Sleep,rest-activity fragmentation and structural brain changes related to the ageing process

[en] Increasing evidence suggests an association between typical age-related changes in sleep and brain structure. Here we review studies exploring the association between human histo-pathological and in vivo neuroimaging markers of brain structure and sleep-wake parameters in healthy older adults. Evidence from both large-scale epidemiological studies and in-lab quantification of specific sleep signatures are reviewed and advantages and pitfalls highlighted. Overall, the results point to an association between sleep-wake disruption and both local and diffuse changes in brain structure. The associative strength largely varies between studies and seems to partially depend on the sleep trait under investigation. The role of specific sleep-wake regulating mechanisms on human cognitive and brain fitness and more particularly their causal relationship remains to be disentangled.

Disciplines :

Neurosciences & behavior

Author, co-author :

Baillet, Marion ; Université de Liège - ULiège > GIGA CRC In vivo Imaging

Schmidt, Christina ; Université de Liège - ULiège > CRC In vivo Imaging-Sleep and chronobiology

Language :

English

Title :

Sleep,rest-activity fragmentation and structural brain changes related to the ageing process

Publication date :

2020

Journal title :

Current Opinion in Behavioral Sciences

ISSN :

2352-1546

eISSN :

2352-1554

Publisher :

Elsevier, United Kingdom

Special issue title :

Cognition and Perception - Sleep and cognition

Volume :

Pages :

8-16

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 23 January 2020

Statistics

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86 (13 by ULiège)

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244 (13 by ULiège)

