Synaptic potentiation and sleep need: Clues from molecular and electrophysiological studies

Current Topics in Medicinal Chemistry

Volumn 11, Issue 19, 2011, Pages 2472-2482

  Hanlon, Erin C ^a   Vyazovskiy, Vladyslav V ^a   Faraguna, Ugo ^a   Tononi, Giulio ^a   Cirelli, Chiara ^a  

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

Author keywords

EEG; Local sleep; Plasticity; Sleep homeostasis; Slow wave activity; Synaptic homeostasis

Indexed keywords

ACETYLCHOLINE; ADRENALIN; SEROTONIN;

BIRD; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; ELECTROENCEPHALOGRAM; HUMAN; MAMMAL; NONHUMAN; NONREM SLEEP; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION; WAKEFULNESS;

EID: 80053501185     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802611797470312     Document Type: Review

References (132)

1. Achermann, P.; Borbely, A. A. Mathematical models of sleep regulation. Front. Biosci., 2003, 8, s683-693.
2. Tobler, I. Phylogeny of sleep regulation. In: Principles and Practice of Sleep Medicine, 4th ed.; M.H. Kryger, T. Roth; W.C. Dement, Eds.; Elsevier Saunders: Philadelphia, 2005; pp. 77-90.
3. Cirelli, C.; Tononi, G. Is sleep essential? PLoS Biol., 2008, 6(8), e216.
4. Werth, E.; Achermann, P.; Borbély, A. A. Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. Neuro. Report, 1996, 8, 123-127.
5. Huber, R.; Deboer, T.; Tobler, I. Topography of EEG dynamics after sleep deprivation in mice. J. Neurophysiol., 2000, 84(4), 1888-1893.
6. Massimini, M.; Huber, R.; Ferrarelli, F.; Hill, S.; Tononi, G. The sleep slow oscillation as a traveling wave. J. Neurosci., 2004, 24(31), 6862-70.
7. Vyazovskiy, V. V.; Faraguna, U.; Cirelli, C.; Tononi, G. 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(4), 1921-1931.
8. Steriade, M.; Timofeev, I.; Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol., 2001, 85(5), 1969-1985.
9. Amzica, F.; Steriade, M. Electrophysiological correlates of sleep delta waves. Electroenceph. Clin. Neurophysiol., 1998, 107, 69-83.
10. Destexhe, A.; Contreras, D.; Steriade, M. Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J. Neurosci., 1999, 19(11), 4595-4608.
11. Steriade, M.; Nunez, A.; Amzica, F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci., 1993, 13(8), 3252-3265.
12. Contreras, D.; Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci., 1995, 15(1 Pt 2), 604-622.
13. Lopes da Silva, F. Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr. Clin. Neurophysiol., 1991, 79(2), 81-93.
14. Esser, S. K.; Hill, S. L.; Tononi, G. Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep, 2007, 30(12), 1617-1630.
15. Riedner, B. A.; Vyazovskiy, V. V.; Huber, R.; Massimini, M.; Esser, S.; Murphy, M.; Tononi, G. Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep, 2007, 30(12), 1643-1657.
16. Vyazovskiy, V. V.; Riedner, B. A.; Cirelli, C.; Tononi, G. T. Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. Sleep, 2007, 30(12), 1631-1642.
17. Vyazovskiy, V. V.; Olcese, U.; Lazimy, Y. M.; Faraguna, U.; Esser, S. K.; Williams, J. C.; Cirelli, C.; Tononi, G. Cortical firing and sleep homeostasis. Neuron, 2009, 63(6), 865-78.
18. Achermann, P.; Borbely, A. A. Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience, 1997, 81(1), 213-22.
19. Achermann, P.; Borbely, A. A. Temporal evolution of coherence and power in the human sleep electroencephalogram. J. Sleep Res., 1998, 7(Suppl 1), 36-41.
20. Campbell, I. G.; Higgins, L. M.; Darchia, N.; Feinberg, I. Homeostatic behavior of fast Fourier transform power in very low frequency non-rapid eye movement human electroencephalogram. Neuroscience, 2006, 140(4), 1395-1399.
