Preprint / Version 1

The association between physical activity and cognitive function is partly explained by better sleep quality

Physical activity, cognitive function and sleep quality

##article.authors##

  • Boris Cheval University of Geneva
  • Silvio Maltagliati
  • Stefan Sieber
  • Stéphane Cullati
  • Liye Zou
  • Andreas Ihle
  • Arthur Kramer
  • Qian Yu
  • David Sander
  • Matthieu Boisgontier

DOI:

https://doi.org/10.51224/SRXIV.89

Keywords:

physical activity, sleep quality, cognitive function, aging, mediation

Abstract

Background: Physical activity has been associated with better cognitive functions and sleep quality. Yet, whether the effect of physical activity on cognitive functions could be explained by better sleep quality in adults who are 50 year of age or older is unclear.

Objective: To investigate whether sleep quality mediates the association between physical activity and cognitive functions in adults 50 year of age or older.

Methods: 97,767 community-dwelling 50 years-of-age or older European adults were included in the study. Physical activity and sleep quality were self-reported, and indicators of cognitive function (i.e., immediate recall, delayed recall, and verbal fluency) were assessed using objective tests. All measures were collected six times between 2004 and 2017. The mediation was tested using multilevel mediation analyses.

Results: Results showed that physical activity was associated with better sleep quality, which was associated in turn with better performance in all three indicators of cognitive function, thereby demonstrating an indirect effect of physical activity on cognitive function through sleep quality. However, the magnitude of this indirect effect was small in comparison to the magnitude of the direct effect of physical activity on cognitive function. Specifically, sleep quality explained 3.8%, 6.5%, and 9.0% of the total association of physical activity with verbal fluency, immediate recall, and delayed recall, respectively.

Conclusions: These findings suggest that self-reported sleep quality partly mediates the association between physical activity and cognitive function, but that the effect of self-reported physical activity on cognitive function is largely independent from self-reported sleep quality. Future studies using devices-based measures of physical activity and sleep quality are needed.

Metrics

Metrics Loading ...

References

WHO (2012) Dementia: a public health priority. Geneva, Switzerland, 2012. 112.

Maasakkers CM, Claassen JA, Gardiner PA, Rikkert MGO, Lipnicki DM, Scarmeas N, Dardiotis E, Yannakoulia M, Anstey KJ, Cherbuin N (2020) The association of sedentary behaviour and cognitive function in people without dementia: a coordinated analysis across five cohort studies from COSMIC. Sports Med 50, 403-413.

Cao Q, Tan C-C, Xu W, Hu H, Cao X-P, Dong Q, Tan L, Yu J-T (2020) The prevalence of dementia: A systematic review and meta-analysis. J Alzheimers Dis 73, 1157-1166.

Ten Brinke LF, Bolandzadeh N, Nagamatsu LS, Hsu CL, Davis JC, Miran-Khan K, Liu-Ambrose T (2015) Aerobic exercise increases hippocampal volume in older women with probable mild cognitive impairment: a 6-month randomised controlled trial. Br J Sports Med 49, 248-254.

Hamer M, Terrera GM, Demakakos P (2018) Physical activity and trajectories in cognitive function: English Longitudinal Study of Ageing. J Epidemiol Community Health 72, 477-483.

Cheval B, Darrous L, Choi KW, Klimentidis YC, Raichlen DA, Alexander GE, Cullati S, Kutalik Z, Boisgontier MP (2020) Physical activity and general cognitive functioning: A Mendelian Randomization study. BioRxiv.

Baumgart M, Snyder HM, Carrillo MC, Fazio S, Kim H, Johns H (2015) Summary of the evidence on modifiable risk factors for cognitive decline and dementia: a population-based perspective. Alzheimer Dement 11, 718-726.

Norton S, Matthews FE, Barnes DE, Yaffe K, Brayne C (2014) Potential for primary prevention of Alzheimer's disease: an analysis of population-based data. Lancet Neurol 13, 788-794.

