Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-05-18T17:53:10.043Z Has data issue: false hasContentIssue false

Concurrent Impairments in Sleep and Memory in Amnestic Mild Cognitive Impairment

Published online by Cambridge University Press:  03 February 2012

Carmen E. Westerberg*
Affiliation:
Psychology Department and Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois Psychology Department, Texas State University, San Marcos, Texas
Bryce A. Mander
Affiliation:
Psychology Department, University of California, Berkeley, California
Susan M. Florczak
Affiliation:
Psychology Department and Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois
Sandra Weintraub
Affiliation:
Psychology Department and Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois Cognitive Neurology and Alzheimer's Disease Center, Feinberg School of Medicine, Northwestern University, Chicago, Illinois Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Chicago, Illinois Neurology Department, Feinberg School of Medicine, Northwestern University, Chicago, Illinois
M.-Marsel Mesulam
Affiliation:
Cognitive Neurology and Alzheimer's Disease Center, Feinberg School of Medicine, Northwestern University, Chicago, Illinois Neurology Department, Feinberg School of Medicine, Northwestern University, Chicago, Illinois
Phyllis C. Zee
Affiliation:
Neurology Department, Feinberg School of Medicine, Northwestern University, Chicago, Illinois
Ken A. Paller
Affiliation:
Psychology Department and Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois
*
Correspondence and reprint requests to: Carmen E. Westerberg, Department of Psychology, Texas State University, San Marcos, 601 University Drive, San Marcos, TX 78666. E-mail: cw54@txstate.edu

Abstract

Whereas patients with Alzheimer's disease (AD) experience difficulties forming and retrieving memories, their memory impairments may also partially reflect an unrecognized dysfunction in sleep-dependent consolidation that normally stabilizes declarative memory storage across cortical areas. Patients with amnestic mild cognitive impairment (aMCI) exhibit circumscribed declarative memory deficits, and many eventually progress to an AD diagnosis. Whether sleep is disrupted in aMCI and whether sleep disruptions contribute to memory impairment is unknown. We measured sleep physiology and memory for two nights and found that aMCI patients had fewer stage-2 spindles than age-matched healthy adults. Furthermore, aMCI patients spent less time in slow-wave sleep and showed lower delta and theta power during sleep compared to controls. Slow-wave and theta activity during sleep appear to reflect important aspects of memory processing, as evening-to-morning change in declarative memory correlated with delta and theta power during intervening sleep in both groups. These results suggest that sleep changes in aMCI patients contribute to memory impairments by interfering with sleep-dependent memory consolidation. (JINS, 2012, 18, 490–500)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2012

