The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation

Neuroscience and Biobehavioral Reviews

Volumn 35, Issue 5, 2011, Pages 1154-1165

  Fogel, Stuart M ^a   Smith, Carlyle T ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b TRENT UNIVERSITY   (Canada)

Author keywords

Consolidation; Intelligence; Learning; Memory; Non REM; Sleep; Spindles

Indexed keywords

BRAIN FUNCTION; COGNITION; DECLARATIVE MEMORY; ELECTROENCEPHALOGRAM; HUMAN; INTELLIGENCE; INTELLIGENCE QUOTIENT; LEARNING; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NERVE EXCITABILITY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROCEDURAL MEMORY; REM SLEEP; REVIEW; SLEEP SPINDLE; SLEEP TIME; SLEEP WAKING CYCLE; SLOW WAVE SLEEP;

ANIMALS; BRAIN MAPPING; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; HUMANS; INTELLIGENCE; LEARNING; MEMORY; SLEEP; WAKEFULNESS;

EID: 79952534366     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2010.12.003     Document Type: Review

References (161)

1. Aeschbach D., Borbély A.A. All-night dynamics of the human sleep EEG. J. Sleep Res. 1993, 2:70-81.
2. Aeschbach D., Cajochen C., Landolt H., Borbély A.A. Homeostatic sleep regulation in habitual short sleepers and long sleepers. Am. J. Physiol. 1996, 270:R41-R53.
3. Anderer P., Klosch G., Gruber G., Trenker E., Pascual-Marqui R.D., Zeitlhofer J., Barbanoj M.J., Rappelsberger P., Saletu B. Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 2001, 103:581-592.
4. Asanuma H., Pavlides C. Neurobiological basis of motor learning in mammals. Neuroreport 1997, 8:i-iv.
5. Bal T., von Krosigk M., McCormick D.A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J. Physiol. 1995, 483:665-685.
6. Bal T., von Krosigk M., McCormick D.A. Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J. Physiol. 1995, 483:641.
7. 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. 2011, 217(1):117-121.
8. Bazhenov M., Timofeev I., Steriade M., Sejnowski T.J. Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat. Neurosci. 1999, 2:168-174.
9. 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. 2000, 84:1076-1087.
10. Bixler E.O., Rhodes J.M. Spindle activity during sleep in cultural-familial mild retardates. Psychophysiology 1968, 5:212.
11. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
12. Bliwise D.L. Principles and Practice of Sleep Medicine 2000, W.B. Saunders. M.H. Kryger, T. Roth (Eds.).
13. Bódizs R., Kis T., Lázár A.S., Havrán L., Rigó P., Clemens Z., Halász P. Prediction of general mental ability based on neural oscillation measures of sleep. J. Sleep Res. 2005, 14:285-292.
14. Borbely A.A. A two process model of sleep regulation. Hum. Neurobiol. 1982, 1:195-204.
15. Brawn T.P., Fenn K.M., Nusbaum H.C., Margoliash D. Consolidating the effects of waking and sleep on motor-sequence learning. J. Neurosci. 2010, 30:13977-13982.
16. Broughton R., Dinges D.F. Napping: a ubiquitous enigma. Chronobiological, Behavioural, and Medical Aspects of Napping 1989, 1-7. Raven Press, New York. D.F. Dinges, R. Broughton (Eds.).
17. Buzsáki G. Long-Term changes of hippocampal sharp-waves following high frequency afferent activation. Brain Res. 1984, 300:179-182.
18. Buzsáki G. Two-Stage model of memory trace formation: a role for " noisy" brain states. Neuroscience 1989, 31:551-570.
19. Campbell K., Bell I., Bastien C. Evoked potential measures of information processing during natural sleep. Sleep Arousal and Performance 1992, 86-116. Birkhauser, Boston. R. Broughton, R.D. Ogilvie (Eds.).
20. 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 2001, 38:232-242.
21. Carskadon M.A., Dement W.C. Normal human sleep: an overview. Principles and Practice of Sleep Medicine 2000, 13-23. W.B. Saunders. M.H. Kryger, T. Roth (Eds.).
