{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,14]],"date-time":"2026-04-14T01:51:41Z","timestamp":1776131501349,"version":"3.50.1"},"reference-count":47,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,12,1]],"date-time":"2017-12-01T00:00:00Z","timestamp":1512086400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,12,1]],"date-time":"2017-12-01T00:00:00Z","timestamp":1512086400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>There are two basic stages of fine motor learning: performance gain might occur during practice (online learning), and improvement might take place without any further practice (offline learning). Offline learning, also called consolidation, has a sleep-dependent stage in terms of both speed and accuracy of the learned movement. Sleep spindle or sigma band characteristics affect motor learning in typically developing individuals. Here we ask whether the earlier found, altered sigma activity in a neurodevelopmental disorder (Williams syndrome, WS) predicts motor learning. TD and WS participants practiced in a sequential finger tapping (FT) task for two days. Although WS participants started out at a lower performance level, TD and WS participants had a comparable amount of online and offline learning in terms of the accuracy of movement. Spectral analysis of WS sleep EEG recordings revealed that motor accuracy improvement is intricately related to WS-specific NREM sleep EEG features in the 8\u201316\u2009Hz range profiles: higher 11\u201313.5\u2009Hz z-transformed power is associated with higher offline FT accuracy improvement; and higher oscillatory peak frequencies are associated with lower offline accuracy improvements. These findings indicate a fundamental relationship between sleep spindle (or sigma band) activity and motor learning in WS.<\/jats:p>","DOI":"10.1038\/s41598-017-12489-y","type":"journal-article","created":{"date-parts":[[2017,11,27]],"date-time":"2017-11-27T12:13:19Z","timestamp":1511784799000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Sigma frequency dependent motor learning in Williams syndrome"],"prefix":"10.1038","volume":"7","author":[{"given":"Andrea","family":"Berencsi","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"R\u00f3bert","family":"B\u00f3dizs","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ferenc","family":"Gombos","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Szandra","family":"L\u00e1szl\u00f3","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ilona","family":"Kov\u00e1cs","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2017,12,1]]},"reference":[{"key":"12489_CR1","doi-asserted-by":"publisher","first-page":"12492","DOI":"10.1073\/pnas.2035019100","volume":"100","author":"M Korman","year":"2003","unstructured":"Korman, M., Raz, N., Flash, T. & Karni, A. Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance. Proc. Natl. Acad. Sci. USA \n                           100, 12492\u201312497, https:\/\/doi.org\/10.1073\/pnas.2035019100 (2003).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"12489_CR2","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1038\/nature01930","volume":"425","author":"MP Walker","year":"2003","unstructured":"Walker, M. P., Brakefield, T., Hobson, J. A. & Stickgold, R. Dissociable stages of human memory consolidation and reconsolidation. Nature \n                           425, 616\u2013620, https:\/\/doi.org\/10.1038\/nature01930 (2003).","journal-title":"Nature"},{"key":"12489_CR3","doi-asserted-by":"publisher","first-page":"11987","DOI":"10.1073\/pnas.182178199","volume":"99","author":"S Fischer","year":"2002","unstructured":"Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. Sleep forms memory for finger skills. Proc. Natl. Acad. Sci. USA \n                           99, 11987\u201311991, https:\/\/doi.org\/10.1073\/pnas.182178199 (2002).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"12489_CR4","first-page":"1149","volume":"31","author":"A Morin","year":"2008","unstructured":"Morin, A. et al. