{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,23]],"date-time":"2026-07-23T23:27:06Z","timestamp":1784849226927,"version":"3.55.0"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1013097","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,6,26]],"date-time":"2025-06-26T00:00:00Z","timestamp":1750896000000}}],"reference-count":148,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2025,6,17]],"date-time":"2025-06-17T00:00:00Z","timestamp":1750118400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["MH135565"],"award-info":[{"award-number":["MH135565"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["NS118440"],"award-info":[{"award-number":["NS118440"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014989","name":"Chan Zuckerberg Initiative","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100014989","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["NSF-1757574"],"award-info":[{"award-number":["NSF-1757574"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Across vertebrate species, sleep consists of repeating cycles of NREM followed by REM. However, their respective functions, and their stereotypic cycling pattern are not well understood. Using a simplified biophysical network model, we investigate the potential role of cholinergic modulation, acting via the muscarinic receptors, on network dynamics and memory consolidation. We show that low and high cholinergic levels associated with NREM and REM sleep, respectively, may play critical, sequential roles in memory consolidation. The network dynamics that facilitate these roles arise through alteration of neural excitability and changes to network-wide excitatory\/inhibitory balance. At low acetylcholine (ACh) levels, reduced activation of inhibitory neurons leads to network-wide disinhibition and bursts of synchronized activity led by engram neurons, driving recruitment of additional excitatory neurons into the engram. In contrast, at high ACh levels, increased network inhibition suppresses firing in all but the most strongly recruited excitatory neurons, pruning the expanded engram population. Together, these results provide a testable hypothesis regarding the role of sleep state-specific cholinergic modulation in the process of memory consolidation.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1013097","type":"journal-article","created":{"date-parts":[[2025,6,17]],"date-time":"2025-06-17T17:56:33Z","timestamp":1750182993000},"page":"e1013097","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":14,"title":["Cholinergic modulation of neural networks supports sequential and complementary roles for NREM and REM states in memory consolidation"],"prefix":"10.1371","volume":"21","author":[{"given":"Michael","family":"Satchell","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edith","family":"Butel-Fry","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zahraa","family":"Noureddine","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexis","family":"Simmons","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolette","family":"Ognjanovski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara J.","family":"Aton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1722-986X","authenticated-orcid":true,"given":"Michal R.","family":"Zochowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,6,17]]},"reference":[{"key":"pcbi.1013097.ref001","doi-asserted-by":"crossref","first-page":"567618","DOI":"10.3389\/fpsyg.2020.567618","article-title":"Evolutionary origin of distinct NREM and REM sleep","volume":"11","author":"R Yamazaki","year":"2020","journal-title":"Front Psychol"},{"issue":"7","key":"pcbi.1013097.ref002","doi-asserted-by":"crossref","DOI":"10.1093\/sleep\/zsz095","article-title":"How rhythms of the sleeping brain tune memory and synaptic plasticity","volume":"42","author":"C Puentes-Mestril","year":"2019","journal-title":"Sleep"},{"key":"pcbi.1013097.ref003","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3389\/fncir.2017.00061","article-title":"Linking Network Activity to Synaptic Plasticity during Sleep: Hypotheses and Recent Data","volume":"11","author":"C Puentes-Mestril","year":"2017","journal-title":"Front Neural Circuits"},{"issue":"2","key":"pcbi.1013097.ref004","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1152\/physrev.00032.2012","article-title":"About sleep\u2019s role in memory","volume":"93","author":"B Rasch","year":"2013","journal-title":"Physiol Rev"},{"issue":"5544","key":"pcbi.1013097.ref005","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1126\/science.1063530","article-title":"Sleep, learning, and dreams: off-line memory reprocessing","volume":"294","author":"R Stickgold","year":"2001","journal-title":"Science"},{"key":"pcbi.1013097.ref006","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.1805517115","article-title":"Cortical circuit activity underlying sleep slow oscillations and spindles","volume":"115","author":"N Niethard","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"key":"pcbi.1013097.ref007","doi-asserted-by":"crossref","first-page":"65","DOI":"10.3389\/fncir.2017.00065","article-title":"Plasticity during Sleep Is Linked to Specific Regulation of Cortical Circuit Activity","volume":"11","author":"N Niethard","year":"2017","journal-title":"Front Neural Circuits"},{"key":"pcbi.1013097.ref008","doi-asserted-by":"crossref","first-page":"2739","DOI":"10.1016\/j.cub.2016.08.035","article-title":"Sleep-stage-specific regulation of cortical excitation and inhibition","volume":"26","author":"N Niethard","year":"2016","journal-title":"Curr Biol"},{"issue":"1","key":"pcbi.1013097.ref009","doi-asserted-by":"crossref","first-page":"4819","DOI":"10.1038\/s41467-020-18592-5","article-title":"REM sleep promotes experience-dependent dendritic spine elimination in the mouse cortex","volume":"11","author":"Y