{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,3]],"date-time":"2026-03-03T06:56:18Z","timestamp":1772520978647,"version":"3.50.1"},"reference-count":103,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2025,11,25]],"date-time":"2025-11-25T00:00:00Z","timestamp":1764028800000},"content-version":"vor","delay-in-days":328,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,10,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Study Objectives<\/jats:title>\n                    <jats:p>Sleep spindles are potential biomarkers for memory decline in aging. However, significant within-person variability in spindle attributes complicates their utility in predicting cognitive deterioration. This study aimed to uncover distinct spindle types and their relevance to memory decline using exploratory, data-driven clustering.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Polysomnography was collected from younger (n\u2009=\u200943, ages 20\u201345\u00a0years) and older cognitively healthy adults (n\u2009=\u200934, ages 60\u201381\u00a0years). Clustering analysis was performed using multiple features and spatiotemporal context, irrespective of participant age.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Resulting clusters were hierarchically defined by the sleep stage, slow oscillation concurrence, and hemisphere. Stage N3 spindles (15%; predominantly coinciding with slow oscillations) formed a distinct group, followed by N2 spindles coinciding with slow oscillations (27%). Remaining N2 spindles were categorized into unilateral (41%) and bilateral clusters (17%). In older adults, there was a lower proportion of N2 bilateral spindles and a higher proportion of N2 spindles concurrent with slow oscillations. Lower proportion of N2 bilateral spindles was associated with better composite memory performance in younger adults, whereas higher spindle power, regardless of cluster belonging, was associated with reduced memory benefit from sleep compared with wakefulness.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our results indicate differing expression of spatiotemporal spindle clusters in older age, as well as intertwined dynamics between spindle propagation, slow oscillation concurrence, and frequency shifts in aging. In addition, spindle heterogeneity aligned with global sleep stage dynamics. These results emphasize the interconnectedness of spindle activity with overall sleep patterns, underscoring the importance of spatiotemporal context within and across sleep stages.<\/jats:p>\n                    <jats:p>Statement of Significance This study used data-driven clustering to explore sleep spindles as potential markers for age-related memory decline. We identified spindle clusters determined by sleep stage, slow oscillation concurrence, and hemisphere propagation. Notably, older adults showed altered expression of these clusters, indicating age-specific dynamics. Further research should focus on distinguishing spindle deterioration from broader sleep changes in older age. Such insights could pave the way for early detection and intervention strategies in cognitive decline, highlighting sleep\u2019s crucial role in maintaining cognitive health and resilience in aging populations. These findings hold promise for developing targeted approaches to enhance mental wellness and quality of life in older adults.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/sleepadvances\/zpaf084","type":"journal-article","created":{"date-parts":[[2025,11,20]],"date-time":"2025-11-20T13:31:41Z","timestamp":1763645501000},"source":"Crossref","is-referenced-by-count":0,"title":["Differential expression of spatiotemporal sleep spindle clusters in aging"],"prefix":"10.1093","volume":"6","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2355-4308","authenticated-orcid":false,"given":"Liisa","family":"Raud","sequence":"first","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martijn J P","family":"Smits","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]},{"name":"Department of Psychology, Clinical Neuroscience Laboratory, Norwegian University of Science and Technology , Trondheim 7491 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7644-7915","authenticated-orcid":false,"given":"Markus H","family":"Sneve","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4312-5482","authenticated-orcid":false,"given":"Hedda