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Sleep Onset/Maintenance Difficulties and Cognitive Function in Nondemented Older Adults: The Role of Cognitive Reserve

Published online by Cambridge University Press:  09 February 2012

Molly E. Zimmerman*
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, New York
Marcelo E. Bigal
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, New York Head of the Merck Investigator Study Program, Global Center for Scientific Affairs, Office of the Chief Medical Officer, Merck Inc., West Point, Pennsylvania
Mindy J. Katz
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, New York
Adam M. Brickman
Affiliation:
Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University College of Physicians and Surgeons, New York, New York
Richard B. Lipton
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, New York
*
Correspondence and reprint requests to: Molly E. Zimmerman, Albert Einstein College of Medicine, Department of Neurology, 1165 Morris Park Avenue, Room 338, Bronx, NY 10461. E-mail: molly.zimmerman@einstein.yu.edu

Abstract

This study examined the relationship between cognitive function and sleep onset/maintenance difficulties (SO/MD) in nondemented older adults. We hypothesized that SO/MD negatively impacts cognition and that older adults with lower education would be especially vulnerable to its effects. The sample comprised 549 older adults from the Einstein Aging Study (EAS), a community-based cohort. Participants completed neuropsychological assessment and a sleep questionnaire. Univariate ANCOVAs were performed with cognitive performance as a dependent variable, SO/MD (present or absent) and education (lower: ⩽12 years; higher: >12 years) as between-subjects factors, and age, ethnicity, gender, depression, and cardiovascular comorbidies as covariates. Participants were an average age of 79.7 ± 5.0 years (range = 71–97 years). Fifty-seven percent (n = 314) of the sample met criteria for SO/MD. Among participants with SO/MD, those with lower education performed more poorly on a test of category fluency than participants with higher education (means: 35.2 vs. 41.0; p < .001); among older adults without SO/MD, educational attainment had no measurable effect on cognition (SO/MD × education interaction (F(1,536) = 14.5; p = .00)). Consistent with the cognitive reserve hypothesis, older adults with lower education appear selectively vulnerable to the negative effects of sleep onset/maintenance difficulties on tests of verbal fluency. (JINS, 2012, 18, 461–470)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2012

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References

REFERENCES

Alchanatis, M., Zias, N., Deligiorgis, N., Amfilochiou, A., Dionellis, G., Orphanidou, D. (2005). Sleep apnea-related cognitive deficits and intelligence: An implication of cognitive reserve theory. Journal of Sleep Research, 14(1), 6975. doi:JSR436 [pii] 10.1111/j.1365-2869.2004.00436.xCrossRefGoogle ScholarPubMed
Altena, E., Van Der Werf, Y.D., Sanz-Arigita, E.J., Voorn, T.A., Rombouts, S.A., Kuijer, J.P., Van Someren, E.J. (2008). Prefrontal hypoactivation and recovery in insomnia. Sleep, 31(9), 12711276.Google ScholarPubMed
Altena, E., Vrenken, H., Van Der Werf, Y.D., van den Heuvel, O.A., Van Someren, E.J. (2010). Reduced orbitofrontal and parietal gray matter in chronic insomnia: A voxel-based morphometric study. Biological Psychiatry, 67(2), 182185. doi:S0006-3223(09)00954-8 [pii] 10.1016/j.biopsych.2009.08.003CrossRefGoogle ScholarPubMed