Zhou","year":"2020","journal-title":"Nat Commun"},{"issue":"6188","key":"pcbi.1013097.ref010","doi-asserted-by":"crossref","first-page":"1173","DOI":"10.1126\/science.1249098","article-title":"Sleep promotes branch-specific formation of dendritic spines after learning","volume":"344","author":"G Yang","year":"2014","journal-title":"Science"},{"issue":"11","key":"pcbi.1013097.ref011","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.1002\/dneu.20996","article-title":"Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex","volume":"72","author":"G Yang","year":"2012","journal-title":"Dev Neurobiol"},{"issue":"5","key":"pcbi.1013097.ref012","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1101\/lm.6.5.500","article-title":"Brain gene expression during REM sleep depends on prior waking experience","volume":"6","author":"S Ribeiro","year":"1999","journal-title":"Learn Mem"},{"key":"pcbi.1013097.ref013","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2019318118","article-title":"Sleep loss drives acetylcholine- and somatostatin interneuron-mediated gating of hippocampal activity to inhibit memory consolidation","volume":"118","author":"J Delorme","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref014","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3389\/fnsys.2014.00061","article-title":"CA1 hippocampal network activity changes during sleep-dependent memory consolidation","volume":"8","author":"N Ognjanovski","year":"2014","journal-title":"Front Syst Neurosci"},{"key":"pcbi.1013097.ref015","doi-asserted-by":"crossref","DOI":"10.1093\/cercor\/bhy174","article-title":"Hippocampal network oscillations rescue memory consolidation deficits caused by sleep loss","volume":"28","author":"N Ognjanovski","year":"2018","journal-title":"Cereb Cortex"},{"issue":"14","key":"pcbi.1013097.ref016","article-title":"Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation","volume":"8","author":"N Ognjanovski","year":"2017","journal-title":"Nat Commun"},{"issue":"39","key":"pcbi.1013097.ref017","doi-asserted-by":"crossref","first-page":"10485","DOI":"10.1073\/pnas.1710613114","article-title":"Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity","volume":"114","author":"J Durkin","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref018","doi-asserted-by":"crossref","first-page":"40","DOI":"10.3389\/fnsys.2018.00040","article-title":"Sleep promotes, and sleep loss inhibits, selective changes in firing rate, response properties and functional connectivity of primary visual cortex neurons","volume":"12","author":"BC Clawson","year":"2018","journal-title":"Front Syst Neurosci"},{"issue":"1","key":"pcbi.1013097.ref019","doi-asserted-by":"crossref","first-page":"155","DOI":"10.5665\/sleep.5338","article-title":"Sleep-dependent potentiation in the visual system is at odds with the synaptic homeostasis hypothesis","volume":"39","author":"J Durkin","year":"2016","journal-title":"Sleep"},{"issue":"1","key":"pcbi.1013097.ref020","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1038\/s41467-021-21471-2","article-title":"Causal role for sleep-dependent reactivation of learning-activated sensory ensembles for fear memory consolidation","volume":"12","author":"BC Clawson","year":"2021","journal-title":"Nat Commun"},{"issue":"6287","key":"pcbi.1013097.ref021","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1126\/science.aad5252","article-title":"Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation","volume":"352","author":"R Boyce","year":"2016","journal-title":"Science"},{"issue":"6291","key":"pcbi.1013097.ref022","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1126\/science.aaf0902","article-title":"Top-down cortical input during NREM sleep consolidates perceptual memory","volume":"352","author":"D Miyamoto","year":"2016","journal-title":"Science"},{"issue":"5","key":"pcbi.1013097.ref023","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1523\/JNEUROSCI.1950-18.2018","article-title":"Hippocampal Reactivation Extends for Several Hours Following Novel Experience","volume":"39","author":"B Giri","year":"2019","journal-title":"J Neurosci"},{"issue":"6594","key":"pcbi.1013097.ref024","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1126\/science.abk2734","article-title":"Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep","volume":"376","author":"M Aime","year":"2022","journal-title":"Science"},{"issue":"7","key":"pcbi.1013097.ref025","doi-asserted-by":"crossref","first-page":"890","DOI":"10.3390\/brainsci12070890","article-title":"The Neuromodulatory Role of the Noradrenergic and Cholinergic Systems and Their Interplay in Cognitive Functions: A Focused Review","volume":"12","author":"C Slater","year":"2022","journal-title":"Brain Sci"},{"key":"pcbi.1013097.ref026","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/j.jsmc.2010.08.003","article-title":"Neuropharmacology of sleep and wakefulness","volume":"5","author":"CJ Watson","year":"2010","journal-title":"Sleep Med Clin"},{"key":"pcbi.1013097.ref027","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.bbr.2010.11.037","article-title":"The cholinergic system and hippocampal plasticity","volume":"221","author":"BD Drever","year":"2011","journal-title":"Behav Brain Res"},{"key":"pcbi.1013097.ref028","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1196\/annals.1417.021","article-title":"Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity","volume":"1129","author":"V Parikh","year":"2008","journal-title":"Ann N Y Acad Sci"},{"key":"pcbi.1013097.ref029","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/fncir.2012.00005","article-title":"Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells","volume":"6","author":"C Barry","year":"2012","journal-title":"Front Neural