016","article-title":"Transitions between multiband oscillatory patterns characterize memory-guided perceptual decisions in prefrontal circuits","volume":"36","author":"K Wimmer","year":"2016","journal-title":"Journal of Neuroscience"},{"issue":"21","key":"pcbi.1008533.ref024","doi-asserted-by":"crossref","first-page":"1846","DOI":"10.1016\/j.cub.2009.08.062","article-title":"Brain oscillatory substrates of visual short-term memory capacity","volume":"19","author":"P Sauseng","year":"2009","journal-title":"Current biology"},{"issue":"5203","key":"pcbi.1008533.ref025","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\u20133","key":"pcbi.1008533.ref026","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1101\/lm.3.2-3.257","article-title":"Novel lists of 7+\/-2 known items can be reliably stored in an oscillatory short-term memory network: interaction with long-term memory","volume":"3","author":"O Jensen","year":"1996","journal-title":"Learning & Memory"},{"issue":"9","key":"pcbi.1008533.ref027","doi-asserted-by":"crossref","first-page":"3779","DOI":"10.1073\/pnas.1019676108","article-title":"Neuronal assembly dynamics in the beta1 frequency range permits short-term memory","volume":"108","author":"N Kopell","year":"2011","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"3","key":"pcbi.1008533.ref028","doi-asserted-by":"crossref","first-page":"032801","DOI":"10.1103\/PhysRevE.87.032801","article-title":"Synchronous dynamics in the presence of short-term plasticity","volume":"87","author":"M di Volo","year":"2013","journal-title":"Physical Review E"},{"issue":"9","key":"pcbi.1008533.ref029","doi-asserted-by":"crossref","first-page":"e1006430","DOI":"10.1371\/journal.pcbi.1006430","article-title":"Network mechanisms underlying the role of oscillations in cognitive tasks","volume":"14","author":"H Schmidt","year":"2018","journal-title":"PLoS computational biology"},{"issue":"3","key":"pcbi.1008533.ref030","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1016\/j.neuroscience.2006.12.072","article-title":"Variability in neuronal activity in primate cortex during working memory tasks","volume":"146","author":"M Shafi","year":"2007","journal-title":"Neuroscience"},{"issue":"1","key":"pcbi.1008533.ref031","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.neuron.2016.02.028","article-title":"Gamma and beta bursts underlie working memory","volume":"90","author":"M Lundqvist","year":"2016","journal-title":"Neuron"},{"issue":"8","key":"pcbi.1008533.ref032","doi-asserted-by":"crossref","first-page":"2747","DOI":"10.1523\/JNEUROSCI.5135-11.2012","article-title":"Memory-guided sensory comparisons in the prefrontal cortex: contribution of putative pyramidal cells and interneurons","volume":"32","author":"CR Hussar","year":"2012","journal-title":"Journal of Neuroscience"},{"issue":"7","key":"pcbi.1008533.ref033","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/nn.2134","article-title":"Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex","volume":"11","author":"S Fujisawa","year":"2008","journal-title":"Nature neuroscience"},{"issue":"4","key":"pcbi.1008533.ref034","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1038\/nn1670","article-title":"Heterogeneity in the pyramidal network of the medial prefrontal cortex","volume":"9","author":"Y Wang","year":"2006","journal-title":"Nature neuroscience"},{"issue":"5869","key":"pcbi.1008533.ref035","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.1126\/science.1150769","article-title":"Synaptic Theory of Working Memory","volume":"319","author":"G Mongillo","year":"2008","journal-title":"Science"},{"issue":"10","key":"pcbi.1008533.ref036","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.1162\/jocn_a_00029","article-title":"Theta and gamma power increases and alpha\/beta power decreases with memory load in an attractor network model","volume":"23","author":"M Lundqvist","year":"2011","journal-title":"Journal of cognitive neuroscience"},{"issue":"6316","key":"pcbi.1008533.ref037","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1126\/science.aah7011","article-title":"Reactivation of latent working memories with transcranial magnetic stimulation","volume":"354","author":"NS Rose","year":"2016","journal-title":"Science"},{"issue":"2","key":"pcbi.1008533.ref038","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/j.neuron.2018.09.023","article-title":"Working Memory 2.0","volume":"100","author":"EK Miller","year":"2018","journal-title":"Neuron"},{"issue":"50","key":"pcbi.1008533.ref039","doi-asserted-by":"crossref","first-page":"21341","DOI":"10.1073\/pnas.0908193106","article-title":"Phase-dependent