Sleep function and synaptic homeostasis

Sleep Medicine Reviews

Volumn 10, Issue 1, 2006, Pages 49-62

  Tononi, Giulio ^a   Cirelli, Chiara ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Consolidation; Delta sleep; Learning; Long term depression; Slow oscillation; Slow waves; Synaptic scaling

Indexed keywords

COGNITIVE DEFECT; GRAY MATTER; HOMEOSTASIS; HYPOTHESIS; LEARNING; MEMORY; MOOD DISORDER; NERVE CELL; PLASTICITY; REVIEW; SLEEP; SLOW WAVE SLEEP; WAKEFULNESS;

BRAIN; HOMEOSTASIS; HUMANS; LEARNING; MEMORY; SLEEP; SYNAPSES; WAKEFULNESS;

EID: 30844435916     PISSN: 10870792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smrv.2005.05.002     Document Type: Review

References (112)

1. G. Tononi, and C. Cirelli Sleep and synaptic homeostasis: a hypothesis Brain Res Bull 62 2 2003 143 150
2. A.A. Borbely, and P. Achermann Sleep homeostasis and models of sleep regulation J Biol Rhythms 14 6 1999 557 568
3. A.Y. Klintsova, and W.T. Greenough Synaptic plasticity in cortical systems Curr Opin Neurobiol 9 2 1999 203 208
4. G.W. Knott, C. Quairiaux, C. Genoud, and E. Welker Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice Neuron 34 2 2002 265 273
5. C. Cirelli, and G. Tononi Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system J Neurosci 20 24 2000 9187 9194
6. C. Cirelli, C.M. Gutierrez, and G. Tononi Extensive and divergent effects of sleep and wakefulness on brain gene expression Neuron 41 1 2004 35 43
7. S.W. Ying, M. Futter, K. Rosenblum, M.J. Webber, S.P. Hunt, and T.V. Bliss Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis J Neurosci 22 5 2002 1532 1540
8. A.J. Silva Molecular and cellular cognitive studies of the role of synaptic plasticity in memory J Neurobiol 54 1 2003 224 237
9. C.S. Wallace, G.S. Withers, I.J. Weiler, J.M. George, D.F. Clayton, and W.T. Greenough Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity Brain Res Mol Brain Res 32 2 1995 211 220
10. C. Cirelli, and G. Tononi Gene expression in the brain across the sleep-waking cycle Brain Res 885 2 2000 303 321
11. A.R. Braun, T.J. Balkin, N.J. Wesenten, R.E. Carson, M. Varga, and P. Baldwin Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study Brain 120 Pt 7 1997 1173 1197
12. V.V. Vyazovskiy, P. Achermann, A.A. Borbely, and I. Tobler The dynamics of spindles and EEG slow-wave activity in NREM sleep in mice Arch Ital Biol 142 4 2004 511 523
13. G. Tononi, and C. Cirelli Some considerations on sleep and neural plasticity Arch Ital Biol 139 3 2001 221 241
14. M. Steriade The corticothalamic system in sleep Front Biosci 8 2003 D878 D899
15. P.J. Sjostrom, G.G. Turrigiano, and S.B. Nelson Rate, timing, and cooperativity jointly determine cortical synaptic plasticity Neuron 32 6 2001 1149 1164
16. G. Tononi, C. Cirelli, and M. Pompeiano Changes in gene expression during the sleep-waking cycle: a new view of activating systems Archives Italiennes De Biologie 134 1 1995 21 37
17. G. Aston-Jones, and F. Bloom Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle J Neurosci 1 1981 876 886
18. S.G. Walling, and C.W. Harley Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: a novel beta-adrenergic- and protein synthesis-dependent mammalian plasticity mechanism J Neurosci 24 3 2004 598 604
19. T.W. Robbins, and B.J. Everitt Central norepinephrine neurons and behavior F.E. Bloom D.J. Kupfer Psychopharmacology: the fourth generation of progress 1995 Raven Press New York 363
20. C. Cirelli, M. Pompeiano, and G. Tononi Neuronal gene expression in the waking state: a role for the locus coeruleus Science 274 5290 1996 1211 1215