Circuits"},{"issue":"2","key":"pcbi.1013097.ref030","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1073\/pnas.1703601115","article-title":"Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons","volume":"115","author":"X Li","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"pcbi.1013097.ref031","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1152\/physrev.1995.75.2.393","article-title":"The septohippocampal pathway: structure and function of a central cholinergic system","volume":"75","author":"P Dutar","year":"1995","journal-title":"Physiol Rev"},{"issue":"2","key":"pcbi.1013097.ref032","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1002\/cne.902390210","article-title":"Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study","volume":"239","author":"M Frotscher","year":"1985","journal-title":"J Comp Neurol"},{"issue":"3","key":"pcbi.1013097.ref033","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S0896-6273(02)00586-X","article-title":"Theta oscillations in the hippocampus","volume":"33","author":"G Buzs\u00e1ki","year":"2002","journal-title":"Neuron"},{"key":"pcbi.1013097.ref034","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1111\/jnc.14052","article-title":"Cholinergic modulation of the hippocampal region and memory fuction","volume":"142","author":"J Haam","year":"2017","journal-title":"Journal of Neurochemistry"},{"key":"pcbi.1013097.ref035","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1152\/physrev.00015.2008","article-title":"Mammalian nicotinic acetylcholine receptors: from structure to function","volume":"89","author":"E Albuquerque","year":"2009","journal-title":"Physiol Rev"},{"key":"pcbi.1013097.ref036","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-23274-9","volume-title":"Muscarinic receptors","author":"A Fryer","year":"2012"},{"issue":"4","key":"pcbi.1013097.ref037","doi-asserted-by":"crossref","first-page":"1888","DOI":"10.1046\/j.1471-4159.1995.64041888.x","article-title":"Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer\u2019s disease","volume":"64","author":"DD Flynn","year":"1995","journal-title":"J Neurochem"},{"issue":"24","key":"pcbi.1013097.ref038","doi-asserted-by":"crossref","first-page":"13541","DOI":"10.1073\/pnas.93.24.13541","article-title":"Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease","volume":"93","author":"AI Levey","year":"1996","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref039","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1152\/jn.00686.2010","article-title":"M1 and M4 receptors modulate hippocampal pyramidal neurons","volume":"105","author":"S Dasari","year":"2011","journal-title":"J Neurophysiol"},{"issue":"16","key":"pcbi.1013097.ref040","doi-asserted-by":"crossref","first-page":"3463","DOI":"10.1113\/jphysiol.2014.275453","article-title":"Direct excitation of parvalbumin-positive interneurons by M1 muscarinic acetylcholine receptors: roles in cellular excitability, inhibitory transmission and cognition","volume":"592","author":"F Yi","year":"2014","journal-title":"J Physiol"},{"key":"pcbi.1013097.ref041","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1113\/jphysiol.1984.sp015378","article-title":"Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro","volume":"354","author":"DV Madison","year":"1984","journal-title":"J Physiol"},{"issue":"3","key":"pcbi.1013097.ref042","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1523\/JNEUROSCI.07-03-00733.1987","article-title":"Voltage clamp analysis of cholinergic action in the hippocampus","volume":"7","author":"DV Madison","year":"1987","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref043","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-51171-9","volume-title":"An introduction to modeling neuronal dynamics","author":"C B\u00f6rgers","year":"2017"},{"issue":"5","key":"pcbi.1013097.ref044","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1162\/089976698300017331","article-title":"Dynamics of membrane excitability determine interspike interval variability: a link between spike generation mechanisms and cortical spike train statistics","volume":"10","author":"BS Gutkin","year":"1998","journal-title":"Neural Comput"},{"key":"pcbi.1013097.ref045","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.jphysparis.2003.09.005","article-title":"Mathematical neuroscience: from neurons to circuits to systems","volume":"97","author":"B Gutkin","year":"2003","journal-title":"J Physiol Paris"},{"key":"pcbi.1013097.ref046","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0003947","article-title":"Cholinergic neuromodulation changes phase response curve shape and type in cortical pyramidal neurons","volume":"3","author":"KM Stiefel","year":"2008","journal-title":"PLoS One"},{"key":"pcbi.1013097.ref047","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.neuropharm.2013.05.026","article-title":"Synaptic muscarinic response types in hippocampal CA1 interneurons depend on different levels of presynaptic activity and different muscarinic receptor subtypes","volume":"73","author":"LA Bell","year":"2013","journal-title":"Neuropharmacology"},{"key":"pcbi.1013097.ref048","doi-asserted-by":"crossref","first-page":"750541","DOI":"10.3389\/fncir.2021.750541","article-title":"The Engram\u2019s Dark Horse: How Interneurons Regulate State-Dependent Memory Processing and Plasticity","volume":"15","author":"F Raven","year":"2021","journal-title":"Front Neural Circuits"},{"key":"pcbi.1013097.ref049","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1038\/s41467-017-00205-3","article-title":"Hipp neurons in the dentate gyrus mediate the cholinergic modulation of background context memory salience","volume":"8","author":"SA Raza","year":"2017","journal-title":"Nat Commun"},{"issue":"6173","key":"pcbi.1013097.ref050","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1126\/science.1247485","article-title":"Dendritic inhibition in the hippocampus supports fear learning","volume":"343","author":"M