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep \n                           31, 1149\u20131156 (2008).","journal-title":"Sleep"},{"key":"12489_CR5","doi-asserted-by":"publisher","first-page":"250","DOI":"10.1111\/j.1365-2869.2006.00522.x","volume":"15","author":"S Fogel","year":"2006","unstructured":"Fogel, S. & Smith, C. T. Learning-dependent changes in sleep spindles and Stage 2 sleep. Journal of Sleep Research \n                           15, 250\u2013255 (2006).","journal-title":"Journal of Sleep Research"},{"key":"12489_CR6","doi-asserted-by":"publisher","first-page":"2918","DOI":"10.1002\/hbm.22116","volume":"34","author":"M Barakat","year":"2013","unstructured":"Barakat, M. et al. Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum. Brain. Mapp \n                           34, 2918\u20132928, https:\/\/doi.org\/10.1002\/hbm.22116 (2013).","journal-title":"Hum. Brain. Mapp"},{"key":"12489_CR7","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.bbr.2010.10.019","volume":"217","author":"M Barakat","year":"2011","unstructured":"Barakat, M. et al. Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. \n                           217, 117\u2013121, https:\/\/doi.org\/10.1016\/j.bbr.2010.10.019 (2011).","journal-title":"Behav. Brain Res."},{"key":"12489_CR8","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1016\/j.neurobiolaging.2016.10.009","volume":"49","author":"S Fogel","year":"2017","unstructured":"Fogel, S. et al. Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation. Neurobiol. Aging \n                           49, 154\u2013164, https:\/\/doi.org\/10.1016\/j.neurobiolaging.2016.10.009 (2017).","journal-title":"Neurobiol. Aging"},{"key":"12489_CR9","doi-asserted-by":"publisher","first-page":"3625","DOI":"10.1002\/hbm.22426","volume":"35","author":"SM Fogel","year":"2014","unstructured":"Fogel, S. M. et al. fMRI and sleep correlates of the age-related impairment in motor memory consolidation. Hum. Brain Mapp. \n                           35, 3625\u20133645, https:\/\/doi.org\/10.1002\/hbm.22426 (2014).","journal-title":"Hum. 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Sleep \n                           31, 204\u2013211 (2008).","journal-title":"Sleep"},{"key":"12489_CR12","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1111\/j.1365-2869.2009.00740.x","volume":"18","author":"MA Tucker","year":"2009","unstructured":"Tucker, M. A. & Fishbein, W. The impact of sleep duration and subject intelligence on declarative and motor memory performance: how much is enough? J. Sleep Res. \n                           18, 304\u2013312, https:\/\/doi.org\/10.1111\/j.1365-2869.2009.00740.x (2009).","journal-title":"J. Sleep Res."},{"key":"12489_CR13","doi-asserted-by":"publisher","first-page":"13894","DOI":"10.1523\/JNEUROSCI.1198-13.2013","volume":"33","author":"M Tamaki","year":"2013","unstructured":"Tamaki, M. et al. Enhanced spontaneous oscillations in the supplementary motor area are associated with sleep-dependent offline learning of finger-tapping motor-sequence task. J. Neurosci. \n                           33, 13894\u201313902, https:\/\/doi.org\/10.1523\/JNEUROSCI.1198-13.2013 (2013).","journal-title":"J. Neurosci."},{"key":"12489_CR14","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1016\/j.psyneuen.2011.11.006","volume":"37","author":"L Genzel","year":"2012","unstructured":"Genzel, L. et al. Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology \n                           37, 987\u2013998, https:\/\/doi.org\/10.1016\/j.psyneuen.2011.11.006 (2012).","journal-title":"Psychoneuroendocrinology"},{"key":"12489_CR15","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1002429","volume":"14","author":"S Laventure","year":"2016","unstructured":"Laventure, S. et al. NREM2 and Sleep Spindles Are Instrumental to the Consolidation of Motor Sequence Memories. PLoS Biology \n                           14, e1002429, https:\/\/doi.org\/10.1371\/journal.pbio.1002429 (2016).","journal-title":"PLoS Biology"},{"key":"12489_CR16","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1016\/j.clinph.2009.03.006","volume":"120","author":"M Tamaki","year":"2009","unstructured":"Tamaki, M., Matsuoka, T., Nittono, H. & Hori, T. Activation of fast sleep spindles at the premotor cortex and parietal areas contributes to motor learning: a study using sLORETA. Clin. Neurophysiol. \n                           120, 878\u2013886, https:\/\/doi.org\/10.1016\/j.clinph.2009.03.006 (2009).","journal-title":"Clin. Neurophysiol."