Sex differences in the association of sleep spindle density and cognitive performance among community-dwelling middle-aged and older adults with obstructive sleep apnea.
aging
cognition
community-dwelling
obstructive sleep apnea
older adults
polysomnography
sleep
sleep apnea
spindles
Journal
Journal of sleep research
ISSN: 1365-2869
Titre abrégé: J Sleep Res
Pays: England
ID NLM: 9214441
Informations de publication
Date de publication:
14 Nov 2023
14 Nov 2023
Historique:
revised:
24
10
2023
received:
15
05
2023
accepted:
26
10
2023
medline:
15
11
2023
pubmed:
15
11
2023
entrez:
14
11
2023
Statut:
aheadofprint
Résumé
Recent studies have found associations between obstructive sleep apnea and cognitive decline. The underlying mechanisms are still unclear. Here, we investigate the associations between changes in micro-architecture, specifically sleep spindles, and cognitive function in community-dwelling middle-aged and older adults, some with obstructive sleep apnea, with a focus on sex differences. A total of 125 voluntary participants (mean age 66.0 ± 6.4 years, 64 females) from a larger cohort (participants of the Brain in Motion Studies I and II) underwent 1 night of in-home polysomnography and a neuropsychological battery (sleep and cognitive testing were conducted within 2 weeks of each other). A semi-automatic computerized algorithm was used to score polysomnography data and detect spindle characteristics in non-rapid eye movement Stages 2 and 3 in both frontal and central electrodes. Based on their apnea-hypopnea index, participants were divided into those with no obstructive sleep apnea (apnea-hypopnea index < 5 per hr, n = 21), mild obstructive sleep apnea (5 ≥ apnea-hypopnea index < 15, n = 47), moderate obstructive sleep apnea (15 ≥ apnea-hypopnea index < 30, n = 34) and severe obstructive sleep apnea (apnea-hypopnea index ≥ 30, n = 23). There were no significant differences in spindle characteristics between the four obstructive sleep apnea severity groups. Spindle density and percentage of fast spindles were positively associated with some verbal fluency measures on the cognitive testing. Sex might be linked with these associations. Biological sex could play a role in the associations between spindle characteristics and some verbal fluency measures. Obstructive sleep apnea severity was not found to be a contributing factor in this non-clinical community-dwelling cohort.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14095Subventions
Organisme : CIHR
ID : FRN: 162166
Pays : Canada
Informations de copyright
© 2023 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.
Références
Antony, J. W., & Paller, K. A. (2017). Using oscillating sounds to manipulate sleep spindles. Sleep, 40(3), 1-8. https://doi.org/10.1093/sleep/zsw068
Baillet, M., & Schmidt, C. (2020). Sleep, rest-activity fragmentation and structural brain changes related to the ageing process. Current Opinion in Behavioral Sciences, 33, 8-16. https://doi.org/10.1016/j.cobeha.2019.11.003
Beaudin, A. E., Hanly, P. J., Raneri, J. K., Sajobi, T. T., Anderson, T. J., & Poulin, M. J. (2019). Vascular responses to hypoxia are not impaired in obstructive sleep apnoea patients free of overt cardiovascular disease. Experimental Physiology, 104(4), 580-600. https://doi.org/10.1113/ep086845
Beaudin, A. E., Raneri, J. K., Ayas, N. T., Skomro, R. P., Fox, N., Hirsch Allen, A. J. M., Bowen, M. W., Nocon, A., Lynch, E. J., Wang, M., Smith, E. E., & Hanly, P. J. (2021). Cognitive function in a sleep clinic cohort of patients with obstructive sleep apnea. Annals of the American Thoracic Society, 18(5), 865-875. https://doi.org/10.1513/AnnalsATS.202004-313OC
