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The model provides a demonstration of how information can be usefully stored in the temporal patterns of activity in a neuronal network rather than just synaptic weights between the neurons in that network.<\/jats:p>","DOI":"10.1073\/pnas.1902305116","type":"journal-article","created":{"date-parts":[[2019,8,1]],"date-time":"2019-08-01T20:07:04Z","timestamp":1564690024000},"page":"16613-16620","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":46,"title":["Parietal low beta rhythm provides a dynamical substrate for a working memory buffer"],"prefix":"10.1073","volume":"116","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1428-0130","authenticated-orcid":false,"given":"Alexandros","family":"Gelastopoulos","sequence":"first","affiliation":[{"name":"Department of Mathematics and Statistics, Boston University, Boston, MA 02215;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0247-1362","authenticated-orcid":false,"given":"Miles A.","family":"Whittington","sequence":"additional","affiliation":[{"name":"Centre for Neuroscience, University of York, York YO10 5DD, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8568-8750","authenticated-orcid":false,"given":"Nancy J.","family":"Kopell","sequence":"additional","affiliation":[{"name":"Department of Mathematics and Statistics, Boston University, Boston, MA 02215;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2019,8]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1162\/08989290152541476","article-title":"The neural substrate of orientation working memory","volume":"13","author":"Cornette L.","year":"2001","unstructured":"L. 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Brain Res."},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9781139174909","volume-title":"Models of Working Memory: Mechanisms of Active Maintenance and Executive Control","author":"Miyake A.","year":"1999","unstructured":"A. Miyake, P. Shah, Models of Working Memory: Mechanisms of Active Maintenance and Executive Control (Cambridge Univ Press, 1999)."},{"key":"e_1_3_4_5_2","first-page":"47","volume-title":"Psychology of Learning and Motivation","author":"Baddeley A. D.","year":"1974","unstructured":"A. D. Baddeley, G. Hitch, \u201cWorking memory\u201d in Psychology of Learning and Motivation, G. H. Bower, Ed. (Elsevier, 1974), Vol. 8, pp. 47\u201389."},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1017\/S0140525X00044411","article-title":"Neuropsychological evidence and the semantic\/episodic distinction","volume":"7","author":"Baddeley A. D.","year":"1984","unstructured":"A. D. 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Brain Res."},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"3849","DOI":"10.1523\/JNEUROSCI.0097-10.2010","article-title":"Dissociation within the frontoparietal network in verbal working memory: A parametric functional magnetic resonance imaging study","volume":"30","author":"Champod A. S.","year":"2010","unstructured":"A. S. Champod, M. Petrides, Dissociation within the frontoparietal network in verbal working memory: A parametric functional magnetic resonance imaging study. J. Neurosci. 30, 3849\u20133856 (2010).","journal-title":"J. Neurosci."},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1038\/72991","article-title":"A multimodal cortical network for the detection of changes in the sensory environment","volume":"3","author":"Downar J.","year":"2000","unstructured":"J. Downar, A. P. Crawley, D. J. Mikulis, K. D. Davis, A multimodal cortical network for the detection of changes in the sensory environment. Nat. 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Kramer , Rhythm generation through period concatenation in rat somatosensory cortex. PLoS Comput. Biol. 4, e1000169 (2008).","journal-title":"PLoS Comput. Biol."},{"key":"e_1_3_4_24_2","first-page":"8","article-title":"Cholinergic neuromodulation controls directed temporal communication in neocortex in vitro","volume":"4","author":"Roopun A. K.","year":"2010","unstructured":"A. K. Roopun , Cholinergic neuromodulation controls directed temporal communication in neocortex in vitro. Front. Neural Circuits 4, 8 (2010).","journal-title":"Front. Neural Circuits"},{"key":"e_1_3_4_25_2","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":"Tallon-Baudry C.","year":"1998","unstructured":"C. Tallon-Baudry, O. Bertrand, F. Peronnet, J. Pernier, Induced \u03b3-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 18, 4244\u20134254 (1998).","journal-title":"J. Neurosci."},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.tins.2007.05.001","article-title":"Human gamma-frequency oscillations associated with attention and memory","volume":"30","author":"Jensen O.","year":"2007","unstructured":"O. Jensen, J. Kaiser, J. P. Lachaux, Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 30, 317\u2013324 (2007).","journal-title":"Trends Neurosci."},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"576","DOI":"10.3389\/fnhum.2017.00576","article-title":"Gamma and beta oscillations in human meg encode the contents of vibrotactile working memory","volume":"11","author":"Lautz V.","year":"2017","unstructured":"V. Lautz , Gamma and beta oscillations in human meg encode the contents of vibrotactile working memory. Front. Hum. Neurosci. 11, 576 (2017).","journal-title":"Front. Hum. Neurosci."},{"key":"e_1_3_4_28_2","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":"Kopell N.","year":"2011","unstructured":"N. Kopell, M. Whittington, M. Kramer, Neuronal assembly dynamics in the beta1 frequency range permits short-term memory. Proc. Natl. Acad. Sci. U.S.A. 108, 3779\u20133784 (2011).