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Bibliography

Daan, S., Beersma, D.G., Borbély, A.A., Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol 246 (1984), R161–183.
Muto, V., Jaspar, M., Meyer, C., Kussé, C., Chellappa, S.L., Degueldre, C., Balteau, E., Shaffii-Le Bourdiec, A., Luxen, A., Middleton, B., et al. Local modulation of human brain responses by circadian rhythmicity and sleep debt. Science 353 (2016), 687–690.
Luik, A.I., Zuurbier, L.A., Hofman, A., Van Someren, E.J.W., Ikram, M.A., Tiemeier, H., Associations of the 24-h activity rhythm and sleep with cognition: a population-based study of middle-aged and elderly persons. Sleep Med 16 (2015), 850–855.
Oosterman, J.M., van Someren, E.J.W., Vogels, R.L.C., Van Harten, B., Scherder, E.J.A., Fragmentation of the rest-activity rhythm correlates with age-related cognitive deficits. J Sleep Res 18 (2009), 129–135.
Tranah, G.J., Blackwell, T., Stone, K.L., Ancoli-Israel, S., Paudel, M.L., Ensrud, K.E., Cauley, J.A., Redline, S., Hillier, T.A., Cummings, S.R., et al. Circadian activity rhythms and risk of incident dementia and mild cognitive impairment in older women. Ann Neurol 70 (2011), 722–732.
Scullin, M.K., Bliwise, D.L., Sleep, cognition, and normal aging: integrating a half century of multidisciplinary research. Perspect Psychol Sci 10 (2015), 97–137.
Ancoli-Israel, S., Sleep and its disorders in aging populations. Sleep Med 10:Suppl. 1 (2009), S7–S11.
Stoffers, D., Moens, S., Benjamins, J., van Tol, M.-J., Penninx, B.W.J.H., Veltman, D.J., Van der Wee, N.J.A., Van Someren, E.J.W., Orbitofrontal gray matter relates to early morning awakening: a neural correlate of insomnia complaints?. Front Neurol, 3, 2012, 105.
Branger, P., Arenaza-Urquijo, E.M., Tomadesso, C., Mézenge, F., André, C., Flores, R., de, Mutlu, J., Sayette V de, L., Eustache, F., Chételat, G., et al. Relationships between sleep quality and brain volume, metabolism, and amyloid deposition in late adulthood. Neurobiol Aging 41 (2016), 107–114.
Liu, Y.-R., Fan, D.-Q., Gui, W.-J., Long, Z.-L., Lei, X., Yu, J., Sleep-related brain atrophy and disrupted functional connectivity in older adults. Behav Brain Res 347 (2018), 292–299.
Sexton, C.E., Storsve, A.B., Walhovd, K.B., Johansen-Berg, H., Fjell, A.M., Poor sleep quality is associated with increased cortical atrophy in community-dwelling adults. Neurology 83 (2014), 967–973.
Lo, J.C., Loh, K.K., Zheng, H., Sim, S.K.Y., Chee, M.W.L., Sleep duration and age-related changes in brain structure and cognitive performance. Sleep 37 (2014), 1171–1178.
Lutsey, P.L., Norby, F.L., Gottesman, R.F., Mosley, T., MacLehose, R.F., Punjabi, N.M., Shahar, E., Jack, C.R., Alonso, A., Sleep apnea, sleep duration and brain MRI markers of cerebral vascular disease and Alzheimer's disease: the atherosclerosis risk in communities study (ARIC). PLoS One, 11, 2016, e0158758.
Spira, A.P., Gonzalez, C.E., Venkatraman, V.K., Wu, M.N., Pacheco, J., Simonsick, E.M., Ferrucci, L., Resnick, S.M., Sleep duration and subsequent cortical thinning in cognitively normal older adults. Sleep 39 (2016), 1121–1128.
Carvalho, D.Z., St Louis, E.K., Boeve, B.F., Mielke, M.M., Przybelski, S.A., Knopman, D.S., Machulda, M.M., Roberts, R.O., Geda, Y.E., Petersen, R.C., et al. Excessive daytime sleepiness and fatigue may indicate accelerated brain aging in cognitively normal late middle-aged and older adults. Sleep Med 32 (2017), 236–243.
Del Brutto, O.H., Mera, R.M., Zambrano, M., Lama, J., Del Brutto, V.J., Castillo, P.R., Poor sleep quality and silent markers of cerebral small vessel disease: a population-based study in community-dwelling older adults (The Atahualpa Project). Sleep Med 16 (2015), 428–431.
Kocevska, D., Cremers, L.G.M., Lysen, T.S., Luik, A.I., Ikram, M.A., Vernooij, M.W., Tiemeier, H., Sleep complaints and cerebral white matter: a prospective bidirectional study. J Psychiatr Res 112 (2019), 77–82, 10.1016/j.jpsychires.2019.02.002.
Prins, N.D., Scheltens, P., White matter hyperintensities, cognitive impairment and dementia: an update. Nat Rev Neurol 11 (2015), 157–165.
Sexton, C.E., Zsoldos, E., Filippini, N., Griffanti, L., Winkler, A., Mahmood, A., Allan, C.L., Topiwala, A., Kyle, S.D., Spiegelhalder, K., et al. Associations between self-reported sleep quality and white matter in community-dwelling older adults: a prospective cohort study. Hum Brain Mapp 38 (2017), 5465–5473, 10.1002/hbm.23739.
Salthouse, T.A., Neuroanatomical substrates of age-related cognitive decline. Psychol Bull 137 (2011), 753–784.