Lovett-Barron","year":"2014","journal-title":"Science"},{"key":"pcbi.1013097.ref051","doi-asserted-by":"crossref","first-page":"32","DOI":"10.3389\/fncel.2018.00032","article-title":"Electrophysiological and Morphological Characterization of Chrna2 Cells in the Subiculum and CA1 of the Hippocampus: An Optogenetic Investigation","volume":"12","author":"H Nichol","year":"2018","journal-title":"Front Cell Neurosci"},{"issue":"5","key":"pcbi.1013097.ref052","doi-asserted-by":"crossref","first-page":"2640","DOI":"10.1152\/jn.90691.2008","article-title":"Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex","volume":"100","author":"EE Fanselow","year":"2008","journal-title":"J Neurophysiol"},{"issue":"6","key":"pcbi.1013097.ref053","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1038\/nn.4002","article-title":"An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity","volume":"18","author":"N Chen","year":"2015","journal-title":"Nat Neurosci"},{"issue":"7","key":"pcbi.1013097.ref054","doi-asserted-by":"crossref","first-page":"2140","DOI":"10.1073\/pnas.0305404101","article-title":"Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation","volume":"101","author":"S Gais","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5","key":"pcbi.1013097.ref055","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1162\/jocn.2006.18.5.793","article-title":"Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation","volume":"18","author":"BH Rasch","year":"2006","journal-title":"J Cogn Neurosci"},{"issue":"2","key":"pcbi.1013097.ref056","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/S0304-3940(97)00489-8","article-title":"Selective M1 muscarinic receptor antagonists disrupt memory consolidation of inhibitory avoidance in rats","volume":"230","author":"G Rold\u00e1n","year":"1997","journal-title":"Neurosci Lett"},{"key":"pcbi.1013097.ref057","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/S0091-3057(02)01007-9","article-title":"Role of hippocampal M1 and M4 muscarinic receptor subtypes in memory consolidation in the rat","volume":"74","author":"A Ferreira","year":"2003","journal-title":"Pharmacol Biochem Behav"},{"issue":"6","key":"pcbi.1013097.ref058","doi-asserted-by":"crossref","first-page":"1416","DOI":"10.1523\/JNEUROSCI.4111-03.2004","article-title":"Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: a mechanism for sleep-dependent plasticity","volume":"24","author":"S Datta","year":"2004","journal-title":"J Neurosci"},{"issue":"10","key":"pcbi.1013097.ref059","doi-asserted-by":"crossref","first-page":"4561","DOI":"10.1523\/JNEUROSCI.5525-12.2013","article-title":"Fear extinction memory consolidation requires potentiation of pontine-wave activity during REM sleep","volume":"33","author":"S Datta","year":"2013","journal-title":"J Neurosci"},{"issue":"3","key":"pcbi.1013097.ref060","doi-asserted-by":"crossref","DOI":"10.1093\/sleep\/zsac301","article-title":"Atypical hypnotic compound ML297 restores sleep architecture immediately following emotionally valenced learning, to promote memory consolidation and hippocampal network activation during recall","volume":"46","author":"JD Martinez","year":"2023","journal-title":"Sleep"},{"key":"pcbi.1013097.ref061","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.nlm.2014.11.015","article-title":"Rem sleep rescues learning from interference","volume":"122","author":"E McDevitt","year":"2015","journal-title":"Neurobiol Learn Mem"},{"issue":"1","key":"pcbi.1013097.ref062","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.neuron.2004.08.031","article-title":"Sleep-dependent learning and memory consolidation","volume":"44","author":"MP Walker","year":"2004","journal-title":"Neuron"},{"key":"pcbi.1013097.ref063","doi-asserted-by":"crossref","first-page":"105574","DOI":"10.1016\/j.neubiorev.2024.105574","article-title":"Mystery of the memory engram: History, current knowledge, and unanswered questions","volume":"159","author":"MR Lopez","year":"2024","journal-title":"Neurosci Biobehav Rev"},{"issue":"18","key":"pcbi.1013097.ref064","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2023.07.042","article-title":"Engram stability and maturation during systems consolidation","volume":"33","author":"R Refaeli","year":"2023","journal-title":"Curr Biol"},{"key":"pcbi.1013097.ref065","doi-asserted-by":"crossref","first-page":"1440","DOI":"10.1126\/science.aad1935","article-title":"Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences","volume":"351","author":"A Grosmark","year":"2016","journal-title":"Science"},{"issue":"1","key":"pcbi.1013097.ref066","doi-asserted-by":"crossref","first-page":"2232","DOI":"10.1038\/s41467-019-09960-x","article-title":"Engram-specific transcriptome profiling of contextual memory consolidation","volume":"10","author":"P Rao-Ruiz","year":"2019","journal-title":"Nat Commun"},{"issue":"9","key":"pcbi.1013097.ref067","doi-asserted-by":"crossref","DOI":"10.1016\/j.neuron.2024.02.007","article-title":"Excitability mediates allocation of pre-configured ensembles to a hippocampal engram supporting contextual conditioned threat in mice","volume":"112","author":"AJ Mocle","year":"2024","journal-title":"Neuron"},{"issue":"6","key":"pcbi.1013097.ref068","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2312281120","article-title":"Structure and function of the hippocampal CA3 module","volume":"121","author":"RP Sammons","year":"2024","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"pcbi.1013097.ref069","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/s41593-023-01551-w","article-title":"Dynamic and selective engrams emerge with memory consolidation","volume":"27","author":"DF Tom\u00e9","year":"2024","journal-title":"Nat Neurosci"},{"issue":"2","key":"pcbi.1013097.ref070","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.neuron.2015.09.024","article-title":"Disinhibition, a