22. Chapman C.A., Trepel C., Ivanco T.L., Froc D.J., Wilson K., Racine R.J. Changes in field potentials and membrane currents in rat sensorimotor cortex following repeated tetanization of the corpus callosum in vivo. Cereb. Cortex 1998, 8:730.
23. Cleeremans A., McClelland J.L. Learning the structure of event sequences. J. Exp. Psychol.: Gen. 1991, 120:235-253.
24. Clemens Z., Fabó D., Halász P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 2005, 132:529-535.
25. Clemens Z., Fabó D., Halász P. Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 2006, 403:52-56.
26. Clemens Z., Mölle M., Eross L., Barsi P., Halász P., Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
27. Colrain I.M. The k-complex: a 7-decade history. Sleep 2005, 28:255-273.
28. Contreras D., Destexhe A., Sejnowski T.J., Steriade M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 1996, 274:771-774.
29. Contreras D., Steriade M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 1995, 15:604-622.
30. Cote K.A., De Lugt D.R., Campbell K.B. Changes in the scalp topography of event-related potentials and behavioral responses during the sleep onset period. Psychophysiology 2002, 39:29-37.
31. Davis H., Davis P.A., Loomis A.L., Harvey E.N., Hobart G. Changes in human brain potentials during the onset of sleep. Science 1937, 86:448-450.
32. Debas K., Carrier J., Orban P., Barakat M., Lungu O., Vandewalle G., HadjTahar 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. 2010, 107(41):17839-17844.
33. Destexhe A., Contreras D., Sejnowski T.J., Steriade M. Modeling the control of reticular thalamic oscillations by neuromodulators. Neuroreport 1994, 5:2217-2220.
34. Destexhe A., Sejnowski T.J. Thalamocortical Assemblies: How Ion Channels, Single Neurons and Large-Scale Networks Organize Sleep Oscillations 2001, Oxford University Press, Oxford.
35. De Koninck J., Lorrain D., Christ G., Proulx G., Coulombe D. Intensive language learning and increases in rapid eye movement sleep: evidence of a performance factor. Int. J. Psychophysiol. 1989, 8:43-47.
36. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
37. 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. 1993, 626:190-199.
38. Doran S.M. The dynamic topography of individual sleep spindles. Sleep Res. Online 2003, 5:133-139.
39. Doyon, J., Orban, P., Barakat, M., Debas, K., Lungu, O., Albouy, G., Fogel, S., Proulx, S., Laventure, S., Carrier, J., Benali, H., in press. Plasticité du Cerveau Associée à l'Apprentissage moteur. Med. Sci. (Paris).
40. Doyon J., Penhune V., Ungerleider L.G. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 2003, 41:252-262.
41. Driver H.S. Sleep in women. J. Psychosom. Res. 1996, 40:227-230.
42. Driver H.S., Dijk D.J., Werth E., Biedermann K., Borbély A.A. Sleep and the sleep electroencephalogram across the menstrual cycle in young healthy women. J. Clin. Endocrinol. Metab. 1996, 81:728.
43. Dudai Y., Eisenberg M. Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron 2004, 44:93-100.
44. De Gennaro L., Ferrara M. Sleep spindles: an overview. Sleep Med. Rev. 2003, 7:423-440.
45. De Gennaro L., Ferrara M., Vecchio F., Curcio G., Bertini M. An electroencephalographic fingerprint of human sleep. Neuroimage 2005, 26:114-122.
46. Eschenko O., Mölle M., Born J., Sara S.J. Elevated sleep spindle density after learning or after retrieval in rats. J. Neurosci. 2006, 26:12914-12920.
47. Fischer S., Drosopoulos S., Tsen J., Born J. Implicit learning - explicit knowing: a role for sleep in memory system interaction. J. Cogn. Neurosci. 2006, 18:311-319.
48. Fogel S.M., Nader R., Cote K.A., Smith C.T. Sleep spindles and learning potential. Behav. Neurosci. 2007, 121:1-10.
49. Fogel S.M., Smith C.T. Learning-dependent changes in sleep spindles and stage 2 sleep. J. Sleep Res. 2006, 15:250-255.