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

Akerstedt, T., Hume, K., Minors, D., Waterhouse, J. (1994). The subjective meaning of good sleep, an intraindividual approach using the Karolinska Sleep Diary. Perceptual and Motor Skills, 79, 287296.CrossRefGoogle ScholarPubMed
Babiloni, C., Vecchio, F., Mirabella, G., Buttiglione, M., Sebastiano, F., Picardi, A., Eusebi, F. (2009). Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during rey auditory verbal learning test. Human Brain Mapping, 30, 20772089.CrossRefGoogle Scholar
Beaulieu-Bonneau, S., Hudon, C. (2009). Sleep disturbances in older adults with mild cognitive impairment. International Psychogeriatrics, 21, 654666.CrossRefGoogle ScholarPubMed
Benca, R.M., Obermeyer, W.H., Thisted, R.A., Gillin, J.C. (1992). Sleep and psychiatric disorders. A meta-analysis. Archives of General Psychiatry, 49, 651668.CrossRefGoogle ScholarPubMed
Bliwise, D.L. (1993). Sleep in normal aging and dementia. Sleep, 16, 4081.CrossRefGoogle ScholarPubMed
Bodizs, R., Bekesy, M., Szucs, A., Barsi, P., Halasz, P. (2001). Sleep-dependent hippocampal slow activity correlates with waking memory performance in humans. Neurobiology of Learning and Memory, 78, 441457.CrossRefGoogle Scholar
Braak, H., Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82, 239259.CrossRefGoogle ScholarPubMed
Buysse, D.J., Reynolds, C.F. III, Monk, T.H., Berman, S.R., Kupfer, D.J. (1989). The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Research, 28, 193213.CrossRefGoogle ScholarPubMed
Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron, 33, 325340.CrossRefGoogle ScholarPubMed
Chee, M.W., Chuah, L.Y. (2008). Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Current Opinion in Neurology, 21, 417423.CrossRefGoogle ScholarPubMed
Clemens, Z., Fabo, D., Halasz, P. (2005). Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience, 132, 529535.CrossRefGoogle ScholarPubMed
Danker-Hopfe, H., Schafer, M., Dorn, H., Anderer, P., Saletu, B., Gruber, G., Dorffner, G. (2005). Percentile reference charts for selected sleep parameters for 20- to 80-year-old healthy subjects from the SIESTA database. Somnologie, 9, 314.CrossRefGoogle Scholar
Diekelmann, S., Born, J. (2010). The memory function of sleep. Nature Reviews Neuroscience, 11, 114126.CrossRefGoogle ScholarPubMed
Drosopoulos, S., Wagner, U., Born, J. (2005). Sleep enhances explicit recollection in recognition memory. Learning & Memory, 12, 4451.CrossRefGoogle ScholarPubMed
Ehlers, C.L., Kupfer, D.J. (1989). Effects of age on delta and REM sleep parameters. Electroencephalography and Clinical Neurophysiology, 72, 118125.CrossRefGoogle ScholarPubMed
Eichenbaum, H., Cohen, N.J. (2001). Conditioning to conscious recollection: Memory systems of the brain. New York, NY: Oxford University Press.Google Scholar
Fogel, S.M., Smith, C.T., Cote, K.A. (2007). Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behavioural Brain Research, 180, 4861.CrossRefGoogle ScholarPubMed
Folstein, M.F., 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, 189198.CrossRefGoogle ScholarPubMed
Goder, R., Aldenhoff, J.B., Boigs, M., Braun, S., Koch, J., Fritzer, G. (2006). Delta power in sleep in relation to neuropsychological performance in healthy subjects and schizophrenia patients. Journal of Neuropsychiatry and Clinical Neurosciences, 18, 529535.CrossRefGoogle ScholarPubMed
Hogan, M.J., Kelly, C.A., Verrier, D., Newell, J., Hasher, L., Robertson, I.H. (2009). Optimal time-of-day and consolidation of learning in younger and older adults. Experimental Aging Research, 28, 107128.CrossRefGoogle Scholar
Hot, P., Rauchs, G., Bertran, F., Denise, P., Desgranges, B., Clochon, P., Eustache, F. (2011). Changes in sleep theta rhythm are related to episodic memory imapriment in early Alzheimer's disease. Biological Psychology, 87, 334339.CrossRefGoogle ScholarPubMed
Huber, R., Ghilardi, M.F., Massimini, M., Tononi, G. (2004). Local sleep and learning. Nature, 430, 7881.CrossRefGoogle ScholarPubMed
Iber, C., Ancoli-Israel, S., Chesson, A.L., Quan, S.F. (2007). The AASM manual for the scoring of sleep and associated events. Westchester, IL: American Academy of Sleep Medicine.Google Scholar
Ji, D., Wilson, M.A. (2007). Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neuroscience, 10, 100107.CrossRefGoogle ScholarPubMed
Johns, M.W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14, 540545.CrossRefGoogle ScholarPubMed