Berry, R. B., Budhiraja, R., Gottlieb, D. J., Gozal, D., Iber, C., Kapur, V. K., Marcus, C. L., Mehra, R., Parthasarathy, S., Quan, S. F., Redline, S., Strohl, K. P., Ward, S. L. D., & Tangredi, M. M. (2012). Rules for scoring respiratory events in sleep: Update of the 2007 AASM manual for the scoring of sleep and associated events. Deliberations of the sleep apnea definitions task force of the American Academy of sleep medicine. Journal of Clinical Sleep Medicine, 8(5), 597-619. https://doi.org/10.5664/jcsm.2172
Berry, R. B., Quan, S. F., Abreu, A. R., Bibbs, M. L., DelRosso, L., Harding, S. M., Vaughn, B. V., & Troester, M. M. (2020). The AASM manual for the scoring of sleep and associated events: Rules, terminology and technical specifications. In The AASM manual for the scoring of sleep and associated events v2.6 (print). American Academy of Sleep Medicine https://learn.aasm.org/Listing/a1341000002XmQtAAK
Boutin, A., & Doyon, J. (2020). A sleep spindle framework for motor memory consolidation. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1799), 20190232. https://doi.org/10.1098/rstb.2019.0232
Brockmann, P. E., Damiani, F., Pincheira, E., Daiber, F., Ruiz, S., Aboitiz, F., Ferri, R., & Bruni, O. (2018). Sleep spindle activity in children with obstructive sleep apnea as a marker of neurocognitive performance: A pilot study. European Journal of Paediatric Neurology, 22(3), 434-439. https://doi.org/10.1016/j.ejpn.2018.02.003
Bubu, O. M., Andrade, A. G., Umasabor-Bubu, O. Q., Hogan, M. M., Turner, A. D., de Leon, M. J., Ogedegbe, G., Ayappa, I., Jean-Louis, G. G., Jackson, M. L., Varga, A. W., & Osorio, R. S. (2020). Obstructive sleep apnea, cognition and Alzheimer's disease: A systematic review integrating three decades of multidisciplinary research. Sleep Medicine Reviews, 50, 101250. https://doi.org/10.1016/j.smrv.2019.101250
Bucks, R. S., Olaithe, M., Rosenzweig, I., & Morrell, M. J. (2017). Reviewing the relationship between OSA and cognition: Where do we go from here? Respirology, 22(7), 1253-1261. https://doi.org/10.1111/resp.13140
Buysse, D. J., Hall, M. L., Strollo, P. J., Kamarck, T. W., Owens, J., Lee, L., Reis, S. E., & Matthews, K. A. (2008). Relationships between the Pittsburgh sleep quality index (PSQI), Epworth sleepiness scale (ESS), and clinical/polysomnographic measures in a community sample. Journal of Clinical Sleep Medicine, 4(6), 563-571. https://doi.org/10.5664/jcsm.27351
Carley, D. W., & Farabi, S. S. (2016). Physiology of sleep. Diabetes Spectrum, 29(1), 5-9. https://doi.org/10.2337/diaspect.29.1.5
Champetier, P., André, C., Weber, F. D., Rehel, S., Ourry, V., Laniepce, A., Lutz, A., Bertran, F., Cabé, N., Pitel, A.-L., Poisnel, G., de la Sayette, V., Vivien, D., Chételat, G., Rauchs, G., & Medit-Ageing Research, G. (2022). Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation. Sleep, zsac282, 1-16. https://doi.org/10.1093/sleep/zsac282
Cox, R., Schapiro, A. C., Manoach, D. S., & Stickgold, R. (2017). Individual differences in frequency and topography of slow and fast sleep spindles. Frontiers in Human Neuroscience, 11(433), 1 - 22. https://doi.org/10.3389/fnhum.2017.00433
D'Atri, A., Gorgoni, M., Scarpelli, S., Cordone, S., Alfonsi, V., Marra, C., Ferrara, M., Rossini, P. M., & De Gennaro, L. (2021). Relationship between cortical thickness and EEG alterations during sleep in the Alzheimer's disease. Brain Sciences, 11(9), 1-11. https://doi.org/10.3390/brainsci11091174
D'Rozario, A. L., Hoyos, C. M., Wong, K. K. H., Unger, G., Kim, J. W., Vakulin, A., Kao, C.-H., Naismith, S. L., Bartlett, D. J., & Grunstein, R. R. (2022). Improvements in cognitive function and quantitative sleep electroencephalogram in obstructive sleep apnea after six months of continuous positive airway pressure treatment. Sleep, 45(6), 1-9. https://doi.org/10.1093/sleep/zsac013
