Light sleep versus slow wave sleep in memory consolidation: A question of global versus local processes?

Trends in Neurosciences

Volumn 37, Issue 1, 2014, Pages 10-19

  Genzel, Lisa ^a   Kroes, Marijn C W ^b   Dresler, Martin ^c   Battaglia, Francesco P ^b,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b RADBOUD UNIVERSITY   (Netherlands)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Downscaling; Memory consolidation; Replay; Sleep; Sleep stages; Spindles; SWR

Indexed keywords

DELTA RHYTHM; ELECTROENCEPHALOGRAM; HOMEOSTASIS; HUMAN; MEMORY CONSOLIDATION; MENTAL DISEASE; NONHUMAN; NONREM SLEEP; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL NOISE RATIO; SLEEP SPINDLE; SLEEP STAGE; SLOW WAVE SLEEP; STAGE 2 SLEEP; BRAIN; MEMORY; SLEEP;

BRAIN; HUMANS; MEMORY; SLEEP;

EID: 84891371467     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2013.10.002     Document Type: Review

References (136)

1. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
2. Rattenborg N.C., et al. Hippocampal memory consolidation during sleep: a comparison of mammals and birds. Biol. Rev. 2011, 86:658-691.
3. Stickgold R. Sleep-dependent memory consolidation. Nature 2005, 437:1272-1278.
4. Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 1997, 9:534-547.
5. Huber R., et al. Local sleep and learning. Nature 2004, 430:78-81.
6. Fischer S., et al. Motor memory consolidation in sleep shapes more effective neuronal representations. J. Neurosci. 2005, 25:11248-11255.
7. Karni A., et al. Dependence on REM sleep of overnight improvement of perceptual skill. Science 1994, 265:679-682.
8. Saletin J.M., Walker M.P. Nocturnal mnemonics: sleep and hippocampal memory processing. Front. Neurol. 2012, 3:59.
9. O'Neill J., et al. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010, 33:220-229.
10. Tononi G., Cirelli C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 2006, 10:49-62.
11. Rechtschaffen A., Kales A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects 1968, US Department of Health, Education and Welfare, Public Health Services.
12. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nat. Rev. Neurosci. 2005, 6:119-130.
13. Chow H.M., et al. Rhythmic alternating patterns of brain activity distinguish rapid eye movement sleep from other states of consciousness. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:10300-10305.
14. Spoormaker V.I., et al. Development of a large-scale functional brain network during human non-rapid eye movement sleep. J. Neurosci. 2010, 30:11379-11387.
15. Amzica F., Steriade M. Electrophysiological correlates of sleep delta waves. Electroencephalogr. Clin. Neurophysiol. 1998, 107:69-83.
16. Morris R.G.M. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci. 2006, 23:2829-2846.
17. Isomura Y., et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 2006, 52:871-882.
18. Nir Y., et al. Regional slow waves and spindles in human sleep. Neuron 2011, 70:153-169.
19. Hahn T.T.G., et al. Phase-locking of hippocampal interneurons' membrane potential to neocortical up-down states. Nat. Neurosci. 2006, 9:1359-1361.
20. Sirota A., et al. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2065-2069.
21. Peyrache A., et al. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:17207-17212.
22. Battaglia F.P., et al. Hippocampal sharp wave bursts coincide with neocortical 'up-state' transitions. Learn. Mem. 2004, 11:697-704.
23. Steriade M., Amzica F. Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J. Sleep Res. 1998, 7:30-35.
24. Massimini M., et al. Slow waves, synaptic plasticity and information processing: insights from transcranial magnetic stimulation and high-density EEG experiments. Eur. J. Neurosci. 2009, 29:1761-1770.
25. Clemens Z., et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
26. Lewis P.A., Durrant S.J. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn. Sci. 2011, 15:343-351.
27. Wilson M., McNaughton B. Reactivation of hippocampal ensemle memories during sleep. Science 1994, 265:676-679.
28. Girardeau G., et al. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009, 12:1222-1223.
29. Ego-Stengel V., Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 2010, 20:1-10.