50. Fogel S.M., Smith C.T., Beninger R.J. Evidence for 2-stage models of sleep and memory: learning-dependent changes in spindles and theta in rats Brain. Res. Bull. 2009, 79:445-451.
51. Fogel S.M., Smith C.T., Beninger R.J. Too much of a good thing? Elevated baseline sleep spindles predict poor avoidance performance in rats. Brain Res. 2010, 1319:112-117.
52. Fogel S.M., Smith C.T., Cote K.A. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav. Brain. Res. 2007, 180:48-61.
53. Frankland P.W., Bontempi B., Talton L.E., Kaczmarek L., Silva A.J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 2004, 304:881-883.
54. Fuentealba P., Timofeev I., Steriade M. Prolonged hyperpolarizing potentials precede spindle oscillations in the thalamic reticular nucleus. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9816-9821.
55. Gabrieli J.D.E. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 1998, 49.
56. Gaillard J.M., Blois R. Spindle density in sleep of normal subjects. Sleep 1981, 4:385.
57. Gais S., Born J. Declarative memory consolidation: mechanisms acting during human sleep. Learn. Mem. 2004, 11:679-685.
58. Gais S., Mölle M., Helms K., Born J. Learning-dependent increases in sleep spindle density. J. Neurosci. 2002, 22:6830-6834.
59. Gibbs E.L., Gibbs F.A. Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science 1962, 138:1106-1107.
60. Godbout R., Bergeron C., Limoges E., Stip E., Mottron L. A laboratory study of sleep in Asperger's syndrome. Neuroreport 2000, 11:127-130.
61. Grafton S.T., Mazziotta J.C., Presty S., Friston K.J., Frackowiak R.S., Phelps M.E. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J. Neurosci. 1992, 12:2542-2548.
62. Guazzelli M., 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. 1986, 63:526-539.
63. Haist F., Bowden Gore J., Mao H. Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat. Neurosci. 2001, 4:1139-1145.
64. Hennevin E., Hars B., Maho C., Bloch V. Processing of learned information in paradoxical sleep: relevance for memory. Behav. Brain Res. 1995, 69:125-135.
65. Himanen S.L., Virkkala J., Huhtala H., Hasan J. Spindle frequencies in sleep EEG show u-shape within first four NREM sleep episodes. J. Sleep Res. 2002, 11:35-42.
66. Huupponen E., Himanen S.L., Varri A., Hasan J., Lehtokangas M., Saarinen J. A study on gender and age differences in sleep spindles. Neuropsychobiology 2002, 45:99-105.
67. Iber C. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications 2007, American Academy of Sleep Medicine, Westchester, IL.
68. Ishizuka Y., Pollak C.P., Shirakawa S., Kakuma T., Azumi K., Usui A., Shiraishi K., Fukuzawa H., Kariya T. Sleep spindle frequency changes during the menstrual cycle. J. Sleep Res. 1994, 3:26-29.
69. Ji D., Wilson M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 2007, 10:100-107.
70. Jobert M., Poiseau E., Jahnig P., Schulz H., Kubicki S. Topographical analysis of sleep spindle activity. Neuropsychobiology 1992, 26:210-217.
71. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
72. Korman M., Doyon J., Doljansky J., Carrier J., Dagan Y., Karni A. Daytime sleep condenses the time course of motor memory consolidation. Nat. Neurosci. 2007, 10:1206-1213.
73. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 1999, 19:4090-4101.
74. Landolt H.P., Borbély A.A. Age-dependent changes in sleep EEG topography. Clin. Neurophysiol. 2001, 112:369-377.
75. Landolt H.P., Roth C., Dijk D.J., Borbély A.A. Late-afternoon ethanol intake affects nocturnal sleep and the sleep EEG in middle-aged men. J. Clin. Psychopharmacol. 1996, 16:428-436.
76. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
77. Loomis A.L., Harvey E.N., Hobart G. Further observations on the potential rhythms of the cerebral cortex during sleep. Science 1935, 82:198-200.
78. Loomis A.L., Harvey E.N., Hobart G. Potential rhythms of the cerebral cortex during sleep. Science 1935, 81:597-598.