de Zambotti, M., Willoughby, A. R., Sassoon, S. A., Colrain, I. M., & Baker, F. C. (2015). Menstrual cycle-related variation in physiological sleep in women in the early menopausal transition. The Journal of Clinical Endocrinology and Metabolism, 100(8), 2918-2926. https://doi.org/10.1210/jc.2015-1844
Driver, H. S., Dijk, D. J., Werth, E., Biedermann, K., & Borbély, A. A. (1996). Sleep and the sleep electroencephalogram across the menstrual cycle in young healthy women. The Journal of Clinical Endocrinology & Metabolism, 81(2), 728-735. https://doi.org/10.1210/jcem.81.2.8636295
Fernandez, L. M. J., & Lüthi, A. (2020). Sleep spindles: Mechanisms and functions. Physiological Reviews, 100(2), 805-868. https://doi.org/10.1152/physrev.00042.2018
Fjell, A. M., Sørensen, Ø., Amlien, I. K., Bartrés-Faz, D., Brandmaier, A. M., Buchmann, N., Demuth, I., Drevon, C. A., Düzel, S., Ebmeier, K. P., Ghisletta, P., Idland, A.-V., Kietzmann, T. C., Kievit, R. A., Kühn, S., Lindenberger, U., Magnussen, F., Macià, D., Mowinckel, A. M., … Walhovd, K. B. (2021). Poor self-reported sleep is related to regional cortical thinning in aging but not memory decline-Results from the Lifebrain consortium. Cerebral Cortex, 31(4), 1953-1969. https://doi.org/10.1093/cercor/bhaa332
Fonseca Costa, S. S., & Ripperger, J. A. (2015). Impact of the circadian clock on the aging process. Frontiers in Neurology, 6(43), 1-5. https://doi.org/10.3389/fneur.2015.00043
Goldschmied, J. R., Lacourse, K., Maislin, G., Delfrate, J., Gehrman, P., Pack, F. M., Younes, M., Kuna, S. T., & Warby, S. C. (2021). Spindles are highly heritable as identified by different spindle detectors. Sleep, 44(4), 1-11. https://doi.org/10.1093/sleep/zsaa230
Gorgoni, M., Lauri, G., Truglia, I., Cordone, S., Sarasso, S., Scarpelli, S., Mangiaruga, A., D'Atri, A., Tempesta, D., Ferrara, M., Marra, C., Rossini, P. M., & De Gennaro, L. (2016). Parietal fast sleep spindle density decrease in Alzheimer's disease and amnesic mild cognitive impairment. Neural Plasticity, 2016, 1-10. https://doi.org/10.1155/2016/8376108
Gu, Y., Gagnon, J.-F., & Kaminska, M. (2023). Sleep electroencephalography biomarkers of cognition in obstructive sleep apnea. Journal of Sleep Research, 32(5), e13831. https://doi.org/10.1111/jsr.13831
Guadagni, V., Byles, H., Tyndall, A. V., Parboosingh, J., Longman, R. S., Hogan, D. B., Hanly, P. J., Younes, M., & Poulin, M. J. (2021). Association of sleep spindle characteristics with executive functioning in healthy sedentary middle-aged and older adults. Journal of Sleep Research, 30(2), e13037. https://doi.org/10.1111/jsr.13037
Guadagni, V., Clark, C. M., Tyndall, A., Raneri, J. K., Parboosingh, J. S., Hogan, D. B., Hanly, P. J., & Poulin, M. J. (2018). Effects of six-month aerobic exercise intervention on sleep in healthy older adults in the brain in motion study: A pilot study. Journal of Alzheimer's Disease Reports, 2(1), 229-238. https://doi.org/10.3233/adr-180079
Hablitz, L. M., Plá, V., Giannetto, M., Vinitsky, H. S., Staeger, F. F., Metcalfe, T., Nguyen, R., Benrais, A., & Nedergaard, M. (2020). Circadian control of brain glymphatic and lymphatic fluid flow. Nature Communications, 11(1), 4411. https://doi.org/10.1038/s41467-020-18115-2
Hobson, J. A., & Pace-Schott, E. F. (2002). The cognitive neuroscience of sleep: Neuronal systems, consciousness and learning. Nature Reviews Neuroscience, 3(9), 679-693. https://doi.org/10.1038/nrn915
Huupponen, E., Himanen, S. L., Värri, A., Hasan, J., Lehtokangas, M., & Saarinen, J. (2002). A study on gender and age differences in sleep spindles. Neuropsychobiology, 45(2), 99-105. https://doi.org/10.1159/000048684
Hödlmoser, K., Herzog, S., & Kerschbaum, H. (2019). The effect of sex hormones on sleep spindles and cognitive performance. Paper presented at the 26th Annual Meeting of the Cognitive Neuroscience Society (CNS).
