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Sleep Mediates Age-Related Executive Function for Older Adults with Limited Cognitive Reserve

Published online by Cambridge University Press:  15 December 2020

Denise Parker ,
Romola S. Bucks ,
Stephanie R. Rainey-Smith ,
Erica Hodgson ,
Lara Fine ,
Hamid R. Sohrabi ,
Ralph N. Martins  and
Michael Weinborn Open the ORCID record for Michael Weinborn [Opens in a new window]
Denise Parker
Affiliation:
School of Psychological Science, University of Western Australia, 35 Stirling Highway, Perth, WA6009, Australia
Romola S. Bucks
Affiliation:
School of Psychological Science, University of Western Australia, 35 Stirling Highway, Perth, WA6009, Australia
Stephanie R. Rainey-Smith
Affiliation:
School of Medical and Health Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA6027, Australia Australian Alzheimer’s Research Foundation, Ralph and Patricia Sarich Neuroscience Research Institute, 8 Verdun Street, Nedlands, WA6008, Australia
Erica Hodgson
Affiliation:
School of Psychological Science, University of Western Australia, 35 Stirling Highway, Perth, WA6009, Australia
Lara Fine
Affiliation:
School of Psychological Science, University of Western Australia, 35 Stirling Highway, Perth, WA6009, Australia
Hamid R. Sohrabi
Affiliation:
Australian Alzheimer’s Research Foundation, Ralph and Patricia Sarich Neuroscience Research Institute, 8 Verdun Street, Nedlands, WA6008, Australia Department of Biomedical Sciences. Macquarie University, Level 1, 75 Talavera Road, NSW2109, Australia Centre for Healthy Ageing, College of Science, Health, Engineering and Education (SHEE), Murdoch University, 90 South Street, Murdoch, WA6150, Australia
Ralph N. Martins
Affiliation:
School of Medical and Health Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA6027, Australia Australian Alzheimer’s Research Foundation, Ralph and Patricia Sarich Neuroscience Research Institute, 8 Verdun Street, Nedlands, WA6008, Australia Department of Biomedical Sciences. Macquarie University, Level 1, 75 Talavera Road, NSW2109, Australia
Michael Weinborn*
Affiliation:
School of Psychological Science, University of Western Australia, 35 Stirling Highway, Perth, WA6009, Australia School of Medical and Health Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA6027, Australia Australian Alzheimer’s Research Foundation, Ralph and Patricia Sarich Neuroscience Research Institute, 8 Verdun Street, Nedlands, WA6008, Australia
*
*Correspondence and reprint requests to: Dr Michael Weinborn, School of Psychological Science, University of Western Australia, Stirling Hwy, Crawley, Western Australia, 6009, Australia. E-mail: michael.weinborn@uwa.edu.au
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Abstract

Objective:

Sleep quantity and quality are associated with executive function (EF) in experimental studies, and in individuals with sleep disorders. With advancing age, sleep quantity and quality decline, as does the ability to perform EF tasks, suggesting that sleep disruption may contribute to age-related EF declines. This cross-sectional cohort study tested the hypothesis that poorer sleep quality (i.e., the frequency and duration of awakenings) and/or quantity may partly account for age-related EF deficits.

Method:

Community-dwelling older adults (N = 184) completed actigraphic sleep monitoring then a range of EF tasks. Two EF factors were extracted using exploratory structural equation modeling. Sleep variables did not mediate the relationship between age and EF factors. Post hoc moderated mediation analyses were conducted to test whether cognitive reserve compensates for sleep-related EF deficits, using years of education as a proxy measure of cognitive reserve.

Results:

We found a significant interaction between cognitive reserve and the number and frequency of awakenings, explaining a small (approximately 3%), but significant amount of variance in EF. Specifically, in individuals with fewer than 11 years of education, greater sleep disturbance was associated with poorer EF, but sleep did not impact EF in those with more education. There was no association between age and sleep quantity.

Conclusions:

This study highlights the role of cognitive reserve in the sleep–EF relationship, suggesting individuals with greater cognitive reserve may be able to counter the impact of disturbed sleep on EF. Therefore, improving sleep may confer some protection against EF deficits in vulnerable older adults.