Circuit Mechanism for Associative Learning and Memory","volume":"88","author":"JJ Letzkus","year":"2015","journal-title":"Neuron"},{"issue":"7501","key":"pcbi.1013097.ref071","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1038\/nature13258","article-title":"Amygdala interneuron subtypes control fear learning through disinhibition","volume":"509","author":"SBE Wolff","year":"2014","journal-title":"Nature"},{"issue":"7377","key":"pcbi.1013097.ref072","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/nature10674","article-title":"A disinhibitory microcircuit for associative fear learning in the auditory cortex","volume":"480","author":"JJ Letzkus","year":"2011","journal-title":"Nature"},{"issue":"2","key":"pcbi.1013097.ref073","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1038\/s41593-022-01223-1","article-title":"Neocortical synaptic engrams for remote contextual memories","volume":"26","author":"J-H Lee","year":"2023","journal-title":"Nat Neurosci"},{"issue":"5748","key":"pcbi.1013097.ref074","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1038\/283673a0","article-title":"Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone","volume":"283","author":"DA Brown","year":"1980","journal-title":"Nature"},{"key":"pcbi.1013097.ref075","doi-asserted-by":"crossref","first-page":"64","DOI":"10.3389\/fnsys.2019.00064","article-title":"Acetylcholine Mediates Dynamic Switching Between Information Coding Schemes in Neuronal Networks","volume":"13","author":"JP Roach","year":"2019","journal-title":"Front Syst Neurosci"},{"issue":"3","key":"pcbi.1013097.ref076","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/S0167-8760(00)00173-2","article-title":"Inhibition-based rhythms: experimental and mathematical observations on network dynamics","volume":"38","author":"MA Whittington","year":"2000","journal-title":"Int J Psychophysiol"},{"issue":"19","key":"pcbi.1013097.ref077","doi-asserted-by":"crossref","first-page":"7002","DOI":"10.1073\/pnas.0502366102","article-title":"Background gamma rhythmicity and attention in cortical local circuits: a computational study","volume":"102","author":"C B\u00f6rgers","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"34","key":"pcbi.1013097.ref078","doi-asserted-by":"crossref","first-page":"10897","DOI":"10.1523\/JNEUROSCI.23-34-10897.2003","article-title":"Sleep-dependent theta oscillations in the human hippocampus and neocortex","volume":"23","author":"JL Cantero","year":"2003","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref079","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1113\/jphysiol.2004.073007","article-title":"Differential involvement of oriens\/pyramidale interneurones in hippocampal network oscillations in vitro","volume":"562","author":"T Gloveli","year":"2005","journal-title":"J Physiol"},{"key":"pcbi.1013097.ref080","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.51156","article-title":"Presynaptic GABAB receptors functionally uncouple somatostatin interneurons from the active hippocampal network","volume":"9","author":"SA Booker","year":"2020","journal-title":"Elife"},{"key":"pcbi.1013097.ref081","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1038\/nature01374","article-title":"Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo","volume":"421","author":"T Klausberger","year":"2003","journal-title":"Nature"},{"issue":"5","key":"pcbi.1013097.ref082","doi-asserted-by":"crossref","first-page":"1228","DOI":"10.1093\/cercor\/bht316","article-title":"Temporal organization of GABAergic interneurons in the intermediate CA1 hippocampus during network oscillations","volume":"25","author":"T Forro","year":"2015","journal-title":"Cereb Cortex"},{"key":"pcbi.1013097.ref083","doi-asserted-by":"crossref","first-page":"8094","DOI":"10.1523\/JNEUROSCI.5665-08.2009","article-title":"GABAergic neurons of the medial septum lead the hippocampal network during theta activity","volume":"29","author":"B Hangya","year":"2009","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref084","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1146\/annurev-neuro-062012-170330","article-title":"Mechanisms and functions of theta rhythms","volume":"36","author":"L Colgin","year":"2013","journal-title":"Annu Rev Neurosci"},{"issue":"1","key":"pcbi.1013097.ref085","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1038\/s41598-018-36710-8","article-title":"Neuronal firing rates diverge during REM and homogenize during non-REM","volume":"9","author":"H Miyawaki","year":"2019","journal-title":"Sci Rep"},{"key":"pcbi.1013097.ref086","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.jneumeth.2017.12.021","article-title":"Functional network stability and average minimal distance - A framework to rapidly assess dynamics of functional network representations","volume":"296","author":"J Wu","year":"2018","journal-title":"J Neurosci Methods"},{"issue":"13","key":"pcbi.1013097.ref087","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.1716933115","article-title":"Resonance with subthreshold oscillatory drive organizes activity and optimizes learning in neural networks","volume":"115","author":"JP Roach","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7330","key":"pcbi.1013097.ref088","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1038\/nature09633","article-title":"Preplay of future place cell sequences by hippocampal cellular assemblies","volume":"469","author":"G Dragoi","year":"2011","journal-title":"Nature"},{"issue":"8","key":"pcbi.1013097.ref089","doi-asserted-by":"crossref","DOI":"10.1016\/j.cell.2024.02.032","article-title":"Barcoding of episodic memories in the hippocampus of a food-caching bird","volume":"187","author":"SN Chettih","year":"2024","journal-title":"Cell"},{"issue":"4","key":"pcbi.1013097.ref090","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1086\/506973","article-title":"A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology","volume":"168","author":"JA