neuronal coding of objects in short-term memory","volume":"106","author":"M Siegel","year":"2009","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"2","key":"pcbi.1008533.ref040","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1073\/pnas.94.2.719","article-title":"The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability","volume":"94","author":"MV Tsodyks","year":"1997","journal-title":"Proceedings of the national academy of sciences"},{"issue":"4","key":"pcbi.1008533.ref041","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1162\/089976698300017502","article-title":"Neural networks with dynamic synapses","volume":"10","author":"M yks","year":"1998","journal-title":"Neural computation"},{"issue":"9","key":"pcbi.1008533.ref042","doi-asserted-by":"crossref","first-page":"5323","DOI":"10.1073\/pnas.95.9.5323","article-title":"Differential signaling via the same axon of neocortical pyramidal neurons","volume":"95","author":"H Markram","year":"1998","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1008533.ref043","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1523\/JNEUROSCI.20-01-j0003.2000","article-title":"Synchrony generation in recurrent networks with frequency-dependent synapses","volume":"20","author":"M Tsodyks","year":"2000","journal-title":"J Neurosci"},{"issue":"9","key":"pcbi.1008533.ref044","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1003823","article-title":"Clique of functional hubs orchestrates population bursts in developmentally regulated neural networks","volume":"10","author":"S Luccioli","year":"2014","journal-title":"PLoS Computational Biology"},{"issue":"1","key":"pcbi.1008533.ref045","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0006-3495(72)86068-5","article-title":"Excitatory and inhibitory interactions in localized populations of model neurons","volume":"12","author":"HR Wilson","year":"1972","journal-title":"Biophysical journal"},{"issue":"2","key":"pcbi.1008533.ref046","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.neuron.2016.12.004","article-title":"Synaptic correlates of working memory capacity","volume":"93","author":"Y Mi","year":"2017","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1008533.ref047","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1073\/pnas.1619449114","article-title":"Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex","volume":"114","author":"JD Murray","year":"2017","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"12","key":"pcbi.1008533.ref048","doi-asserted-by":"crossref","first-page":"3207","DOI":"10.1162\/NECO_a_00525","article-title":"Complete classification of the macroscopic behavior of a heterogeneous network of theta neurons","volume":"25","author":"TB Luke","year":"2013","journal-title":"Neural computation"},{"issue":"1","key":"pcbi.1008533.ref049","doi-asserted-by":"crossref","first-page":"010901","DOI":"10.1103\/PhysRevE.90.010901","article-title":"Derivation of a neural field model from a network of theta neurons","volume":"90","author":"CR Laing","year":"2014","journal-title":"Physical Review E"},{"key":"pcbi.1008533.ref050","first-page":"021028","article-title":"Macroscopic Description for Networks of Spiking Neurons","volume":"5","author":"E Montbri\u00f3","year":"2015","journal-title":"Phys Rev X"},{"issue":"2","key":"pcbi.1008533.ref051","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1137\/0146017","article-title":"Parabolic bursting in an excitable system coupled with a slow oscillation","volume":"46","author":"GB Ermentrout","year":"1986","journal-title":"SIAM Journal on Applied Mathematics"},{"issue":"3","key":"pcbi.1008533.ref052","doi-asserted-by":"crossref","first-page":"037113","DOI":"10.1063\/1.2930766","article-title":"Low dimensional behavior of large systems of globally coupled oscillators","volume":"18","author":"E Ott","year":"2008","journal-title":"Chaos: An Interdisciplinary Journal of Nonlinear Science"},{"issue":"12","key":"pcbi.1008533.ref053","doi-asserted-by":"crossref","first-page":"e1005881","DOI":"10.1371\/journal.pcbi.1005881","article-title":"Firing rate equations require a spike synchrony mechanism to correctly describe fast oscillations in inhibitory networks","volume":"13","author":"F Devalle","year":"2017","journal-title":"PLoS computational biology"},{"key":"pcbi.1008533.ref054","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1002\/9781119159193.ch37","article-title":"Phase oscillator network models of brain dynamics","author":"CR Laing","year":"2017","journal-title":"Computational models of brain and behavior"},{"key":"pcbi.1008533.ref055","first-page":"1","volume-title":"Nonlinear