},{"key":"12489_CR17","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1037\/bne0000131","volume":"130","author":"ER Appleman","year":"2016","unstructured":"Appleman, E. R., Albouy, G., Doyon, J., Cronin-Golomb, A. & King, B. R. Sleep quality influences subsequent motor skill acquisition. Behavioral Neuroscience \n                           130, 290\u2013297, https:\/\/doi.org\/10.1037\/bne0000131 (2016).","journal-title":"Behavioral Neuroscience"},{"key":"12489_CR18","doi-asserted-by":"publisher","DOI":"10.3389\/fnhum.2014.00910","volume":"8","author":"RG Astill","year":"2014","unstructured":"Astill, R. G. et al. Sleep spindle and slow wave frequency reflect motor skill performance in primary school-age children. Front. Hum. Neurosci. \n                           8, 910, https:\/\/doi.org\/10.3389\/fnhum.2014.00910 (2014).","journal-title":"Front. Hum. Neurosci."},{"key":"12489_CR19","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1016\/j.neuroimage.2005.01.020","volume":"26","author":"L De Gennaro","year":"2005","unstructured":"De Gennaro, L., Ferrara, M., Vecchio, F., Curcio, G. & Bertini, M. An electroencephalographic fingerprint of human sleep. Neuroimage \n                           26, 114\u2013122, https:\/\/doi.org\/10.1016\/j.neuroimage.2005.01.020 (2005).","journal-title":"Neuroimage"},{"key":"12489_CR20","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1002\/ana.21434","volume":"64","author":"L De Gennaro","year":"2008","unstructured":"De Gennaro, L. et al. The electroencephalographic fingerprint of sleep is genetically determined: a twin study. Annals of Neurology \n                           64, 455\u2013460, https:\/\/doi.org\/10.1002\/ana.21434 (2008).","journal-title":"Annals of Neurology"},{"key":"12489_CR21","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.ridd.2011.09.004","volume":"33","author":"R Bodizs","year":"2012","unstructured":"Bodizs, R., Gombos, F. & Kovacs, I. Sleep EEG fingerprints reveal accelerated thalamocortical oscillatory dynamics in Williams syndrome. Res. Dev. Disabil. \n                           33, 153\u2013164, https:\/\/doi.org\/10.1016\/j.ridd.2011.09.004 (2012).","journal-title":"Res. Dev. Disabil."},{"key":"12489_CR22","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1111\/jir.12317","volume":"60","author":"A Berencsi","year":"2016","unstructured":"Berencsi, A., Gombos, F. & Kovacs, I. Capacity to improve fine motor skills in Williams syndrome. J. Intellect. Disabil. Res. \n                           60, 956\u2013968, https:\/\/doi.org\/10.1111\/jir.12317 (2016).","journal-title":"J. Intellect. Disabil. Res."},{"issue":"Suppl 1","key":"12489_CR23","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1162\/089892900561959","volume":"12","author":"U Bellugi","year":"2000","unstructured":"Bellugi, U., Lichtenberger, L., Jones, W., Lai, Z. & St George, M. I. The neurocognitive profile of Williams Syndrome: a complex pattern of strengths and weaknesses. Journal of Cognitive Neuroscience \n                           12(Suppl 1), 7\u201329 (2000).","journal-title":"Journal of Cognitive Neuroscience"},{"key":"12489_CR24","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1002\/1096-8628(200022)97:2<164::AID-AJMG8>3.0.CO;2-F","volume":"97","author":"D Donnai","year":"2000","unstructured":"Donnai, D. & Karmiloff-Smith, A. Williams syndrome: from genotype through to the cognitive phenotype. American Journal of Medical Genetics \n                           97, 164\u2013171 (2000).","journal-title":"American Journal of Medical Genetics"},{"key":"12489_CR25","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1016\/j.pediatrneurol.2004.09.013","volume":"32","author":"X Carrasco","year":"2005","unstructured":"Carrasco, X., Castillo, S., Aravena, T., Rothhammer, P. & Aboitiz, F. Williams syndrome: pediatric, neurologic, and cognitive development. Pediatr. Neurol. \n                           32, 166\u2013172, https:\/\/doi.org\/10.1016\/j.pediatrneurol.2004.09.013 (2005).","journal-title":"Pediatr. Neurol."