Lesku","year":"2006","journal-title":"Am Nat"},{"issue":"4","key":"pcbi.1013097.ref091","article-title":"Daily Oscillation of the Excitation-Inhibition Balance in Visual Cortical Circuits","volume":"105","author":"MCD Bridi","year":"2020","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1013097.ref092","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.smrv.2005.05.002","article-title":"Sleep function and synaptic homeostasis","volume":"10","author":"G Tononi","year":"2006","journal-title":"Sleep Med Rev"},{"key":"pcbi.1013097.ref093","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1016\/j.neuron.2012.09.007","article-title":"Sleep to upscale, sleep to downscale: balancing homeostasis and plasticity","volume":"75","author":"J Born","year":"2012","journal-title":"Neuron"},{"issue":"7","key":"pcbi.1013097.ref094","article-title":"Differential roles of sleep spindles and sleep slow oscillations in memory consolidation","volume":"14","author":"Y Wei","year":"2018","journal-title":"PLoS Comput Biol"},{"issue":"1","key":"pcbi.1013097.ref095","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1038\/s41467-022-28339-z","article-title":"Coordinated hippocampal-thalamic-cortical communication crucial for engram dynamics underneath systems consolidation","volume":"13","author":"DF Tom\u00e9","year":"2022","journal-title":"Nat Commun"},{"issue":"12","key":"pcbi.1013097.ref096","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1038\/nn.4418","article-title":"Functional and structural underpinnings of neuronal assembly formation in learning","volume":"19","author":"A Holtmaat","year":"2016","journal-title":"Nat Neurosci"},{"issue":"10","key":"pcbi.1013097.ref097","doi-asserted-by":"crossref","first-page":"5019","DOI":"10.1073\/pnas.97.10.5019","article-title":"Microcolumns in the cerebral cortex","volume":"97","author":"EG Jones","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref098","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1038\/nn.2337","article-title":"Replay of rule-learning related neural patterns in the prefrontal cortex during sleep","volume":"12","author":"A Peyrache","year":"2009","journal-title":"Nat Neurosci"},{"issue":"2","key":"pcbi.1013097.ref099","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1038\/nn2037","article-title":"Reactivation of experience-dependent cell assembly patterns in the hippocampus","volume":"11","author":"J O\u2019Neill","year":"2008","journal-title":"Nat Neurosci"},{"key":"pcbi.1013097.ref100","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1126\/science.aat5397","article-title":"The hippocampal engram maps experience but not place","volume":"361","author":"KZ Tanaka","year":"2018","journal-title":"Science"},{"issue":"6","key":"pcbi.1013097.ref101","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/j.neuron.2012.08.015","article-title":"REM sleep reorganizes hippocampal excitability","volume":"75","author":"AD Grosmark","year":"2012","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1013097.ref102","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1038\/nn.2384","article-title":"Selective suppression of hippocampal ripples impairs spatial memory","volume":"12","author":"G Girardeau","year":"2009","journal-title":"Nat Neurosci"},{"issue":"7","key":"pcbi.1013097.ref103","doi-asserted-by":"crossref","first-page":"2148","DOI":"10.1523\/JNEUROSCI.3083-15.2016","article-title":"REM Sleep Is Causal to Successful Consolidation of Dangerous and Safety Stimuli and Reduces Return of Fear after Extinction","volume":"36","author":"MM Menz","year":"2016","journal-title":"J Neurosci"},{"issue":"7","key":"pcbi.1013097.ref104","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1038\/npp.2009.6","article-title":"Impaired off-line consolidation of motor memories after combined blockade of cholinergic receptors during REM sleep-rich sleep","volume":"34","author":"B Rasch","year":"2009","journal-title":"Neuropsychopharmacology"},{"key":"pcbi.1013097.ref105","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1037\/bul0000223","article-title":"Promoting memory consolidation during sleep: a meta-analysis of targeted memory reactivation","volume":"146","author":"X Hu","year":"2020","journal-title":"Psychol Bull"},{"issue":"25","key":"pcbi.1013097.ref106","doi-asserted-by":"crossref","first-page":"10130","DOI":"10.1073\/pnas.0900271106","article-title":"REM, not incubation, improves creativity by priming associative networks","volume":"106","author":"DJ Cai","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref107","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.tics.2018.03.009","article-title":"How memory replay in sleep boosts creative problem-solving","volume":"22","author":"P Lewis","year":"2018","journal-title":"Trends Cogn Sci"},{"key":"pcbi.1013097.ref108","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.conb.2020.09.007","article-title":"Neural inhibition for continual learning and memory","volume":"67","author":"HC Barron","year":"2021","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1013097.ref109","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.cobeha.2019.12.009","article-title":"Neural correlates of sleep, stress, and selective memory consolidation","volume":"33","author":"S Kim","year":"2020","journal-title":"Curr Opin Behav Sci"},{"issue":"6297","key":"pcbi.1013097.ref110","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1126\/science.aaf0594","article-title":"Competition between engrams influences fear memory formation and recall","volume":"353","author":"AJ Rashid","year":"2016","journal-title":"Science"},{"issue":"7","key":"pcbi.1013097.ref111","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.1016\/j.neuron.2023.03.005","article-title":"Sleep-A