Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation

Neurobiology of Aging

Volumn 49, Issue , 2017, Pages 154-164

  Fogel, Stuart ^a,b,c   Vien, Catherine ^a,b   Karni, Avi ^d   Benali, Habib ^a,e   Carrier, Julie ^a,b,f   Doyon, Julien ^a,b  

^a CENTRE DE RECHERCHE   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

^d UNIVERSITY OF HAIFA   (Israel)

^e INSERM   (France)

^f HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

Author keywords

Age; Cerebellum; Consolidation; Hippocampus; Learning; Memory; Motor sequence learning; Motor skills; Procedural memory; Sleep; Spindle

Indexed keywords

ADULT; AGE; AGED; AMNESIA; ARTICLE; CEREBELLUM; CINGULATE GYRUS; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; MOTOR PERFORMANCE; NEUROIMAGING; NONREM SLEEP; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL CORTEX; POLYSOMNOGRAPHY; PRIORITY JOURNAL; REM SLEEP; SLEEP QUALITY; SLEEP SPINDLE; SLEEP TIME; SLOW WAVE SLEEP; TASK PERFORMANCE; WAKEFULNESS; AGING; DIAGNOSTIC IMAGING; LEARNING; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; SLEEP; SLEEP STAGE; YOUNG ADULT;

BIOLOGICAL MARKER;

ADULT; AGED; AGING; BIOMARKERS; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MEMORY CONSOLIDATION; MIDDLE AGED; MOTOR SKILLS; NEUROIMAGING; PSYCHOMOTOR PERFORMANCE; SLEEP; SLEEP STAGES; YOUNG ADULT;

EID: 84994804560     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.10.009     Document Type: Article

References (136)