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_29_2","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":"Compte A.","year":"2000","unstructured":"A. Compte, N. Brunel, P. S. Goldman-Rakic, X. J. Wang, Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb. Cortex 10, 910\u2013923 (2000).","journal-title":"Cereb. Cortex"},{"key":"e_1_3_4_30_2","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":"Lundqvist M.","year":"2016","unstructured":"M. Lundqvist , Gamma and beta bursts underlie working memory. Neuron 90, 152\u2013164 (2016).","journal-title":"Neuron"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1038\/s41467-017-02791-8","article-title":"Gamma and beta bursts during working memory readout suggest roles in its volitional control","volume":"9","author":"Lundqvist M.","year":"2018","unstructured":"M. Lundqvist, P. Herman, M. R. Warden, S. L. Brincat, E. K. Miller, Gamma and beta bursts during working memory readout suggest roles in its volitional control. Nat. Commun. 9, 394 (2018).","journal-title":"Nat. Commun."},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"1860","DOI":"10.1126\/science.1138071","article-title":"Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices","volume":"315","author":"Buschman T. J.","year":"2007","unstructured":"T. J. Buschman, E. K. Miller, Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860\u20131862 (2007).","journal-title":"Science"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"6698","DOI":"10.1523\/JNEUROSCI.3771-16.2017","article-title":"Top-down beta enhances bottom-up gamma","volume":"37","author":"Richter C. G.","year":"2017","unstructured":"C. G. Richter, W. H. Thompson, C. A. Bosman, P. Fries, Top-down beta enhances bottom-up gamma. J. Neurosci. 37, 6698\u20136711 (2017).","journal-title":"J. Neurosci."},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"13687","DOI":"10.1073\/pnas.1517629112","article-title":"Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks","volume":"112","author":"Feingold J.","year":"2015","unstructured":"J. Feingold, D. J. Gibson, B. DePasquale, A. M. Graybiel, Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks. Proc. Natl. Acad. Sci. U.S.A. 112, 13687\u201313692 (2015).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"E4885","DOI":"10.1073\/pnas.1604135113","article-title":"Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice","volume":"113","author":"Sherman M. A.","year":"2016","unstructured":"M. A. Sherman , Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice. Proc. Natl. Acad. Sci. U.S.A. 113, E4885\u2013E4894 (2016).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"433","DOI":"10.3389\/fpsyg.2013.00433","article-title":"What is working memory capacity, and how can we measure it?","volume":"4","author":"Wilhelm O.","year":"2013","unstructured":"O. Wilhelm, A. H. Hildebrandt, K. Oberauer, What is working memory capacity, and how can we measure it? Front. Psychol. 4, 433 (2013).","journal-title":"Front. Psychol."},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1038\/nature08935","article-title":"Lateral competition for cortical space by layer-specific horizontal circuits","volume":"464","author":"Adesnik H.","year":"2012","unstructured":"H. Adesnik, M. Scanziani, Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155\u20131160 (2012).","journal-title":"Nature"},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.pneurobio.2011.06.002","article-title":"Cholinergic modulation of cognition: Insights from human pharmacological functional neuroimaging","volume":"94","author":"Bentley P.","year":"2011","unstructured":"P. Bentley, J. Driver, R. J. Dolan, Cholinergic modulation of cognition: Insights from human pharmacological functional neuroimaging. Prog. Neurobiol. 94, 360\u2013388 (2011).","journal-title":"Prog. Neurobiol."},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"2215","DOI":"10.1152\/jn.00493.2006","article-title":"Heterogeneity of phasic cholinergic signaling in neocortical neurons","volume":"97","author":"Gulledge A. T.","year":"2007","unstructured":"A. T. Gulledge, S. B. Park, Y. Kawaguchi, G. J. Stuart, Heterogeneity of phasic cholinergic signaling in neocortical neurons. J. Neurophysiol. 97, 2215\u20132229 (2007).","journal-title":"J. Neurophysiol."},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"aac9462","DOI":"10.1126\/science.aac9462","article-title":"Principles of connectivity among morphologically defined cell types in adult neocortex","volume":"350","author":"Jiang X.","year":"2015","unstructured":"X. Jiang , Principles of connectivity among morphologically defined cell types in adult neocortex. Science 350, aac9462 (2015).","journal-title":"Science"},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1038\/nn.4554","article-title":"Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior","volume":"20","author":"Kamigaki T.","year":"2017","unstructured":"T. Kamigaki, Y. Dan, Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior. Nat. Neurosci. 20, 854\u2013863 (2017).","journal-title":"Nat. Neurosci."},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","first-page":"11519","DOI":"10.1523\/JNEUROSCI.1157-14.2014","article-title":"A class of gabaergic neurons in the prefrontal cortex sends long-range projections to the nucleus accumbens and elicits acute avoidance behavior","volume":"34","author":"Lee A. T.","year":"2014","unstructured":"A. T. Lee, D. Vogt, J. L. Rubenstein, V. S. Sohal, A class of gabaergic neurons in the prefrontal cortex sends long-range projections to the nucleus accumbens and elicits acute avoidance behavior. J. Neurosci. 34, 11519\u201311525 (2014).","journal-title":"J. Neurosci."},{"key":"e_1_3_4_43_2","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":"Funahashi S.","year":"1989","unstructured":"S. Funahashi, C. J. Bruce, P. S. Goldman-Rakic, Mnemonic coding of visual space in the monkey\u2019s dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331\u2013349 (1989).","journal-title":"J. Neurophysiol."},{"key":"e_1_3_4_44_2","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":"Murray J. D.","year":"2017","unstructured":"J. D. Murray , Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 114, 394\u2013399 (2017).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"7298","DOI":"10.1073\/pnas.0800360105","article-title":"Hyperpolarization-activated graded persistent activity in the prefrontal cortex","volume":"105","author":"Winograd M.","year":"2008","unstructured":"M. Winograd, A. 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