21. G. Tononi, C. Cirelli, and P.J. Shaw Molecular correlates of sleep, the waking state, and sleep deprivation A. Borbély O. Hayaishi T.J. Sejnowski J.S. Altman The regulation of sleep 2000 HSFP Strasbourg 155 168
22. M.P. Kelly, and S.A. Deadwyler Experience-dependent regulation of the immediate-early gene arc differs across brain regions J Neurosci 23 16 2003 6443 6451
23. P. Meerlo, E.A. de Bruin, A.M. Strijkstra, and S. Daan A social conflict increases EEG slow-wave activity during subsequent sleep Physiol Behav 73 3 2001 331 335
24. R. Huber, M.F. Ghilardi, M. Massimini, and G. Tononi Local sleep and learning Nature 430 6995 2004 78 81
25. M. Ghilardi, C. Ghez, V. Dhawan, J. Moeller, M. Mentis, and T. Nakamura Patterns of regional brain activation associated with different forms of motor learning Brain Res 871 1 2000 127 145
26. H. Kattler, D.J. Dijk, and A.A. Borbely Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans J Sleep Res 3 3 1994 159 164
27. V. Vyazovskiy, A.A. Borbely, and I. Tobler Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat J Sleep Res 9 4 2000 367 371
28. J.M. Krueger, and F. Obal A neuronal group theory of sleep function J Sleep Res 2 2 1993 63 69
29. J.M. Krueger, F. Obal Jr, L. Kapas, and J. Fang Brain organization and sleep function Behav Brain Res 69 1-2 1995 177 185
30. L.A. Finelli, A.A. Borbely, and P. Achermann Functional topography of the human nonREM sleep electroencephalogram Eur J Neurosci 13 12 2001 2282 2290
31. R. Huber, T. Deboer, and I. Tobler Topography of EEG dynamics after sleep deprivation in mice J Neurophysiol 84 4 2000 1888 1893
32. J. Grutzendler, N. Kasthuri, and W.B. Gan Long-term dendritic spine stability in the adult cortex Nature 420 6917 2002 812 816
33. J.T. Trachtenberg, B.E. Chen, G.W. Knott, G. Feng, J.R. Sanes, and E. Welker Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex Nature 420 6917 2002 788 794
34. Feinberg I. Effects of maturation and aging on slow-wave sleep in man: Implications for neurobiology. In: Wauquier A DC, Radulovacki M, editor. Slow Wave Sleep: Physiological, Pathophysiological and Functional Aspects. New York: Raven Press; 1989.
35. I. Feinberg, H.C. Thode Jr, H.T. Chugani, and J.D. March Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density J Theor Biol 142 2 1990 149 161
36. P.R. Huttenlocher, and A.S. Dabholkar Regional differences in synaptogenesis in human cerebral cortex J Comp Neurol 387 2 1997 167 178
37. E.R. Sowell, P.M. Thompson, K.D. Tessner, and A.W. Toga Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation J Neurosci 21 22 2001 8819 8829
38. D. Petit, J.F. Gagnon, M.L. Fantini, L. Ferini-Strambi, and J. Montplaisir Sleep and quantitative EEG in neurodegenerative disorders J Psychosom Res 56 5 2004 487 496
39. I. Feinberg Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17 4 1982 319 334
40. A.J. Heynen, B.J. Yoon, C.H. Liu, H.J. Chung, R.L. Huganir, and M.F. Bear Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation Nat Neurosci 6 8 2003 854 862
41. H. Miyamoto, H. Katagiri, and T. Hensch Experience-dependent slow-wave sleep development Nat Neurosci 6 6 2003 553 554
42. S. Hill, and G. Tononi Modeling sleep and wakefulness in the thalamocortical system J Neurophysiol 93 3 2005 1671 1698
43. M. Bazhenov, I. Timofeev, M. Steriade, and T.J. Sejnowski Model of thalamocortical slow-wave sleep oscillations and transitions to activated States J Neurosci 22 19 2002 8691 8704
44. A. Compte, M.V. Sanchez-Vives, D.A. McCormick, and X.J. Wang Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model J Neurophysiol 89 5 2003 2707 2725
45. D. Aeschbach, J.R. Matthews, T.T. Postolache, M.A. Jackson, H.A. Giesen, and T.A. Wehr Dynamics of the human EEG during prolonged wakefulness: evidence for frequency-specific circadian and homeostatic influences Neurosci Lett 239 2-3 1997 121 124