Piercy KL, Troiano RP, Ballard RM, Carlson SA, Fulton JE, Galuska DA, George SM, Olson RD (2018) The physical activity guidelines for Americans. JAMA 320, 2020-2028.

Colcombe S, Kramer AF (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 14, 125-130.

Hamer M, Chida Y (2009) Physical activity and risk of neurodegenerative disease: a systematic review of prospective evidence. Psychol Med 39, 3-11.

Stillman CM, Cohen J, Lehman ME, Erickson KI (2016) Mediators of physical activity on neurocognitive function: a review at multiple levels of analysis. Front Hum Neurosci 10, 626.

Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25, 295-301.

Hillman CH, Erickson KI, Kramer AF (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 9, 58-65.

Cotman CW, Berchtold NC, Christie L-A (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30, 464-472.

Van Praag H (2008) Neurogenesis and exercise: past and future directions. Neuromolecular Med 10, 128-140.

Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM (2011) Exercise training increases size of hippocampus and improves memory. PNAS 108, 3017-3022.

Makizako H, Liu-Ambrose T, Shimada H, Doi T, Park H, Tsutsumimoto K, Uemura K, Suzuki T (2015) Moderate-intensity physical activity, hippocampal volume, and memory in older adults with mild cognitive impairment. J Gerontol A Biol Sci Med Sci 70, 480-486.

Weinstein AM, Voss MW, Prakash RS, Chaddock L, Szabo A, White SM, Wojcicki TR, Mailey E, McAuley E, Kramer AF (2012) The association between aerobic fitness and executive function is mediated by prefrontal cortex volume. Brain Behav Immun 26, 811-819.

Verstynen TD, Lynch B, Miller DL, Voss MW, Prakash RS, Chaddock L, Basak C, Szabo A, Olson EA, Wojcicki TR (2012) Caudate nucleus volume mediates the link between cardiorespiratory fitness and cognitive flexibility in older adults. J Aging Res 2012, 939285.

Oberlin LE, Verstynen TD, Burzynska AZ, Voss MW, Prakash RS, Chaddock-Heyman L, Wong C, Fanning J, Awick E, Gothe N (2016) White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults. Neuroimage 131, 91-101.

Sexton CE, Betts JF, Demnitz N, Dawes H, Ebmeier KP, Johansen-Berg H (2016) A systematic review of MRI studies examining the relationship between physical fitness and activity and the white matter of the ageing brain. Neuroimage 131, 81-90.

Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Elavsky S (2004) Cardiovascular fitness, cortical plasticity, and aging. PNAS 101, 3316-3321.

Hillman CH, Pontifex MB, Castelli DM, Khan NA, Raine LB, Scudder MR, Drollette ES, Moore RD, Wu C-T, Kamijo K (2014) Effects of the FITKids randomized controlled trial on executive control and brain function. Pediatrics 134, e1063-e1071.

Yu Q, Herold F, Becker B, Klugah-Brown B, Zhang Y, Perrey S, Veronese N, Müller NG, Kramer AF, Zou L (2021) Cognitive benefits of exercise interventions: an fMRI activation likelihood estimation meta-analysis. Brain Struct Funct, 1-19.

Kredlow MA, Capozzoli MC, Hearon BA, Calkins AW, Otto MW (2015) The effects of physical activity on sleep: a meta-analytic review. J Behav Med 38, 427-449.

Youngstedt SD (2005) Effects of exercise on sleep. Clin Sports Med 24, 355-365.

King AC, Oman RF, Brassington GS, Bliwise DL, Haskell WL (1997) Moderate-intensity exercise and self-rated quality of sleep in older adults: a randomized controlled trial. JAMA 277, 32-37.

Singh NA, Clements KM, Fiatarone MA (1997) A randomized controlled trial of the effect of exercise on sleep. Sleep 20, 95-101.

Chennaoui M, Arnal PJ, Sauvet F, Léger D (2015) Sleep and exercise: a reciprocal issue? Sleep Med Rev 20, 59-72.