79. Maquet P. The role of sleep in learning and memory. Science 2001, 294:1048.
80. Marshall L., Helgadóttir H., Mölle M., Born J. Boosting slow oscillations during sleep potentiates memory. Nature 2006, 444:610-613.
81. Marshall L., Mölle M., Born J. Spindle and slow wave rhythms at slow wave sleep transitions are linked to strong shifts in the cortical direct current potential. Neuroscience 2003, 121:1047-1053.
82. Mednick S., Nakayama K., Stickgold R. Sleep-dependent learning: a nap is as good as a night. Nat. Neurosci. 2003, 6:697-698.
83. Merica H. Fast and slow frequency spindles in sleep: two generators?. Clin. Neurophysiol. 2000, 111:1704-1706.
84. Milner C.E., Fogel S.M., Cote K.A. Habitual napping moderates motor performance improvements following a short daytime nap. Biol. Psychol. 2006, 73:141-156.
85. Milner B., Squire L.R., Kandel E.R. Cognitive neuroscience and the study of memory. Neuron 1998, 20:445-468.
86. Morin A., Doyon J., Dostie V., Barakat M., HadjTahar A., Korman M., Benali H., Karni A., Ungerleider L.G., Carrier J. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 2008, 31:1149-1156.
87. Mölle M., Eschenko O., Gais S., Sara S.J., Born J. The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci. 2009, 29:1071-1081.
88. Mölle M., Marshall L., Gais S., Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 2002, 22:10941-10947.
89. Mölle M., Yeshenko O., Marshall L., Sara S.J., Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol. 2006, 96:62-70.
90. Nadasdy Z., Hirase H., Czurko A., Csicsvari J., Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 1999, 19:9497-9507.
91. Nader R.S., Smith C.T. The relationship between stage 2 sleep spindles and intelligence. Sleep 2001, 24:A160.
92. Nader R., Smith C. A role for stage 2 sleep in memory processing. Sleep and Brain Plasticity 2003, 87-99. Oxford University Press, Oxford. P. Maquet, C.R. Smith (Eds.).
93. Nader R., Smith C., Muir D., Scharfe E. The existence of " super-fast" spindles in adolescent girls. Sleep 2003, 26:A73.
94. Nicolas A., Petit D., Rompré S., Montplaisir J. Sleep spindle characteristics in healthy subjects of different age groups. Clin. Neurophysiol. 2001, 112:521-527.
95. Nishida M., Walker M.P. Daytime naps, motor memory consolidation and regionally specific sleep spindles. Plos. One 2007, 2:e341.
96. Ogilvie R.D. The process of falling asleep. Sleep Med. Rev. 2001, 5:247-270.
97. Ogilvie R.D., Simons I.A., Kuderian R.H., MacDonald T., Rustenburg J. Behavioral, event-related potential, and EEG/FFT changes at sleep onset. Psychophysiology 1991, 28:54-64.
98. Pavlides C., Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J. Neurosci. 1989, 9:2907-2918.
99. Peters K.R., Smith V., Smith C.T. Changes in sleep architecture following motor learning depend on initial skill level. J. Cogn. Neurosci. 2007, 19:817-829.
100. Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 1997, 9:534-547.
101. Rapp P.R., Amaral D.G. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci. 1992, 15:340-345.
102. Rasch B., Gais S., Born J. Impaired off-line consolidation of motor memories after combined blockade of cholinergic receptors during REM sleep-rich sleep. Neuropsychopharma 2009, 34:1843-1853.
103. Rasch B., Pommer J., Diekelmann S., Born J. Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat. Neurosci. 2009, 12:396-397.
104. Ray L.B., Fogel S.M., Smith C.T., Peters K.R. Validating an automated sleep spindle detection algorithm using an individualized approach. J. Sleep Res. 2010, 19:374-378.
105. Rechtschaffen A., Hauri P., Zeitlin M. Auditory awakening thresholds in REM and NREM sleep stages. Percept. Mot. Skills 1966, 22:927-942.
106. Rechtschaffen A., Kales A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects 1968, National Institutes of Health.