},{"key":"12489_CR26","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1177\/088307389601100116","volume":"11","author":"CA Chapman","year":"1996","unstructured":"Chapman, C. A., du Plessis, A. & Pober, B. R. Neurologic findings in children and adults with Williams syndrome. J. Child Neurol. \n                           11, 63\u201365 (1996).","journal-title":"J. Child Neurol."},{"key":"12489_CR27","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/j.ridd.2010.09.008","volume":"32","author":"D Annaz","year":"2011","unstructured":"Annaz, D., Hill, C. M., Ashworth, A., Holley, S. & Karmiloff-Smith, A. Characterisation of sleep problems in children with Williams syndrome. Res. Dev. Disabil. \n                           32, 164\u2013169, https:\/\/doi.org\/10.1016\/j.ridd.2010.09.008 (2011).","journal-title":"Res. 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In 12th International Professional Conference on Williams Syndrome."},{"key":"12489_CR31","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1111\/j.1365-2788.2010.01354.x","volume":"55","author":"F Gombos","year":"2011","unstructured":"Gombos, F., Bodizs, R. & Kovacs, I. Atypical sleep architecture and altered EEG spectra in Williams syndrome. J. Intellect. Disabil. Res. \n                           55, 255\u2013262, https:\/\/doi.org\/10.1111\/j.1365-2788.2010.01354.x (2011).","journal-title":"J. Intellect. Disabil. Res."},{"key":"12489_CR32","doi-asserted-by":"publisher","first-page":"892","DOI":"10.1016\/j.sleep.2011.05.003","volume":"12","author":"TB Mason","year":"2011","unstructured":"Mason, T. B. et al. Sleep in children with Williams Syndrome. Sleep Medicine \n                           12, 892\u2013897, https:\/\/doi.org\/10.1016\/j.sleep.2011.05.003 (2011).","journal-title":"Sleep Medicine"},{"key":"12489_CR33","doi-asserted-by":"publisher","first-page":"491","DOI":"10.5664\/jcsm.3692","volume":"10","author":"S Landry","year":"2014","unstructured":"Landry, S., Anderson, C., Andrewartha, P., Sasse, A. & Conduit, R. The impact of obstructive sleep apnea on motor skill acquisition and consolidation. J. Clin. Sleep. Med. \n                           10, 491\u2013496, https:\/\/doi.org\/10.5664\/jcsm.3692 (2014).","journal-title":"J. Clin. Sleep. Med."},{"key":"12489_CR34","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1016\/j.biopsych.2004.09.012","volume":"56","author":"DS Manoach","year":"2004","unstructured":"Manoach, D. S. et al. A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biol. Psychiatry \n                           56, 951\u2013956, https:\/\/doi.org\/10.1016\/j.biopsych.2004.09.012 (2004).","journal-title":"Biol. Psychiatry"},{"key":"12489_CR35","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.jpsychires.2009.06.011","volume":"44","author":"DS Manoach","year":"2010","unstructured":"Manoach, D. S. et al. Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J. Psychiatr. Res. \n                           44, 112\u2013120, https:\/\/doi.org\/10.1016\/j.jpsychires.2009.06.011 (2010).","journal-title":"J. Psychiatr. Res."},{"key":"12489_CR36","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.1016\/j.ridd.2011.01.048","volume":"32","author":"E Adi-Japha","year":"2011","unstructured":"Adi-Japha, E., Fox, O. & Karni, A. Atypical acquisition and atypical expression of memory consolidation gains in a motor skill in young female adults with ADHD. Res. Dev. 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