1. Albouy, G., Fogel, S., King, B.R., Laventure, S., Benali, H., Karni, A., Carrier, J., Robertson, E.M., Doyon, J., Maintaining vs. enhancing motor sequence memories: respective roles of striatal and hippocampal systems. Neuroimage 108 (2015), 423–434.
2. Albouy, G., Fogel, S., Pottiez, H., Nguyen, V.A., Ray, L., Lungu, O., Carrier, J., Robertson, E., Doyon, J., Daytime sleep enhances consolidation of the spatial but not motoric representation of motor sequence memory. PLoS One, 8, 2013, e52805.
3. Albouy, G., King, B.R., Maquet, P., Doyon, J., Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus 23 (2013), 985–1004.
4. Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T.T., Darsaud, A., Ruby, P., Luppi, P.-H., Degueldre, C., Peigneux, P., Luxen, A., Maquet, P., Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 58 (2008), 261–272.
5. Albouy, G., Sterpenich, V., Vandewalle, G., Darsaud, A., Gais, S., Rauchs, G., Desseilles, M., Boly, M., Dang-Vu, T.T., Balteau, E., Degueldre, C., Phillips, C., Luxen, A., Maquet, P., Interaction between hippocampal and striatal systems predicts subsequent consolidation of motor sequence memory. PLoS One, 8, 2013, e59490.
6. Andersson, J., Jenkinson, M., Smith, S., Non-linear Registration, Aka Spatial Normalisation. FMRIB Technical Report TR07JA2., 2007, Oxford, United Kingdom, FMRIB Centre.
7. Barakat, M., Carrier, J., Debas, K., Lungu, O., Fogel, S., Vandewalle, G., Hoge, R.D., Bellec, P., Karni, A., Ungerleider, L.G., Benali, H., Doyon, J., Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum. Brain Mapp. 34 (2012), 2918–2928.
8. Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., Martin, N., Lafortune, M., Karni, A., Ungerleider, L.G., Benali, H., Carrier, J., Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. 217 (2011), 117–121.
9. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T., Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat. Neurosci. 2 (1999), 168–174.
10. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T., Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. J. Neurophysiol. 84 (2000), 1076–1087.
11. Beck, A.T., Epstein, N., Brown, G., Steer, R.A., An inventory for measuring clinical anxiety: psychometric properties. J. Consult. Clin. Psychol. 56 (1988), 893–897.
12. Beck, A.T., Rial, W.Y., Rickels, K., Short form of depression inventory: cross-validation. Psychol. Rep. 34 (1974), 1184–1186.
13. Bergmann, T.O., Mölle, M., Marshall, L., Kaya-Yildiz, L., Born, J., Roman Siebner, H., A local signature of LTP- and LTD-like plasticity in human NREM sleep. Eur. J. Neurosci. 27 (2008), 2241–2249.
14. Bixler, E.O., Kales, A., Jacoby, J.A., Soldatos, C.R., Vela-Bueno, A., Nocturnal sleep and wakefulness: effects of age and sex in normal sleepers. Int. J. Neurosci. 23 (1984), 33–42.
15. Bonjean, M., Baker, T., Bazhenov, M., Cash, S., Halgren, E., Sejnowski, T., Interactions between core and matrix thalamocortical projections in human sleep spindle synchronization. J. Neurosci. 32 (2012), 5250–5263.
16. Bonjean, M., Baker, T., Lemieux, M., Timofeev, I., Sejnowski, T., Bazhenov, M., Corticothalamic feedback controls sleep spindle duration in vivo. J. Neurosci. 31 (2011), 9124–9134.
17. Bowersox, S.S., Kaitin, K.I., Dement, W.C., EEG spindle activity as a function of age: relationship to sleep continuity. Brain Res. 334 (1985), 303–308.
18. Brown, R.M., Robertson, E., Press, D.Z., Sequence skill acquisition and off-line learning in normal aging. PLoS One, 4, 2009, e6683.
19. Buysse, D.J., Browman, K.E., Monk, T.H., Reynolds, C.F., Fasiczka, A.L., Kupfer, D.J., Napping and 24-hour sleep/wake patterns in healthy elderly and young adults. J. Am. Geriatr. Soc. 40 (1992), 779–786.
20. Cajochen, C., Münch, M., Knoblauch, V., Blatter, K., Wirz-Justice, A., Age-related changes in the circadian and homeostatic regulation of human sleep. Chronobiol. Int. 23 (2006), 461–474.
