{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T07:17:31Z","timestamp":1780471051909,"version":"3.54.1"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2021,4,18]],"date-time":"2021-04-18T00:00:00Z","timestamp":1618704000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["T32-NS073547"],"award-info":[{"award-number":["T32-NS073547"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","award":["5F31MH094076"],"award-info":[{"award-number":["5F31MH094076"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000053","name":"The National Eye Institute","doi-asserted-by":"publisher","award":["R01-EY012135"],"award-info":[{"award-number":["R01-EY012135"]}],"id":[{"id":"10.13039\/100000053","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,7,29]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Working memory, the ability to maintain and transform information, is critical for cognition. Spatial working memory is particularly well studied. The premier model for spatial memory is the continuous attractor network, which posits that cells maintain constant activity over memory periods. Alternative models propose complex dynamics that result in a variety of cell activity time courses. We recorded from neurons in the frontal eye fields and dorsolateral prefrontal cortex of 2 macaques during long (5\u201315\u00a0s) memory periods. We found that memory cells turn on early after stimulus presentation, sustain activity for distinct and fixed lengths of time, then turn off and stay off for the remainder of the memory period. These dynamics are more complex than the dynamics of a canonical bump attractor network model (either decaying or nondecaying) but more constrained than the dynamics of fully heterogeneous memory models. We speculate that memory may be supported by multiple attractor networks working in parallel, with each network having its own characteristic mean turn-off time such that mnemonic resources are gradually freed up over time.<\/jats:p>","DOI":"10.1093\/cercor\/bhab079","type":"journal-article","created":{"date-parts":[[2021,3,21]],"date-time":"2021-03-21T04:06:50Z","timestamp":1616299610000},"page":"4206-4219","source":"Crossref","is-referenced-by-count":5,"title":["Primate Spatial Memory Cells Become Tuned Early and Lose Tuning at Cell-Specific Times"],"prefix":"10.1093","volume":"31","author":[{"given":"Charalampos","family":"Papadimitriou","sequence":"first","affiliation":[{"name":"Department of Neuroscience, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles D","family":"Holmes","sequence":"additional","affiliation":[{"name":"Department of Neuroscience, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA"},{"name":"Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lawrence H","family":"Snyder","sequence":"additional","affiliation":[{"name":"Department of Neuroscience, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA"},{"name":"Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,4,19]]},"reference":[{"key":"2022041900013713900_ref1","volume-title":"Modeling brain function: the world of attractor neural networks","author":"Amit","year":"1992"},{"key":"2022041900013713900_ref2","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1093\/cercor\/7.3.237","article-title":"Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex","volume":"7","author":"Amit","year":"1997","journal-title":"Cereb Cortex"},{"key":"2022041900013713900_ref3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms1476","article-title":"Information processing using a single dynamical node as complex system","volume":"2","author":"Appeltant","year":"2011","journal-title":"Nat Commun."},{"key":"2022041900013713900_ref4","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S0896-6273(03)00597-X","article-title":"Dynamics of population code for working memory in the prefrontal cortex","volume":"40","author":"Baeg","year":"2003","journal-title":"Neuron"},{"key":"2022041900013713900_ref5","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.pneurobio.2013.02.002","article-title":"From fixed points to chaos: three models of delayed discrimination","volume":"103","author":"Barak","year":"2013","journal-title":"Prog Neurobiol"},{"key":"2022041900013713900_ref6","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1167\/9.10.7","article-title":"The precision of visual working memory is set by allocation of a shared resource","volume":"9","author":"Bays","year":"2009","journal-title":"J Vis"},{"key":"2022041900013713900_ref7","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/nn.2752","article-title":"A reservoir of time constants for memory traces in cortical neurons","volume":"14","author":"Bernacchia","year":"2011","journal-title":"Nat Neurosci"},{"key":"2022041900013713900_ref8","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1093\/cercor\/bhg100","article-title":"Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex","volume":"13","author":"Brody","year":"2003","journal-title":"Cereb Cortex"},{"key":"2022041900013713900_ref9","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1152\/jn.1985.53.3.603","article-title":"Primate frontal eye fields. I. Single neurons discharging before saccades","volume":"53","author":"Bruce","year":"1985","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref10","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1162\/neco.1996.8.8.1677","article-title":"Hebbian learning of context in recurrent neural networks","volume":"8","author":"Brunel","year":"1996","journal-title":"Neural