T","family":"Ness","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Line","family":"Folvik","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7607-3415","authenticated-orcid":false,"given":"Bj\u00f6rn","family":"Rasch","sequence":"additional","affiliation":[{"name":"Department of Psychology, Division of Cognitive Biopsychology and Methods, University of Fribourg, Fribourg 1700 ,","place":["Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anders M","family":"Fjell","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Lifespan Changes in Brain and Cognition, University of Oslo , Oslo 0373 ,","place":["Norway"]},{"name":"Department of Radiology and Nuclear Medicine, Computational Radiology and Artificial Intelligence, Oslo University Hospital , Oslo 0372 ,","place":["Norway"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2025,11,25]]},"reference":[{"issue":"2","key":"2026030301023486300_ref1","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.jsmc.2022.02.007","article-title":"Sleep in normal aging","volume":"17","author":"Li","year":"2022","journal-title":"Sleep Med Clin"},{"issue":"1","key":"2026030301023486300_ref2","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.neuron.2017.02.004","article-title":"Sleep and human aging","volume":"94","author":"Mander","year":"2017","journal-title":"Neuron."},{"issue":"1","key":"2026030301023486300_ref3","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1177\/1745691614556680","article-title":"Sleep, cognition, and normal aging: integrating a half century of multidisciplinary research","volume":"10","author":"Scullin","year":"2015","journal-title":"Perspect Psychol Sci"},{"key":"2026030301023486300_ref4","doi-asserted-by":"publisher","first-page":"101184","DOI":"10.1016\/j.arr.2020.101184","article-title":"Biological and environmental predictors of heterogeneity in neurocognitive ageing: evidence from Betula and other longitudinal studies","volume":"64","author":"Nyberg","year":"2020","journal-title":"Ageing Res Rev"},{"issue":"5","key":"2026030301023486300_ref5","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.tics.2012.04.005","article-title":"Memory aging and brain maintenance","volume":"16","author":"Nyberg","year":"2012","journal-title":"Trends Cogn Sci"},{"issue":"2","key":"2026030301023486300_ref6","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1152\/physrev.00032.2012","article-title":"About Sleep\u2019s role in memory","volume":"93","author":"Rasch","year":"2013","journal-title":"Physiol Rev"},{"issue":"2","key":"2026030301023486300_ref7","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1007\/s00426-011-0335-6","article-title":"System consolidation of memory during sleep","volume":"76","author":"Born","year":"2012","journal-title":"Psychol Res"},{"issue":"2","key":"2026030301023486300_ref8","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1038\/nrn2762","article-title":"The memory function of sleep","volume":"11","author":"Diekelmann","year":"2010","journal-title":"Nat Rev Neurosci"},{"issue":"1","key":"2026030301023486300_ref9","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.jneumeth.2009.09.001","article-title":"Time-frequency analysis methods to quantify the time-varying microstructure of sleep EEG spindles: possibility for dementia biomarkers?","volume":"185","author":"Ktonas","year":"2009","journal-title":"J Neurosci Methods"},{"key":"2026030301023486300_ref10","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.sleep.2020.07.044","article-title":"Sleep spindle abnormalities related to Alzheimer\u2019s disease: a systematic mini-review","volume":"75","author":"Weng","year":"2020","journal-title":"Sleep Med"},{"issue":"2","key":"2026030301023486300_ref11","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1007\/s11325-019-01970-9","article-title":"Sleep spindles, K-complexes, limb movements and sleep stage proportions may be biomarkers for amnestic mild cognitive impairment and Alzheimer\u2019s disease","volume":"24","author":"Liu","year":"2020","journal-title":"Sleep Breath"},{"key":"2026030301023486300_ref12","doi-asserted-by":"publisher","first-page":"8376108","DOI":"10.1155\/2016\/8376108","article-title":"Parietal fast sleep spindle density decrease in Alzheimer\u2019s disease and amnesic mild cognitive impairment","volume":"2016","author":"Gorgoni","year":"2016","journal-title":"Neural Plast"},{"issue":"2","key":"2026030301023486300_ref13","doi-asserted-by":"publisher","first-page":"1083","DOI":"10.1016\/j.neurobiolaging.2014.09.009","article-title":"Sleep spindles in Parkinson\u2019s disease may predict the development of