American Psychological Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association.Google Scholar
Ancoli-Israel, S., Lieberman, J.A. III. (2004). Insomnia in primary care: Overcoming diagnostic and treatment barriers. Introduction. Postgraduate Medicine, 116(6 Suppl Insomnia), 46. doi:10.3810/pgm.12.2004.suppl38.256Google ScholarPubMed
Anstey, K.J., Low, L.F. (2004). Normal cognitive changes in aging. Australian Family Physician, 33(10), 783787.Google ScholarPubMed
Army Individual Test Battery. (1944). Manual of directions and scoring. Washington, DC: War Department, Adjutant Generals Office.Google Scholar
Barr, A., Brandt, J. (1996). Word-list generation deficits in dementia. Journal of Clinical and Experimental Neuropsychology, 18(6), 810822. doi:10.1080/01688639608408304CrossRefGoogle ScholarPubMed
Beaulieu-Bonneau, S., Hudon, C. (2009). Sleep disturbances in older adults with mild cognitive impairment. International Psychogeriatrics, 21(4), 654666. doi:S1041610209009120 [pii]10.1017/S1041610209009120CrossRefGoogle ScholarPubMed
Beck, A.T., Epstein, N., Brown, G., Steer, R.A. (1988). An inventory for measuring clinical anxiety: Psychometric properties. J of Consulting and Clinical Psychology, 56(6), 893897.CrossRefGoogle ScholarPubMed
Benton, A.L., Hamsher, K. (1989). Multilingual aphasia examination. Iowa City, Iowa: AJA Associates.Google Scholar
Blessed, G., Tomlinson, B.E., Roth, M. (1968). The association between quantitative measures of dementia and of senile change in the cerebral grey matter of elderly subjects. British Journal of Psychiatry, 114(512), 797811.CrossRefGoogle ScholarPubMed
Brickman, A.M., Paul, R.H., Cohen, R.A., Williams, L.M., MacGregor, K.L., Jefferson, A.L., Gordon, E. (2005). Category and letter verbal fluency across the adult lifespan: Relationship to EEG theta power. Archives of Clinical Neuropsychology, 20(5), 561573. doi:S0887-6177(05)00009-0 [pii] 10.1016/j.acn.2004.12.006CrossRefGoogle ScholarPubMed
Brickman, A.M., Zimmerman, M.E., Paul, R.H., Grieve, S.M., Tate, D.F., Cohen, R.A., Gordon, E. (2006). Regional white matter and neuropsychological functioning across the adult lifespan. Biological Psychiatry, 60(5), 444453.CrossRefGoogle ScholarPubMed
Buschke, H. (1984). Cued recall in amnesia. Journal of Clinical Neuropsychology, 6(4), 433440.CrossRefGoogle ScholarPubMed
Christensen, H. (2001). What cognitive changes can be expected with normal ageing? Australian and New Zealand Journal of Psychiatry, 35(6), 768775.CrossRefGoogle ScholarPubMed
Cole, J.C., Dubois, D., Kosinski, M. (2007). Use of patient-reported sleep measures in clinical trials of pain treatment: A literature review and synthesis of current sleep measures and a conceptual model of sleep disturbance in pain. [Research Support, Non-U.S. Gov't]. Clinical Therapeutics, 29(Suppl), 25802588. doi:10.1016/j.clinthera.2007.12.005CrossRefGoogle Scholar
Cricco, M., Simonsick, E.M., Foley, D.J. (2001). The impact of insomnia on cognitive functioning in older adults. Journal of the American Geriatrics Society, 49(9), 11851189.CrossRefGoogle ScholarPubMed
Flegal, K.M., Carroll, M.D., Ogden, C.L., Curtin, L.R. (2010). Prevalence and trends in obesity among US adults, 1999–2008. Journal of the American Medical Association, 303(3), 235241. doi:2009.2014 [pii] 10.1001/jama.2009.2014CrossRefGoogle ScholarPubMed
Foley, D., Monjan, A., Masaki, K., Ross, W., Havlik, R., White, L., Launer, L. (2001). Daytime sleepiness is associated with 3-year incident dementia and cognitive decline in older Japanese-American men. Journal of the American Geriatrics Society, 49(12), 16281632.Google ScholarPubMed