Iotchev, I. B., Kis, A., Turcsán, B., Fernández, T., de Lara, D. R., Reicher, V., & Kubinyi, E. (2019). Age-related differences and sexual dimorphism in canine sleep spindles. Scientific Reports, 9(1), 10092. https://doi.org/10.1038/s41598-019-46434-y
Johns, M. W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14(6), 540-545. https://doi.org/10.1093/sleep/14.6.540
Kaestner, E. J., Wixted, J. T., & Mednick, S. C. (2013). Pharmacologically increasing sleep spindles enhances recognition for negative and high-arousal memories. Journal of Cognitive Neuroscience, 25(10), 1597-1610. https://doi.org/10.1162/jocn_a_00433
Kamel, N. S., & Gammack, J. K. (2006). Insomnia in the elderly: Cause, approach, and treatment. The American Journal of Medicine, 119(6), 463-469. https://doi.org/10.1016/j.amjmed.2005.10.051
Khawaja, I. S., Olson, E. J., van der Walt, C., Bukartyk, J., Somers, V., Dierkhising, R., & Morgenthaler, T. I. (2010). Diagnostic accuracy of split-night polysomnograms. Journal of Clinical Sleep Medicine, 6(4), 357-362. https://doi.org/10.5664/jcsm.27877
Krysta, K., Bratek, A., Zawada, K., & Stepańczak, R. (2017). Cognitive deficits in adults with obstructive sleep apnea compared to children and adolescents. Journal of Neural Transmission (Vienna), 124(Suppl 1), 187-201. https://doi.org/10.1007/s00702-015-1501-6
Krüger, R. L., Clark, C. M., Dyck, A. M., Anderson, T. J., Clement, F., Hanly, P. J., Hanson, H. M., Hill, M. D., Hogan, D. B., Holroyd-Leduc, J., Longman, R. S., McDonough, M., Pike, G. B., Rawling, J. M., Sajobi, T., & Poulin, M. J. (2021). The brain in motion II study: Study protocol for a randomized controlled trial of an aerobic exercise intervention for older adults at increased risk of dementia. Trials, 22(1), 394. https://doi.org/10.1186/s13063-021-05336-z
Lafortune, M., Gagnon, J. F., Martin, N., Latreille, V., Dubé, J., Bouchard, M., Bastien, C., & Carrier, J. (2014). Sleep spindles and rapid eye movement sleep as predictors of next morning cognitive performance in healthy middle-aged and older participants. Journal of Sleep Research, 23(2), 159-167. https://doi.org/10.1111/jsr.12108
Lal, C., Ayappa, I., Ayas, N., Beaudin, A. E., Hoyos, C., Kushida, C. A., Kaminska, M., Mullins, A., Naismith, S. L., Osorio, R. S., Phillips, C. L., Parekh, A., Stone, K. L., Turner, A. D., & Varga, A. W. (2022). The link between obstructive sleep apnea and neurocognitive impairment: An official American Thoracic Society workshop report. Annals of the American Thoracic Society, 19(8), 1245-1256. https://doi.org/10.1513/AnnalsATS.202205-380ST
Latreille, V., Willment, K. C., Sarkis, R. A., & Pavlova, M. (2019). Neuropsychological correlates of obstructive sleep apnea severity in patients with epilepsy. Epileptic Disorders, 21(1), 78-86. https://doi.org/10.1684/epd.2019.1029
Lee, H.-J., Lee, D. A., Shin, K. J., & Park, K. M. (2022). Glymphatic system dysfunction in obstructive sleep apnea evidenced by DTI-ALPS. Sleep Medicine, 89, 176-181. https://doi.org/10.1016/j.sleep.2021.12.013
Li, S.-B., Damonte, V. M., Chen, C., Wang, G. X., Kebschull, J. M., Yamaguchi, H., Bian, W.-J., Purmann, C., Pattni, R., Urban, A. E., Mourrain, P., Kauer, J. A., Scherrer, G., & de Lecea, L. (2022). Hyperexcitable arousal circuits drive sleep instability during aging. Science, 375(6583) 1-14. https://doi.org/10.1126/science.abh3021