Comput"},{"key":"2022041900013713900_ref11","doi-asserted-by":"crossref","first-page":"2919","DOI":"10.1152\/jn.1998.79.6.2919","article-title":"Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task","volume":"79","author":"Chafee","year":"1998","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref12","doi-asserted-by":"crossref","first-page":"10907","DOI":"10.1523\/JNEUROSCI.1450-12.2012","article-title":"Persistent spatial information in the frontal eye field during object-based short-term memory","volume":"32","author":"Clark","year":"2012","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref13","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","year":"2000","journal-title":"Cereb Cortex"},{"key":"2022041900013713900_ref14","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/85179","article-title":"The sensory nature of mnemonic representation in the primate prefrontal cortex","volume":"4","author":"Constantinidis","year":"2001","journal-title":"Nat Neurosci"},{"key":"2022041900013713900_ref15","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":"Constantinidis","year":"2018","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref16","doi-asserted-by":"crossref","first-page":"3487","DOI":"10.1152\/jn.00188.2002","article-title":"Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex","volume":"88","author":"Constantinidis","year":"2002","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref17","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1097\/00001756-199904260-00030","article-title":"Activity of prefrontal neurons during location and color delayed matching tasks","volume":"10","author":"Ferrera","year":"1999","journal-title":"Neuroreport"},{"key":"2022041900013713900_ref18","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","year":"1989","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref19","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1038\/365753a0","article-title":"Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task","volume":"365","author":"Funahashi","year":"1993","journal-title":"Nature"},{"key":"2022041900013713900_ref20","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":"Fuster","year":"1971","journal-title":"Science"},{"key":"2022041900013713900_ref21","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1002\/(SICI)1096-9861(19960122)364:4<567::AID-CNE1>3.0.CO;2-1","article-title":"Local circuit neurons in the medial prefrontal cortex (areas 24a, b, c, 25 and 32) in the monkey: I. Cell morphology and morphometrics","volume":"364","author":"Gabbott","year":"1996","journal-title":"J Comp Neurol"},{"key":"2022041900013713900_ref22","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.neuron.2008.12.012","article-title":"Memory without feedback in a neural network","volume":"61","author":"Goldman","year":"2009","journal-title":"Neuron"},{"key":"2022041900013713900_ref23","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1038\/nature10918","article-title":"Choice-specific sequences in parietal cortex during a virtual-navigation decision task","volume":"484","author":"Harvey","year":"2012","journal-title":"Nature"},{"key":"2022041900013713900_ref24","doi-asserted-by":"crossref","first-page":"8177","DOI":"10.1523\/JNEUROSCI.3629-17.2018","article-title":"Dissociation of LFP power and tuning in the frontal cortex during memory","volume":"38","author":"Holmes","year":"2018","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref25","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1523\/JNEUROSCI.2062-09.2010","article-title":"Heterogenous population coding of a short-term memory and decision task","volume":"30","author":"Jun","year":"2010","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref26","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/0006-8993(82)91145-3","article-title":"Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response","volume":"248","author":"Kojima","year":"1982","journal-title":"Brain Res"},{"key":"2022041900013713900_ref27","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1152\/jn.00214.2005","article-title":"Delay-period activity in visual, visuomovement, and movement neurons in the frontal eye field","volume":"94","author":"Lawrence","year":"2005","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref28","doi-asserted-by":"crossref","first-page":"2405","DOI":"10.1093\/cercor\/bhx142","article-title":"A quadrantic bias in prefrontal representation of visual-mnemonic space","volume":"28","author":"Leavitt","year":"2018","journal-title":"Cereb Cortex"},{"key":"2022041900013713900_ref29","doi-asserted-by":"crossref","first-page":"7013","DOI":"10.1523\/JNEUROSCI.2485-17.2018","article-title":"Working memory: delay activity, yes! Persistent activity? Maybe not","volume":"38","author":"Lundqvist","year":"2018","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref30","doi-asserted-by":"crossref","first-page":"2531","DOI":"10.1162\/089976602760407955","article-title":"Real-time computing without stable states: a new framework for neural computation based on perturbations","volume":"14","author":"Maass","year":"2002","journal-title":"Neural Comput"},{"key":"2022041900013713900_ref31","doi-asserted-by":"crossref","first-page":"11084","DOI":"10.1073\/pnas.1504172112","article-title":"Multiple component networks support working memory in prefrontal cortex","volume":"112","author":"Markowitz","year":"2015","journal-title":"Proc Natl Acad Sci"},{"key":"2022041900013713900_ref32","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":"Mendoza-Halliday","year":"2014","journal-title":"Nat