Keywords

CognitionAgingActigraphySleep disturbance
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 7 , August 2021 , pp. 711 - 721
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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References

REFERENCES

Adrover-Roig, D., Sesé, A., Barcelo, F., & Palmer, A. (2012). A latent variable approach to executive control in healthy ageing. Brain and Cognition, 78, 284–299.CrossRefGoogle ScholarPubMed
Alapin, I., Fichten, C.S., Libman, E., Creti, L., Bailes, S., & Wright, J. (2000). How is good and poor sleep in older adults and college students related to daytime sleepiness, fatigue, and ability to concentrate? Journal of Psychosomatic Research, 49(5), 381–390.CrossRefGoogle Scholar
Ancoli-Israel, S., Cole, R., Alessi, C., Chambers, M., Moorcroft, W., & Pollak, C.P. (2003). The role of actigraphy in the study of sleep and circadian rhythms. Sleep, 26(3), 342–392.CrossRefGoogle Scholar
Anderson, C. & Horne, J.A. (2003). Prefrontal cortex: Links between low frequency delta EEG in sleep and neuropsychological performance in healthy, older people. Psychophysiology, 40(3), 349–357.CrossRefGoogle ScholarPubMed
Baddeley, A. (1996). Exploring the central executive. The Quarterly Journal of Experimental Psychology, 49A(1), 5–28.CrossRefGoogle Scholar
Ballesio, A. (2017). Executive function impairments in insomnia: A Systematic review and meta-analysis. Sleep Medicine, 40, e23.CrossRefGoogle Scholar
Baron, K.G., Reid, K.J., Malkani, R.G., Kang, J., & Zee, P.C. (2017). Sleep variability among older adults with insomnia: associations with sleep quality and cardiometabolic disease risk. Behavioral Sleep Medicine, 15(2), 144–157.CrossRefGoogle ScholarPubMed
Bastien, C.H., Fortier-Brochu, E., Rioux, I., LeBlanc, M., Daley, M., & Morin, C.M. (2003). Cognitive performance and sleep quality in the elderly suffering from chronic insomnia. Relationship between objective and subjective measures. Journal of Psychosomatic Research, 54, 849–859.CrossRefGoogle ScholarPubMed
Beebe, D.W. & Gozal, D. (2002). Obstructive sleep apnea and the prefrontal cortex: Towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. Journal of Sleep Research, 11, 1–16.CrossRefGoogle ScholarPubMed
Bei, B., Wiley, J.F., Trinder, J., & Manber, R. (2016). Beyond the mean: A systematic review of daily intraindividual variability of sleep/wake patterns. Sleep Medicine Reviews, 28, 108–124.CrossRefGoogle ScholarPubMed
Benton, L.A., Hamsher, K.D., & Sivan, A.B. (1994). Controlled oral word association test. In Multilingual Aphasia examination. Lutz, FL, USA. Psychological Assessment Resources.Google Scholar
Blackwell, T., Yaffe, K., Ancoli-Israel, S., Schneider, J.L., Cauley, J.A., Hillier, T.A., … Stone, K.L. (2006). Poor sleep is associated with impaired cognitive function in older women: the study of osteoporotic fractures. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 61(4), 405–410.CrossRefGoogle Scholar
Blackwell, T., Yaffe, K., Ancoli-Israel, S., Redline, S., Ensrud, K.E., Stefanick, M.L., … & Osteoporotic Fractures in Men (MrOS) Study Group. (2011). Association of sleep characteristics and cognition in older community-dwelling men: The MrOS sleep study. Sleep, 34(10), 1347.CrossRefGoogle ScholarPubMed
Bucks, R.S., Olaithe, M., & Eastwood, P. (2013). Neurocognitive function in sleep apnoea: A meta-review. Respirology, 18(1), 61–70.CrossRefGoogle ScholarPubMed
Cabeza, R., Anderson, N.D., Locantore, J.K., & McIntosh, A.R. (2002). Aging gracefully: Compensatory brain activity in high-performing older adults. NeuroImage, 17(3), 1394–1402.CrossRefGoogle ScholarPubMed
Carney, C.E., Buysse, D.J., Ancoli-Israel, S., Edinger, J.D., Krystal, A.D., Lichstein, K.L., & Morin, C.M. (2012). The consensus sleep diary: Standardizing prospective sleep self-monitoring. Sleep, 35(2), 287.CrossRefGoogle ScholarPubMed