Dynamics in Computational Neuroscience","author":"S Coombes","year":"2019"},{"issue":"5","key":"pcbi.1008533.ref056","doi-asserted-by":"crossref","first-page":"e1007019","DOI":"10.1371\/journal.pcbi.1007019","article-title":"Macroscopic phase resetting-curves determine oscillatory coherence and signal transfer in inter-coupled neural circuits","volume":"15","author":"G Dumont","year":"2019","journal-title":"PLoS computational biology"},{"issue":"12","key":"pcbi.1008533.ref057","doi-asserted-by":"crossref","first-page":"128301","DOI":"10.1103\/PhysRevLett.121.128301","article-title":"Transition from asynchronous to oscillatory dynamics in balanced spiking networks with instantaneous synapses","volume":"121","author":"M di Volo","year":"2018","journal-title":"Physical review letters"},{"issue":"47","key":"pcbi.1008533.ref058","article-title":"Theta-nested gamma oscillations in next generation neural mass models","volume":"14","author":"M Segneri","year":"2020","journal-title":"Front Comput Neurosci"},{"issue":"5","key":"pcbi.1008533.ref059","doi-asserted-by":"crossref","first-page":"053121","DOI":"10.1063\/1.5125216","article-title":"Cross frequency coupling in next generation inhibitory neural mass models","volume":"30","author":"A Ceni","year":"2020","journal-title":"Chaos: An Interdisciplinary Journal of Nonlinear Science"},{"issue":"1","key":"pcbi.1008533.ref060","doi-asserted-by":"crossref","first-page":"013042","DOI":"10.1103\/PhysRevResearch.2.013042","article-title":"Coexistence of fast and slow gamma oscillations in one population of inhibitory spiking neurons","volume":"2","author":"H Bi","year":"2020","journal-title":"Physical Review Research"},{"issue":"12","key":"pcbi.1008533.ref061","doi-asserted-by":"crossref","first-page":"4440","DOI":"10.1523\/JNEUROSCI.5062-09.2010","article-title":"The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats","volume":"30","author":"M Okun","year":"2010","journal-title":"Journal of neuroscience"},{"issue":"12","key":"pcbi.1008533.ref062","doi-asserted-by":"crossref","first-page":"4496","DOI":"10.1523\/JNEUROSCI.6041-09.2010","article-title":"Oscillatory correlates of vibrotactile frequency processing in human working memory","volume":"30","author":"B Spitzer","year":"2010","journal-title":"Journal of Neuroscience"},{"issue":"7067","key":"pcbi.1008533.ref063","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/nature04171","article-title":"Neural measures reveal individual differences in controlling access to working memory","volume":"438","author":"EK Vogel","year":"2005","journal-title":"Nature"},{"issue":"3","key":"pcbi.1008533.ref064","first-page":"237","article-title":"Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex","volume":"7","author":"DJ Amit","year":"1997","journal-title":"Cerebral cortex (New York, NY: 1991)"},{"issue":"6","key":"pcbi.1008533.ref065","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"},{"issue":"1","key":"pcbi.1008533.ref066","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13408-020-00082-z","article-title":"Mesoscopic population equations for spiking neural networks with synaptic short-term plasticity","volume":"10","author":"V Schmutz","year":"2020","journal-title":"The Journal of Mathematical Neuroscience"},{"issue":"6","key":"pcbi.1008533.ref067","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/j.neuron.2009.09.009","article-title":"Cortical enlightenment: are attentional gamma oscillations driven by ING or PING?","volume":"63","author":"P Tiesinga","year":"2009","journal-title":"Neuron"},{"issue":"31","key":"pcbi.1008533.ref068","doi-asserted-by":"crossref","first-page":"12828","DOI":"10.1073\/pnas.1303270110","article-title":"Flexible frequency control of cortical oscillations enables computations required for working memory","volume":"110","author":"M Dipoppa","year":"2013","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"7","key":"pcbi.1008533.ref069","doi-asserted-by":"crossref","first-page":"2694","DOI":"10.1523\/JNEUROSCI.0567-09.2010","article-title":"Hippocampal gamma oscillations increase with memory load","volume":"30","author":"MK van Vugt","year":"2010","journal-title":"Journal of Neuroscience"},{"issue":"36","key":"pcbi.1008533.ref070","doi-asserted-by":"crossref","first-page":"12411","DOI":"10.1523\/JNEUROSCI.0421-12.2012","article-title":"Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory","volume":"32","author":"F Roux","year":"2012","journal-title":"Journal of Neuroscience"},{"issue":"1","key":"pcbi.1008533.ref071","first-page":"1","article-title":"Competition between items in working memory leads to forgetting","volume":"5","author":"JA