107. Rickard T.C., Cai D.J., Rieth C.A., Jones J., Ard M.C. Sleep does not enhance motor sequence learning. J. Exp. Psychol.: Learn. Mem. Cog. 2008, 34:834-842.
108. Rosanova M., Ulrich D. Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 2005, 25:9398-9405.
109. Roth M., Shaw J., Green J. The form voltage distribution and physiological significance of the k-complex. Electroencephalogr. Clin. Neurophysiol. 1956, 8:385-402.
110. 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. 2007, 104:13164-13169.
111. Schabus M., Gruber G., Parapatics S., Sauter C., Klösch G., Anderer P., Klimesch W., Saletu B., Zeitlhofer J. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004, 27:1479-1485.
112. Schabus M., Hödlmoser K., Pecherstorfer T., Anderer P., Gruber G., Parapatics S., Sauter C., Kloesch G., Klimesch W., Saletu B., Zeitlhofer J. Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res. 2008, 1191:127-135.
113. Schabus M., Hödlmoser K., Gruber G., Sauter C., Anderer P., Klösch G., Parapatics S., Saletu B., Klimesch W., Zeitlhofer J. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur. J. Neurosci. 2006, 23:1738-1746.
114. Schacter D.L. The cognitive neuroscience of memory: perspectives from neuroimaging research. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1997, 352:1689-1695.
115. Schiffelholz T., Aldenhoff J.B. Novel object presentation affects sleep-wake behavior in rats. Neurosci. Lett. 2002, 328:41-44.
116. Schmidt C., Peigneux P., Muto V., Schenkel M., Knoblauch V., Münch M., de Quervain D.J., Wirz-Justice A., Cajochen C. Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J. Neurosci. 2006, 26:8976-8982.
117. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 1957, 20:11-21.
118. Shibagaki M., Kiyono S. Duration of spindle bursts during nocturnal sleep in mentally retarded children. Electroencephalogr. Clin. Neurophysiol. 1983, 55:645-651.
119. Siapas A.G., Wilson M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 1998, 21:1123-1128.
120. Siegel J.M. The REM sleep-memory consolidation hypothesis. Science 2001, 294:1058-1063.
121. Silverstein L.D., Levy C.M. The stability of the sigma sleep spindle. Electroencephalogr. Clin. Neurophysiol. 1976, 40:666-670.
122. Sirota A., Buzsáki G. Interaction between neocortical and hippocampal networks via slow oscillations. Thal. and Rel. Systems 2005, 3:245-259.
123. Smith C. Sleep states and learning: a review of the animal literature. Neurosci. Biobehav. Rev. 1985, 9:157-168.
124. Smith C. Sleep states and memory processes. Behav. Brain Res. 1995, 69:137-145.
125. Smith C. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med. Rev. 2001, 5:491-506.
126. Smith C. The REM sleep window and memory processing. Sleep and Brain Plasticity 2003, 117-135. Oxford University Press, Oxford. P. Maquet, C.R. Smith (Eds.).
127. Smith C.T., Aubrey J.B., Peters K.R. Different roles for REM and stage 2 sleep in motor learning: a proposed model. Psychol. Belg. 2004, 44:81-104.
128. Smith C., Lapp L. Increases in number of REMS and REM density in humans following an intensive learning period. Sleep 1991, 14:325-330.
129. Smith C., MacNeill C. Impaired motor memory for a pursuit rotor task following stage 2 sleep loss in college students. J. Sleep Res. 1994, 3:206-213.
130. Smith C.T., Nixon M.R., Nader R.S. Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn. Mem. 2004, 11:714-719.
131. Squire L.R., Zola S.M. Episodic memory, semantic memory, and amnesia. Hippocampus 1998, 8:205-211.
132. Steriade M. Brainstem activation of thalamocortical systems. Brain Res. Bull. 1999, 50:391-392.
133. Steriade M., Amzica F. Coalescence of sleep rhythms and their chronology in corticothalamic networks. Sleep Res. Online 1998, 1:1-10.
134. Steriade M., Amzica F. Slow sleep oscillation, rhythmic k-complexes, and their paroxysmal developments. J. Sleep Res. 1998, 7:30-35.