30. McNaughton B.L., et al. Off-line reprocessing of recent memory and its role in memory consolidation: a progress report. Sleep Brain Plast. 2003, 10.1093/acprof:oso/9780198574002.003.0013.
31. Peyrache A., et al. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 2009, 12:919-926.
32. Ji D., Wilson M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 2007, 10:100-107.
33. Lansink C.S., et al. Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 2009, 7:e1000173.
34. Kudrimoti H.S., et al. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 1999, 19:4090-4101.
35. Peigneux P., et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron 2004, 44:535-545.
36. Yotsumoto Y., et al. Location-specific cortical activation changes during sleep after training for perceptual learning. Curr. Biol. 2009, 19:1278-1282.
37. Rasch B., Born J. Maintaining memories by reactivation. Curr. Opin. Neurobiol. 2007, 17:698-703.
38. Diekelmann S., et al. Labile or stable:opposing consequences for memory when reactivated during waking and sleep. Nat. Neurosci. 2011, 14:381-386.
39. Diekelmann S., et al. Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations. Neurobiol. Learn. Mem. 2012, 98:103-111.
40. Rudoy J., et al. Strengthening individual memories by reactivating them during sleep. Science 2009, 326:1079.
41. Antony J.W., et al. Cued memory reactivation during sleep influences skill learning. Nat. Neurosci. 2012, 15:1114-1116.
42. Bendor D., Wilson M.A. Biasing the content of hippocampal replay during sleep. Nat. Neurosci. 2012, 15:1439-1444.
43. Jadhav S.P., et al. Awake hippocampal sharp-wave ripples support spatial memory. Science 2012, 336:1454-1458.
44. Ribeiro S., et al. Long-lasting novelt-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2004, 2:E24.
45. Tatsuno M., et al. Methodological considerations on the use of template matching to study long-lasting memory trace replay. J. Neurosci. 2006, 26:10727-10742.
46. Grosmark A., et al. REM sleep reorganizes hippocampal excitability. Neuron 2012, 75:1001-1007.
47. Johnson L.A., et al. Stored-trace reactivation in rat prefrontal cortex is correlated with down-to-up state fluctuation density. J. Neurosci. 2010, 30:2650-2661.
48. Chauvette S., et al. Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 2012, 75:1105-1113.
49. Wierzynski C.M., et al. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 2009, 61:587-596.
50. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 1991, 313:574-586.
51. Euston D.R., et al. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 2007, 318:1147-1150.
52. Sejnowski T.J., Destexhe A. Why do we sleep?. Brain Res. 2000, 886:208-223.
53. Genzel L., et al. Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology 2012, 37:987-989.
54. Fogel S.M., Smith C. Learning-dependent changes in sleep spindles and stage 2 sleep. J. Sleep Res. 2006, 15:250-255.
55. Nishida M., Walker M.P. Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2007, 2:e341.
56. Schabus M., et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004, 27:1479-1485.
57. Siapas A.G., Wilson M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 1998, 21:1123-1128.
58. Contreras D., Steriade M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J. Physiol. 1996, 490:159-179.
59. Clemens Z., et al. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur. J. Neurosci. 2011, 33:511-520.
60. Dang-Vu T.T., et al. Spontaneous brain rhythms predict sleep stability in the face of noise. Curr. Biol. 2010, 20:R626-R627.
61. Kim A., et al. Optogenetically induced sleep spindle rhythms alter sleep architectures in mice. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:20673-20678.
62. Czisch M., et al. Functional MRI during sleep: BOLD signal decreases and their electrophysiological correlates. Eur. J. Neurosci. 2004, 20:566-574.
63. Andrade K., et al. Sleep spindles and hippocampal functional connectivity in human NREM sleep. J. Neurosci. 2011, 31:10331-10339.
64. Logothetis N.K., et al. Hippocampal-cortical interaction during periods of subcortical silence. Nature 2012, 491:547-553.
65. Steriade M. Coherent oscillations and short-term plasticity in corticothalamic networks. Trends Neurosci. 1999, 22:337-345.
66. Dang-Vu T.T., et al. Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15438-15443.
