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Cited by 606Sleep and Wakefulness ResearchMemory and Neural MechanismsSleep and related disorders

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Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging

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Mander, Bryce A, Rao, Vikram, Lu, Brandon, Saletin, Jared M, Lindquist, John R, Ancoli-Israel, Sonia, Jagust, William, Walker, Matthew P·2013·Nature Neuroscience
DOI 10.1038/nn.3324PMC PMC4286370
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Abstract

Aging has independently been associated with regional brain atrophy, reduced slow wave activity (SWA) during non-rapid eye movement (NREM) sleep and impaired long-term retention of episodic memories. However, whether the interaction of these factors represents a neuropatholgical pathway associated with cognitive decline in later life remains unknown. We found that age-related medial prefrontal cortex (mPFC) gray-matter atrophy was associated with reduced NREM SWA in older adults, the extent to which statistically mediated the impairment of overnight sleep-dependent memory retention. Moreover, this memory impairment was further associated with persistent hippocampal activation and reduced task-related hippocampal-prefrontal cortex functional connectivity, potentially representing impoverished hippocampal-neocortical memory transformation. Together, these data support a model in which age-related mPFC atrophy diminishes SWA, the functional consequence of which is impaired long-term memory. Such findings suggest that sleep disruption in the elderly, mediated by structural brain changes, represents a contributing factor to age-related cognitive decline in later life.