Jorm, A.F. (1994). A short form of the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): Development and cross-validation. Psychological Medicine, 24, 145153.CrossRefGoogle Scholar
Kaplan, E., Goodglass, H., Weintraub, S. (1983). The Boston naming test. Philadelphia, PA: Lea & Febiger.Google Scholar
Klimesch, W., Doppelmayr, M., Russegger, H., Pachinger, T. (1996). Theta band power in the human scalp EEG and the encoding of new information. Neuroreport, 7, 12351240.CrossRefGoogle ScholarPubMed
Landolt, H.P., Borbely, A.A. (2001). Age-dependent changes in sleep EEG topography. Clinical Neurophysiology, 112, 369377.CrossRefGoogle ScholarPubMed
Maquet, P. (2001). The role of sleep in learning and memory. Science, 294, 10481052.CrossRefGoogle ScholarPubMed
Marshall, L., Born, J. (2007). The contribution of sleep to hippocampus-dependent memory consolidation. Trends in Cognitive Sciences, 11, 442450.CrossRefGoogle ScholarPubMed
Marshall, L., Helgadottir, H., Molle, M., Born, J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature, 444, 610613.CrossRefGoogle ScholarPubMed
Marshall, L., Molle, M., Hallschmid, M., Born, J. (2004). Transcranial direct current stimulation during sleep improves declarative memory. Journal of Neuroscience, 24, 99859992.CrossRefGoogle ScholarPubMed
Mayes, A., Montaldi, D., Migo, E. (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11, 126135.CrossRefGoogle ScholarPubMed
McCurry, S.M., Ancoli-Israel, S. (2003). Sleep dysfunction in Alzheimer's disease and other dementias. Current Treatment Options in Neurology, 5, 261272.CrossRefGoogle ScholarPubMed
Mesulam, M. (2004). The cholinergic lesion of Alzheimer's disease: Pivotal factor or side show? Learning and Memory, 11, 4349.CrossRefGoogle ScholarPubMed
Mesulam, M., Shaw, P., Mash, D., Weintraub, S. (2004). Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Annals of Neurology, 55, 815828.CrossRefGoogle ScholarPubMed
Montgomery, S.M., Sirota, A., Buzsaki, G. (2008). Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. Journal of Neuroscience, 28, 67316741.CrossRefGoogle ScholarPubMed
Morris, J.C., Heyman, A., Mohs, R.C., Hughes, J.P., van Belle, G., Fillenbaum, G., Clark, C. (1989). The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology, 39, 11591165.Google Scholar
Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., Rosenbaum, R.S. (2006). The cognitive neuroscience of remote episodic, semantic and spatial memory. Current Opinion in Neurobiology, 16, 179190.CrossRefGoogle ScholarPubMed
Nishida, M., Pearsall, J., Buckner, R.L., Walker, M.P. (2009). REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cerebral Cortex, 19, 11581166.CrossRefGoogle ScholarPubMed
Paller, K.A. (1997). Consolidating dispersed neocortical memories: The missing link in amnesia. Memory, 5, 7388.CrossRefGoogle ScholarPubMed
Paller, K.A. (2009). Memory consolidation: Systems. In L.R. Squire (Ed.), Encyclopedia of Neuroscience. Oxford: Academic Press.Google Scholar
Pavlides, C., Winson, J. (1989). Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journaal of Neuroscience, 9, 29072918.CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183194.CrossRefGoogle ScholarPubMed
Petersen, R.C., Parisi, J.E., Dickson, D.W., Johnson, K.A., Knopman, D.S., Boeve, B.F., Kokmen, E. (2006). Neuropathologic features of amnestic mild cognitive impairment. Archives of Neurology, 63, 665672.CrossRefGoogle ScholarPubMed
Petit, D., Montplaisir, J., Lorrain, D., Gauthier, S. (1992). Spectral analysis of the rapid eye movement sleep electroencephalogram in right and left temporal regions: A biological marker of Alzheimer's disease. Annals of Neurology, 32, 172176.CrossRefGoogle ScholarPubMed
Pfeffer, R.I., Kurosaki, T.T., Harrah, C.H. Jr., Chance, J.M., Filos, S. (1982). Measurement of functional activities in older adults in the community. Journal of Gerontology, 37, 323329.CrossRefGoogle ScholarPubMed
Plihal, W., Born, J. (1997). Effects of early and late nocturnal sleep on declarative and procedural memory. Journal of Cognitive Neuroscience, 9, 534547.CrossRefGoogle ScholarPubMed
Power, A.E. (2004). Slow-wave sleep, acetylcholine, and memory consolidation. Proceedings of the National Academy of Sciences of the United States of America, 101, 17951796.CrossRefGoogle ScholarPubMed
Prinz, P.N., Larsen, L.H., Moe, K.E., Vitiello, M.V. (1992). EEG markers of early Alzheimer's disease in computer selected tonic REM sleep. Electroencephalography and Clinical Neurophysiology, 83, 3643.CrossRefGoogle ScholarPubMed