dementia","volume":"36","author":"Latreille","year":"2015","journal-title":"Neurobiol Aging"},{"key":"2026030301023486300_ref14","doi-asserted-by":"publisher","first-page":"101308","DOI":"10.1016\/j.smrv.2020.101308","article-title":"Objective measurement of sleep in mild cognitive impairment: a systematic review and meta-analysis","volume":"52","author":"D\u2019Rozario","year":"2020","journal-title":"Sleep Med Rev"},{"key":"2026030301023486300_ref15","doi-asserted-by":"publisher","first-page":"108661","DOI":"10.1016\/j.neuropsychologia.2023.108661","article-title":"Spindle-dependent memory consolidation in healthy adults: a meta-analysis","volume":"189","author":"Kumral","year":"2023","journal-title":"Neuropsychologia."},{"issue":"1","key":"2026030301023486300_ref16","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1186\/s13024-019-0309-5","article-title":"Sleep oscillation-specific associations with Alzheimer\u2019s disease CSF biomarkers: novel roles for sleep spindles and tau","volume":"14","author":"Kam","year":"2019","journal-title":"Mol Neurodegener"},{"issue":"9","key":"2026030301023486300_ref17","doi-asserted-by":"publisher","first-page":"zsac135","DOI":"10.1093\/sleep\/zsac135","article-title":"Inflammation, tau pathology, and synaptic integrity associated with sleep spindles and memory prior to \u03b2-amyloid positivity","volume":"45","author":"Mander","year":"2022","journal-title":"Sleep."},{"issue":"22","key":"2026030301023486300_ref18","doi-asserted-by":"publisher","first-page":"4517","DOI":"10.1523\/JNEUROSCI.1786-21.2022","article-title":"Human spindle variability","volume":"42","author":"Gonzalez","year":"2022","journal-title":"J Neurosci"},{"issue":"2","key":"2026030301023486300_ref19","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1152\/physrev.00042.2018","article-title":"Sleep spindles: mechanisms and functions","volume":"100","author":"Fernandez","year":"2020","journal-title":"Physiol Rev"},{"key":"2026030301023486300_ref20","doi-asserted-by":"publisher","first-page":"5787423","DOI":"10.1155\/2016\/5787423","article-title":"Spindle activity orchestrates plasticity during development and sleep","volume":"2016","author":"Lindemann","year":"2016","journal-title":"Neural Plast"},{"issue":"1","key":"2026030301023486300_ref21","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.1038\/s41467-021-21298-x","article-title":"Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans","volume":"12","author":"Dickey","year":"2021","journal-title":"Nat Commun"},{"issue":"41","key":"2026030301023486300_ref22","doi-asserted-by":"publisher","first-page":"9398","DOI":"10.1523\/JNEUROSCI.2149-05.2005","article-title":"Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train","volume":"25","author":"Rosanova","year":"2005","journal-title":"J Neurosci"},{"issue":"5","key":"2026030301023486300_ref23","doi-asserted-by":"publisher","first-page":"e1004241","DOI":"10.1371\/journal.pcbi.1004241","article-title":"Synaptic homeostasis and restructuring across the sleep-wake cycle","volume":"11","author":"Blanco","year":"2015","journal-title":"PLoS Comput Biol"},{"issue":"40","key":"2026030301023486300_ref24","doi-asserted-by":"publisher","first-page":"15675","DOI":"10.1523\/JNEUROSCI.0247-13.2013","article-title":"Non-Hebbian long-term potentiation of inhibitory synapses in the thalamus","volume":"33","author":"Sieber","year":"2013","journal-title":"J Neurosci"},{"issue":"6188","key":"2026030301023486300_ref25","doi-asserted-by":"publisher","first-page":"1173","DOI":"10.1126\/science.1249098","article-title":"Sleep promotes branch-specific formation of dendritic spines after learning","volume":"344","author":"Yang","year":"2014","journal-title":"Science."},{"issue":"8","key":"2026030301023486300_ref26","doi-asserted-by":"publisher","first-page":"1429","DOI":"10.1038\/s41593-023-01381-w","article-title":"How coupled slow oscillations, spindles and ripples coordinate neuronal processing and communication during human sleep","volume":"26","author":"Staresina","year":"2023","journal-title":"Nat Neurosci"},{"issue":"2","key":"2026030301023486300_ref27","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1038\/nrn1607","article-title":"The organization of recent and remote memories","volume":"6","author":"Frankland","year":"2005","journal-title":"Nat Rev Neurosci"},{"issue":"1","key":"2026030301023486300_ref28","doi-asserted-by":"publisher","first-page":"15930","DOI":"10.1038\/ncomms15930","article-title":"Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource","volume":"8","author":"Purcell","year":"2017","journal-title":"Nat