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Himanen","year":"2003","journal-title":"Neuropsychobiology."},{"key":"ref28","doi-asserted-by":"crossref","first-page":"e17267","DOI":"10.7554\/eLife.17267","article-title":"Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night","volume":"5","author":"L Muller","year":"2016","journal-title":"eLife"},{"issue":"12","key":"ref29","doi-asserted-by":"crossref","first-page":"2217","DOI":"10.1002\/hbm.21183","article-title":"Emergence of synchronous EEG spindles from asynchronous MEG spindles","volume":"32","author":"N Dehghani","year":"2011","journal-title":"Hum Brain Mapp"},{"key":"ref30","author":"M Steriade","year":"1990"},{"issue":"4","key":"ref31","doi-asserted-by":"crossref","first-page":"1924","DOI":"10.1073\/pnas.98.4.1924","article-title":"Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study","volume":"98","author":"I 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Theta bursts precede, and spindles follow, cortical and thalamic downstates in human NREM sleep. bioRxiv. 2018. <comment>doi: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"https:\/\/doi.org\/10.1101\/260786\" xlink:type=\"simple\">10.1101\/260786<\/ext-link><\/comment>","DOI":"10.1101\/260786"},{"issue":"2","key":"ref37","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":"2","key":"ref38","doi-asserted-by":"crossref","first-page":"R598","DOI":"10.1152\/ajpregu.2001.280.2.R598","article-title":"Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking","volume":"280","author":"J Vazquez","year":"2001","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"issue":"40","key":"ref39","doi-asserted-by":"crossref","first-page":"10292","DOI":"10.1523\/JNEUROSCI.2341-06.2006","article-title":"Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse","volume":"26","author":"K Takahashi","year":"2006","journal-title":"J Neurosci"},{"issue":"4","key":"ref40","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/0301-0082(92)90012-4","article-title":"Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity","volume":"39","author":"DA McCormick","year":"1992","journal-title":"Progress in neurobiology"},{"issue":"6","key":"ref41","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.physrep.2003.10.015","article-title":"Effects of noise in excitable systems","volume":"392","author":"B Lindner","year":"2004","journal-title":"Physics reports"},{"issue":"2","key":"ref42","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.cell.2015.09.029","article-title":"Reconstruction and simulation of neocortical microcircuitry","volume":"163","author":"H Markram","year":"2015","journal-title":"Cell"},{"issue":"5780","key":"ref43","doi-asserted-by":"crossref","first-page":"1622","DOI":"10.1126\/science.1124593","article-title":"Cortex is driven by weak but synchronously active thalamocortical synapses","volume":"312","author":"RM Bruno","year":"2006","journal-title":"Science"},{"issue":"Pt 1","key":"ref44","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1113\/jphysiol.1996.sp021133","article-title":"Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm","volume":"490","author":"D Contreras","year":"1996","journal-title":"The Journal of physiology"},{"issue":"49","key":"ref45","doi-asserted-by":"crossref","first-page":"17821","DOI":"10.1523\/JNEUROSCI.2604-11.2011","article-title":"Sleep spindles in humans: insights from intracranial EEG and unit recordings","volume":"31","author":"T Andrillon","year":"2011","journal-title":"Journal of Neuroscience"},{"issue":"2","key":"ref46","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.clinph.2010.06.018","article-title":"Topographical frequency dynamics within EEG and MEG sleep spindles","volume":"122","author":"N Dehghani","year":"2011","journal-title":"Clinical Neurophysiology"},{"key":"ref47","doi-asserted-by":"crossref","unstructured":"Rosen BQ, Krishnan G, Sanda P, Komarov M, Sejnowski T, Rulkov N, et al. Simulating human sleep spindle MEG and EEG from ion channel and circuit level dynamics. bioRxiv. 2017.","DOI":"10.1101\/202606"},{"issue":"24","key":"ref48","doi-asserted-by":"crossref","first-page":"10941","DOI":"10.1523\/JNEUROSCI.22-24-10941.2002","article-title":"Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep","volume":"22","author":"M Molle","year":"2002","journal-title":"J Neurosci"},{"issue":"47","key":"ref49","doi-asserted-by":"crossref","first-page":"18469","DOI":"10.1523\/JNEUROSCI.2197-13.2013","article-title":"Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles","volume":"33","author":"RJ Gardner","year":"2013","journal-title":"J Neurosci"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.neuroimage.2014.05.028","article-title":"Local sleep spindle modulations in relation to specific memory 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