Prinz, P.N., Poceta, J.S., McCurry, S. (2002). Sleep in the dementing disorders. In T.L. Lee-Chiong, M.J. Sateia, & M.A. Carskadon (Eds.), Sleep medicine. Philadelphia: Hanley & Belfus, Inc.Google Scholar
Rasch, B., Buchel, C., Gais, S., Born, J. (2007). Odor cues during slow-wave sleep prompt declarative memory consolidation. Science, 315, 14261429.CrossRefGoogle ScholarPubMed
Rauchs, G., Bertran, F., Guillery-Girard, B., Desgranges, B., Kerrouche, N., Denise, P., Eustache, F. (2004). Consolidation of strictly episodic memories mainly requires rapid eye movement sleep. Sleep, 27, 395401.CrossRefGoogle ScholarPubMed
Rauchs, G., Schabus, M., Parapatics, S., Bertran, F., Clochon, P., Hot, P., Anderer, P. (2008). Is there a link between sleep changes and memory in Alzheimer's disease? Neuroreport, 19, 11591162.CrossRefGoogle Scholar
Reitan, R.M. (1992). Trail Making Test: Manual for administration and scoring. Tucson, AZ: Reitan Neuropsychology Laboratory.Google Scholar
Rey, A. (1970). L'examen Clinique en Psychologie. Paris: Presses Universitaires de France.Google Scholar
Rudoy, J.D., Voss, J.L., Westerberg, C.E., Paller, K.A. (2009). Strengthening individual memories by reactivating them during sleep. Science, 326, 1079.CrossRefGoogle ScholarPubMed
Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klosch, G., Anderer, P., Zeithofer, J. (2004). Sleep spindles and their significance for declarative memory consolidation. Sleep, 27, 14791485.CrossRefGoogle ScholarPubMed
Schabus, M., Hoedlmoser, K., Pecherstorfer, T., Anderer, P., Gruber, G., Parapatics, S., Zeithofer, J. (2008). Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Research, 1191, 127135.CrossRefGoogle ScholarPubMed
Schmidt, C., Peigneux, P., Muto, V., Schenkel, M., Knoblauch, V., Munch, M., Cajochen, C. (2006). Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. Journal of Neuroscience, 26, 89768982.CrossRefGoogle ScholarPubMed
Sirota, A., Csicsvari, J., Buhl, D., Buzsaki, G. (2003). Communication between neocortex and hippocampus during sleep in rodents. Proceedings of the National Academy of Sciences of the United States of America, 100, 20652069.CrossRefGoogle ScholarPubMed
Stickgold, R. (2005). Sleep-dependent memory consolidation. Nature, 437, 12721278.CrossRefGoogle ScholarPubMed
Stickgold, R. (2009). How do I remember? Let me count the ways. Sleep Medicine Reviews, 13, 305308.CrossRefGoogle ScholarPubMed
Sutherland, R.J., Lehmann, H. (2011). Alternative conceptions of memory consolidation and the role of the hippocampus at the systems level in rodents. Current Opinions in Neurobiology, 21, 446451.CrossRefGoogle ScholarPubMed
Tamaki, M., Matsuoka, T., Nittono, H., Hori, T. (2008). Fast sleep spindle (13–15 hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep, 31, 204211.CrossRefGoogle ScholarPubMed
Van Cauter, E., Leproult, R., Plat, L. (2000). Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. Journal of the American Medical Association, 284, 861868.CrossRefGoogle ScholarPubMed
Wamsley, E.J., Tucker, M.A., Payne, J.D., Stickgold, R. (2010). A brief nap is beneficial for human route-learning: The role of navigation experience and EEG spectral power. Learning and Memory, 17, 332336.CrossRefGoogle ScholarPubMed
Watson, D., Clark, L.A., Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychololgy, 54, 10631070.CrossRefGoogle ScholarPubMed
Wechsler, D. (1981). The Wechsler Adult Intelligence Scale-Revised Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Wechsler, D. (1987). The Wechsler Memory Scale-Revised Manual. New York, NY: Psychological Corporation.Google Scholar
Weiss, S., Rappelsberger, P. (2000). Long-range EEG synchronization during word encoding correlates with successful memory performance. Cognitive Brain Research, 9, 299312.CrossRefGoogle ScholarPubMed
Westerberg, C.E., Lundgren, E.M., Florczak, S.M., Mesulam, M.M., Weintraub, S., Zee, P.C., Paller, K.A. (2010). Sleep influences the severity of memory disruption in amnestic mild cognitive impairment: Results from sleep self-assessment and continuous activity monitoring. Alzheimer's Disease and Associated Disorders, 24, 325333.CrossRefGoogle ScholarPubMed
Wilson, M.A., McNaughton, B.L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science, 265, 676679.CrossRefGoogle ScholarPubMed
Zygierewicz, J., Blinowska, K.J., Durka, P.J., Szelenberger, W., Niemcewicz, S., Androsiuk, W. (1999). High resolution study of sleep spindles. Clinical Neurophysiology, 110, 21362147.CrossRefGoogle ScholarPubMed