Hostname: page-component-848d4c4894-wg55d Total loading time: 0 Render date: 2024-05-22T10:17:20.592Z Has data issue: false hasContentIssue false
  • English
  • Français

The Impact of Sleep Quality on Cognitive Functioning in Parkinson's Disease

Published online by Cambridge University Press:  09 December 2011

Karina Stavitsky ,
Sandy Neargarder ,
Yelena Bogdanova ,
Patrick McNamara  and
Alice Cronin-Golomb
Karina Stavitsky
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts
Sandy Neargarder
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts Department of Psychology, Bridgewater State University, Bridgewater, Massachusetts
Yelena Bogdanova
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts Psychology Research, VA Boston Healthcare System, Boston, Massachusetts Department of Psychiatry, Harvard Medical School, Boston, Massachusetts
Patrick McNamara
Affiliation:
Department of Neurology, Boston University School of Medicine, Boston, Massachusetts Department of Neurology, VA Boston Healthcare System, Boston, Massachusetts
Alice Cronin-Golomb*
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts
*
Corresponding author: Alice Cronin-Golomb, Department of Psychology, Boston University, 648 Beacon Street, 2nd Floor, Boston, MA 02215. E-mail: alicecg@bu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

In healthy individuals and those with insomnia, poor sleep quality is associated with decrements in performance on tests of cognition, especially executive function. Sleep disturbances and cognitive deficits are both prevalent in Parkinson's disease (PD). Sleep problems occur in over 75% of patients, with sleep fragmentation and decreased sleep efficiency being the most common sleep complaints, but their relation to cognition is unknown. We examined the association between sleep quality and cognition in PD. In 35 non-demented individuals with PD and 18 normal control adults (NC), sleep was measured using 24-hr wrist actigraphy over 7 days. Cognitive domains tested included attention and executive function, memory and psychomotor function. In both groups, poor sleep was associated with worse performance on tests of attention/executive function but not memory or psychomotor function. In the PD group, attention/executive function was predicted by sleep efficiency, whereas memory and psychomotor function were not predicted by sleep quality. Psychomotor and memory function were predicted by motor symptom severity. This study is the first to demonstrate that sleep quality in PD is significantly correlated with cognition and that it differentially impacts attention and executive function, thereby furthering our understanding of the link between sleep and cognition. (JINS, 2012, 18, 108–117)

Keywords

Parkinson's diseaseSleepCognitionExecutive functionActigraphyMemory
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 1 , January 2012 , pp. 108 - 117
Copyright
Copyright © The International Neuropsychological Society 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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), 1271–1276.Google ScholarPubMed
Altena, E., Van Der Werf, Y.D., Strijers, R.L., Van Someren, E.J. (2008). Sleep loss affects vigilance: Effects of chronic insomnia and sleep therapy. Journal of Sleep Research, 17(3), 335–343.CrossRefGoogle ScholarPubMed
Alves, G., Larsen, J.P., Emre, M., Wentzel-Larsen, T., Aarsland, D. (2006). Changes in motor subtype and risk for incident dementia in Parkinson's disease. Movement Disorders, 21(8), 1123–1130.CrossRefGoogle ScholarPubMed
Amick, M.M., Grace, J., Chou, K.L. (2006). Body side of motor symptom onset in Parkinson's disease is associated with memory performance. Journal of the International Neuropsychological Society, 12(5), 736–740.CrossRefGoogle ScholarPubMed
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
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(1), 39–49.CrossRefGoogle ScholarPubMed
Beck, A.T., Steer, R.A. (1993). Beck anxiety inventory manual. San Antonio, TX: Psychological Corporation.Google Scholar
Beck, A.T., Steer, R.A., Brown, G.K. (1996). BDI-II, Beck depression inventory manual (2nd ed.). San Antonio, TX: Psychological Corporation.Google Scholar