Yaffe, K., Nasrallah, I., Hoang, T.D., Lauderdale, D.S., Knutson, K.L., Carnethon, M.R., Launer, L.J., Lewis, C.E., Sidney, S., Sleep duration and white matter quality in middle-aged adults. Sleep 39 (2016), 1743–1747.
Ramos, A.R., Dong, C., Rundek, T., Elkind, M.S.V., Boden-Albala, B., Sacco, R.L., Wright, C.B., Sleep duration is associated with white matter hyperintensity volume in older adults: the Northern Manhattan study. J Sleep Res 23 (2014), 524–530.
Tucker, A.M., Dinges, D.F., Van Dongen, H.P.A., Trait interindividual differences in the sleep physiology of healthy young adults. J Sleep Res 16 (2007), 170–180.
Koo, P.C., Marshall, L., Neuroscience: a sleep rhythm with multiple facets. Curr Biol 26 (2016), R813–815.
Bódizs, R., Kis, T., Lázár, A.S., Havrán, L., Rigó, P., Clemens, Z., Halász, P., Prediction of general mental ability based on neural oscillation measures of sleep. J Sleep Res 14 (2005), 285–292.
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., et al. Roles of aging in sleep. Neurosci Biobehav Rev 98 (2019), 177–184.
Gelber, R.P., Launer, L.J., White, L.R., The Honolulu-Asia aging study: epidemiologic and neuropathologic research on cognitive impairment. Curr Alzheimer Res 9 (2012), 664–672.
Gelber, R.P., Redline, S., Ross, G.W., Petrovitch, H., Sonnen, J.A., Zarow, C., Uyehara-Lock, J.H., Masaki, K.H., Launer, L.J., White, L.R., Associations of brain lesions at autopsy with polysomnography features before death. Neurology 84 (2015), 296–303.
Dubé, J., Lafortune, M., Bedetti, C., Bouchard, M., Gagnon, J.F., Doyon, J., Evans, A.C., Lina, J.-M., Carrier, J., Cortical thinning explains changes in sleep slow waves during adulthood. J Neurosci 35 (2015), 7795–7807.
Mander, B.A., Rao, V., Lu, B., Saletin, J.M., Lindquist, J.R., Ancoli-Israel, S., Jagust, W., Walker, M.P., Prefrontal atrophy, disrupted NREM slow waves, and impaired hippocampal-dependent memory in aging. Nat Neurosci 16 (2013), 357–364.
Varga, A.W., Ducca, E.L., Kishi, A., Fischer, E., Parekh, A., Koushyk, V., Yau, P.L., Gumb, T., Leibert, D.P., Wohlleber, M.E., et al. Effects of aging on slow-wave sleep dynamics and human spatial navigational memory consolidation. Neurobiol Aging 42 (2016), 142–149.
Helfrich, R.F., Mander, B.A., Jagust, W.J., Knight, R.T., Walker, M.P., Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting. Neuron 97 (2018), 221–230.e4 Recent study reporting an association between slow wave — sleep spindle coupling and specific age-related grey matter atrophy over the medial prefrontal cortex.
Fogel, S., Vien, C., Karni, A., Benali, H., Carrier, J., Doyon, J., Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation. Neurobiol Aging 49 (2017), 154–164.
Mander, B.A., Zhu, A.H., Lindquist, J.R., Villeneuve, S., Rao, V., Lu, B., Saletin, J.M., Ancoli-Israel, S., Jagust, W.J., Walker, M.P., White matter structure in older adults moderates the benefit of sleep spindles on motor memory consolidation. J Neurosci 37 (2017), 11675–11687.
Gaudreault, P.-O., Gosselin, N., Lafortune, M., Deslauriers-Gauthier, S., Martin, N., Bouchard, M., Dubé, J., Lina, J.-M., Doyon, J., Carrier, J., The association between white matter and sleep spindles differs in young and older individuals. Sleep, 41, 2018.
Bennett, D.A., Schneider, J.A., Buchman, A.S., Mendes de Leon, C., Bienias, J.L., Wilson, R.S., The rush memory and aging project: study design and baseline characteristics of the study cohort. Neuroepidemiology 25 (2005), 163–175.
Lim, A.S.P., Ellison, B.A., Wang, J.L., Yu, L., Schneider, J.A., Buchman, A.S., Bennett, D.A., Saper, C.B., Sleep is related to neuron numbers in the ventrolateral preoptic/intermediate nucleus in older adults with and without Alzheimer's disease. Brain 137 (2014), 2847–2861.
Lim, A.S.P., Yu, L., Schneider, J.A., Bennett, D.A., Buchman, A.S., Sleep fragmentation, cerebral arteriolosclerosis, and brain infarct pathology in community-dwelling older people. Stroke 47 (2016), 516–518 Post-mortem study reporting an association between actigraphy-estimated sleep fragmentation and cerebrovascular pathologies.
Wang, J.L., Lim, A.S., Chiang, W.-Y., Hsieh, W.-H., Lo, M.-T., Schneider, J.A., Buchman, A.S., Bennett, D.A., Hu, K., Saper, C.B., Suprachiasmatic neuron numbers and rest-activity circadian rhythms in older humans. Ann Neurol 78 (2015), 317–322 Post-mortem study reporting an association between actigraphy-estimated rest-activity patterns and number of VIP-expressing neurons in the suprachiasmatic nucleus.