Holfeld B, Ruthig JC (2014) A longitudinal examination of sleep quality and physical activity in older adults. J Appl Gerontol 33, 791-807.

Yaffe K, Falvey CM, Hoang T (2014) Connections between sleep and cognition in older adults. Lancet Neurol 13, 1017-1028.

Walker MP (2009) The role of sleep in cognition and emotion. Ann N Y Acad Sci 1156, 168-197.

Ellenbogen JM (2005) Cognitive benefits of sleep and their loss due to sleep deprivation. Neurology 64, E25-E27.

McSorley VE, Bin YS, Lauderdale DS (2019) Associations of sleep characteristics with cognitive function and decline among older adults. Am J Epidemiol 188, 1066-1075.

Foley DJ, Monjan AA, Brown SL, Simonsick EM, Wallace RB, Blazer DG (1995) Sleep complaints among elderly persons: an epidemiologic study of three communities. Sleep 18, 425-432.

Crowley K (2011) Sleep and sleep disorders in older adults. Neuropsychol Rev 21, 41-53.

Neikrug AB, Ancoli-Israel S (2010) Sleep disorders in the older adult–a mini-review. Gerontology 56, 181-189.

da Silva RAPC (2015) Sleep disturbances and mild cognitive impairment: a review. Sleep Sci 8, 36-41.

Falck RS, Best JR, Davis JC, Liu-Ambrose T (2018) The independent associations of physical activity and sleep with cognitive function in older adults. J Alzheimers Dis 63, 1469-1484.

Sewell K, Erickson KI, Rainey-Smith SR, Peiffer JJ, Sohrabi HR, Brown BM (2021) Relationships between physical activity, sleep and cognitive function: A narrative review. Neurosci Biobehav Rev 130, 369-378.

Wilckens KA, Erickson KI, Wheeler ME (2018) Physical activity and cognition: a mediating role of efficient sleep. Behav Sleep Med 16, 569-586.

Li L, Yu Q, Zhao W, Herold F, Cheval B, Kong Z, Li J, Mueller N, Kramer AF, Cui J (2021) Physical Activity and Inhibitory Control: The Mediating Role of Sleep Quality and Sleep Efficiency. Brain Sci 11, 664.

Won J, Alfini AJ, Weiss LR, Nyhuis CC, Spira AP, Callow DD, Carson Smith J (2019) Caudate volume mediates the interaction between total sleep time and executive function after acute exercise in healthy older adults. Brain Plast 5, 69-82.

Yuan M, Fu H, Liu R, Fang Y (2020) Effect of frequency of exercise on cognitive function in older adults: Serial mediation of depression and quality of sleep. Int J Environ Res Public Health 17, 709.

Börsch-Supan A, Brandt M, Hunkler C, Kneip T, Korbmacher J, Malter F, Schaan B, Stuck S, Zuber S (2013) Data resource profile: the Survey of Health, Ageing and Retirement in Europe (SHARE). Int J Epidemiol 42, 992-1001.

Aartsen MJ, Cheval B, Sieber S, Van der Linden BW, Gabriel R, Courvoisier DS, Guessous I, Burton-Jeangros C, Blane D, Ihle A (2019) Advantaged socioeconomic conditions in childhood are associated with higher cognitive functioning but stronger cognitive decline in older age. PNAS 116, 5478-5486.

Rosen WG (1980) Verbal fluency in aging and dementia. J Clin Exp Neuropsychol 2, 135-146.

Harris S, Dowson J (1982) Recall of a 10-word list in the assessment of dementia in the elderly. Br J Psychiatry 141, 524-527.

Cheval B, Orsholits D, Sieber S, Courvoisier DC, Cullati S, Boisgontier MP (2020) Relationship between decline in cognitive resources and physical activity. Health Psychol 39, 519-528.