Commun"},{"key":"2026030301023486300_ref29","doi-asserted-by":"publisher","first-page":"6936381","DOI":"10.1155\/2016\/6936381","article-title":"Form and function of sleep spindles across the lifespan","volume":"2016","author":"Clawson","year":"2016","journal-title":"Neural Plast"},{"issue":"3","key":"2026030301023486300_ref30","doi-asserted-by":"publisher","first-page":"e91047","DOI":"10.1371\/journal.pone.0091047","article-title":"Age differences in the variability and distribution of sleep spindle and rapid eye movement densities","volume":"9","author":"Peters","year":"2014","journal-title":"PloS One"},{"issue":"2","key":"2026030301023486300_ref31","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1016\/j.neurobiolaging.2012.05.020","article-title":"Topography of age-related changes in sleep spindles","volume":"34","author":"Martin","year":"2013","journal-title":"Neurobiol Aging"},{"key":"2026030301023486300_ref32","doi-asserted-by":"publisher","first-page":"3","DOI":"10.3389\/fneur.2012.00176","article-title":"NREM sleep oscillations and brain plasticity in aging","volume":"3","author":"Fogel","year":"2012","journal-title":"Front Neurol"},{"issue":"1","key":"2026030301023486300_ref33","doi-asserted-by":"publisher","first-page":"778","DOI":"10.1186\/s12877-024-05364-9","article-title":"Age-related changes in sleep spindle characteristics in individuals over 75 years of age: a retrospective and comparative study","volume":"24","author":"Poirson","year":"2024","journal-title":"BMC Geriatr"},{"key":"2026030301023486300_ref34","doi-asserted-by":"publisher","first-page":"101304","DOI":"10.1016\/j.smrv.2020.101304","article-title":"Episodic memory consolidation during sleep in healthy aging","volume":"52","author":"Muehlroth","year":"2020","journal-title":"Sleep Med Rev"},{"key":"2026030301023486300_ref35","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1016\/j.neurobiolaging.2016.10.009","article-title":"Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation","volume":"49","author":"Fogel","year":"2017","journal-title":"Neurobiol Aging"},{"issue":"2","key":"2026030301023486300_ref36","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/s41380-023-02335-1","article-title":"Sleep spindle architecture associated with distinct clinical phenotypes in older adults at risk for dementia","volume":"29","author":"Orlando","year":"2024","journal-title":"Mol Psychiatry"},{"key":"2026030301023486300_ref37","doi-asserted-by":"publisher","first-page":"433","DOI":"10.3389\/fnhum.2017.00433","article-title":"Individual differences in frequency and topography of slow and fast sleep spindles","volume":"11","author":"Cox","year":"2017","journal-title":"Front Hum Neurosci"},{"issue":"6","key":"2026030301023486300_ref38","doi-asserted-by":"publisher","first-page":"905","DOI":"10.5665\/sleep.2722","article-title":"Differential effects on fast and slow spindle activity, and the sleep slow oscillation in humans with carbamazepine and flunarizine to antagonize voltage-dependent Na+ and Ca2+ channel activity","volume":"36","author":"Ayoub","year":"2013","journal-title":"Sleep."},{"issue":"10","key":"2026030301023486300_ref39","doi-asserted-by":"publisher","first-page":"1411","DOI":"10.5665\/SLEEP.1290","article-title":"Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing","volume":"34","author":"M\u00f6lle","year":"2011","journal-title":"Sleep."},{"issue":"1","key":"2026030301023486300_ref40","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1038\/s41562-020-00964-y","article-title":"Macro and micro sleep architecture and cognitive performance in older adults","volume":"5","author":"Djonlagic","year":"2021","journal-title":"Nat Hum Behav"},{"issue":"8","key":"2026030301023486300_ref41","doi-asserted-by":"publisher","first-page":"zsac132","DOI":"10.1093\/sleep\/zsac132","article-title":"The space-time profiles of sleep spindles and their coordination with slow oscillations on the electrode manifold","volume":"45","author":"Malerba","year":"2022","journal-title":"Sleep."},{"key":"2026030301023486300_ref42","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1016\/j.neuroimage.2016.11.010","article-title":"Spatiotemporal characteristics of sleep spindles depend on cortical location","volume":"146","author":"Piantoni","year":"2017","journal-title":"Neuroimage."