21. Caporro, M., Haneef, Z., Yeh, H.J., Lenartowicz, A., Buttinelli, C., Parvizi, J., Stern, J.M., Functional MRI of sleep spindles and K-complexes. Clin. Neurophysiol. 123 (2012), 303–309.
22. Carrier, J., Land, S., Buysse, D.J., Kupfer, D.J., Monk, T.H., The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20-60 years old). Psychophysiology 38 (2001), 232–242.
23. Carrier, J., Viens, I., Poirier, G., Robillard, R., Lafortune, M., Vandewalle, G., Martin, N., Barakat, M., Paquet, J., Filipini, D., Sleep slow wave changes during the middle years of life. Eur. J. Neurosci. 33 (2011), 758–766.
24. Carskadon, M.A., Dement, W.C., Normal human sleep: an overview. Kryger, M.H., Roth, T., Dement, W.C., (eds.) Principles and Practice of Sleep Medicine, 2011, St. Louis, Missouri, Saunders/Elsevier, 16–26.
25. Cockrell, J.R., Folstein, M.F., Mini-mental state examination (MMSE). Psychopharmacol. Bull. 24 (1988), 689–692.
26. Contreras, D., Steriade, M., Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J. Physiol. 490:Pt 1 (1996), 159–179.
27. Cote, K.A., Epps, T.M., Campbell, K., The role of the spindle in human information processing of high-intensity stimuli during sleep. J. Sleep Res. 9 (2000), 19–26.
28. Crowley, K., Trinder, J., Colrain, I.M., Evoked K-complex generation: the impact of sleep spindles and age. Clin. Neurophysiol. 115 (2004), 471–476.
29. Crowley, K., Trinder, J., Kim, Y., Carrington, M., Colrain, I.M., The effects of normal aging on sleep spindle and K-complex production. Clin. Neurophysiol. 113 (2002), 1615–1622.
30. Dang-Vu, T.T., McKinney, S.M., Buxton, O.M., Solet, J.M., Ellenbogen, J.M., Spontaneous brain rhythms predict sleep stability in the face of noise. Curr. Biol. 20 (2010), R626–R627.
31. Darchia, N., Campbell, I.G., Feinberg, I., Rapid eye movement density is reduced in the normal elderly. Sleep 26 (2003), 973–977.
32. De Gennaro, L., Ferrara, M., Sleep spindles: an overview. Sleep Med. Rev. 7 (2003), 423–440.
33. De Gennaro, L., Ferrara, M., Bertini, M., Topographical distribution of spindles: variations between and within nrem sleep cycles. Sleep Res. Online 3 (2000), 155–160.
34. De Gennaro, L., Ferrara, M., Vecchio, F., Curcio, G., Bertini, M., An electroencephalographic fingerprint of human sleep. Neuroimage 26 (2005), 114–122.
35. Debas, K., Carrier, J., Orban, P., Barakat, M., Lungu, O., Vandewalle, G., Hadj Tahar, A., Bellec, P., Karni, A., Ungerleider, L.G., Benali, H., Doyon, J., Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 17839–17844.
36. Dehghani, N., Cash, S., Halgren, E., Topographical frequency dynamics within EEG and MEG sleep spindles. Clin. Neurophysiol. 122 (2011), 229–235.
37. Dinges, D.F., Powell, J.W., Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav. Res. Methods 17 (1985), 652–655.
38. Doran, S.M., The dynamic topography of individual sleep spindles. Sleep Res. Online 5 (2003), 133–139.
39. Douaud, G., Smith, S., Jenkinson, M., Behrens, T., Johansen-Berg, H., Vickers, J., James, S., Voets, N., Watkins, K., Matthews, P.M., James, A., Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 130 (2007), 2375–2386.
40. Doyon, J., Benali, H., Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 15 (2005), 161–167.
41. Doyon, J., Penhune, V.B., Ungerleider, L.G., Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41 (2003), 252–262.
42. Doyon, J., Ungerleider, L.G., Functional anatomy of motor skill learning. Neuropsychol. Mem. 3 (2002), 225–238.
43. Feinberg, I., Changes in sleep cycle patterns with age. J. Psychiatr. Res. 10 (1974), 283–306.
44. Feinberg, I., Koresko, R.L., Heller, N., EEG sleep patterns as a function of normal and pathological aging in man. J. Psychiatr. Res. 5 (1967), 107–144.
45. Ferrarelli, F., Peterson, M.J., Sarasso, S., Riedner, B.A., Murphy, M.J., Benca, R.M., Bria, P., Kalin, N.H., Tononi, G., Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am. J. Psychiatry 167 (2010), 1339–1348.
46. Fjell, A.M., Walhovd, K.B., Structural brain changes in aging: courses, causes and cognitive consequences. Rev. Neurosci. 21 (2010), 187–221.