Lohela, T. J., Lilius, T. O., & Nedergaard, M. (2022). The glymphatic system: Implications for drugs for central nervous system diseases. Nature Reviews. Drug Discovery, 21, 763-779. https://doi.org/10.1038/s41573-022-00500-9
Lustenberger, C., Patel, Y. A., Alagapan, S., Page, J. M., Price, B., Boyle, M. R., & Fröhlich, F. (2018). High-density EEG characterization of brain responses to auditory rhythmic stimuli during wakefulness and NREM sleep. NeuroImage, 169, 57-68. https://doi.org/10.1016/j.neuroimage.2017.12.007
Mander, B. A., Dave, A., Lui, K. K., Sprecher, K. E., Berisha, D., Chappel-Farley, M. G., Chen, I. Y., Riedner, B. A., Heston, M., Suridjan, I., Kollmorgen, G., Zetterberg, H., Blennow, K., Carlsson, C. M., Okonkwo, O. C., Asthana, S., Johnson, S. C., Bendlin, B. B., & Benca, R. M. (2022). Inflammation, tau pathology, and synaptic integrity associated with sleep spindles and memory prior to β-amyloid positivity. Sleep, zsac135, 1-21. https://doi.org/10.1093/sleep/zsac135
Mander, B. A., Winer, J. R., & Walker, M. P. (2017). Sleep and human aging. Neuron, 94(1), 19-36. https://doi.org/10.1016/j.neuron.2017.02.004
Martin, N., Lafortune, M., Godbout, J., Barakat, M., Robillard, R., Poirier, G., Bastien, C., & Carrier, J. (2013). Topography of age-related changes in sleep spindles. Neurobiology of Aging, 34(2), 468-476. https://doi.org/10.1016/j.neurobiolaging.2012.05.020
McDevitt, E. A., Krishnan, G. P., Bazhenov, M., & Mednick, S. C. (2017). The role of sleep spindles in sleep-dependent memory consolidation. In N. Axmacher & B. Rasch (Eds.), Cognitive neuroscience of memory consolidation (pp. 209-226). Springer International Publishing.
McSorley, V. E., Bin, Y. S., & Lauderdale, D. S. (2019). Associations of sleep characteristics with cognitive function and decline among older adults. American Journal of Epidemiology, 188(6), 1066-1075. https://doi.org/10.1093/aje/kwz037
Mednick, S. C., McDevitt, E. A., Walsh, J. K., Wamsley, E., Paulus, M., Kanady, J. C., & Drummond, S. P. (2013). The critical role of sleep spindles in hippocampal-dependent memory: A pharmacology study. The Journal of Neuroscience, 33(10), 4494-4504. https://doi.org/10.1523/jneurosci.3127-12.2013
Mohammadi, H., Aarabi, A., Rezaei, M., Khazaie, H., & Brand, S. (2021). Sleep spindle characteristics in obstructive sleep apnea syndrome (OSAS). Frontiers in Neurology, 12, 598632. https://doi.org/10.3389/fneur.2021.598632
Muñoz-Torres, Z., Jiménez-Correa, U., & Montes-Rodríguez, C. J. (2020). Sex differences in brain oscillatory activity during sleep and wakefulness in obstructive sleep apnea. Journal of Sleep Research, 29(4), e12977. https://doi.org/10.1111/jsr.12977
Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J. L., & Chertkow, H. (2005). The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695-699. https://doi.org/10.1111/j.1532-5415.2005.53221.x
Ohayon, M. M., Carskadon, M. A., Guilleminault, C., & Vitiello, M. V. (2004). Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: Developing normative sleep values across the human lifespan. Sleep, 27(7), 1255-1273. https://doi.org/10.1093/sleep/27.7.1255
Olaithe, M., Bucks, R. S., Hillman, D. R., & Eastwood, P. R. (2018). Cognitive deficits in obstructive sleep apnea: Insights from a meta-review and comparison with deficits observed in COPD, insomnia, and sleep deprivation. Sleep Medicine Reviews, 38, 39-49. https://doi.org/10.1016/j.smrv.2017.03.005