},{"issue":"1","key":"2026030301023486300_ref43","doi-asserted-by":"publisher","first-page":"1940","DOI":"10.1038\/s41598-018-36557-z","article-title":"Precise slow oscillation-spindle coupling promotes memory consolidation in younger and older adults","volume":"9","author":"Muehlroth","year":"2019","journal-title":"Sci Rep"},{"issue":"1","key":"2026030301023486300_ref44","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1016\/j.neuron.2017.11.020","article-title":"Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting","volume":"97","author":"Helfrich","year":"2018","journal-title":"Neuron."},{"issue":"5","key":"2026030301023486300_ref45","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1053\/smrv.2002.0252","article-title":"Sleep spindles: an overview","volume":"7","author":"De Gennaro","year":"2003","journal-title":"Sleep Med Rev"},{"issue":"1-2","key":"2026030301023486300_ref46","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/s0006-8993(96)01275-9","article-title":"Dynamics of EEG spindle frequency activity during extended sleep in humans: relationship to slow-wave activity and time of day","volume":"748","author":"Aeschbach","year":"1997","journal-title":"Brain Res"},{"issue":"2","key":"2026030301023486300_ref47","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1111\/j.1365-2869.1993.tb00065.x","article-title":"All-night dynamics of the human sleep EEG","volume":"2","author":"Aeschbach","year":"1993","journal-title":"J Sleep Res"},{"key":"2026030301023486300_ref48","doi-asserted-by":"publisher","first-page":"727","DOI":"10.3389\/fnins.2019.00727","article-title":"Spatiotemporal dynamics of sleep spindle sources across NREM sleep cycles","volume":"13","author":"Alfonsi","year":"2019","journal-title":"Front Neurosci"},{"issue":"3","key":"2026030301023486300_ref49","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/0361-9230(94)90205-4","article-title":"Dynamic relationships between sleep spindles and delta waves during a NREM period","volume":"33","author":"Uchida","year":"1994","journal-title":"Brain Res Bull"},{"issue":"2","key":"2026030301023486300_ref50","doi-asserted-by":"publisher","first-page":"e2405276121","DOI":"10.1073\/pnas.2405276121","article-title":"Individualized temporal patterns drive human sleep spindle timing","volume":"122","author":"Chen","year":"2025","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"2026030301023486300_ref51","doi-asserted-by":"publisher","first-page":"e1602026","DOI":"10.1126\/sciadv.1602026","article-title":"Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep","volume":"3","author":"Lecci","year":"2017","journal-title":"Sci Adv"},{"issue":"1799","key":"2026030301023486300_ref52","doi-asserted-by":"publisher","first-page":"20190232","DOI":"10.1098\/rstb.2019.0232","article-title":"A sleep spindle framework for motor memory consolidation","volume":"375","author":"Boutin","year":"2020","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2026030301023486300_ref53","doi-asserted-by":"publisher","first-page":"803387","DOI":"10.3389\/fnins.2022.803387","article-title":"Visuomotor adaptation modulates the clustering of sleep spindles into trains","volume":"16","author":"Solano","year":"2022","journal-title":"Front Neurosci"},{"issue":"8","key":"2026030301023486300_ref54","doi-asserted-by":"publisher","first-page":"107314","DOI":"10.1016\/j.isci.2023.107314","article-title":"Sleep-related motor skill consolidation and generalizability after physical practice, motor imagery, and action observation","volume":"26","author":"Conessa","year":"2023","journal-title":"iScience."},{"issue":"2014","key":"2026030301023486300_ref55","doi-asserted-by":"publisher","first-page":"20231408","DOI":"10.1098\/rspb.2023.1408","article-title":"Temporal cluster-based organization of sleep spindles underlies motor memory consolidation","volume":"291","author":"Boutin","year":"2024","journal-title":"Proc Biol Sci"},{"issue":"5","key":"2026030301023486300_ref56","doi-asserted-by":"publisher","first-page":"zsac282","DOI":"10.1093\/sleep\/zsac282","article-title":"Age-related changes in fast spindle clustering during non-rapid eye movement sleep and their relevance for memory consolidation","volume":"46","author":"Champetier","year":"2023","journal-title":"Sleep."