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  1. Buckner, R.L. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 44, 195–208 (2004). · DOI · Paper page
  2. Backhaus, J. et al. Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep. Learn. Mem. 14, 336–341 (2007). · DOI · Paper page
  3. Sowell, E.R. et al. Mapping cortical change across the human life span. Nat. Neurosci. 6, 309–315 (2003). · DOI · Paper page
  4. Dijk, D.J., Beersma, D.G. & van den Hoofdakker, R.H. All night spectral analysis of EEG sleep in young adult and middle-aged male subjects. Neurobiol. Aging 10, 677–682 (1989). · DOI
  5. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010). · DOI · Paper page
  6. Walker, M.P. The role of sleep in cognition and emotion. Ann. NY Acad. Sci. 1156, 168–197 (2009). · DOI
  7. Takashima, A. et al. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc. Natl. Acad. Sci. USA 103, 756–761 (2006). · DOI · Paper page
  8. Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996). · DOI · Paper page
  9. Frankland, P.W. & Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119–130 (2005). · DOI · Paper page
  10. Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997). · DOI · Paper page
  11. Gais, S. et al. Sleep transforms the cerebral trace of declarative memories. Proc. Natl. Acad. Sci. USA 104, 18778–18783 (2007). · DOI · Paper page
  12. Westerberg, C.E. et al. Concurrent impairments in sleep and memory in amnestic mild cognitive impairment. J. Int. Neuropsychol. Soc. 18, 490–500 (2012). · DOI
  13. Vitiello, M.V. Recent advances in understanding sleep and sleep disturbances in older adults: growing older does not mean sleeping poorly. Curr. Dir. Psychol. Sci. 18, 316–320 (2009). · DOI
  14. Marzano, C., Ferrara, M., Curcio, G. & De Gennaro, L. The effects of sleep deprivation in humans: topographical electroencephalogram changes in non-rapid eye movement (NREM) sleep versus REM sleep. J. Sleep Res. 19, 260–268 (2010). · DOI · Paper page
  15. Nadel, L., Campbell, J. & Ryan, L. Autobiographical memory retrieval and hippocampal activation as a function of repetition and the passage of time. Neural Plast. 2007, 90472 (2007). · DOI
  16. Dijk, D.J., Hayes, B. & Czeisler, C.A. Dynamics of electroencephalographic sleep spindles and slow wave activity in men: effect of sleep deprivation. Brain Res. 626, 190–199 (1993). · DOI · Paper page
  17. MacKinnon, D.P., Warsi, G. & Dwyer, J.H. A simulation study of mediated effect measures. Multivariate Behav. Res. 30, 41–62 (1995). · DOI
  18. Mormino, E.C. et al. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 132, 1310–1323 (2009). · DOI · Paper page
  19. Horne, J.A. & Ostberg, O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 4, 97–110 (1976).
  20. Mander, B.A., Santhanam, S., Saletin, J.M. & Walker, M.P. Wake deterioration and sleep restoration of human learning. Curr. Biol. 21, R183–R184 (2011). · DOI · Paper page
  21. Kang, J.E. et al. Amyloid-beta dynamics are regulated by orexin and the sleep-wake cycle. Science 326, 1005–1007 (2009). · DOI · Paper page
  22. Albert, M.S. The ageing brain: normal and abnormal memory. Phil. Trans. R. Soc. Lond. B 352, 1703–1709 (1997). · DOI
  23. Davis, H.P. et al. Acquisition, recall and forgetting of verbal information in long-term memory by young, middle-aged, and elderly individuals. Cortex 39, 1063–1091 (2003). · DOI
  24. Buchmann, A. et al. EEG sleep slow-wave activity as a mirror of cortical maturation. Cereb. Cortex 21, 607–615 (2011). · DOI · Paper page
  25. Naylor, E. et al. Daily social and physical activity increases slow-wave sleep and daytime neuropsychological performance in the elderly. Sleep 23, 87–95 (2000). · DOI
  26. Van Cauter, E. et al. Simultaneous stimulation of slow-wave sleep and growth hormone secretion by gamma-hydroxybutyrate in normal young Men. J. Clin. Invest. 100, 745–753 (1997). · DOI · Paper page
  27. Otten, L.J., Sveen, J. & Quayle, A.H. Distinct patterns of neural activity during memory formation of nonwords versus words. J. Cogn. Neurosci. 19, 1776–1789 (2007). · DOI
  28. Nelson, D.L., McEvoy, C.L. & Schreiber, T.A. The University of South Florida free association, rhyme and word fragment norms. Behav. Res. Methods Instrum. Comput. 36, 402–407 (2004). · DOI
  29. Rush, A.J. et al. The 16-Item quick inventory of depressive symptomatology (QIDS), clinician rating (QIDS-C) and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression. Biol. Psychiatry 54, 573–583 (2003). · DOI · Paper page
  30. Yesavage, J.A. et al. Development and validation of a geriatric depression screening scale: a preliminary report. J. Psychiatr. Res. 17, 37–49 (1982). · DOI · Paper page
  31. Reitan, R.M. Validity of the trail-making test as an indication of organic brain damage. Percept. Mot. Skills 8, 271–276 (1958). · DOI
  32. Zec, R.F. The stroop color-word test: a paradigm for procedural learning. Arch. Clin. Neuropsychol. 1, 274–275 (1986). · DOI
  33. Young, T., Peppard, P.E. & Gottlieb, D.J. Epidemiology of obstructive sleep apnea: a population health perspective. Am. J. Respir. Crit. Care Med. 165, 1217–1239 (2002). · DOI · Paper page
  34. Münch, M., Silva, E.J., Ronda, J.M., Czeisler, C.A. & Duffy, J.F. EEG sleep spectra in older adults across all circadian phases during NREM sleep. Sleep 33, 389–401 (2010). · DOI · Paper page
  35. Cohen, D.A. & Robertson, E.M. Preventing interference between different memory tasks. Nat. Neurosci. 14, 953–955 (2011). · DOI
  36. Bollinger, J., Rubens, M.T., Masangkay, E., Kalkstein, J. & Gazzaley, A. An expectation-based memory deficit in aging. Neuropsychologia 49, 1466–1475 (2011). · DOI
  37. Buckner, R.L. et al. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23, 724–738 (2004). · DOI
  38. Daselaar, S.M., Veltman, D.J., Rombouts, S.A., Raaijmakers, J.G. & Jonker, C. Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. Brain 126, 43–56 (2003). · DOI
  39. Spaniol, J. et al. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 47, 1765–1779 (2009). · DOI · Paper page
  40. Lieberman, M.D. & Cunningham, W.A. Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc. Cogn. Affect. Neurosci. 4, 423–428 (2009). · DOI · Paper page
  41. Friston, K.J. et al. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6, 218–229 (1997). · DOI · Paper page
  42. Gitelman, D.R., Penny, W.D., Ashburner, J. & Friston, K.J. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 19, 200–207 (2003). · DOI
  43. Nieuwenhuis, I.L. & Takashima, A. The role of the ventromedial prefrontal cortex in memory consolidation. Behav. Brain Res. 218, 325–334 (2011). · DOI
  44. Brett, M., Anton, J.L., Valabregue, R. & Poline, J.B. Region of interest analysis using an SPM toolbox [abstract]. in 8th Int. Conf. Funct. Mapp. Hum. Brain 16, 2 (NeuroImage, Sendai, Japan, 2002).
  45. Ashburner, J. & Friston, K.J. Voxel-based morphometry–the methods. Neuroimage 11, 805–821 (2000). · DOI · Paper page
  46. Mak, H.K. et al. Efficacy of voxel-based morphometry with DARTEL and standard registration as imaging biomarkers in Alzheimer's disease patients and cognitively normal older adults at 3.0 Tesla MR imaging. J. Alzheimers Dis. 23, 655–664 (2011). · DOI
  47. Rajapakse, J.C., Giedd, J.N. & Rapoport, J.L. Statistical approach to segmentation of single-channel cerebral MR images. IEEE Trans. Med. Imaging 16, 176–186 (1997). · DOI
  48. Brodmann, K. Brodmann's Localisation in the Cerebral Cortex: the Principles of Comparative Localisation in the Cerebral Cortex based on Cytoarchitectonics (Springer, New York, 1909).
  49. Gasser, T., Bacher, P. & Steinberg, H. Test-retest reliability of spectral parameters of the EEG. Electroencephalogr. Clin. Neurophysiol. 60, 312–319 (1985). · DOI
  50. Mander, B.A. et al. EEG measures index neural and cognitive recovery from sleep deprivation. J. Neurosci. 30, 2686–2693 (2010). · DOI