Parker, J. L., Appleton, S. L., Melaku, Y. A., D'Rozario, A. L., Wittert, G. A., Martin, S. A., Toson, B., Catcheside, P. G., Lechat, B., Teare, A. J., Adams, R. J., & Vakulin, A. (2022a). The association between sleep microarchitecture and cognitive function in middle-aged and older men: A community-based cohort study. Journal of Clinical Sleep Medicine, 18(6), 1593-1608. https://doi.org/10.5664/jcsm.9934
Parker, J. L., Melaku, Y. A., D'Rozario, A. L., Wittert, G. A., Martin, S. A., Catcheside, P. G., Lechat, B., Teare, A. J., Adams, R. J., Appleton, S. L., & Vakulin, A. (2022b). The association between obstructive sleep apnea and sleep spindles in middle-aged and older men: A community-based cohort study. Sleep, 45(3), 1-9. https://doi.org/10.1093/sleep/zsab282
Paßmann, S., Külzow, N., Ladenbauer, J., Antonenko, D., Grittner, U., Tamm, S., & Flöel, A. (2016). Boosting slow oscillatory activity using tDCS during early nocturnal slow wave sleep does not improve memory consolidation in healthy older adults. Brain Stimulation, 9(5), 730-739. https://doi.org/10.1016/j.brs.2016.04.016
Plamberger, C. P., Van Wijk, H. E., Kerschbaum, H., Pletzer, B. A., Gruber, G., Oberascher, K., Dresler, M., Hahn, M. A., & Hoedlmoser, K. (2021). Impact of menstrual cycle phase and oral contraceptives on sleep and overnight memory consolidation. Journal of Sleep Research, 30(4), e13239. https://doi.org/10.1111/jsr.13239
Plante, D. T., Goldstein, M. R., Landsness, E. C., Peterson, M. J., Riedner, B. A., Ferrarelli, F., Wanger, T., Guokas, J. J., Tononi, G., & Benca, R. M. (2013). Topographic and sex-related differences in sleep spindles in major depressive disorder: A high-density EEG investigation. Journal of Affective Disorders, 146(1), 120-125. https://doi.org/10.1016/j.jad.2012.06.016
Purcell, S. M., Manoach, D. S., Demanuele, C., Cade, B. E., Mariani, S., Cox, R., Panagiotaropoulou, G., Saxena, R., Pan, J. Q., Smoller, J. W., Redline, S., & Stickgold, R. (2017). Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nature Communications, 8, 1-16. https://doi.org/10.1038/ncomms15930
Regidor, P. A. (2014). Progesterone in peri- and Postmenopause: A review. Geburtshilfe Und Frauenheilkunde, 74(11), 995-1002. https://doi.org/10.1055/s-0034-1383297
Reynolds, C. M., Short, M. A., & Gradisar, M. (2018). Sleep spindles and cognitive performance across adolescence: A meta-analytic review. Journal of Adolescence, 66, 55-70. https://doi.org/10.1016/j.adolescence.2018.04.003
Ricci, A., He, F., Calhoun, S. L., Fang, J., Vgontzas, A. N., Liao, D., Bixler, E. O., Younes, M., & Fernandez-Mendoza, J. (2021). Sex and pubertal differences in the maturational trajectories of sleep spindles in the transition from childhood to adolescence: A population-based study. eNeuro, 8(4), 1-13. https://doi.org/10.1523/eneuro.0257-21.2021
Sattari, N., McDevitt, E. A., Panas, D., Niknazar, M., Ahmadi, M., Naji, M., Baker, F. C., & Mednick, S. C. (2017). The effect of sex and menstrual phase on memory formation during a nap. Neurobiology of Learning and Memory, 145, 119-128. https://doi.org/10.1016/j.nlm.2017.09.007
Scullin, M. K. (2017). Do older adults need sleep? A review of neuroimaging, sleep, and aging studies. Current Sleep Medicine Reports, 3(3), 204-214. https://doi.org/10.1007/s40675-017-0086-z
Smith, A. (1982). Symbol digit modalities test. Western Psychological Services Los Angeles.