Foley, D.J., Monjan, A.A., Brown, S.L., Simonsick, E.M., Wallace, R.B., Blazer, D.G. (1995). Sleep complaints among elderly persons: An epidemiologic study of three communities. Sleep, 18(6), 425432.CrossRefGoogle ScholarPubMed
Grober, E., Buschke, H. (1987). Genuine memory deficits in dementia. Developmental Neuropsychology, 3, 1336.CrossRefGoogle Scholar
Grober, E., Kawas, C. (1997). Learning and retention in preclinical and early Alzheimer's disease. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Psychology and Aging, 12(1), 183188.CrossRefGoogle ScholarPubMed
Grober, E., Lipton, R.B., Hall, C., Crystal, H. (2000). Memory impairment on free and cued selective reminding predicts dementia. Neurology, 54(4), 827832.CrossRefGoogle ScholarPubMed
Grober, E., Lipton, R.B., Katz, M., Sliwinski, M. (1998). Demographic influences on free and cued selective reminding performance in older persons. [Research Support, U.S. Gov't, P.H.S.]. Journal of Clinical and Experimental Neuropsychology, 20(2), 221226. doi:10.1076/jcen.20.2.221.1177CrossRefGoogle ScholarPubMed
Haimov, I., Hanuka, E., Horowitz, Y. (2008). Chronic insomnia and cognitive functioning among older adults. Behavioral Sleep Medicine, 6(1), 3254. doi:10.1080/15402000701796080CrossRefGoogle ScholarPubMed
Hall, C.B., Derby, C., LeValley, A., Katz, M.J., Verghese, J., Lipton, R.B. (2007). Education delays accelerated decline on a memory test in persons who develop dementia. [Research Support, N.I.H., Extramural]. Neurology, 69(17), 16571664. doi:10.1212/01.wnl.0000278163.82636.30CrossRefGoogle ScholarPubMed
Harrison, Y., Horne, J.A. (1997). Sleep deprivation affects speech. Sleep, 20(10), 871877.CrossRefGoogle ScholarPubMed
Hays, R.D., Martin, S.A., Sesti, A.M., Spritzer, K.L. (2005). Psychometric properties of the Medical Outcomes Study Sleep measure. Sleep Medicine, 6(1), 4144.CrossRefGoogle ScholarPubMed
Hoyt, B.D. (2005). Sleep in patients with neurologic and psychiatric disorders. Primary Care, 32(2), 535548, ix. doi:S0095-4543(05)00027-8 [pii] 10.1016/j.pop.2005.02.013CrossRefGoogle ScholarPubMed
Ivnik, R.J., Smith, G.E., Lucas, J.A., Tangalos, E.G., Kokmen, E., Petersen, R.C. (1997). Free and cued selective reminding test: MOANS norms. [Clinical Trial Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Journal of Clinical and Experimental Neuropsychology, 19(5), 676691. doi:10.1080/01688639708403753CrossRefGoogle ScholarPubMed
Jelicic, M., Bosma, H., Ponds, R.W., Van Boxtel, M.P., Houx, P.J., Jolles, J. (2002). Subjective sleep problems in later life as predictors of cognitive decline. Report from the Maastricht Ageing Study (MAAS). International Journal of Geriatric Psychiatry, 17(1), 7377. doi:10.1002/gps.529 [pii]CrossRefGoogle ScholarPubMed
Julian, L.J., Gregorich, S.E., Earnest, G., Eisner, M.D., Chen, H., Blanc, P.D., Katz, P.P. (2009). Screening for depression in chronic obstructive pulmonary disease. Chronic Obstructive Pulmonary Disease, 6(6), 452458. doi:10.3109/15412550903341463CrossRefGoogle ScholarPubMed
Karsten, J., Nolen, W.A., Penninx, B.W., Hartman, C.A. (2010). Subthreshold anxiety better defined by symptom self-report than by diagnostic interview. Journal of Affective Disorders 1. doi:S0165-0327(10)00574-4 [pii] 10.1016/j.jad.2010.09.006Google ScholarPubMed
Katz, D.A., McHorney, C.A. (2002). The relationship between insomnia and health-related quality of life in patients with chronic illness. Journal of Family Practice, 51(3), 229235.Google ScholarPubMed