46. C. Cajochen, D.P. Brunner, K. Krauchi, P. Graw, and A. Wirz-Justice Power density in theta/alpha frequencies of the waking EEG progressively increases during sustained wakefulness Sleep 18 10 1995 890 894
47. C. Cajochen, R. Foy, and D.J. Dijk Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans Sleep Res Online 2 3 1999 65 69
48. C. Cajochen, V. Knoblauch, K. Krauchi, C. Renz, and A. Wirz-Justice Dynamics of frontal EEG activity, sleepiness and body temperature under high and low sleep pressure Neuroreport 12 10 2001 2277 2281
49. A.A. Borbely, I. Tobler, and M. Hanagasioglu Effect of sleep deprivation on sleep and EEG power spectra in the rat Behav Brain Res 14 3 1984 171 182
50. R. Huber, T. Deboer, and I. Tobler Effects of sleep deprivation on sleep and sleep EEG in three mouse strains: empirical data and simulations Brain Res 857 1-2 2000 8 19
51. D.J. Dijk, D.G. Beersma, and S. Daan EEG power density during nap sleep: reflection of an hourglass measuring the duration of prior wakefulness J Biol Rhythms 2 3 1987 207 219
52. G.G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same Trends Neurosci 22 5 1999 221 227
53. N.S. Desai, R.H. Cudmore, S.B. Nelson, and G.G. Turrigiano Critical periods for experience-dependent synaptic scaling in visual cortex Nat Neurosci 5 8 2002 783 789
54. N. Kemp, and Z.I. Bashir Long-term depression: a cascade of induction and expression mechanisms Prog Neurobiol 65 4 2001 339 365
55. R. Malinow, and R.C. Malenka AMPA receptor trafficking and synaptic plasticity Annu Rev Neurosci 25 2002 103 126
56. G.G. Turrigiano AMPA receptors unbound: membrane cycling and synaptic plasticity Neuron 26 1 2000 5 8
57. D.J. Dijk, D.G. Beersma, S. Daan, G.M. Bloem, and R.H. Van den Hoofdakker Quantitative analysis of the effects of slow wave sleep deprivation during the first 3 h of sleep on subsequent EEG power density Eur Arch Psychiatry Neurol Sci 236 6 1987 323 328
58. H.S. Kudrimoti, C.A. Barnes, and B.L. McNaughton Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics J Neurosci 19 10 1999 4090 4101
59. L.L. Colgin, D. Kubota, Y. Jia, C.S. Rex, and G. Lynch Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves J Physiol 558 Pt3 2004 953 961
60. C. Simon, G. Brandenberger, J. Saini, J. Ehrhart, and M. Follenius Slow oscillations of plasma glucose and insulin secretion rate are amplified during sleep in humans under continuous enteral nutrition Sleep 17 4 1994 333 338
61. H.Y. Man, J.W. Lin, W.H. Ju, G. Ahmadian, L. Liu, and L.E. Becker Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization Neuron 25 3 2000 649 662
62. C. Cirelli, and G. Tononi Changes in anti-phosphoserine and anti-phosphothreonine antibody binding during the sleep-waking cycle and after lesions of the locus coeruleus Sleep Res Online 1 1998 11 18
63. M.D. Eyre, G. Richter-Levin, A. Avital, and M.G. Stewart Morphological changes in hippocampal dentate gyrus synapses following spatial learning in rats are transient Eur J Neurosci 17 9 2003 1973 1980
64. M.G. Frank, N.P. Issa, and M.P. Stryker Sleep enhances plasticity in the developing visual cortex Neuron 30 1 2001 275 287
65. M. Sheng, and S. Hyoung Lee AMPA receptor trafficking and synaptic plasticity: major unanswered questions Neurosci Res 46 2 2003 127 134
66. D.J. Dijk, D.P. Brunner, and A.A. Borbely Time course of EEG power density during long sleep in humans Am J Physiol 258 3 Pt 2 1990 R650 R661
67. D. Attwell, and S.B. Laughlin An energy budget for signaling in the grey matter of the brain J Cereb Blood Flow Metab 21 10 2001 1133 1145