47. Floyd, J.A., Janisse, J.J., Jenuwine, E.S., Ager, J.W., Changes in REM-sleep percentage over the adult lifespan. Sleep 30 (2007), 829–836.
48. Fogel, S., Albouy, G., Vien, C., Popovicci, R., King, B.R., Hoge, R.D., Jbabdi, S., Benali, H., Karni, A., Maquet, P., Carrier, J., Doyon, J., fMRI and sleep correlates of the age-related impairment in motor memory consolidation. Hum. Brain Mapp. 35 (2014), 3625–3645.
49. Fogel, S., Martin, N., Lafortune, M., Barakat, M., Debas, K., Laventure, S., Latreille, V., Gagnon, J.F., Doyon, J., Carrier, J., Nrem sleep oscillations and brain plasticity in aging. Front. Neurol., 3, 2012, 176.
50. Fogel, S., Ray, L.B., Binnie, L., Owen, A.M., How to become an expert: a new perspective on the role of sleep in the mastery of procedural skills. Neurobiol. Learn. Mem. 125 (2015), 236–248.
51. Fogel, S., Smith, C., The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci. Biobehav. Rev. 35 (2011), 1154–1165.
52. Fogel, S., Smith, C., Cote, K.A., Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav. Brain Res. 180 (2007), 48–61.
53. Fogel, S., Smith, C.T., Learning-dependent changes in sleep spindles and Stage 2 sleep. J. Sleep Res. 15 (2006), 250–255.
54. Friston, K., Penny, W., Glaser, D.E., Conjunction revisited. Neuroimage 25 (2005), 661–667.
55. Gaser, C., Schlaug, G., Gray matter differences between musicians and nonmusicians. Ann. N. Y. Acad. Sci. 999 (2003), 514–517.
56. Gaudreau, H., Carrier, J., Montplaisir, J., Age-related modifications of NREM sleep EEG: from childhood to middle age. J. Sleep Res. 10 (2001), 165–172.
57. Good, C.D., Johnsrude, I.S., Ashburner, J., Henson, R.N., Friston, K.J., Frackowiak, R.S., A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14 (2001), 21–36.
58. Groussard, M., Viader, F., Landeau, B., Desgranges, B., Eustache, F., Platel, H., The effects of musical practice on structural plasticity: the dynamics of grey matter changes. Brain Cogn. 90 (2014), 174–180.
59. Gryga, M., Taubert, M., Dukart, J., Vollmann, H., Conde, V., Sehm, B., Villringer, A., Ragert, P., Bidirectional gray matter changes after complex motor skill learning. Front. Syst. Neurosci., 6, 2012, 37.
60. Guazzelli, M., Feinberg, I., Aminoff, M., Fein, G., Floyd, T.C., Maggini, C., Guazzelli, N., Feinberg, I., Aminoff, M., Fein, G., Floyd, T.C., Maggini, C., Sleep spindles in normal elderly: comparison with young adult patterns and relation to nocturnal awakening, cognitive function and brain atrophy. Electroencephalogr. Clin. Neurophysiol. 63 (1986), 526–539.
61. Gunning-Dixon, F.M., Head, D., McQuain, J., Acker, J.D., Raz, N., Differential aging of the human striatum: a prospective MR imaging study. AJNR Am. J. Neuroradiol. 19 (1998), 1501–1507.
62. Hamzei, F., Glauche, V., Schwarzwald, R., May, A., Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction. Neuroimage 59 (2012), 3364–3372.
63. Horne, J.A., Ostberg, O., A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 4 (1976), 97–110.
64. Howard, J.H., Howard, D.V., Aging mind and brain: is implicit learning spared in healthy aging?. Front. Psychol., 4, 2013, 817.
65. Huupponen, E., Himanen, S.L., Varri, A., Hasan, J., Lehtokangas, M., Saarinen, J., A study on gender and age differences in sleep spindles. Neuropsychobiology 45 (2002), 99–105.
66. 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.
67. Jenkinson, M., Beckmann, C.F., Behrens, T.E.J., Woolrich, M.W., Smith, S.M., FSL. Neuroimage 62 (2012), 782–790.
68. Jobert, M., Poiseau, E., Jahnig, P., Schulz, H., Kubicki, S., Topographical analysis of sleep spindle activity. Neuropsychobiology 26 (1992), 210–217.
69. Karni, A., Meyer, G., Jezzard, P., Adams, M.M., Turner, R., Ungerleider, L.G., Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377 (1995), 155–158.
70. Kennedy, K.M., Raz, N., Age, sex and regional brain volumes predict perceptual-motor skill acquisition. Cortex 41 (2005), 560–569.