67. Ramadan W., et al. Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS ONE 2009, 4:e6697.
68. Eschenko O., et al. Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb. Cortex 2012, 22:426-435.
69. Eschenko O., Sara S.J. Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation?. Cereb. Cortex 2008, 18:2596-2603.
70. Amzica F., Steriade M. The functional significance of K-complexes. Sleep Med. Rev. 2002, 6:139-149.
71. Genzel L., et al. Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep 2009, 32:302-310.
72. Gais S., et al. Learning-dependent increases in sleep spindle density. J. Neurosci. 2002, 22:6830-6834.
73. Schabus M., et al. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur. J. Neurosci. 2006, 23:1738-1746.
74. Marshall L., Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 2007, 11:442-450.
75. Plihal W., Born J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 1999, 36:571-582.
76. Rasch B., et al. Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat. Neurosci. 2009, 12:396-397.
77. Backhaus J., Junghanns K. Daytime naps improve procedural motor memory. Sleep Med. 2006, 7:508-512.
78. Korman M., et al. Daytime sleep condenses the time course of motor memory consolidation. Nat. Neurosci. 2007, 10:1206-1213.
79. Tucker M.A., et al. A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol. Learn. Mem. 2006, 86:241-247.
80. Lahl O., et al. An ultra short episode of sleep is sufficient to promote declarative memory performance. J. Sleep Res. 2008, 17:3-10.
81. van Dongen E.V., et al. Functional connectivity during light sleep is correlated with memory performance for face-location associations. Neuroimage 2011, 57:262-270.
82. Lancel M., Steiger A. Sleep and its modulation by drugs that affect GABAA receptor function. Angew. Chem. Int. Ed. Engl. 1999, 38:2852-2864.
83. Wixted J.T. The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 2004, 55:235-269.
84. Dresler M., et al. A double dissociation of memory impairments in major depression. J. Psychiatr. Res. 2011, 45:1593-1599.
85. Steriade M., Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 2003, 37:563-576.
86. Perrett S.P., et al. LTD induction in adult visual cortex: role of stimulus timing and inhibition. J. Neurosci. 2001, 21:2308-2319.
87. Borbély A.A., Achermann P. Sleep homeostasis and models of sleep regulation. J. Biol. Rhythms 1999, 14:557-568.
88. Vyazovskiy V.V., et al. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 2008, 11:200-208.
89. Vyazovskiy V.V., et al. Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. J. Neurophysiol. 2009, 101:1921-1931.
90. Dash M.B., et al. Long-term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states. J. Neurosci. 2009, 29:620-629.
91. Frank M.G. Erasing synapses in sleep: is it time to be SHY?. Neural Plast. 2012, 2012:264378.
92. Aton S.J., et al. Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 2009, 61:454-466.
93. Shannon B.J., et al. Morning-evening variation in human brain metabolism and memory circuits. J. Neurophysiol. 2013, 109:1444-1456.
94. Esser S.K., et al. A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res. Bull. 2006, 69:86-94.
95. Huber R., et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci. 2006, 9:1169-1176.
96. Vyazovskiy V.V., et al. Local sleep in awake rats. Nature 2011, 472:443-447.
97. Van Der Werf Y.D., et al. 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.
98. Yoo S.S., et al. A deficit in the ability to form new human memories without sleep. Nat. Neurosci. 2007, 10:385-392.
99. Van Der Werf Y.D., et al. Sleep benefits subsequent hippocampal functioning. Nat. Neurosci. 2009, 12:122-123.
100. Takashima A., et al. Shift from hippocampal to neocortical centered retrieval network with consolidation. J. Neurosci. 2009, 29:10087-10093.
101. Wilckens K., et al. Age-related decline in controlled retrieval: the role of the PFC and sleep. Neural Plast. 2012, 2012:624795.
102. Tse D., et al. Schema-dependent gene activation and memory encoding in neocortex. Science 2011, 333:891-895.
103. Battaglia F.P., et al. Structured cognition and neural systems: from rats to language. Neurosci. Biobehav. Rev. 2012, 36:1626-1639.