Cole, R.J., Kripke, D.F., Gruen, W., Mullaney, D.J., & Gillin, J.C. (1992). Automatic sleep/wake identification from wrist activity. Sleep, 15, 461–469.CrossRefGoogle ScholarPubMed
Crowley, K. (2011). Sleep and sleep disorders in older adults. Neuropsychology Review, 21, 41–53.CrossRefGoogle ScholarPubMed
Davis, J.C., Marra, C.A., Najafzadeh, M., & Liu-Ambrose, T. (2010). The independent contribution of executive functions to health related quality of life in older women. BMC Geriatrics, 10(16), 1–8.CrossRefGoogle ScholarPubMed
De Souza, L., Benedito-Silva, A.A., Pires, M.L.N., Poyares, D., Tufik, S., & Calil, H.M. (2003). Further validation of Actigraphy for sleep studies. Sleep, 26(1), 81–85.CrossRefGoogle ScholarPubMed
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Delis-Kaplan Executive Function System (D-KEFS). San Antonio, TX: Psychological Corporation.Google Scholar
Dijk, D., Duffy, J.F., Silva, E.J., Shanahan, T.L., Boivin, D.B., & Czeisler, C.A. (2012). Amplitude reduction and phase shifts of melatonin, cortisol and other circadian rhythms after a gradual advance of sleep and light exposure. PLoS ONE, 7(2), e30037.CrossRefGoogle ScholarPubMed
Fernandez-Mendoza, J., Calhoun, S., Bixler, E.O., Pejovic, S., Karataki, M., Liao, D., … Vgontzas, A.N. (2010). Insomnia with objective short sleep duration is associated with deficits in neuropsychological performance: a general population study. Sleep, 33(4), 459–465.CrossRefGoogle ScholarPubMed
Fine, L., Weinborn, M., Ng, A., Loft, S., Yanqi, R.L., Hodgson, E., … Bucks, R.S. (2019). Sleep disruption explains age-related prospective memory deficits: implications for cognitive aging and intervention. Aging, Neuropsychology, and Cognition, 26(4), 621–636.CrossRefGoogle ScholarPubMed
Fisk, J.E. & Sharp, C.A. (2004). Age-related impairment in executive functioning: updating, inhibition, shifting, and access. Journal of Clinical and Experimental Neuropsychology, 26(7), 874–890.CrossRefGoogle ScholarPubMed
Folstein, M., Folstein, S.E., & McHugh, P.R. (1975). “Mini-Mental State” a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.CrossRefGoogle ScholarPubMed
Fortier-Brochu, E., Beaulieu-Bonneau, S., Ivers, H., & Morin, C.M. (2012). Insomnia and daytime cognitive performance: a meta-analysis. Sleep Medicine Review, 16(1), 83–94.CrossRefGoogle ScholarPubMed
Hayes, A.F. (2013). Introduction to Mediation, Moderation, and Condition Process Analysis: A Regression-Based Approach. New York, NY, USA. Guildford Press.Google Scholar
Iverson, G.L. (1998). Interpretation of Mini-Mental State Examination scores in community-dwelling elderly and geriatric neuropsychiatry patients. International Journal of Geriatric Psychiatry, 13(10), 661–666.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Kay, D.B., Karim, H.T., Soehner, A.M., Hasler, B.P., Wilckens, K.A., James, J.A., … & Buysse, D.J. (2016). Sleep-wake differences in relative regional cerebral metabolic rate for glucose among patients with insomnia compared with good sleepers. Sleep, 39(10), 1779–1794.CrossRefGoogle ScholarPubMed
Kramer, J.H., Mungas, D., Possin, K.L., Rankin, K.P., Boxer, A.L., Rosen, H.J., … & Widmeyer, M. (2014). NIH EXAMINER: Conceptualization and development of an executive function battery. Journal of the International Neuropsychological Society, 20(01), 11–19.CrossRefGoogle ScholarPubMed
Kroenke, K. & Spitzer, R.L. (2002). The PHQ-9: a new depression diagnostic and severity measure. Psychiatric Annals, 32(9), 509–515.CrossRefGoogle Scholar
Krueger, J.M., Frank, M.G., Wisor, J.P., & Roy, S. (2016). Sleep function: Toward elucidating an enigma. Sleep Medicine Reviews, 28, 46–54.CrossRefGoogle ScholarPubMed
Landry, G.J., Best, J.R., & Liu-Ambrose, T. (2015). Measuring sleep quality in older adults: a comparison using subjective and objective methods. Frontiers in Aging Neuroscience, 7, 1–10.CrossRefGoogle ScholarPubMed