71. King, B.R., Fogel, S., Albouy, G., Doyon, J., Neural correlates of the age-related changes in motor sequence learning and motor adaptation in older adults. Front. Hum. Neurosci., 7, 2013, 142.
72. Knoblauch, V., Münch, M., Blatter, K., Martens, W.L.J., Schröder, C., Schnitzler, C., Wirz-Justice, A., Cajochen, C., Age-related changes in the circadian modulation of sleep-spindle frequency during nap sleep. Sleep 28 (2005), 1093–1101.
73. Lafortune, M., Gagnon, J.F., Martin, N., Latreille, V., Dubé, J., Bouchard, M., Bastien, C., Carrier, J., Sleep spindles and rapid eye movement sleep as predictors of next morning cognitive performance in healthy middle-aged and older participants. J. Sleep Res. 23 (2014), 159–167.
74. Landolt, H., Borbely, A.A., Age-dependent changes in sleep EEG topography. Clin. Neurophysiol. 112 (2001), 369–377.
75. Landolt, H., Dijk, D.J., Achermann, P., Borbely, A.A., Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men. Brain Res. 738 (1996), 205–212.
76. Leclercq, Y., Schrouff, J., Noirhomme, Q., Maquet, P., Phillips, C., fMRI artefact rejection and sleep scoring toolbox. Comput. Intell. Neurosci., 2011, 2011, 598206.
77. MacLean, A.W., Fekken, G.C., Saskin, P., Knowles, J.B., Psychometric evaluation of the Stanford Sleepiness Scale. J. Sleep Res. 1 (1992), 35–39.
78. Mander, B.A., Marks, S.M., Vogel, J.W., Rao, V., Lu, B., Saletin, J.M., Ancoli-Israel, S., Jagust, W.J., Walker, M.P., β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat. Neurosci. 18 (2015), 1051–1057.
79. Mander, B.A., Rao, V., Lu, B., Saletin, J.M., Ancoli-Israel, S., Jagust, W., Walker, M., Impaired prefrontal sleep spindle regulation of hippocampal-dependent learning in older adults. Cereb. Cortex 24 (2014), 3301–3309.
80. Mander, B.A., Rao, V., Lu, B., Saletin, J.M., Lindquist, J.R., Ancoli-Israel, S., Jagust, W., Walker, M., Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat. Neurosci. 16 (2013), 357–364.
81. Martin, N., Lafortune, M., Godbout, J., Barakat, M., Robillard, R., Poirier, G., Bastien, C., Carrier, J., Topography of age-related changes in sleep spindles. Neurobiol. Aging 34 (2013), 468–476.
82. Milner, C.E., Fogel, S., Cote, K.A., Habitual napping moderates motor performance improvements following a short daytime nap. Biol. Psychiatry 73 (2006), 141–156.
83. Nemeth, D., Janacsek, K., Londe, Z., Ullman, M.T., Howard, D.V., Howard, J.H., Sleep has no critical role in implicit motor sequence learning in young and old adults. Exp. Brain Res. 201 (2010), 351–358.
84. Nichols, T.E., Holmes, A.P., Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 15 (2002), 1–25.
85. Nicolas, A., Petit, D., Rompré, S., Montplaisir, J., Sleep spindle characteristics in healthy subjects of different age groups. Clin. Neurophysiol. 112 (2001), 521–527.
86. Nielsen, T., O'Reilly, C., Carr, M., Dumel, G., Godin, I., Solomonova, E., Lara-Carrasco, J., Blanchette-Carrière, C., Paquette, T., Overnight improvements in two REM sleep-sensitive tasks are associated with both REM and NREM sleep changes, sleep spindle features, and awakenings for dream recall. Neurobiol. Learn Mem. 122 (2015), 88–97.
87. Nishida, M., Walker, M., Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One, 2, 2007, e341.
88. Ohayon, M.M., Carskadon, M.A., Guilleminault, C., Vitiello, M.V., Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. Sleep 27 (2004), 1255–1273.
89. Oldfield, R.C., The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 (1971), 97–113.
90. Pace-Schott, E.F., Spencer, R.M.C., Age-related changes in the cognitive function of sleep. Prog. Brain Res. 191 (2011), 75–89.
91. Peters, K.R., Ray, L., Fogel, S., Smith, V., Smith, C., Age differences in the variability and distribution of sleep spindle and rapid eye movement densities. PLoS One, 9, 2014, e91047.
92. Peters, K.R., Ray, L., Smith, V., Smith, C., Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. J. Sleep Res. 17 (2008), 23–33.