Katz, M.J., Lipton, R.B., Hall, C.B., Zimmerman, M.E., Sanders, A.E., Verghese, J., Derby, C.A. (2011). Age and sex specific prevalence and incidence of mild cognitive impairment, dementia and Alzheimer's disease in blacks and whites: A report from the Einstein Aging Study. Alzheimer's Disease and Associated Disorders, [Epub ahead of print].Google Scholar
Koenigs, M., Holliday, J., Solomon, J., Grafman, J. (2010). Left dorsomedial frontal brain damage is associated with insomnia. Journal of Neuroscience, 30(47), 1604116043. doi:30/47/16041 [pii] 10.1523/JNEUROSCI.3745-10.2010CrossRefGoogle ScholarPubMed
Kryger, M., Monjan, A., Bliwise, D., Ancoli-Israel, S. (2004). Sleep, health, and aging. Bridging the gap between science and clinical practice. Geriatrics, 59(1), 2426, 29–30.Google Scholar
Lane, E.M., Paul, R.H., Moser, D.J., Fletcher, T.D., Cohen, R.A. (2011). Influence of education on subcortical hyperintensities and global cognitive status in vascular dementia. Journal of the International Neuropsychological Society, 9, 16. doi:10.1017/S1355617711000324Google Scholar
Lezak, M.D., Howieson, D.B., Loring, D.L. (2004). Neuropsychological assessment (4th ed.). New York: Oxford University Press.Google Scholar
Lipton, R.B., Katz, M.J., Kuslansky, G., Sliwinski, M.J., Stewart, W.F., Verghese, J., Buschke, H. (2003). Screening for dementia by telephone using the memory impairment screen. Journal of the American Geriatrics Society, 51(10), 13821390.CrossRefGoogle ScholarPubMed
McCrae, C.S., Wilson, N.M., Lichstein, K.L., Durrence, H.H., Taylor, D.J., Bush, A.J., Riedel, B.W. (2003). ‘Young old’ and ‘old old’ poor sleepers with and without insomnia complaints. Journal of Psychosomatic Research, 54(1), 1119. doi:S0022399902005433 [pii]CrossRefGoogle ScholarPubMed
McCurry, S.M., Ancoli-Israel, S. (2003). Sleep dysfunction in Alzheimer's disease and other dementias. Current Treament Options in Neurology, 5(3), 261272.CrossRefGoogle ScholarPubMed
McDowd, J., Hoffman, L., Rozek, E., Lyons, K.E., Pahwa, R., Burns, J., Kemper, S. (2011). Understanding verbal fluency in healthy aging, Alzheimer's disease, and Parkinson's disease. Neuropsychology, 25(2), 210225. doi:2011-04169-007 [pii] 10.1037/a0021531CrossRefGoogle ScholarPubMed
Merlino, G., Piani, A., Gigli, G.L., Cancelli, I., Rinaldi, A., Baroselli, A., Valente, M. (2010). Daytime sleepiness is associated with dementia and cognitive decline in older Italian adults: A population-based study. Sleep Medicine, 11(4), 372377. doi:S1389-9457(10)00061-4 [pii] 10.1016/j.sleep.2009.07.018CrossRefGoogle ScholarPubMed
Monsch, A.U., Bondi, M.W., Butters, N., Salmon, D.P., Katzman, R., Thal, L. (1992). Comparisons of verbal fluency tasks in the detection of dementia of the Alzheimer type. Archives of Neurology, 49, 12531258.CrossRefGoogle ScholarPubMed
Naismith, S.L., Rogers, N.L., Hickie, I.B., Mackenzie, J., Norrie, L.M., Lewis, S.J. (2010). Sleep well, think well: Sleep-wake disturbance in mild cognitive impairment. Journal of Geriatric Psychiatry and Neurology, 23(2), 123130. doi:0891988710363710 [pii] 10.1177/0891988710363710CrossRefGoogle 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. Journals of Gerontology Series B: Psychological Sciences and Socical Sciences, 64(2), 180187. doi:gbn037 [pii] 10.1093/geronb/gbn037CrossRefGoogle ScholarPubMed
Neikrug, A.B., Ancoli-Israel, S. (2010). Sleep disorders in the older adult: A mini-review. Gerontology, 56(2), 181189. doi:000236900 [pii] 10.1159/000236900CrossRefGoogle ScholarPubMed
Ohayon, M.M. (2002). Epidemiology of insomnia: What we know and what we still need to learn. Sleep Medicine Reviews, 6(2), 97111. doi:S1087079202901863 [pii]CrossRefGoogle ScholarPubMed