Stevens, D., Leong, C. W. Y., Cheung, H., Arciuli, J., Vakulin, A., Kim, J.-W., Openshaw, H. D., Rae, C. D., Wong, K. K. H., Dijk, D.-J., Leow, J. W. S., Saini, B., Grunstein, R. R., & D'Rozario, A. L. (2021). Sleep spindle activity correlates with implicit statistical learning consolidation in untreated obstructive sleep apnea patients. Sleep Medicine, 86, 126-134. https://doi.org/10.1016/j.sleep.2021.01.035
Tyndall, A. V., Davenport, M. H., Wilson, B. J., Burek, G. M., Arsenault-Lapierre, G., Haley, E., Eskes, G. A., Friedenreich, C. M., Hill, M. D., Hogan, D. B., Longman, R. S., Anderson, T. J., Leigh, R., Smith, E. E., & Poulin, M. J. (2013). The brain-in-motion study: Effect of a 6-month aerobic exercise intervention on cerebrovascular regulation and cognitive function in older adults. BMC Geriatrics, 13, 1-10. https://doi.org/10.1186/1471-2318-13-21
Ujma, P. P., Gombos, F., Genzel, L., Konrad, B. N., Simor, P., Steiger, A., Dresler, M., & Bódizs, R. (2015). A comparison of two sleep spindle detection methods based on all night averages: Individually adjusted vs. fixed frequencies. Frontiers in Human Neuroscience, 9(52), 1-11. https://doi.org/10.3389/fnhum.2015.00052
Ujma, P. P., Konrad, B. N., Genzel, L., Bleifuss, A., Simor, P., Pótári, A., Pawlowski, M., Steiger, A., Bódizs, R., & Dresler, M. (2014). Sleep spindles and intelligence: Evidence for a sexual dimorphism. The Journal of Neuroscience, 34(49) 16358-16368. https://doi.org/10.1523/JNEUROSCI.1857-14.2014
Vermeulen, M. C. M., Van der Heijden, K. B., Swaab, H., & Van Someren, E. J. W. (2019). Sleep spindle characteristics and sleep architecture are associated with learning of executive functions in school-age children. Journal of Sleep Research, 28(1), e12779. https://doi.org/10.1111/jsr.12779
Yetkin, O., & Aydogan, D. (2018). Effect of CPAP on sleep spindles in patients with OSA. Respiratory Physiology & Neurobiology, 247, 71-73. https://doi.org/10.1016/j.resp.2017.09.008
Younes, M., Gerardy, B., Pack, A. I., Kuna, S. T., Castro-Diehl, C., & Redline, S. (2022). Sleep architecture based on sleep depth and propensity: Patterns in different demographics and sleep disorders and association with health outcomes. Sleep, zsac059, 1-15. https://doi.org/10.1093/sleep/zsac059
Younes, M., Younes, M., & Giannouli, E. (2016). Accuracy of automatic polysomnography scoring using frontal electrodes. Journal of Clinical Sleep Medicine, 12(5), 735-746. https://doi.org/10.5664/jcsm.5808
Zhong, H.-H., Yu, B., Luo, D., Yang, L.-Y., Zhang, J., Jiang, S.-S., Hu, S.-J., Luo, Y.-Y., Yang, M.-W., Hong, F.-F., & Yang, S.-L. (2019). Roles of aging in sleep. Neuroscience & Biobehavioral Reviews, 98, 177-184. https://doi.org/10.1016/j.neubiorev.2019.01.013