68. G. Buzsaki, J. Csicsvari, G. Dragoi, K. Harris, D. Henze, and H. Hirase Homeostatic maintenance of neuronal excitability by burst discharges in vivo Cereb Cortex 12 9 2002 893 899
69. D.B. Chklovskii, T. Schikorski, and C.F. Stevens Wiring optimization in cortical circuits Neuron 34 3 2002 341 347
70. S. Cohen-Cory The developing synapse: construction and modulation of synaptic structures and circuits Science 298 5594 2002 770 776
71. J.W. Krakauer, M.F. Ghilardi, M. Mentis, A. Barnes, M. Veytsman, and D. Eidelberg Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study J Neurophysiol 91 2 2004 924 933
72. K.M. Fenn, H.C. Nusbaum, and D. Margoliash Consolidation during sleep of perceptual learning of spoken language Nature 425 6958 2003 614 616
73. S. Fischer, M. Hallschmid, A.L. Elsner, and J. Born Sleep forms memory for finger skills Proc Natl Acad Sci USA 99 18 2002 11987 11991
74. S. Gais, W. Plihal, U. Wagner, and J. Born Early sleep triggers memory for early visual discrimination skills Nat Neurosci 3 12 2000 1335 1339
75. A. Karni, D. Tanne, B.S. Rubenstein, J.J. Askenasy, and D. Sagi Dependence on REM sleep of overnight improvement of a perceptual skill [see comments] Science 265 5172 1994 679 682
76. P. Maquet, S. Schwartz, R. Passingham, and C. Frith Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging J Neurosci 23 4 2003 1432 1440
77. S. Mednick, K. Nakayama, and R. Stickgold Sleep-dependent learning: a nap is as good as a night Nat Neurosci 6 7 2003 697 698
78. R. Stickgold, L. James, and J.A. Hobson Visual discrimination learning requires sleep after training Nat Neurosci 3 12 2000 1237 1238
79. M.P. Walker, T. Brakefield, A. Morgan, J.A. Hobson, and R. Stickgold Practice with sleep makes perfect: sleep-dependent motor skill learning Neuron 35 1 2002 205 211
80. T.J. Sejnowski, and A. Destexhe Why do we sleep? Brain Res 886 1-2 2000 208 223
81. D.L. Rothman, K.L. Behar, F. Hyder, and R.G. Shulman In vivo NMR studies of the glutamate neurotransmitter flux and neuroenergetics: implications for brain function Annu Rev Physiol 65 2003 401 427
82. C. Pavlides, and J. Winson Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes J Neurosci 9 8 1989 2907 2918
83. V.V. Vyazovskiy, E. Welker, J.M. Fritschy, and I. Tobler Regional pattern of metabolic activation is reflected in the sleep EEG after sleep deprivation combined with unilateral whisker stimulation in mice Eur J Neurosci 20 5 2004 1363 1370
84. T. Kuboyama, A. Hori, T. Sato, T. Mikami, T. Yamaki, and S. Ueda Changes in cerebral blood flow velocity in healthy young men during overnight sleep and while awake Electroencephalogr Clin Neurophysiol 102 2 1997 125 131
85. G. Hajak, J. Klingelhofer, M. Schulz-Varszegi, G. Matzander, D. Sander, and B. Conrad Relationship between cerebral blood flow velocities and cerebral electrical activity in sleep Sleep 17 1 1994 11 19
86. P. Maquet, P. Peigneux, S. Laureys, M. Boly, T. Dang-Vu, and M. Desseilles Memory processing during human sleep as assessed by functional neuroimaging Rev Neurol (Paris) 159 11 2003 6S27 6S29
87. P. Peigneux, S. Laureys, S. Fuchs, F. Collette, F. Perrin, and J. Reggers Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44 3 2004 535 545
88. P. Peigneux, S. Laureys, S. Fuchs, A. Destrebecqz, F. Collette, and X. Delbeuck Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep Neuroimage 20 1 2003 125 134
89. M.A. Wilson, and B.L. McNaughton Reactivation of hippocampal ensemble memories during sleep Science 265 5172 1994 676 679
90. H. Hirase, X. Leinekugel, A. Czurko, J. Csicsvari, and G. Buzsaki Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience Proc Natl Acad Sci USA 98 16 2001 9386 9390