135. Steriade M., Deschenes M., Domich L., Mulle C. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J. Neurophysiol. 1985, 54:1473.
136. Steriade M., Domich L., Oakson G., Deschenes M. The deafferented reticular thalamic nucleus generates spindle rhythmicity. J. Neurophysiol. 1987, 57:260.
137. Steriade M., Nunez A., Amzica F. A novel slow (< 1Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 1993, 13:3252.
138. Steriade M., Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 2003, 37:563-576.
139. Stickgold R., Walker M.P. Sleep and memory: the ongoing debate. Sleep 2005, 28:1225-1227.
140. Stickgold R., Walker M.P. Sleep-dependent memory consolidation and reconsolidation. Sleep Med. 2007, 8:331-343.
141. Tamaki M., Matsuoka T., Nittono H., Hori T. Fast sleep spindle (13-15Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 2008, 31:204-211.
142. 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. 2009, 120:878-886.
143. Trepel C., Racine R.J. Long-term potentiation in the neocortex of the adult, freely moving rat. Cereb. Cortex 1998, 8:719-729.
144. Tyson P.D., Ogilvie R.D., Hunt H.T. Lucid, prelucid, and nonlucid dreams related to the amount of EEG alpha activity during REM sleep. Psychophysiology 1984, 21:442-451.
145. Uchida S., Atsumi Y., Kojima T. Dynamic relationships between sleep spindles and delta waves during a NREM period. Brain Res. Bull. 1994, 33:351-355.
146. Uchida S., Maloney T., March J.D., Azari R., Feinberg I. Sigma (12-15Hz) and delta (0.3-3Hz) EEG oscillate reciprocally within NREM sleep. Brain Res. Bull. 1991, 27:93-96.
147. Ueda K., Nittono H., Hayashi M., Hori T. Spatiotemporal changes of slow wave activities before and after 14Hz/12Hz sleep spindles during stage 2 sleep. Psychiatry Clin. Neurosci. 2001, 55:183-184.
148. Ungerleider L.G., Doyon J., Karni A. Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 2002, 78:553-564.
149. Vertes R.P., Siegel J.M. Time for the sleep community to take a critical look at the purported role of sleep in memory processing. Sleep 2005, 28:1228-1229. (Discussion 1230-3).
150. vonKrosigk M., Bal T., McCormick D.A. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 1993, 261:361-364.
151. Wang X.J., Rinzel J. Spindle rhythmicity in the reticularis thalami nucleus: synchronization among mutually inhibitory neurons. Neuroscience 1993, 53:899-904.
152. Warrington E.K. Studies of retrograde memory: a long-term view. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13523-13526.
153. Wei H.G., Riel E., Czeisler C.A., Dijk D.J. Attenuated amplitude of circadian and sleep-dependent modulation of electroencephalographic sleep spindle characteristics in elderly human subjects. Neurosci. Lett. 1999, 260:29-32.
154. 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 2005, 131:793-800.
155. Werth E., Achermann P., Borbély A.A. Fronto-occipital EEG power gradients in human sleep. J. Sleep Res. 1997, 6:102-112.
156. Werth E., Achermann P., Dijk D.J., Borbély A.A. Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. Electroencephalogr. Clin. Neurophysiol. 1997, 103:535-542.
157. Wierzynski C.M., Lubenov E.V., Gu M., Siapas A.G. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 2009, 61:587-596.
158. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
159. Winocur G. The hippocampus and thalamus: their roles in short- and long-term memory and the effects of interference. Behav. Brain Res. 1985, 16:135-152.
160. Zeitlhofer J., Gruber G., Anderer P., Asenbaum S., Schimicek P., Saletu B. Topographic distribution of sleep spindles in young healthy subjects. J. Sleep Res. 1997, 6:149-155.
161. Zola-Morgan S., Squire L.R., Rempel N.L., Clower R.P., Amaral D.G. Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J. Neurosci. 1992, 12:2582-2596.