},{"issue":"6","key":"2026030301023486300_ref57","doi-asserted-by":"publisher","first-page":"e1006171","DOI":"10.1371\/journal.pcbi.1006171","article-title":"Thalamocortical and intracortical laminar connectivity determines sleep spindle properties","volume":"14","author":"Krishnan","year":"2018","journal-title":"PLoS Comput Biol"},{"key":"2026030301023486300_ref58","doi-asserted-by":"publisher","first-page":"3024342","DOI":"10.1155\/2016\/3024342","article-title":"The contribution of thalamocortical Core and matrix pathways to sleep spindles","volume":"2016","author":"Piantoni","year":"2016","journal-title":"Neural Plast"},{"issue":"8","key":"2026030301023486300_ref59","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1016\/j.tics.2021.04.009","article-title":"Aperiodic sleep networks promote memory consolidation","volume":"25","author":"Helfrich","year":"2021","journal-title":"Trends Cogn Sci"},{"issue":"4","key":"2026030301023486300_ref60","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1016\/0959-4388(94)90056-6","article-title":"Sensory gating mechanisms of the thalamus","volume":"4","author":"McCormick","year":"1994","journal-title":"Curr Opin Neurobiol"},{"key":"2026030301023486300_ref61","doi-asserted-by":"publisher","first-page":"40","DOI":"10.3389\/fneur.2012.00040","article-title":"The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation","volume":"3","author":"Schabus","year":"2012","journal-title":"Front Neurol"},{"issue":"37","key":"2026030301023486300_ref62","doi-asserted-by":"publisher","first-page":"15438","DOI":"10.1073\/pnas.1112503108","article-title":"Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep","volume":"108","author":"Dang-Vu","year":"2011","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"2026030301023486300_ref63","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1152\/physiol.00004.2019","article-title":"Brain rhythms during sleep and memory consolidation: neurobiological insights","volume":"35","author":"Marshall","year":"2020","journal-title":"Physiology."},{"issue":"2","key":"2026030301023486300_ref64","doi-asserted-by":"publisher","first-page":"538","DOI":"10.1002\/hbm.24393","article-title":"Changes in EEG multiscale entropy and power-law frequency scaling during the human sleep cycle","volume":"40","author":"Miskovic","year":"2019","journal-title":"Hum Brain Mapp"},{"issue":"11","key":"2026030301023486300_ref65","doi-asserted-by":"publisher","first-page":"1736","DOI":"10.1016\/j.cub.2018.04.020","article-title":"Sleep spindle refractoriness segregates periods of memory reactivation","volume":"28","author":"Antony","year":"2018","journal-title":"Curr Biol"},{"key":"2026030301023486300_ref66","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.neuropsychologia.2017.02.001","article-title":"Age-related differences in sleep-based memory consolidation: a meta-analysis","volume":"97","author":"Gui","year":"2017","journal-title":"Neuropsychologia."},{"key":"2026030301023486300_ref67","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.conb.2020.06.002","article-title":"How robust are sleep-mediated memory benefits?","volume":"67","author":"Cordi","year":"2021","journal-title":"Curr Opin Neurobiol"},{"key":"2026030301023486300_ref68","doi-asserted-by":"publisher","first-page":"750","DOI":"10.3389\/fpsyg.2013.00750","article-title":"Accelerated long-term forgetting in aging and intra-sleep awakenings","volume":"4","author":"Mary","year":"2013","journal-title":"Front Psychol"},{"issue":"11","key":"2026030301023486300_ref69","doi-asserted-by":"publisher","first-page":"2358","DOI":"10.1093\/cercor\/bhab331","article-title":"Reduced hippocampal-striatal interactions during formation of durable episodic memories in aging","volume":"32","author":"Ness","year":"2022","journal-title":"Cereb Cortex"},{"issue":"6","key":"2026030301023486300_ref70","doi-asserted-by":"publisher","first-page":"bhae233","DOI":"10.1093\/cercor\/bhae233","article-title":"Recalled through this day but forgotten next week?\u2014retrieval activity predicts durability of partly consolidated memories","volume":"34","author":"Ness","year":"2024","journal-title":"Cereb Cortex"},{"key":"2026030301023486300_ref71"},{"key":"2026030301023486300_ref72","doi-asserted-by":"publisher","first-page":"120309","DOI":"10.1016\/j.neuroimage.2023.120309","article-title":"Hippocampal-cortical functional connectivity during memory encoding and retrieval","volume":"279","author":"Raud","year":"2023","journal-title":"NeuroImage."