brain-state serving systems memory consolidation","volume":"111","author":"S Brodt","year":"2023","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1013097.ref112","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1038\/s41593-019-0467-3","article-title":"Mechanisms of systems memory consolidation during sleep","volume":"22","author":"JG Klinzing","year":"2019","journal-title":"Nat Neurosci"},{"key":"pcbi.1013097.ref113","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1038\/s41386-023-01583-7","article-title":"M1 acetylcholine receptors in somatostatin interneurons contribute to gabaergic and glutamatergic plasticity in the mpfc and antidepressant-like responses","volume":"48","author":"M Fogaca","year":"2023","journal-title":"Neuropsychopharmacol"},{"issue":"2","key":"pcbi.1013097.ref114","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.bbr.2010.02.025","article-title":"Localisation of pre- and postsynaptic cholinergic markers in the human brain","volume":"221","author":"A Wevers","year":"2011","journal-title":"Behav Brain Res"},{"key":"pcbi.1013097.ref115","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.65998","article-title":"Impaired spatial learning and suppression of sharp wave ripples by cholinergic activation at the goal location","volume":"10","author":"P Jarzebowski","year":"2021","journal-title":"Elife"},{"issue":"31","key":"pcbi.1013097.ref116","doi-asserted-by":"crossref","first-page":"9888","DOI":"10.1523\/JNEUROSCI.1366-09.2009","article-title":"M1 receptors mediate cholinergic modulation of excitability in neocortical pyramidal neurons","volume":"29","author":"AT Gulledge","year":"2009","journal-title":"J Neurosci"},{"issue":"3","key":"pcbi.1013097.ref117","article-title":"Activation of M1 cholinergic receptors in mouse somatosensory cortex enhances information processing and detection behaviour","volume":"7","author":"W Mishra","journal-title":"Commun Biol"},{"issue":"1","key":"pcbi.1013097.ref118","doi-asserted-by":"crossref","first-page":"4101","DOI":"10.1038\/s41467-018-06628-w","article-title":"Lateral inhibition by Martinotti interneurons is facilitated by cholinergic inputs in human and mouse neocortex","volume":"9","author":"J Obermayer","year":"2018","journal-title":"Nat Commun"},{"key":"pcbi.1013097.ref119","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3389\/fnsys.2012.00079","article-title":"Cell-type-specific modulation of neocortical activity by basal forebrain input","volume":"6","author":"HJ Alitto","year":"2013","journal-title":"Front Syst Neurosci"},{"issue":"23","key":"pcbi.1013097.ref120","doi-asserted-by":"crossref","first-page":"5338","DOI":"10.1523\/JNEUROSCI.0566-18.2018","article-title":"Synaptic Release of Acetylcholine Rapidly Suppresses Cortical Activity by Recruiting Muscarinic Receptors in Layer 4","volume":"38","author":"R Dasgupta","year":"2018","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref121","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1111\/j.1460-9568.2009.07058.x","article-title":"Nicotine facilitates long-term potentiation induction in oriens-lacunosum moleculare cells via Ca2 entry through non-alpha7 nicotinic acetylcholine receptors","volume":"31","author":"Y Jia","year":"2010","journal-title":"Eur J Neurosci"},{"key":"pcbi.1013097.ref122","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/0024-3205(90)90300-G","article-title":"Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis","volume":"47","author":"H Kametani","year":"1990","journal-title":"Life Sci"},{"issue":"4","key":"pcbi.1013097.ref123","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1016\/j.celrep.2016.12.085","article-title":"Coordinated Acetylcholine Release in Prefrontal Cortex and Hippocampus Is Associated with Arousal and Reward on Distinct Timescales","volume":"18","author":"LM Teles-Grilo Ruivo","year":"2017","journal-title":"Cell Rep"},{"key":"pcbi.1013097.ref124","doi-asserted-by":"crossref","first-page":"4365","DOI":"10.1523\/JNEUROSCI.0178-05.2005","article-title":"Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep","volume":"25","author":"M Lee","year":"2005","journal-title":"J Neurosci"},{"issue":"2","key":"pcbi.1013097.ref125","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0166-4328(00)00257-6","article-title":"Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep","volume":"115","author":"R Szymusiak","year":"2000","journal-title":"Behav Brain Res"},{"issue":"6","key":"pcbi.1013097.ref126","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1016\/j.neuron.2012.08.034","article-title":"Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity","volume":"75","author":"S Chauvette","year":"2012","journal-title":"Neuron"},{"issue":"4","key":"pcbi.1013097.ref127","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/j.neuron.2016.03.036","article-title":"Network Homeostasis and State Dynamics of Neocortical Sleep","volume":"90","author":"BO Watson","year":"2016","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1013097.ref128","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1523\/JNEUROSCI.19-01-00274.1999","article-title":"Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat","volume":"19","author":"J Csicsvari","year":"1999","journal-title":"J Neurosci"},{"issue":"2","key":"pcbi.1013097.ref129","doi-asserted-by":"crossref","DOI":"10.1523\/JNEUROSCI.22-02-j0001.2002","article-title":"Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge","volume":"22","author":"L Marshall","year":"2002","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref130","doi-asserted-by":"crossref","first-page":"10521","DOI":"10.1073\/pnas.1508785112","article-title":"Local generation of multineuronal spike sequences in the hippocampal CA1 region","volume":"112","author":"E