Cheval B, Rebar AL, Miller MM, Sieber S, Orsholits D, Baranyi G, Courvoisier DC, Cullati S, Sander D, Boisgontier MP (2019) Cognitive resources moderate the adverse impact of poor neighborhood conditions on physical activity. Prev Med 126, 105741.

de Souto Barreto P, Cesari M, Andrieu S, Vellas B, Rolland Y (2017) Physical activity and incident chronic diseases: a longitudinal observational study in 16 European countries. Am J Prev Med 52, 373-378.

Cheval B, Sieber S, Guessous I, Orsholits D, Courvoisier DC, Kliegel M, Stringhini S, Swinnen S, Burton-Jeangros C, Cullati S, Boisgontier MP (2018) Effect of early-and adult-life socioeconomic circumstances on physical inactivity. Med Sci Sports Exerc 50, 476-485.

Boisgontier M, Orsholits D, von Arx M, Sieber S, Courvoisier D, Iversen M, Cullati S, Cheval B (2020) Adverse Childhood Experiences, Depressive Symptoms, Functional Dependence, and Physical Activity: A Moderated Mediation Model. J Phys Act Health 17, 79-799.

Chalabaev A, Boisgontier M, Sieber S, Sander D, Cullati S, Maltagliati S, Sarrazin P, Cheval B (in press) Early-life socioeconomic circumstances and physical activity in older age: women pay the price. Psychol Sci.

van de Straat V, Cheval B, Schmidt RE, Sieber S, Courvoisier D, Kliegel M, Burton-Jeangros C, Cullati S, Bracke P (2020) Early predictors of impaired sleep: a study on life course socioeconomic conditions and sleeping problems in older adults. Aging Ment Health 24, 322-332.

United Nations Educational (2006) International Standard Classification of Education 1997. UNESCO, Paris

Prince MJ, Reischies F, Beekman AT, Fuhrer R, Jonker C, Kivela S-L, Lawlor BA, Lobo A, Magnusson H, Fichter M (1999) Development of the EURO–D scale–a European Union initiative to compare symptoms of depression in 14 European centres. Br J Psychiatry 174, 330-338.

Boisgontier MP, Cheval B (2016) The anova to mixed model transition. Neurosci Biobehav Rev 68, 1004-1005.

Raudenbush SW, Bryk AS (2002) Hierarchical linear models: Applications and data analysis methods, Sage.

Yzerbyt V, Muller D, Batailler C, Judd CM (2018) New recommendations for testing indirect effects in mediational models: The need to report and test component paths. J Pers Soc Psychol 115, 929-943.

MacKinnon DP, Lockwood CM, Hoffman JM, West SG, Sheets V (2002) A comparison of methods to test mediation and other intervening variable effects. Psychol Methods 7, 83-104.

Biesanz JC, Falk CF, Savalei V (2010) Assessing mediational models: Testing and interval estimation for indirect effects. Multivariate Behav Res 45, 661-701.

Tofighi D, MacKinnon DP (2011) RMediation: An R package for mediation analysis confidence intervals. Behav Res Methods 43, 692-700.

MacKinnon DP, Lockwood CM, Williams J (2004) Confidence limits for the indirect effect: Distribution of the product and resampling methods. Multivariate Behav Res 39, 99-128.

Barton K (2018) MuMIn: Multi-model inference. R package version 1.42.1. https://CRAN.R-project.org/package=MuMIn.

Cheval B, Maltagliati S, Sieber S, Beran D, Chalabaev A, Sander D, Cullati S, Boisgontier MP (2021) Why are individuals with diabetes less active? The mediating role of physical, emotional, and cognitive factors. Ann Behav Med 55, 904-917.

Buman MP, King AC (2010) Exercise as a treatment to enhance sleep. Am J Lifestyle Med 4, 500-514.

Rebar AL, Stanton R, Geard D, Short C, Duncan MJ, Vandelanotte C (2015) A meta-meta-analysis of the effect of physical activity on depression and anxiety in non-clinical adult populations. Health Psychol Rev 9, 366-378.