},{"issue":"8","key":"2026030301023486300_ref73","doi-asserted-by":"publisher","first-page":"4844","DOI":"10.1093\/cercor\/bhac384","article-title":"Sustained upregulation of widespread hippocampal-neocortical coupling following memory encoding","volume":"33","author":"Folvik","year":"2022","journal-title":"Cereb Cortex"},{"key":"2026030301023486300_ref74","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.neurobiolaging.2025.01.004","article-title":"Network segregation during episodic memory shows age-invariant relations with memory performance from 7 to 82 years","volume":"148","author":"Grydeland","year":"2025","journal-title":"Neurobiol Aging"},{"key":"2026030301023486300_ref75","year":"24, 2015"},{"issue":"7","key":"2026030301023486300_ref76","doi-asserted-by":"publisher","first-page":"746","DOI":"10.1038\/mp.2014.1","article-title":"Rewards of beauty: the opioid system mediates social motivation in humans","volume":"19","author":"Chelnokova","year":"2014","journal-title":"Mol Psychiatry"},{"issue":"5","key":"2026030301023486300_ref77","doi-asserted-by":"publisher","first-page":"e10773","DOI":"10.1371\/journal.pone.0010773","article-title":"The Bank of Standardized Stimuli (BOSS), a new set of 480 normative photos of objects to Be used as visual stimuli in cognitive research","volume":"5","author":"Brodeur","year":"2010","journal-title":"PloS One"},{"issue":"9","key":"2026030301023486300_ref78","doi-asserted-by":"publisher","first-page":"e106953","DOI":"10.1371\/journal.pone.0106953","article-title":"Bank of Standardized Stimuli (BOSS) phase II: 930 new normative photos","volume":"9","author":"Brodeur","year":"2014","journal-title":"PloS One"},{"issue":"3","key":"2026030301023486300_ref79","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/S0022-5371(83)90229-3","article-title":"Do laboratory tests predict everyday memory? A neuropsychological study","volume":"22","author":"Sunderland","year":"1983","journal-title":"J Verbal Learn Verbal Behav"},{"issue":"2","key":"2026030301023486300_ref80","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1080\/01688638408401204","article-title":"Memory failures in everyday life following severe head injury","volume":"6","author":"Sunderland","year":"1984","journal-title":"J Clin Neuropsychol"},{"key":"2026030301023486300_ref81"},{"key":"2026030301023486300_ref82","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3389\/fnins.2013.00267","article-title":"MEG and EEG data analysis with MNE-python","volume":"7","author":"Gramfort","year":"2013","journal-title":"Front Neurosci"},{"key":"2026030301023486300_ref83","doi-asserted-by":"publisher","first-page":"e70092","DOI":"10.7554\/eLife.70092","article-title":"An open-source, high-performance tool for automated sleep staging","volume":"10","author":"Vallat","year":"2021","journal-title":"eLife"},{"issue":"5","key":"2026030301023486300_ref84","doi-asserted-by":"publisher","first-page":"665","DOI":"10.5664\/jcsm.6576","article-title":"AASM scoring manual updates for 2017 (version 2.4)","volume":"13","author":"Berry","year":"2017","journal-title":"J Clin Sleep Med"},{"issue":"1","key":"2026030301023486300_ref85","doi-asserted-by":"publisher","first-page":"81","DOI":"10.5664\/jcsm.2350","article-title":"The American Academy of sleep medicine inter-scorer reliability program: sleep stage scoring","volume":"9","author":"Rosenberg","journal-title":"J Clin Sleep Med"},{"key":"2026030301023486300_ref86","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.jneumeth.2018.08.014","article-title":"A sleep spindle detection algorithm that emulates human expert spindle scoring","volume":"316","author":"Lacourse","year":"2019","journal-title":"J Neurosci Methods"},{"key":"2026030301023486300_ref87"},{"issue":"3","key":"2026030301023486300_ref88","doi-asserted-by":"publisher","first-page":"e13523","DOI":"10.1111\/psyp.13523","article-title":"Understanding the interplay of sleep and aging: methodological challenges","volume":"57","author":"Muehlroth","year":"2020","journal-title":"Psychophysiology."},{"issue":"31","key":"2026030301023486300_ref89","doi-asserted-by":"publisher","first-page":"6862","DOI":"10.1523\/JNEUROSCI.1318-04.2004","article-title":"The sleep slow oscillation as a traveling wave","volume":"24","author":"Massimini","year":"2004","journal-title":"J Neurosci"},{"issue":"4","key":"2026030301023486300_ref90","doi-asserted-by":"publisher","first-page":"758","DOI":"10.1111\/j.1460-9568.2010.07543.x","article-title":"Sleep slow wave changes during the middle years of life","volume":"33","author":"Carrier","year":"2011","journal-title":"Eur J Neurosci"},{"issue":"3","key":"2026030301023486300_ref91","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1111\/j.1469-8986.1979.tb02991.x","article-title":"Systematic trends across the night in human sleep cycles","volume":"16","author":"Feinberg","year":"1979","journal-title":"Psychophysiology."