Benedict, R.H. (2005). Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis. Journal of the International Neuropsychological Society, 11(6), 727–736.CrossRefGoogle ScholarPubMed
Benton, A., Hamsher, K. (1989). Multilingual aphasia examination. Iowa City: AJA Associates.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. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 61(4), 405–410.CrossRefGoogle ScholarPubMed
Blood, M.L., Sack, R.L., Percy, D.C., Pen, J.C. (1997). A comparison of sleep detection by wrist actigraphy, behavioral response, and polysomnography. Sleep, 20(6), 388–395.Google ScholarPubMed
Bordelon, Y.M., Fahn, S. (2006). Gender differences in movement disorders. In P.W. Kaplan (Ed.), Neurologic disease in women. New York: Demos Medical Publishing.Google Scholar
Braak, H., Ghebremedhin, E., Rub, U., Bratzke, H., Del Tredici, K. (2004). Stages in the development of Parkinson's disease-related pathology. Cell Tissue Research, 318(1), 121–134.CrossRefGoogle ScholarPubMed
Bronnick, K., Aarsland, D., Larsen, J.P. (2005). Neuropsychiatric disturbances in Parkinson's disease clusters in five groups with different prevalence of dementia. Acta Psychiatrica Scandinavica, 112(3), 201–207.CrossRefGoogle ScholarPubMed
Brown, R.G., Marsden, C.D. (1988). Internal versus external cues and the control of attention in Parkinson's disease. Brain, 111(Pt 2), 323–345.CrossRefGoogle ScholarPubMed
Clark, C., Dupont, R., Lehr, P., Yeung, D., Halpern, S., Golshan, S., Gillin, J.C. (1998). Is there a relationship between delta sleep at night and afternoon cerebral blood flow, assessed by HMPAO-SPECT in depressed patients and normal control subjects? Preliminary data. Psychiatry Research, 84(2–3), 89–99.CrossRefGoogle Scholar
Comella, C.L. (2003). Sleep disturbances in Parkinson's disease. Current Neurology and Neuroscience Reports, 3(2), 173–180.CrossRefGoogle ScholarPubMed
Comella, C.L. (2006). Sleep disturbances and excessive daytime sleepiness in Parkinson disease: An overview. Journal of Neural Transmission. Supplementum, (70), 349–355.Google ScholarPubMed
Cronin-Golomb, A. (2010). Parkinson's disease as a disconnection syndrome. Neuropsychology Review, 20(2), 191–208.CrossRefGoogle ScholarPubMed
Decary, A., Rouleau, I., Montplaisir, J. (2000). Cognitive deficits associated with sleep apnea syndrome: A proposed neuropsychological test battery. Sleep, 23(3), 369–381.CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A. (2000). California verbal learning test-second edition (CVLT-II). San Antonio, TX: Psychological Corporation.Google Scholar
Fahn, S. (2003). Description of Parkinson's disease as a clinical syndrome. Annals of the New York Academy of Sciences, 991, 1–14.CrossRefGoogle ScholarPubMed
Fowler, M.J., Sullivan, M.J., Ekstrand, B.R. (1973). Sleep and memory. Science, 179(70), 302–304.CrossRefGoogle ScholarPubMed
Gagnon, J.F., Petit, D., Latreille, V., Montplaisir, J. (2008). Neurobiology of sleep disturbances in neurodegenerative disorders. Current Pharmaceutical Design, 14(32), 3430–3445.CrossRefGoogle ScholarPubMed
Gais, S., Plihal, W., Wagner, U., Born, J. (2000). Early sleep triggers memory for early visual discrimination skills. Nature Neuroscience, 3(12), 1335–1339.CrossRefGoogle ScholarPubMed
Gjerstad, M.D., Boeve, B., Wentzel-Larsen, T., Aarsland, D., Larsen, J.P. (2008). Occurrence and clinical correlates of REM sleep behaviour disorder in patients with Parkinson's disease over time. Journal of Neurology, Neurosurgery, and Psychiatry, 79(4), 387–391.CrossRefGoogle ScholarPubMed
Goel, N., Rao, H., Durmer, J.S., Dinges, D.F. (2009). Neurocognitive consequences of sleep deprivation. Seminars in Neurology, 29(4), 320–339.CrossRefGoogle ScholarPubMed
Grinberg, L.T., Rueb, U., Alho, A.T., Heinsen, H. (2009). Brainstem pathology and non-motor symptoms in PD. Journal of Neurological Science, 289(1–2), 81–88.CrossRefGoogle ScholarPubMed
Groeger, J.A., Lo, J.C., Burns, C.G., Dijk, D.J. (2011). Effects of sleep inertia after daytime naps vary with executive load and time of day. Behavioral Neuroscience, 125(2), 252–260.CrossRefGoogle ScholarPubMed