Park, D.C. (2000). The basic mechanisms accounting for age-related decline in cognition function. In D.C. Park & N. Schwarz (Eds.), Cognitive aging: A primer (pp. 321). Philadelphia: Psychology Press.Google Scholar
Perlis, M.L., Smith, L.J., Lyness, J.M., Matteson, S.R., Pigeon, W.R., Jungquist, C.R., Tu, X. (2006). Insomnia as a risk factor for onset of depression in the elderly. Behavioral Sleep Medicine, 4(2), 104113. doi:10.1207/s15402010bsm0402_3CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183194. doi:10.1111/j.1365-2796.2004.01388.x JIM1388 [pii]CrossRefGoogle ScholarPubMed
Pleiss, J.R., Ward, B.W., Lucas, J. (2010). Summary health statistics for U.S. adults: National Health Interview Survey, 2009 Vital Health Statistics (Vol. 10). Washington, DC: National Center for Health Statistics.Google Scholar
Sarazin, M., Berr, C., De Rotrou, J., Fabrigoule, C., Pasquier, F., Legrain, S., Dubois, B. (2007). Amnestic syndrome of the medial temporal type identifies prodromal AD: A longitudinal study. [Comparative Study Research Support, Non-U.S. Gov't]. Neurology, 69(19), 18591867. doi:10.1212/01.wnl.0000279336.36610.f7CrossRefGoogle ScholarPubMed
Schmutte, T., Harris, S., Levin, R., Zweig, R., Katz, M., Lipton, R. (2007). The relation between cognitive functioning and self-reported sleep complaints in nondemented older adults: Results from the Bronx aging study. Behavioral Sleep Medicine, 5(1), 3956.CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 20152028. doi:S0028-3932(09)00123-7 [pii] 10.1016/j.neuropsychologia.2009.03.004CrossRefGoogle ScholarPubMed
Thal, L.J., Grundman, M., Golden, R. (1986). Alzheimer's disease: A correlational analysis of the Blessed Information-Memory-Concentration Test and the Mini-Mental State Exam. [Comparative Study]. Neurology, 36(2), 262264.CrossRefGoogle ScholarPubMed
Tomer, R., Levin, B.E. (1993). Differential effects of aging on two verbal fluency tasks. Perceptual Motor Skills, 76(2), 465466.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler adult intelligence scale—Third edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Wilkinson, G.S. (1993). Wide range achievement test 3 administration manual. Wilmington, DE: Wide Range, Inc.Google Scholar
Yaouhi, K., Bertran, F., Clochon, P., Mezenge, F., Denise, P., Foret, J., Desgranges, B. (2009). A combined neuropsychological and brain imaging study of obstructive sleep apnea. Journal of Sleep Research, 18(1), 3648. doi:JSR705 [pii] 10.1111/j.1365-2869.2008.00705.xCrossRefGoogle ScholarPubMed
Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., Leirer, V.O. (1982). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatry Research, 17(1), 3749.CrossRefGoogle Scholar
Zimmerman, M.E., Brickman, A.M. (2009). Neuropsychology of healthy aging. In R.H. Paul, N.C. Sactor, V. Valcour & K.T. Toshima (Eds.), HIV and the brain: New challenges in the modern era (pp. 347368). Totowa, NJ: Humana Press.CrossRefGoogle Scholar
Zimmerman, M.E., Brickman, A.M., Paul, R.H., Grieve, S.M., Tate, D.F., Gunstad, J., Gordon, E. (2006). The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. American Journal of Geriatric Psychiatry, 14(10), 823833.CrossRefGoogle ScholarPubMed
Zimmerman, M.E., Lipton, R.B., Santoro, N., McConnell, D.S., Derby, C.A., Katz, M.J., Saunders-Pullman, R. (2011). Endogenous estradiol is associated with verbal memory in nondemented older men. [Research Support, N.I.H., Extramural]. Brain and Cognition, 76(1), 158165. doi:10.1016/j.bandc.2011.01.011CrossRefGoogle ScholarPubMed