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Metadata

Authors
Mander, B. A., Rao, V., Lu, B., Saletin, J. M., Lindquist, J. R., Ancoli-Israel, S., Jagust, W., & Walker, M. P.
Affiliations
  • University of California, Berkeley (US)
  • California Pacific Medical Center (US)
  • Lawrence Berkeley National Laboratory (US)
Corresponding author
  • Mander, Bryce A
  • Walker, Matthew P
ORCID
Venue
Nature Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2013-01-27
Volume
16
Issue
3
Pages
357-364
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
DOI
10.1038/nn.3324
PMC
PMC4286370
OpenAlex
W2030353060
Cited by
606
References
7
Citations by year
2026: 43 · 2025: 53 · 2024: 43 · 2023: 46 · 2022: 47 · 2021: 55 · 2020: 60 · 2019: 60 · 2018: 37 · 2017: 40 · 2016: 42 · 2015: 32 · 2014: 31 · 2013: 16
FWCI
18.00
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders
  • National Institutes of Health
  • National Institute on Aging (R01AG008415, F32AG039170, R01AG031164, R01AG034570)
  • National Institute of Mental Health (R01MH093537)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
Keywords
gray matter atrophy, slow-wave sleep, hippocampal-dependent memory, memory consolidation, aging, age-related cognitive decline, hippocampal activation, sleep disruption
MeSH terms
Adolescent, Aged, Aged, 80 and over, Aging, Atrophy, Brain Mapping, Female, Hippocampus, Humans, Image Processing, Computer-Assisted, Male, Memory, Neuropsychological Tests, Organ Size, Sleep, Polysomnography, Prefrontal Cortex, Young Adult, Brain Waves, Memory, Episodic

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