Stark","year":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref131","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1016\/j.neuron.2015.10.032","article-title":"Monolithically integrated muleds on silicon neural probes for high-resolution optogenetic studies in behaving animals","volume":"88","author":"F Wu","year":"2015","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1013097.ref132","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.cub.2012.11.019","article-title":"Reactivation of neural ensembles during the retrieval of recent and remote memory","volume":"23","author":"KK Tayler","year":"2013","journal-title":"Curr Biol"},{"issue":"5","key":"pcbi.1013097.ref133","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1016\/j.neuron.2016.01.024","article-title":"Hippocampal Somatostatin Interneurons Control the Size of Neuronal Memory Ensembles","volume":"89","author":"T Stefanelli","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1013097.ref134","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.nlm.2018.04.018","article-title":"Circuit mechanisms of hippocampal reactivation during sleep","volume":"160","author":"P Malerba","year":"2019","journal-title":"Neurobiol Learn Mem"},{"issue":"4","key":"pcbi.1013097.ref135","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1004880","article-title":"Hippocampal CA1 Ripples as Inhibitory Transients","volume":"12","author":"P Malerba","year":"2016","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1013097.ref136","doi-asserted-by":"crossref","first-page":"3124","DOI":"10.1523\/JNEUROSCI.0188-17.2018","article-title":"Hippocampal ripple oscillations and inhibition-first network models: frequency dynamics and response to GABA modulators","volume":"38","author":"J Donoso","year":"2018","journal-title":"J Neurosci"},{"issue":"6","key":"pcbi.1013097.ref137","doi-asserted-by":"crossref","first-page":"3898","DOI":"10.1523\/JNEUROSCI.14-06-03898.1994","article-title":"Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology","volume":"14","author":"ME Hasselmo","year":"1994","journal-title":"J Neurosci"},{"key":"pcbi.1013097.ref138","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0079-6123(03)45015-2","article-title":"High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation","volume":"145","author":"ME Hasselmo","year":"2004","journal-title":"Prog Brain Res"},{"issue":"22","key":"pcbi.1013097.ref139","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2021.10.028","article-title":"Noradrenaline: sleep on it","volume":"31","author":"N Matosevich","year":"2021","journal-title":"Curr Biol"},{"issue":"7","key":"pcbi.1013097.ref140","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1038\/nn.4304","article-title":"Hippocampo-cortical coupling mediates memory consolidation during sleep","volume":"19","author":"N Maingret","year":"2016","journal-title":"Nat Neurosci"},{"key":"pcbi.1013097.ref141","doi-asserted-by":"crossref","first-page":"100","DOI":"10.3389\/fncir.2017.00100","article-title":"Cholinergic Modulation of Cortical Microcircuits Is Layer-Specific: Evidence from Rodent, Monkey and Human Brain","volume":"11","author":"J Obermayer","year":"2017","journal-title":"Front Neural Circuits"},{"key":"pcbi.1013097.ref142","doi-asserted-by":"crossref","first-page":"795325","DOI":"10.3389\/fncir.2021.795325","article-title":"Muscarinic Acetylcholine Receptor Localization on Distinct Excitatory and Inhibitory Neurons Within the ACC and LPFC of the Rhesus Monkey","volume":"15","author":"A Tsolias","year":"2022","journal-title":"Front Neural Circuits"},{"issue":"38","key":"pcbi.1013097.ref143","article-title":"Unraveling why we sleep: Quantitative analysis reveals abrupt transition from neural reorganization to repair in early development","volume":"6","author":"J Cao","year":"2020","journal-title":"Sci Adv"},{"key":"pcbi.1013097.ref144","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1010628","article-title":"Sleep prevents catastrophic forgetting in spiking neural networks by forming a joint synaptic weight representation","volume":"18","author":"R Golden","year":"2022","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"pcbi.1013097.ref145","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1007\/s10827-008-0111-9","article-title":"The effects of cholinergic neuromodulation on neuronal phase-response curves of modeled cortical neurons","volume":"26","author":"KM Stiefel","year":"2009","journal-title":"J Comput Neurosci"},{"issue":"3","key":"pcbi.1013097.ref146","article-title":"A dynamical role for acetylcholine in synaptic renormalization","volume":"9","author":"CG Fink","year":"2013","journal-title":"PLoS Comput Biol"},{"issue":"8","key":"pcbi.1013097.ref147","doi-asserted-by":"crossref","first-page":"3101","DOI":"10.1073\/pnas.1208093110","article-title":"Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons","volume":"110","author":"SJ Aton","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013097.ref148","doi-asserted-by":"crossref","DOI":"10.1101\/lm.48803","article-title":"Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning","volume":"10","author":"L Graves","year":"2003","journal-title":"Learn Mem"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1013097","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,6,26]],"date-time":"2025-06-26T00:00:00Z","timestamp":1750896000000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013097","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,6,26]],"date-time":"2025-06-26T18:03:38Z","timestamp":1750961018000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013097"}},"subtitle":[],"editor":[{"given":"Daniel","family":"Bush,","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,6,17]]},"references-count":148,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2025,6,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1013097","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,17]]}}}