93. Peters, K.R., Smith, V., Smith, C., Changes in sleep architecture following motor learning depend on initial skill level. J. Cogn. Neurosci. 19 (2007), 817–829.
94. Pivik, R.T., Joncas, S., Busby, K.A., Sleep spindles and arousal: the effects of age and sensory stimulation. Sleep Res. Online 2 (1999), 89–100.
95. Principe, J.C., Smith, J.R., Sleep spindle characteristics as a function of age. Sleep 5 (1982), 73–84.
96. Ramanand, P., Bruce, M.C., Bruce, E.N., Mutual information analysis of EEG signals indicates age-related changes in cortical interdependence during sleep in middle-aged versus elderly women. J. Clin. Neurophysiol. 27 (2010), 274–284.
97. Ramanathan, D.S., Gulati, T., Ganguly, K., Sleep-dependent reactivation of ensembles in motor cortex promotes skill consolidation. PLoS Biol., 13, 2015, e1002263.
98. Rasch, B., Born, J., About sleep's role in memory. Physiol. Rev. 93 (2013), 681–766.
99. Ray, L.B., Sockeel, S., Soon, M., Bore, A., Myhr, A., Stojanoski, B., Cusack, R., Owen, A.M., Doyon, J., Fogel, S., Expert and crowd-sourced validation of an individualized sleep spindle detection method employing complex demodulation and individualized normalization. Front. Hum. Neurosci., 9, 2015, 507.
100. Raz, N., Daugherty, A.M., Bender, A.R., Dahle, C.L., Land, S., Volume of the hippocampal subfields in healthy adults: differential associations with age and a pro-inflammatory genetic variant. Brain Struct. Funct. 220 (2015), 2663–2674.
101. Raz, N., Lindenberger, U., Rodrigue, K.M., Kennedy, K.M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., Acker, J.D., Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 15 (2005), 1676–1689.
102. Redline, S., Gottlieb, D.J., Kapur, V., Kirchner, H.L., Quan, S.F., Newman, A., The effects of age, sex, ethnicity, and sleep-disordered breathing on sleep architecture. Arch. Intern. Med. 164 (2004), 406–418.
103. Rieckmann, A., Fischer, H., Bäckman, L., Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: relations to performance. Neuroimage 50 (2010), 1303–1312.
104. Rosanova, M., Ulrich, D., Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 25 (2005), 9398–9405.
105. Saletin, J.M., van der Helm, E., Walker, M.P., Structural brain correlates of human sleep oscillations. Neuroimage 83 (2013), 658–668.
106. Sargolzaei, S., Sargolzaei, A., Cabrerizo, M., Chen, G., Goryawala, M., Noei, S., Zhou, Q., Duara, R., Barker, W., Adjouadi, M., A practical guideline for intracranial volume estimation in patients with Alzheimer's disease. BMC Bioinformatics, 16, 2015, S8.
107. Schabus, M., Dang-Vu, T.T., Albouy, G., Balteau, E., Boly, M., Carrier, J., Darsaud, A., Degueldre, C., Desseilles, M., Gais, S., Phillips, C., Rauchs, G., Schnakers, C., Sterpenich, V., Vandewalle, G., Luxen, A., Maquet, P., Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 13164–13169.
108. Schabus, M., Dang-Vu, T.T., Heib, D.P.J., Boly, M., Desseilles, M., Vandewalle, G., Schmidt, C., Albouy, G., Darsaud, A., Gais, S., Degueldre, C., Balteau, E., Phillips, C., Luxen, A., Maquet, P., The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front Neurol., 3, 2012, 40.
109. Silber, M.H., Ancoli-Israel, S., Bonnet, M.H., Chokroverty, S., Grigg-Damberger, M.M., Hirshkowitz, M., Kapen, S., Keenan, S., Kryger, M.H., Penzel, T., The visual scoring of sleep in adults. J. Clin. Sleep Med. 3 (2007), 121–131.
110. Simon, J.R., Howard, J.H., Howard, D.V., Age differences in implicit learning of probabilistic unstructured sequences. J. Gerontol. B. Psychol. Sci. Soc. Sci. 66 (2011), 32–38.
111. Smith, C., Smith, D., Ingestion of ethanol just prior to sleep onset impairs memory for procedural but not declarative tasks. Sleep 26 (2003), 185–191.
112. Smith, S.M., Fast robust automated brain extraction. Hum. Brain Mapp. 17 (2002), 143–155.
113. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E.J., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., Matthews, P.M., Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1 (2004), S208–S219.
