Effects of aging on slow-wave sleep dynamics and human spatial navigational memory consolidation

Neurobiology of Aging

Volumn 42, Issue , 2016, Pages 142-149

  Varga, Andrew W ^a,b   Ducca, Emma L ^a   Kishi, Akifumi ^c   Fischer, Esther ^a   Parekh, Ankit ^d   Koushyk, Viachaslau ^a   Yau, Po Lai ^a   Gumb, Tyler ^a   Leibert, David P ^a   Wohlleber, Margaret E ^a   Burschtin, Omar E ^a   Convit, Antonio ^a   Rapoport, David M ^a   Osorio, Ricardo S ^a   Ayappa, Indu ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d POLYTECHNIC UNIVERSITY   (United States)

Author keywords

Brain imaging; Maze; Prefrontal cortex; Psychomotor vigilance; Sleep fragmentation

Indexed keywords

ADULT; AGED; AGING; ALERTNESS; ARTICLE; BRAIN SIZE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; NEUROIMAGING; NONREM SLEEP; NORMAL HUMAN; POLYSOMNOGRAPHY; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; REM SLEEP; SLEEP QUALITY; SLOW WAVE SLEEP; SPATIAL MEMORY; SPATIAL ORIENTATION; ADOLESCENT; BRAIN; DIAGNOSTIC IMAGING; MAZE TEST; MEMORY; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOLOGY; SLEEP; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; AGED; AGED, 80 AND OVER; AGING; BRAIN; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MAZE LEARNING; MEMORY; MIDDLE AGED; PSYCHOMOTOR PERFORMANCE; SLEEP; SPATIAL NAVIGATION; YOUNG ADULT;

EID: 84962828395     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.03.008     Document Type: Article

References (42)