Gunn, D.G., Naismith, S.L., Lewis, S.J. (2010). Sleep disturbances in Parkinson disease and their potential role in heterogeneity. Journal of Geriatric Psychiatry and Neurology, 23(2), 131–137.CrossRefGoogle ScholarPubMed
Haimov, I., Hanuka, E., Horowitz, Y. (2008). Chronic insomnia and cognitive functioning among older adults. Behavavioral Sleep Medicine, 6(1), 32–54.CrossRefGoogle ScholarPubMed
Hauri, P.J. (1997). Cognitive deficits in insomnia patients. Acta Neurologica Belgica, 97(2), 113–117.Google ScholarPubMed
Henry, J.D., Crawford, J.R. (2004). Verbal fluency deficits in Parkinson's disease: A meta-analysis. Journal of the International Neuropsychological Society, 10(4), 608–622.CrossRefGoogle ScholarPubMed
Hobson, J.A., Stickgold, R., Pace-Schott, E.F. (1998). The neuropsychology of REM sleep dreaming. Neuroreport, 9(3), R1–R14.CrossRefGoogle ScholarPubMed
Hoehn, M.M., Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427–442.CrossRefGoogle ScholarPubMed
Jean-Louis, G., von Gizycki, H., Zizi, F., Fookson, J., Spielman, A., Nunes, J., Taub, H. (1996). Determination of sleep and wakefulness with the actigraph data analysis software (ADAS). Sleep, 19(9), 739–743.Google ScholarPubMed
Johns, M.W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14(6), 540–545.CrossRefGoogle ScholarPubMed
Karni, A., Tanne, D., Rubenstein, B.S., Askenasy, J.J., Sagi, D. (1994). Dependence on REM sleep of overnight improvement of a perceptual skill. Science, 265(5172), 679–682.CrossRefGoogle ScholarPubMed
Kuriyama, K., Mishima, K., Suzuki, H., Aritake, S., Uchiyama, M. (2008). Sleep accelerates the improvement in working memory performance. Journal of Neuroscience, 28(40), 10145–10150.CrossRefGoogle ScholarPubMed
Maetzler, W., Liepelt, I., Berg, D. (2009). Progression of Parkinson's disease in the clinical phase: Potential markers. Lancet Neurology, 8(12), 1158–1171.CrossRefGoogle ScholarPubMed
McKeith, I.G., Dickson, D.W., Lowe, J., Emre, M., O'Brien, J.T., Feldman, H., Yamada, M. (2005). Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium. Neurology, 65(12), 1863–1872.CrossRefGoogle ScholarPubMed
Mednick, S.C., Makovski, T., Cai, D.J., Jiang, Y.V. (2009). Sleep and rest facilitate implicit memory in a visual search task. Vision Research, 49(21), 2557–2565.CrossRefGoogle Scholar
Mendelson, W.B., Garnett, D., Gillin, J.C., Weingartner, H. (1984). The experience of insomnia and daytime and nighttime functioning. Psychiatry Research, 12(3), 235–250.CrossRefGoogle ScholarPubMed
Middleton, F.A., Strick, P.L. (2001). Cerebellar projections to the prefrontal cortex of the primate. Journal of Neuroscience, 21(2), 700–712.CrossRefGoogle Scholar
Miller, I.N., Cronin-Golomb, A. (2010). Gender differences in Parkinson's disease: Clinical characteristics and cognition. Movement Disorders, 25, 2695–2703.CrossRefGoogle ScholarPubMed
Muslimovic, D., Post, B., Speelman, J.D., De Haan, R.J., Schmand, B. (2009). Cognitive decline in Parkinson's disease: A prospective longitudinal study. Journal of the International Neuropsychological Society, 15(3), 426–437.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. Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 64(2), 180–187.CrossRefGoogle ScholarPubMed
Owen, A.M., Iddon, J.L., Hodges, J.R., Summers, B.A., Robbins, T.W. (1997). Spatial and non-spatial working memory at different stages of Parkinson's disease. Neuropsychologia, 35(4), 519–532.CrossRefGoogle ScholarPubMed
Purdue, F.R. (1948). Purdue pegboard test. Lafayette, IN: Lafayette Instrument Co.Google Scholar
Rasch, B., Buchel, C., Gais, S., Born, J. (2007). Odor cues during slow-wave sleep prompt declarative memory consolidation. Science, 315(5817), 1426–1429.CrossRefGoogle ScholarPubMed
Ruff, R.M., Light, R.H., Evans, R.W. (1987). The Ruff figural fluency test: A normative study with adults. Developmental Neuropsychology, 3, 37–52.CrossRefGoogle Scholar
Rupp, T., Arnedt, T.J., Acebo, C., Carskadon, M.A. (2004). Performance on a dual driving simulation and subtraction task following sleep restriction. Perceptual and Motor Skills, 99, 739–753.CrossRefGoogle ScholarPubMed