114. Spencer, R.M.C., Gouw, A.M., Ivry, R.B., Age-related decline of sleep-dependent consolidation. Learn. Mem. 14 (2007), 480–484.
115. Steriade, M., Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci. 28 (2005), 317–324.
116. Steriade, M., Grouping of brain rhythms in corticothalamic systems. Neuroscience 137 (2006), 1087–1106.
117. Tamaki, M., Matsuoka, T., Nittono, H., Hori, T., Fast sleep spindle (13-15 Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31 (2008), 204–211.
118. Tamaki, M., Matsuoka, T., Nittono, H., Hori, T., Activation of fast sleep spindles at the premotor cortex and parietal areas contributes to motor learning: a study using sLORETA. Clin. Neurophysiol. 120 (2009), 878–886.
119. Timofeev, I., Contribution of intrinsic and synaptic factors in the desynchronization of thalamic oscillatory activity. Thalamus Relat. Syst. 1 (2001), 53–69.
120. Timofeev, I., Chauvette, S., The spindles: are they still thalamic?. Sleep 36 (2013), 825–826.
121. Tombaugh, T.N., McIntyre, N.J., The mini-mental state examination: a comprehensive review. J. Am. Geriatr. Soc. 40 (1992), 922–935.
122. Tyvaert, L., Levan, P., Grova, C., Dubeau, F., Gotman, J., Effects of fluctuating physiological rhythms during prolonged EEG-fMRI studies. Clin. Neurophysiol. 119 (2008), 2762–2774.
123. Vaquero, L., Hartmann, K., Ripollés, P., Rojo, N., Sierpowska, J., François, C., Càmara, E., van Vugt, F.T., Mohammadi, B., Samii, A., Münte, T.F., Rodríguez-Fornells, A., Altenmüller, E., Structural neuroplasticity in expert pianists depends on the age of musical training onset. Neuroimage 126 (2016), 106–119.
124. Vien, C., Boré, A., Lungu, O., Benali, H., Carrier, J., Fogel, S., Doyon, J., Age-related white matter correlates of motor sequence learning and consolidation. Neurobiol. Aging 48 (2016), 13–22.
125. Walker, M., Stickgold, R., Alsop, D., Gaab, N., Schlaug, G., Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133 (2005), 911–917.
126. Wamsley, E., Shinn, A.K., Tucker, M.A., Ono, K.E., McKinley, S., Ely, A.V., Goff, D.C., Stickgold, R., Manoach, D.S., The effects of eszopiclone on sleep spindles and memory consolidation in schizophrenia: a randomized placebo-controlled trial. Sleep 36 (2013), 1369–1376.
127. Wamsley, E., Tucker, M.A., Shinn, A.K., Ono, K.E., McKinley, S., Ely, A.V., Goff, D.C., Stickgold, R., Manoach, D.S., Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?. Biol. Psychiatry 71 (2012), 154–161.
128. Werk, C.M., Harbour, V.L., Chapman, C.A., Induction of long-term potentiation leads to increased reliability of evoked neocortical spindles in vivo. Neuroscience 131 (2005), 793–800.
129. Werth, E., Achermann, P., Borbely, A.A., Fronto-occipital EEG power gradients in human sleep. J. Sleep Res. 6 (1997), 102–112.
130. Werth, E., Achermann, P., Dijk, D.J., Borbely, A.A., Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. Electroencephalogr. Clin. Neurophysiol. 103 (1997), 535–542.
131. Wilhelm, I., Metzkow-Mészàros, M., Knapp, S., Born, J., Sleep-dependent consolidation of procedural motor memories in children and adults: the pre-sleep level of performance matters. Dev. Sci. 15 (2012), 506–515.
132. Wilson, K., Baran, B., Pace-Schott, E.F., Ivry, R.B., Spencer, R.M.C., Sleep modulates word-pair learning but not motor sequence learning in healthy older adults. Neurobiol. Aging 33 (2012), 991–1000.
133. Winkler, A.M., Ridgway, G.R., Webster, M.A., Smith, S.M., Nichols, T.E., Permutation inference for the general linear model. Neuroimage 92 (2014), 381–397.
134. Zeitlhofer, J., Gruber, G., Anderer, P., Asenbaum, S., Schimicek, P., Saletu, B., Topographic distribution of sleep spindles in young healthy subjects. J. Sleep Res. 6 (1997), 149–155.
135. Zepelin, H., McDonald, C.S., Age differences in autonomic variables during sleep. J. Gerontol. 42 (1987), 142–146.
136. Zhang, Y., Brady, M., Smith, S., Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 20 (2001), 45–57.