Cheval B, Sivaramakrishnan H, Maltagliati S, Fessler L, Forestier C, Sarrazin P, Orsholits D, Chalabaev A, Sander D, Ntoumanis N (2021) Relationships between changes in self-reported physical activity, sedentary behaviour and health during the coronavirus (COVID-19) pandemic in France and Switzerland. J Sports Sci 39, 699-704.

Goldberg JH, King AC (2007) Physical activity and weight management across the lifespan. Annu. Rev. Public Health 28, 145-170.

Lee I-M, Djoussé L, Sesso HD, Wang L, Buring JE (2010) Physical activity and weight gain prevention. JAMA 303, 1173-1179.

Swift DL, Johannsen NM, Lavie CJ, Earnest CP, Church TS (2014) The role of exercise and physical activity in weight loss and maintenance. Prog Cardiovasc Dis 56, 441-447.

Manini TM, Pahor M (2009) Physical activity and maintaining physical function in older adults. Br J Sports Med 43, 28-31.

Young T, Peppard PE, Taheri S (2005) Excess weight and sleep-disordered breathing. J App Physiol 99, 1592-1599.

Hung HC, Yang YC, Ou HY, Wu JS, Lu FH, Chang CJ (2013) The association between self‐reported sleep quality and overweight in a Chinese population. Obesity 21, 486-492.

Rahe C, Czira ME, Teismann H, Berger K (2015) Associations between poor sleep quality and different measures of obesity. Sleep Med 16, 1225-1228.

Morin CM, Bootzin RR, Buysse DJ, Edinger JD, Espie CA, Lichstein KL (2006) Psychological and behavioral treatment of insomnia: update of the recent evidence (1998–2004). Sleep 29, 1398-1414.

Ensrud KE, Blackwell TL, Redline S, Ancoli‐Israel S, Paudel ML, Cawthon PM, Dam TTL, Barrett‐Connor E, Leung PC, Stone KL (2009) Sleep disturbances and frailty status in older community‐dwelling men. J Am Geriatr Soc 57, 2085-2093.

Wilckens KA, Hall MH, Nebes RD, Monk TH, Buysse DJ (2016) Changes in cognitive performance are associated with changes in sleep in older adults with insomnia. Behav Sleep Med 14, 295-310.

Blackwell T, Yaffe K, Ancoli-Israel S, Schneider JL, Cauley JA, Hillier TA, Fink HA, Stone KL (2006) Poor sleep is associated with impaired cognitive function in older women: the study of osteoporotic fractures. J Gerontol A Biol Sci Med Sci 61, 405-410.

Nebes RD, Buysse DJ, Halligan EM, Houck PR, Monk TH (2009) Self-reported sleep quality predicts poor cognitive performance in healthy older adults. J Gerontol B Psychol Sci Soc Sci 64, 180-187.

Kang J-E, Lim MM, Bateman RJ, Lee JJ, Smyth LP, Cirrito JR, Fujiki N, Nishino S, Holtzman DM (2009) Amyloid-β dynamics are regulated by orexin and the sleep-wake cycle. Science 326, 1005-1007.

Zhu B, Dong Y, Xu Z, Gompf HS, Ward SA, Xue Z, Miao C, Zhang Y, Chamberlin NL, Xie Z (2012) Sleep disturbance induces neuroinflammation and impairment of learning and memory. Neurobiol Dis 48, 348-355.

Meerlo P, Mistlberger RE, Jacobs BL, Heller HC, McGinty D (2009) New neurons in the adult brain: the role of sleep and consequences of sleep loss. Sleep Med Rev 13, 187-194.

Porkka‐Heiskanen T, Zitting KM, Wigren HK (2013) Sleep, its regulation and possible mechanisms of sleep disturbances. Acta physiologica 208, 311-328.

Prince SA, Adamo KB, Hamel ME, Hardt J, Gorber SC, Tremblay M (2008) A comparison of direct versus self-report measures for assessing physical activity in adults: a systematic review. Int J Behav Nutr Phys Act 5, 56.

Downloads

Posted

2021-12-03