Sadeh, A., Acebo, C. (2002). The role of actigraphy in sleep medicine. Sleep Medicine Reviews, 6(2), 113–124.CrossRefGoogle ScholarPubMed
Sinforiani, E., Zangaglia, R., Manni, R., Cristina, S., Marchioni, E., Nappi, G., Pacchetti, C. (2006). REM sleep behavior disorder, hallucinations, and cognitive impairment in Parkinson's disease. Movement Disorders, 21(4), 462–466.CrossRefGoogle ScholarPubMed
Smith, C. (1993). In M.K.A. Moffit & R. Hoffman (Eds.), The functions of dreaming. New York: SUNY Press.Google Scholar
Smith, C. (2001). Sleep states and memory processes in humans: Procedural versus declarative memory systems. Sleep Medicine Reviews, 5(6), 491–506.CrossRefGoogle ScholarPubMed
Stavitsky, K., Cronin-Golomb, A. (2011). Sleep quality in Parkinson's disease: An examination of clinical variables. Cognitive and Behavioral Neurology, 24(2), 43–49.CrossRefGoogle ScholarPubMed
Stavitsky, K., McNamara, P., Durso, R., Harris, E., Auerbach, S., Cronin-Golomb, A. (2008). Hallucinations, dreaming, and frequent dozing in Parkinson disease: Impact of right-hemisphere neural networks. Cognitive and Behavioral Neurology, 21(3), 143–149.CrossRefGoogle ScholarPubMed
Stavitsky, K., Saurman, J.L., McNamara, P., Cronin-Golomb, A. (2010). Sleep in Parkinson's disease: A comparison of actigraphy and subjective measures. Parkinsonism and Related Disorders, 16(4), 280–283.CrossRefGoogle ScholarPubMed
Stern, Y., Sano, M., Paulson, J., Mayeux, R. (1987). Modified Mini-Mental State Examination:validity and reliability [abstract]. Neurology, 37(Suppl. 1), 179.Google Scholar
Stickgold, R. (2005). Sleep-dependent memory consolidation. Nature, 437(7063), 1272–1278.CrossRefGoogle ScholarPubMed
Stickgold, R., Hobson, J.A., Fosse, R., Fosse, M. (2001). Sleep, learning, and dreams: Off-line memory reprocessing. Science, 294(5544), 1052–1057.CrossRefGoogle ScholarPubMed
Stickgold, R., James, L., Hobson, J.A. (2000). Visual discrimination learning requires sleep after training. Nature Neuroscience, 3(12), 1237–1238.CrossRefGoogle ScholarPubMed
Stickgold, R., Whidbee, D., Schirmer, B., Patel, V., Hobson, J.A. (2000). Visual discrimination task improvement: A multi-step process occurring during sleep. Journal of Cognitive Neuroscience, 12(2), 246–254.CrossRefGoogle ScholarPubMed
Stroop, J.R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 121(1), 15–23.CrossRefGoogle Scholar
Tombaugh, T.N. (2004). Trail making test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203–214.CrossRefGoogle Scholar
Tucker, A.M., Whitney, P., Belenky, G., Hinson, J.M., Van Dongen, H.P.A. (2010). Effects of sleep deprivation on associated components of executive functioning. Sleep, 33(1), 47–57.CrossRefGoogle ScholarPubMed
Van Dongen, H.P., 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
Vendette, M., Gagnon, J.F., Decary, A., Massicotte-Marquez, J., Postuma, R.B., Doyon, J., Montplaisir, J. (2007). REM sleep behavior disorder predicts cognitive impairment in Parkinson disease without dementia. Neurology, 69(19), 1843–1849.CrossRefGoogle ScholarPubMed
Verbaan, D., Marinus, J., Visser, M., van Rooden, S.M., Stiggelbout, A.M., Middelkoop, H.A., van Hilten, J.J. (2007). Cognitive impairment in Parkinson's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 78(11), 1182–1187.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler adult intelligence scale. San Antonio, TX: The Psychological Corporation.Google Scholar
Woodward, T.S., Bub, D.N., Hunter, M.A. (2002). Task switching deficits associated with Parkinson's disease reflect depleted attentional resources. Neuropsychologia, 40(12), 1948–1955.CrossRefGoogle ScholarPubMed
Zgaljardic, D.J., Borod, J.C., Foldi, N.S., Mattis, P. (2003). A review of the cognitive and behavioral sequelae of Parkinson's disease: Relationship to frontostriatal circuitry. Cognitive and Behavioral Neurology, 16(4), 193–210.CrossRefGoogle ScholarPubMed
Zgaljardic, D.J., Borod, J.C., Foldi, N.S., Mattis, P.J., Gordon, M.F., Feigin, A., Eidelberg, D. (2006). An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson's disease. Journal of Clinical and Experimental Neuropsychology, 28(7), 1127–1144.CrossRefGoogle ScholarPubMed