Lewis-Peacock","year":"2014","journal-title":"Nature Communications"},{"key":"pcbi.1008533.ref072","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4419-6987-3","volume-title":"Transient chaos: complex dynamics on finite time scales","author":"YC Lai","year":"2011"},{"issue":"41","key":"pcbi.1008533.ref073","doi-asserted-by":"crossref","first-page":"16610","DOI":"10.1073\/pnas.1316071110","article-title":"Short-term synaptic plasticity in the deterministic Tsodyks\u2013Markram model leads to unpredictable network dynamics","volume":"110","author":"JM Cortes","year":"2013","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1008533.ref074","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/2190-8567-2-12","article-title":"Stability of the splay state in networks of pulse-coupled neurons","volume":"2","author":"S Olmi","year":"2012","journal-title":"The Journal of Mathematical Neuroscience"},{"issue":"2","key":"pcbi.1008533.ref075","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1080\/17470216508416422","article-title":"Short-term temporal changes in free recall","volume":"17","author":"L Postman","year":"1965","journal-title":"Quarterly journal of experimental psychology"},{"key":"pcbi.1008533.ref076","doi-asserted-by":"crossref","first-page":"6","DOI":"10.3389\/fnhum.2014.00006","article-title":"Primacy and recency effects as indices of the focus of attention","volume":"8","author":"AB Morrison","year":"2014","journal-title":"Frontiers in human neuroscience"},{"issue":"9","key":"pcbi.1008533.ref077","doi-asserted-by":"crossref","first-page":"3772","DOI":"10.1093\/cercor\/bhv182","article-title":"Stimulus load and oscillatory activity in higher cortex","volume":"26","author":"S Kornblith","year":"2016","journal-title":"Cerebral Cortex"},{"issue":"1","key":"pcbi.1008533.ref078","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1017\/S0140525X01003922","article-title":"The magical number 4 in short-term memory: A reconsideration of mental storage capacity","volume":"24","author":"N Cowan","year":"2001","journal-title":"Behavioral and brain sciences"},{"issue":"1","key":"pcbi.1008533.ref079","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1177\/0963721409359277","article-title":"The magical mystery four: How is working memory capacity limited, and why?","volume":"19","author":"N Cowan","year":"2010","journal-title":"Current directions in psychological science"},{"issue":"4","key":"pcbi.1008533.ref080","doi-asserted-by":"crossref","first-page":"042214","DOI":"10.1103\/PhysRevE.98.042214","article-title":"Dynamics of a large system of spiking neurons with synaptic delay","volume":"98","author":"F Devalle","year":"2018","journal-title":"Physical Review E"},{"issue":"4","key":"pcbi.1008533.ref081","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1038\/nn1670","article-title":"Heterogeneity in the pyramidal network of the medial prefrontal cortex","volume":"9","author":"Y Wang","year":"2006","journal-title":"Nature neuroscience"},{"key":"pcbi.1008533.ref082","unstructured":"Doedel EJ, Fairgrieve TF, Sandstede B, Champneys AR, Kuznetsov YA, Wang X. AUTO-07P: Continuation and bifurcation software for ordinary differential equations; 2007."},{"key":"pcbi.1008533.ref083","unstructured":"Dayan P, Abbott LF. Theoretical neuroscience: computational and mathematical modeling of neural systems. Computational Neuroscience Series; 2001."},{"key":"pcbi.1008533.ref084","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":"12","key":"pcbi.1008533.ref085","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1000239","article-title":"Encoding of Naturalistic Stimuli by Local Field Potential Spectra in Networks of Excitatory and Inhibitory Neurons","volume":"4","author":"A Mazzoni","year":"2008","journal-title":"PLOS Computational Biology"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1008533","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,12,29]],"date-time":"2020-12-29T00:00:00Z","timestamp":1609200000000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008533","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,29]],"date-time":"2020-12-29T14:20:07Z","timestamp":1609251607000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008533"}},"subtitle":[],"editor":[{"given":"Peter Neal","family":"Taylor","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2020,12,15]]},"references-count":85,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2020,12,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1008533","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.06.24.168880","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,15]]}}}