1. Backhaus J., Born J., Hoeckesfeld R., Fokuhl S., Hohagen F., Junghanns K. Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep. Learn Mem. 2007, 14:336-341.
2. Bjorness T.E., Riley B.T., Tysor M.K., Poe G.R. REM restriction persistently alters strategy used to solve a spatial task. Learn Mem. 2005, 12:352-359.
3. Bohbot V.D., McKenzie S., Konishi K., Fouquet C., Kurdi V., Schachar R., Boivin M., Robaey P. Virtual navigation strategies from childhood to senescence: evidence for changes across the life span. Front. Aging Neurosci. 2012, 4:28.
4. Brown R.M., Robertson E.M., Press D.Z. Sequence skill acquisition and off-line learning in normal aging. PLoS One 2009, 4:e6683.
5. Cherdieu M., Reynaud E., Uhlrich J., Versace R., Mazza S. Does age worsen sleep-dependent memory consolidation?. J. Sleep Res. 2014, 23:53-60.
6. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
7. Dinges D.F., Pack F., Williams K., Gillen K.A., Powell J.W., Ott G.E., Aptowicz C., Pack A.I. Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5 hours per night. Sleep 1997, 20:267-277.
8. Ferrara M., Iaria G., Tempesta D., Curcio G., Moroni F., Marzano C., De Gennaro L., Pacitti C. Sleep to find your way: the role of sleep in the consolidation of memory for navigation in humans. Hippocampus 2008, 18:844-851.
9. Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009, 12:1222-1223.
10. Glodzik L., Rusinek H., Brys M., Tsui W.H., Switalski R., Mosconi L., Mistur R., Pirraglia E., de Santi S., Li Y., Goldowsky A., de Leon M.J. Framingham cardiovascular risk profile correlates with impaired hippocampal and cortical vasoreactivity to hypercapnia. J. Cereb. Blood Flow Metab. 2011, 31:671-679.
11. Gudberg C., Wulff K., Johansen-Berg H. Sleep-dependent motor memory consolidation in older adults depends on task demands. Neurobiol. Aging 2015, 36:1409-1416.
12. Iber C., Ancoli-Israel S., Chesson A.L., Quan S.F. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Technical Specifications 2007, American Academy of Sleep Medicine, Westchester, IL. first ed.
13. Kishi A., Natelson B.H., Togo F., Struzik Z.R., Rapoport D.M., Yamamoto Y. Sleep-stage dynamics in patients with chronic fatigue syndrome with or without fibromyalgia. Sleep 2011, 34:1551-1560.
14. Klerman E.B., Wang W., Duffy J.F., Dijk D.J., Czeisler C.A., Kronauer R.E. Survival analysis indicates that age-related decline in sleep continuity occurs exclusively during NREM sleep. Neurobiol. Aging 2013, 34:309-318.
15. Konishi K., Etchamendy N., Roy S., Marighetto A., Rajah N., Bohbot V.D. Decreased functional magnetic resonance imaging activity in the hippocampus in favor of the caudate nucleus in older adults tested in a virtual navigation task. Hippocampus 2013, 23:1005-1014.
16. Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001, 29:145-156.
17. Mander B.A., Rao V., Lu B., Saletin J.M., Lindquist J.R., Ancoli-Israel S., Jagust W., Walker M.P. Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat. Neurosci. 2013, 16:357-364.
18. Marshall L., Helgadottir H., Molle M., Born J. Boosting slow oscillations during sleep potentiates memory. Nature 2006, 444:610-613.
19. Massimini M., Huber R., Ferrarelli F., Hill S., Tononi G. The sleep slow oscillation as a traveling wave. J. Neurosci. 2004, 24:6862-6870.
20. Moffat S.D., Zonderman A.B., Resnick S.M. Age differences in spatial memory in a virtual environment navigation task. Neurobiol. Aging 2001, 22:787-796.
21. Murphy M., Riedner B.A., Huber R., Massimini M., Ferrarelli F., Tononi G. Source modeling sleep slow waves. Proc. Natl. Acad. Sci. U S A 2009, 106:1608-1613.
22. Ngo H.V., Martinetz T., Born J., Molle M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 2013, 78:545-553.
23. Nguyen N.D., Tucker M.A., Stickgold R., Wamsley E.J. Overnight sleep enhances hippocampus-dependent aspects of spatial memory. Sleep 2013, 36:1051-1057.
24. Norman R.G., Scott M.A., Ayappa I., Walsleben J.A., Rapoport D.M. Sleep continuity measured by survival curve analysis. Sleep 2006, 29:1625-1631.
25. Peigneux P., Laureys S., Fuchs S., Collette F., Perrin F., Reggers J., Phillips C., Degueldre C., Del Fiore G., Aerts J., Luxen A., Maquet P. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron 2004, 44:535-545.
26. Reuter M., Schmansky N.J., Rosas H.D., Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 2012, 61:1402-1418.
27. Ringli M., Huber R. Developmental aspects of sleep slow waves: linking sleep, brain maturation and behavior. Prog. Brain Res. 2011, 193:63-82.
28. Salat D.H., Kaye J.A., Janowsky J.S. Greater orbital prefrontal volume selectively predicts worse working memory performance in older adults. Cereb. Cortex 2002, 12:494-505.
29. Scullin M.K. Sleep, memory, and aging: the link between slow-wave sleep and episodic memory changes from younger to older adults. Psychol. Aging 2013, 28:105-114.
30. Siapas A.G., Wilson M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 1998, 21:1123-1128.
31. Sirota A., Csicsvari J., Buhl D., Buzsaki G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U S A 2003, 100:2065-2069.
32. Smith C., Rose G.M. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol. Behav. 1996, 59:93-97.
33. Spencer R.M., Gouw A.M., Ivry R.B. Age-related decline of sleep-dependent consolidation. Learn Mem. 2007, 14:480-484.
34. Stickgold R., Walker M.P. Sleep-dependent memory triage: evolving generalization through selective processing. Nat. Neurosci. 2013, 16:139-145.
35. Van Der Werf Y.D., Altena E., Vis J.C., Koene T., Van Someren E.J. Reduction of nocturnal slow-wave activity affects daytime vigilance lapses and memory encoding but not reaction time or implicit learning. Prog. Brain Res. 2011, 193:245-255.
36. Varga A.W., Kishi A., Mantua J., Lim J., Koushyk V., Leibert D.P., Osorio R.S., Rapoport D.M., Ayappa I. Apnea-induced rapid eye movement sleep disruption impairs human spatial navigational memory. J. Neurosci. 2014, 34:14571-14577.
37. Wamsley E.J., Tucker M.A., Payne J.D., Stickgold R. A brief nap is beneficial for human route-learning: the role of navigation experience and EEG spectral power. Learn Mem. 2010, 17:332-336.
38. Ware J.C., McBrayer R.H., Scott J.A. Influence of sex and age on duration and frequency of sleep apnea events. Sleep 2000, 23:165-170.
39. Westerberg C.E., Florczak S.M., Weintraub S., Mesulam M.M., Marshall L., Zee P.C., Paller K.A. Memory improvement via slow-oscillatory stimulation during sleep in older adults. Neurobiol. Aging 2015, 36:2577-2586.
40. Wilson J.K., Baran B., Pace-Schott E.F., Ivry R.B., Spencer R.M. Sleep modulates word-pair learning but not motor sequence learning in healthy older adults. Neurobiol. Aging 2012, 33:991-1000.
41. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
42. Yau P.L., Kang E.H., Javier D.C., Convit A. Preliminary evidence of cognitive and brain abnormalities in uncomplicated adolescent obesity. Obesity (Silver Spring) 2014, 22:1865-1871.