Lim, A.S.P., Fleischman, D.A., Dawe, R.J., Yu, L., Arfanakis, K., Buchman, A.S., Bennett, D.A., Regional neocortical gray matter structure and sleep fragmentation in older adults. Sleep 39 (2016), 227–235.
André, C., Tomadesso, C., de Flores, R., Branger, P., Rehel, S., Mézenge, F., Landeau, B., Sayette, V., de la, Eustache, F., Chételat, G., et al. Brain and cognitive correlates of sleep fragmentation in elderly subjects with and without cognitive deficits. Alzheimers Dement (Amst) 11 (2019), 142–150.
Van Someren, E.J.W., Oosterman, J.M., Van Harten, B., Vogels, R.L., Gouw, A.A., Weinstein, H.C., Poggesi, A., Scheltens, P., Scherder, E.J.A., Medial temporal lobe atrophy relates more strongly to sleep-wake rhythm fragmentation than to age or any other known risk. Neurobiol Learn Mem 160 (2018), 132–138, 10.1016/j.nlm.2018.05.017.
Baillet, M., Dilharreguy, B., Pérès, K., Dartigues, J.-F., Mayo, W., Catheline, G., Activity/rest cycle and disturbances of structural backbone of cerebral networks in aging. Neuroimage 146 (2017), 814–820 Diffusion tensor imaging study reporting an association between actigraphy-estimated rest-activity patterns and white matter modifications.
Kocevska, D., Tiemeier, H., Lysen, T.S., de Groot, M., Muetzel, R.L., Van Someren, E.J.W., Ikram, M.A., Vernooij, M.W., Luik, A.I., The prospective association of objectively measured sleep and cerebral white matter microstructure in middle-aged and older persons. Sleep, 42, 2019, 10.1093/sleep/zsz140 Longitudinal study reporting an association between actigraphy-estimated sleep quality and white matter modifications up to seven years later, but no with diffusion parameters changes over time.
Oosterman, J., van Harten, B., Vogels, R., Gouw, A., Weinstein, H., Scheltens, P., Scherder, E., Distortions in rest-activity rhythm in aging relate to white matter hyperintensities. Neurobiol Aging 29 (2008), 1265–1271.
Hofman, A., Breteler, M.M.B., van Duijn, C.M., Krestin, G.P., Pols, H.A., Stricker, B.H.C.H., Tiemeier, H., Uitterlinden, A.G., Vingerling, J.R., Witteman, J.C.M., The rotterdam study: objectives and design update. Eur J Epidemiol 22 (2007), 819–829.
Zuurbier, L.A., Ikram, M.A., Luik, A.I., Hofman, A., Van Someren, E.J.W., Vernooij, M.W., Tiemeier, H., Cerebral small vessel disease is related to disturbed 24-h activity rhythms: a population-based study. Eur J Neurol 22 (2015), 1482–1487.
Wardlaw, J.M., Smith, C., Dichgans, M., Small vessel disease: mechanisms and clinical implications. Lancet Neurol 18 (2019), 684–696.
Kharabian Masouleh, S., Eickhoff, S.B., Hoffstaedter, F., Genon, S., Alzheimer's disease neuroimaging initiative: empirical examination of the replicability of associations between brain structure and psychological variables. eLife, 8, 2019.
Finelli, L.A., Achermann, P., Borbély, A.A., Individual “fingerprints” in human sleep EEG topography. Neuropsychopharmacology 25 (2001), S57–S62.
Scullin, M.K., Gao, C., Dynamic contributions of slow wave sleep and REM sleep to cognitive longevity. Curr Sleep Med Rep 4 (2018), 284–293.
della Monica, C., Johnsen, S., Atzori, G., Groeger, J.A., Dijk, D.-J., Rapid eye movement sleep, sleep continuity and slow wave sleep as predictors of cognition, mood, and subjective sleep quality in healthy men and women, aged 20–84 years. Front Psychiatry, 9, 2018.
Schmidt, C., Peigneux, P., Cajochen, C., Age-related changes in sleep and circadian rhythms: impact on cognitive performance and underlying neuroanatomical networks. Front Neurol, 3, 2012.
Huang, Y.-L., Liu, R.-Y., Wang, Q.-S., Van Someren, E.J.W., Xu, H., Zhou, J.-N., Age-associated difference in circadian sleep-wake and rest-activity rhythms. Physiol Behav 76 (2002), 597–603.
Lauriola, M., Esposito, R., Pizzi, S.D., de Zambotti, M., Londrillo, F., Kramer, J.H., Rabinovici, G.D., Tartaro, A., Sleep changes without medial temporal lobe or brain cortical changes in community-dwelling individuals with subjective cognitive decline. Alzheimer's Dement 13 (2017), 783–791.
Lucey, B.P., McCullough, A., Landsness, E.C., Toedebusch, C.D., McLeland, J.S., Zaza, A.M., Fagan, A.M., McCue, L., Xiong, C., Morris, J.C., et al. Reduced non–rapid eye movement sleep is associated with tau pathology in early Alzheimer's disease. Sci Transl Med, 11, 2019, eaau6550.
Van Egroo, M., Narbutas, J., Chylinski, D., Villar González, P., Maquet, P., Salmon, E., Bastin, C., Collette, F., Vandewalle, G., Sleep-wake regulation and the hallmarks of the pathogenesis of Alzheimer's disease. Sleep, 42, 2019.