Landry, G.J. & Liu-Ambrose, T. (2014). Buying time: A rationale for examining the use of circadian rhythm and sleep interventions to delay progression of mild cognitive impairment to Alzheimer’s disease. Frontiers in Aging Neuroscience, 6, 325–345.CrossRefGoogle ScholarPubMed
Littner, M., Kushida, C.A., Anderson, W.M., Bailey, D., Berry, R.B., Davila, D.G., … Johnson, S.F. (2003). Practice parameters for the role of actigraphy in the study of sleep and circadian rhythms: An Update for 2002. Sleep, 26(3), 337–341.CrossRefGoogle Scholar
Lo, J.C., Groeger, J.A., Cheng, G.H., Dijk, D.J., & Chee, M.W. (2016). Self-reported sleep duration and cognitive performance in older adults: A Systematic review and meta-analysis. Sleep Medicine, 17, 87–98.CrossRefGoogle ScholarPubMed
Lo, J.C., Loh, K.K., Zheng, H., Sim, S.K.Y., & Chee, M.W.L. (2014). Sleep duration and age-related changes in brain structure and cognitive performance. Sleep, 37(7), 1171–1178.CrossRefGoogle ScholarPubMed
Lugtenburg, A., Voshaar, R.C.O., Van Zelst, W., Schoevers, R.A., Enriquez-Geppert, S., & Zuidersma, M. (2017). The relationship between depression and executive function and the impact of vascular disease burden in younger and older adults. Age and Aging, 46(4), 697–701.CrossRefGoogle ScholarPubMed
Luszcz, M. (2011). Executive function and cognitive aging. In Handbook of the psychology of aging (7th ed.). Massachusetts, CT: Academic Press.Google Scholar
Mander, B.A., Winder, J.R., & Walker, M.P. (2017). Sleep and human aging. Neuron, 94(1), 19–36.CrossRefGoogle ScholarPubMed
Marino, M., Li, Y., Reuschman, M.N., Winkelman, J.W., Ellenbogen, J.M., Solet, J.M., … & Buxton, O.M. (2013). Measuring sleep: Accuracy, sensitivity, and specificity of wrist actigraphy compared to polysomnography. Sleep, 36(11), 1745–1755.CrossRefGoogle ScholarPubMed
Martin, S.E., Engleman, H.M., Deary, I.J., & Douglas, N.J. (1996). The effects of sleep fragmentation on daytime function. American Journal of Respiratory and Critical Care Medicine, 153(4), 1328–1332.CrossRefGoogle ScholarPubMed
McCrae, C.S., Rowe, M., Tierney, C.G., Dautovich, N.D., DeFinis, A.L., & McNamara, J.P.H. (2005). Sleep complaints, subjective and objective sleep patterns, healthy, psychological adjustment, and daytime functioning in community-dwelling older adults. Journal of Gerontology, 60B(4), 182–189.CrossRefGoogle Scholar
Miyake, A. & Friedman, N.P. (2012). The nature and organization of individual differences in executive functions: Four general conclusions. Current Directions in Psychological Science, 21(1), 8–14.CrossRefGoogle ScholarPubMed
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., & Wager, T.D. (2000). The unity and diversity of executive functions and their contributions to complex frontal lobe tasks: A latent variable analysis. Cognitive Psychology, 41, 49–100.CrossRefGoogle ScholarPubMed
Miyata, S., Noda, A., Iwamoto, K., Kawano, N., Okuda, M., & Ozaki, N. (2013). Poor sleep impairs cognitive performance in older adults. Journal of Sleep Research, 22(5), 535–541.CrossRefGoogle ScholarPubMed
Muzur, A., Pace-Schott, E., & Hobson, J.A. (2002). The prefrontal cortex in sleep. Trends in Cognitive Sciences, 16(11), 475–481.CrossRefGoogle Scholar
Naismith, S., Rogers, N.L., Hickie, I.B., McKenzie, J., Norrie, L.M., & Lewis, S.J.G. (2010). Sleep well, think well: Sleep-wake disturbance in mild cognitive impairment. Journal of Geriatric Psychiatry and Neurology, 23(2), 123–130.CrossRefGoogle ScholarPubMed
Nebes, R.D., Buysse, D.J., Halligan, E.M., Houck, P.R. & Monk, T.H. (2009). Self-reported sleep quality predicts poor cognitive performance in healthy older adults. Journal of Gerontology: Pscyhological Sciences, 64B(2), 180–187.CrossRefGoogle Scholar