},{"key":"2026030301023486300_ref92","doi-asserted-by":"publisher","first-page":"101318","DOI":"10.1016\/j.mex.2021.101318","article-title":"\u2018SleepCycles\u2019 package for R - a free software tool for the detection of sleep cycles from sleep staging","volume":"8","author":"Blume","year":"2021","journal-title":"MethodsX."},{"issue":"2","key":"2026030301023486300_ref93","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1016\/j.datak.2007.03.016","article-title":"A k-mean clustering algorithm for mixed numeric and categorical data","volume":"63","author":"Ahmad","year":"2007","journal-title":"Data Knowl Eng"},{"key":"2026030301023486300_ref94"},{"issue":"32","key":"2026030301023486300_ref95","doi-asserted-by":"publisher","first-page":"13164","DOI":"10.1073\/pnas.0703084104","article-title":"Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep","volume":"104","author":"Schabus","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2026030301023486300_ref96","doi-asserted-by":"publisher","first-page":"58","DOI":"10.3389\/fnagi.2019.00058","article-title":"Young and older adults benefit from sleep, but not from active wakefulness for memory consolidation of what-where-when naturalistic events","volume":"11","author":"Abichou","year":"2019","journal-title":"Front Aging Neurosci"},{"issue":"3","key":"2026030301023486300_ref97","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1080\/09658211003601548","article-title":"The effects of sleep on episodic memory in older and younger adults","volume":"18","author":"Aly","year":"2010","journal-title":"Memory."},{"issue":"5","key":"2026030301023486300_ref98","doi-asserted-by":"publisher","first-page":"991","DOI":"10.1016\/j.neurobiolaging.2011.06.029","article-title":"Sleep modulates word-pair learning but not motor sequence learning in healthy older adults","volume":"33","author":"Wilson","year":"2012","journal-title":"Neurobiol Aging"},{"issue":"7","key":"2026030301023486300_ref99","doi-asserted-by":"publisher","first-page":"2272","DOI":"10.1016\/j.neurobiolaging.2015.03.010","article-title":"Sleep protects memories from interference in older adults","volume":"36","author":"Sonni","year":"2015","journal-title":"Neurobiol Aging"},{"issue":"13","key":"2026030301023486300_ref100","doi-asserted-by":"publisher","first-page":"3923","DOI":"10.1002\/hbm.25893","article-title":"Spindle-slow oscillation coupling correlates with memory performance and connectivity changes in a hippocampal network after sleep","volume":"43","author":"Bastian","year":"2022","journal-title":"Hum Brain Mapp"},{"key":"2026030301023486300_ref101","doi-asserted-by":"publisher","first-page":"e78191","DOI":"10.7554\/eLife.78191","article-title":"Timely coupling of sleep spindles and slow waves linked to early amyloid-\u03b2 burden and predicts memory decline","volume":"11","author":"Chylinski","year":"2022","journal-title":"Elife."},{"issue":"12","key":"2026030301023486300_ref102","doi-asserted-by":"publisher","first-page":"1655","DOI":"10.1038\/s41593-020-00744-x","article-title":"Parameterizing neural power spectra into periodic and aperiodic components","volume":"23","author":"Donoghue","year":"2020","journal-title":"Nat Neurosci"},{"key":"2026030301023486300_ref103","doi-asserted-by":"publisher","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":"Muller","year":"2016","journal-title":"Elife"}],"container-title":["SLEEP Advances"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/sleepadvances\/advance-article-pdf\/doi\/10.1093\/sleepadvances\/zpaf084\/65499011\/zpaf084.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/sleepadvances\/article-pdf\/6\/4\/zpaf084\/65499011\/zpaf084.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/sleepadvances\/article-pdf\/6\/4\/zpaf084\/65499011\/zpaf084.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,3]],"date-time":"2026-03-03T06:02:44Z","timestamp":1772517764000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/sleepadvances\/article\/doi\/10.1093\/sleepadvances\/zpaf084\/8342278"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025]]},"references-count":103,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2025,10,2]]}},"URL":"https:\/\/doi.org\/10.1093\/sleepadvances\/zpaf084","relation":{},"ISSN":["2632-5012"],"issn-type":[{"value":"2632-5012","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025]]},"published":{"date-parts":[[2025]]},"article-number":"zpaf084"}}