104. Tamminen J., et al. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J. Neurosci. 2010, 30:14356-14360.
105. Hupbach A., et al. Nap-dependent learning in infants. Dev. Sci. 2009, 12:1007-1012.
106. Gomez Beldarrain M., et al. Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions. Clin. Neurol. Neurosurg. 2008, 110:245-252.
107. Gomez R.L., et al. Naps promote abstraction in language-learning infants. Psychol. Sci. 2006, 17:670-674.
108. Kumara D., McClelland J. Generalization through the recurrent interaction of episodic memories. Psychol. Rev. 2012, 119:573-616.
109. Wang S.H., Morris R.G.M. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 2009, 61:49-79.
110. Tse D., et al. Schemas and memory consolidation. Science 2007, 316:76-82.
111. Kroes M., Fernández G. Dynamic neural systems enable adaptive, flexible memories. Neurosci. Biobehav. Rev. 2012, 36:1646-1666.
112. van Kesteren M.T.R., et al. How schema and novelty augment memory formation. Trends Neurosci. 2012, 35:211-219.
113. Takashima A., et al. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:756-761.
114. Hagewoud R., et al. Coping with sleep deprivation:shifts in regional brain activity and learning strategy. Sleep 2010, 33:1465-1473.
115. Dang-Vu T.T., et al. Spontaneous neural activity during human slow wave sleep. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:15160-15165.
116. Achermann P., Borbély A.A. Low-frequency oscillations in the human sleep electroencephalogram. Neuroscience 1997, 81:213-222.
117. Dresler M., et al. Neuroscience-driven discovery development of sleep therapeutics. Pharmacol. Ther. 2013, (in press).
118. Steiger A., Kimura M. Wake and sleep-EEg provide biomarkers in depression. J. Psychiatr. Res. 2010, 44:242-252.
119. Armitage R. Sleep and circadian rhythms in mood disorders. Acta Psychiatr. Scand. 2007, 433:104-115.
120. Siegel J.M. The REM sleep-memory consolidation hypothesis. Science 2001, 294:1058-1063.
121. Vertes R., Siegel J. Time for the sleep community to take a critical look at the purported role of sleep in memory processing. Sleep 2005, 28:1228-1229.
122. Dresler M., et al. Impaired off-line memory consolidation in depression. Eur. Neuropsychopharmacol. 2010, 20:553-561.
123. Genzel L., et al. Sleep-dependent memory consolidation of a new task is inhibited in psychiatric patients. J. Psychiatr. Res. 2011, 45:555-560.
124. Dresler M., et al. Off-line memory consolidation impairments in multiple sclerosis patients receiving high-dose corticosteroid treatment mirror consolidation impairments in depression. Psychoneuroendocrinology 2010, 35:1194-1202.
125. Ferrarelli M., et al. Reduced sleep spindle activity in schizophrenia patients. Am. J. Psychiatry 2007, 164:483-489.
126. Lopez J., et al. Reduced sleep spindle activity in early-onset and elevated risk for depression. J. Am. Acad. Child Adolesc. Psychiatry 2010, 49:934-943.
127. de Maertelear V., et al. Sleep spindle activity changes in patients with affective disorders. Sleep 1987, 10:443-451.
128. Goetz R., et al. Spindle characteristics in prepubertal major depressives during an episode and after sustained recoverz: a controlled study. Sleep 1983, 6:369-375.
129. Reynolds C.F., et al. EEG sleep in elderly depressed, demented, and healthy subjects. Biol. Psychiatry 1985, 20:431-442.
130. Plante D.T., et al. Topographic and sex-related differences in sleep spindles in major depressive disorder: a high-density EEG investigation. J. Affect. Disord. 2013, 146:120-125.
131. Manoach D.S., et al. Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J. Psychiatr. Res. 2010, 44:112-120.
132. Wamsley E.J., et al. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?. Biol. Psychiatry 2012, 71:154-161.
133. Ferrarelli F., et al. Thalamic dzsfunction in schizophrenia suggested bz whole-night deficits in slow and fast spindles. Am. J. Psychiatry 2010, 167:1339-1348.
134. Chouinard S., et al. Sleep in untreated patients with schizophrenia: a meta-analysis. Schizophr. Bull. 2004, 30:957-967.
135. Göder R., et al. Impairment of visuospatial memory is associated with decreased slow wave sleep in schizophrenia. J. Psychiatr. Res. 2004, 38:591-599.
136. Phillips K., et al. Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 2012, 76:526-533.