Netzer, N.C., Stoohs, S.A., Netzer, C.M., Clark, K., & Strohl, K.P., (1999) Using the Berlin questionnaire to identify patients at risk for the sleep apnea syndrome. Annals of Internal Medicine, 131(7), 485–491.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Organisation for Economic Co-operation and Development. (2012). Education at a Glance: OECD Indicators 2012. Paris, France: OECD.Google Scholar
Perneger, T.V. (1998). What’s wrong with Bonferroni adjustments? BMJ, 316, 1236–1238.CrossRefGoogle ScholarPubMed
Piatt, A.L., Fields, J.A., Paolo, A.M., & Tröster, A.I. (1999). Action (verb naming) fluency as an executive function measure: Convergent and divergent evidence of validity. Neuropsychologia, 37(13), 1499–1503.CrossRefGoogle ScholarPubMed
Preacher, K.J. & Hayes, A.F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments and Computers, 36(4), 717–731.CrossRefGoogle ScholarPubMed
Reitan, R.M. & Wolfson, D. (1985). The Halstead-Reitan neuropsychological test battery: Theory and clinical interpretation, Vol. 4. Tucson, AZ: Reitan Neuropsychology.Google Scholar
Ritchie, S.J., Bates, T.C., Der, G., Starr, J.M., & Deary, J. (2013). Education is associated with higher later life IQ scores, but not with faster cognitive processing speed. Psychology and Aging, 28(2), 515–521.CrossRefGoogle Scholar
Robertson, I.H., Ward, T., Ridgeway, V., Nimmo-Smith, I., & McAnespie, A.W. (1991). The Test of Everyday Attention (TEA) . Bury St. Edmonds, UK: Thames Valley Test Company.Google Scholar
Schmutte, T., Harris, S., Levin, R., Zweig, R., Kataz, M., & Lipton, R. (2007). The relation between cognitive functioning and self-reported sleep complaints in non-demented older adults: Results from the Bronx aging study. Behavioral Sleep Medicine, 5(1), 39–56.CrossRefGoogle Scholar
Scullin, M.K. & Bliwise, D. (2015). Sleep, cognition, and normal aging: Integrating a half-century of multidisciplinary research. Perspectives on Psychological Science, 10(1), 97–137.CrossRefGoogle ScholarPubMed
Spiller, S.A., Fitzsimmons, G.G., Lynch, J.G. & McClelland, G.H. (2013). Spotlights, floodlights, and the magic number zero: Simple effects tests in moderated regression. Journal of Marketing Research, L, 277–288.CrossRefGoogle Scholar
Stern, Y. (2012). Cognitive reserve in aging and Alzheimer’s Disease, Lancet Neurology, 11(11), 1006–1012.CrossRefGoogle ScholarPubMed
Van Cauter, E., Leproult, R., & Kupfer, D.J. (1996). Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol. Journal of Clinical Endocrinology and Metabolism, 81(7), 2468–2473.Google ScholarPubMed
Van Dongen, P.A., Maislin, G., Mullington, J.M., & Dinges, D.F. (2003). The cumulative cost of additional wakefulness: Dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep, 26(2), 117–126.CrossRefGoogle ScholarPubMed
Vignola, A., Lemoureux, C., Bastien, C.H., & Morin, C.M. (2000). Effects of chronic insomnia and use of benzodiazepines on daytime performance in older adults. Journal of Gerontology, 55B, 54–62.Google ScholarPubMed
Vitiello, M.V., Larsen, L.H., & Moe, K.E. (2004). Age-related sleep change: Gender and estrogen effects on the subjective-objective sleep quality relationships of healthy, non-complaining older men and women. Journal of Psychosomatic Research, 56, 503–510.CrossRefGoogle Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale–Third Edition (WAIS–III). San Antonio, TX, USA. Harcourt Assessment.Google Scholar
Wilckens, K.A., Woo, S.G., Kirk, A.R., Erickson, K.I., & Wheeler, M.E. (2014). The role of sleep continuity and total sleep time in executive function across the lifespan. Psychology and Aging, 29(3), 658–665.CrossRefGoogle Scholar
Yaffe, K., Falvey, C.M., & Hoang, T. (2014). Connections between sleep and cognition in older adults. The Lancet Neurology, 13(10), 1017–1028.CrossRefGoogle ScholarPubMed