Neurosci"},{"key":"2022041900013713900_ref33","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","year":"2017","journal-title":"Proc Natl Acad Sci"},{"key":"2022041900013713900_ref34","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1523\/JNEUROSCI.13-03-01227.1993","article-title":"Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate","volume":"13","author":"Pellegrino","year":"1993","journal-title":"J Neurosci"},{"key":"2022041900013713900_ref35","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":"Romo","year":"1999","journal-title":"Nature"},{"key":"2022041900013713900_ref36","volume-title":"Bashtage\/arch: Release 4.15","author":"Sheppard","year":"2020"},{"key":"2022041900013713900_ref37","doi-asserted-by":"crossref","first-page":"1673","DOI":"10.1152\/jn.2001.85.4.1673","article-title":"Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus","volume":"85","author":"Sommer","year":"2001","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref38","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/j.tics.2015.05.004","article-title":"Activity-silent\u2019working memory in prefrontal cortex: a dynamic coding framework","volume":"19","author":"Stokes","year":"2015","journal-title":"Trends Cogn Sci"},{"key":"2022041900013713900_ref39","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.neuron.2013.01.039","article-title":"Dynamic coding for cognitive control in prefrontal cortex","volume":"78","author":"Stokes","year":"2013","journal-title":"Neuron"},{"key":"2022041900013713900_ref40","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1152\/jn.00249.2001","article-title":"Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks","volume":"87","author":"Takeda","year":"2002","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref41","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.1093\/cercor\/bhh093","article-title":"Population vector analysis of primate prefrontal activity during spatial working memory","volume":"14","author":"Takeda","year":"2004","journal-title":"Cereb Cortex"},{"key":"2022041900013713900_ref42","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1152\/jn.2001.86.5.2344","article-title":"Spatial processing in the monkey frontal eye field. II. Memory responses","volume":"86","author":"Umeno","year":"2001","journal-title":"J Neurophysiol"},{"key":"2022041900013713900_ref43","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.21105\/joss.01026","article-title":"Pingouin: statistics in python","volume":"3","author":"Vallat","year":"2018","journal-title":"J Open Source Software"},{"key":"2022041900013713900_ref44","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.neunet.2007.04.003","article-title":"An experimental unification of reservoir computing methods","volume":"20","author":"Verstraeten","year":"2007","journal-title":"Neural Netw"},{"key":"2022041900013713900_ref45","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":"Virtanen","year":"2020","journal-title":"Nat Methods"},{"key":"2022041900013713900_ref46","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/B978-008045046-9.01397-8","volume-title":"Encyclopedia of neuroscience","author":"Wang","year":"2009"},{"key":"2022041900013713900_ref47","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1073\/pnas.0305337101","article-title":"Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory","volume":"101","author":"Wang","year":"2004","journal-title":"Proc Natl Acad Sci"},{"key":"2022041900013713900_ref48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-018-05961-4","article-title":"Intrinsic neuronal dynamics predict distinct functional roles during working memory","volume":"9","author":"Wasmuht","year":"2018","journal-title":"Nat Commun"},{"key":"2022041900013713900_ref49","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/nn.3645","article-title":"Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory","volume":"17","author":"Wimmer","year":"2014","journal-title":"Nat Neurosci"},{"key":"2022041900013713900_ref50","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1111\/j.1467-9280.2009.02322.x","article-title":"Sudden death and gradual decay in visual working memory","volume":"20","author":"Zhang","year":"2009","journal-title":"Psychol Sci"},{"key":"2022041900013713900_ref51","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1152\/jn.01151.2011","article-title":"Neurons with inverted tuning during the delay periods of working memory tasks in the dorsal prefrontal and posterior parietal cortex","volume":"108","author":"Zhou","year":"2012","journal-title":"J Neurophysiol"}],"container-title":["Cerebral Cortex"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/cercor\/article-pdf\/31\/9\/4206\/39376616\/bhab079.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cercor\/article-pdf\/31\/9\/4206\/39376616\/bhab079.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,19]],"date-time":"2022-04-19T00:04:00Z","timestamp":1650326640000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cercor\/article\/31\/9\/4206\/6236058"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,19]]},"references-count":51,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,4,19]]},"published-print":{"date-parts":[[2021,7,29]]}},"URL":"https:\/\/doi.org\/10.1093\/cercor\/bhab079","relation":{},"ISSN":["1047-3211","1460-2199"],"issn-type":[{"value":"1047-3211","type":"print"},{"value":"1460-2199","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,9]]},"published":{"date-parts":[[2021,4,19]]}}}