91. Z. Nadasdy, H. Hirase, A. Czurko, J. Csicsvari, and G. Buzsaki Replay and time compression of recurring spike sequences in the hippocampus J Neurosci 19 21 1999 9497 9507
92. C.M. Pennartz, E. Lee, J. Verheul, P. Lipa, C.A. Barnes, and B.L. McNaughton The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples J Neurosci 24 29 2004 6446 6456
93. S. Ribeiro, D. Gervasoni, E.S. Soares, Y. Zhou, S.C. Lin, and J. Pantoja Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas PLoS Biol 2 1 2004 E24
94. T. Roth, and T. Roehrs Insomnia: epidemiology, characteristics, and consequences Clin Cornerstone 5 3 2003 5 15
95. R.M. Benca, S. Ancoli-Israel, and H. Moldofsky Special considerations in insomnia diagnosis and management: depressed, elderly, and chronic pain populations J Clin Psychiatry 65 supplement 8 2004 26 35
96. C.L. Drake, T. Roehrs, and T. Roth Insomnia causes, consequences, and therapeutics: an overview Depress Anxiety 18 4 2003 163 176
97. M.H. Bonnet, and D.L. Arand Hyperarousal and insomnia Sleep Med Rev 1 2 1997 97 108
98. E.A. Nofzinger, D.J. Buysse, A. Germain, J.C. Price, J.M. Miewald, and D.J. Kupfer Functional neuroimaging evidence for hyperarousal in insomnia Am J Psychiatry 161 11 2004 2126 2128
99. C.M. Morin, P.J. Hauri, C.A. Espie, A.J. Spielman, D.J. Buysse, and R.R. Bootzin Nonpharmacologic treatment of chronic insomnia. An American academy of sleep medicine review Sleep 22 8 1999 1134 1156
100. D. Riemann, and U. Voderholzer Primary insomnia: a risk factor to develop depression? J Affect Disord 76 1-3 2003 255 259
101. D. Riemann, M. Berger, and U. Voderholzer Sleep and depression - results from psychobiological studies: an overview Biol Psychol 57 1-3 2001 67 103
102. R. Armitage Microarchitectural findings in sleep EEG in depression: diagnostic implications Biol Psychiatry 37 2 1995 72 84
103. A. Germain, E.A. Nofzinger, D.J. Kupfer, and D.J. Buysse Neurobiology of non-REM sleep in depression: further evidence for hypofrontality and thalamic dysregulation Am J Psychiatry 161 10 2004 1856 1863
104. H. Giedke, and F. Schwarzler Therapeutic use of sleep deprivation in depression Sleep Med Rev 6 5 2002 361 377
105. J.L. Payne, J.A. Quiroz, C.A. Zarate Jr, and H.K. Manji Timing is everything: does the robust upregulation of noradrenergically regulated plasticity genes underlie the rapid antidepressant effects of sleep deprivation? Biol Psychiatry 52 10 2002 921 926
106. E. Reinink, A.L. Bouhuys, M.C. Gordijn, and R.H. Van Den Hoofdakker Prediction of the antidepressant response to total sleep deprivation of depressed patients: longitudinal versus single day assessment of diurnal mood variation Biol Psychiatry 34 7 1993 471 481
107. D.J. Dijk, and C.A. Czeisler Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans J Neurosci 15 5 Pt 1 1995 3526 3538
108. D.J. Dijk, T.L. Shanahan, J.F. Duffy, J.M. Ronda, and C.A. Czeisler Variation of electroencephalographic activity during non-rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans J Physiol 505 Pt 3 1997 851 858
109. G.W. Davis, and I. Bezprozvanny Maintaining the stability of neural function: a homeostatic hypothesis Annu Rev Physiol 63 2001 847 869
110. D.P. Brunner, D.J. Dijk, and A.A. Borbely Repeated partial sleep deprivation progressively changes in EEG during sleep and wakefulness Sleep 16 2 1993 100 113
111. H.P. Van Dongen, G. Maislin, J.M. Mullington, and D.F. Dinges The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation Sleep 26 2 2003 117 126
112. C. Cirelli, R. Huber, A. Gopalakrishnan, TL. Southard, and G. Tononi Locus ceruleus control of slow-wave homeostasis J. Neurosci 25 18 2005 4503 4511