21. Dijk, D. J.; Beersma, D. G.; Daan, S. EEG power density during nap sleep: reflection of an hourglass measuring the duration of prior wakefulness. J. Biol. Rhythms, 1987, 2(3), 207-219.
22. Bersagliere, A.; Achermann, P. Slow oscillations in human nonrapid eye movement sleep electroencephalogram: effects of increased sleep pressure. J. Sleep Res., 2010, 19(1 Pt 2), 228-237.
23. Aeschbach, D.; Cutler, A. J.; Ronda, J. M. A role for non-rapideye-movement sleep homeostasis in perceptual learning. J. Neurosci., 2008, 28(11), 2766-2772.
24. Landsness, E. C.; Crupi, D.; Hulse, B. K.; Peterson, M. J.; Huber, R.; Ansari, H.; Coen, M.; Cirelli, C.; Benca, R. M.; Ghilardi, M. F.; Tononi, G. Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep, 2009, 32(10), 1273-1284.
25. Marshall, L.; Helgadottir, H.; Molle, M.; Born, J. Boosting slow oscillations during sleep potentiates memory. Nature, 2006, 444(7119), 610-613.
26. Walsh, J. K.; Randazzo, A. C.; Stone, K.; Eisenstein, R.; Feren, S. D.; Kajy, S.; Dickey, P.; Roehrs, T.; Roth, T.; Schweitzer, P. K. Tiagabine is associated with sustained attention during sleep restriction: evidence for the value of slow-wave sleep enhancement? Sleep, 2006, 29(4), 433-443.
27. Tononi, G.; Cirelli, C. Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull., 2003, 62(2), 143-150.
28. Tononi, G.; Cirelli, C. Sleep function and synaptic homeostasis. Sleep Med. Rev., 2006, 10(1), 49-62.
29. Krueger, J. M.; Obal, F., Jr.; Kapas, L.; Fang, J. Brain organization and sleep function. Behav. Brain Res., 1995, 69(1/2), 177-185.
30. Krueger, J. M.; Rector, D. M.; Roy, S.; Van Dongen, H. P.; Belenky, G.; Panksepp, J. Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci., 2008, 9(12), 910-919.
31. Vyazovskiy, V.; Borbely, A. A.; Tobler, I. Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J. Sleep Res., 2000, 9(4), 367-371.
32. Vyazovskiy, V. V.; Welker, E.; Fritschy, J. M.; Tobler, I. Regional pattern of metabolic activation is reflected in the sleep EEG after sleep deprivation combined with unilateral whisker stimulation in mice. Eur. J. Neurosci., 2004, 20(5), 1363-1370.
33. Kattler, H.; Dijk, D. J.; Borbely, A. A. Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep Res., 1994, 3(3), 159-164.
34. Vyazovskiy, V. V.; Cirelli, C.; Pfister-Genskow, M.; Faraguna, U.; Tononi, G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci., 2008, 11(2), 200-208.
35. Collingridge, G. L.; Isaac, J. T.; Wang, Y. T. Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci., 2004, 5(12), 952-962.
36. Malenka, R. C.; Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron, 2004, 44(1), 5-21.
37. Rall, W. Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J. Neurophysiol., 1967, 30(5), 1138-1168.
38. Bliss, T. V.; Lomo, T., Plasticity in a monosynaptic cortical pathway. J. Physiol., 1970, 207(2), 61P.
39. Glazewski, S.; Herman, C.; McKenna, M.; Chapman, P. F.; Fox, K. Long-term potentiation in vivo in layers II/III of rat barrel cortex. Neuropharmacology, 1998, 37(4/5), 581-592.
40. Dash, M. B.; Douglas, C. L.; Vyazovskiy, V. V.; Cirelli, C.; Tononi, G. Long-term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states. J. Neurosci., 2009, 29(3), 620-629.
41. Liu, Z. W.; Faraguna, U.; Cirelli, C.; Tononi, G.; Gao, X. B. Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. J. Neurosci., 2010, 30(25), 8671-8675.
42. Rao, Y.; Liu, Z. W.; Borok, E.; Rabenstein, R. L.; Shanabrough, M.; Lu, M.; Picciotto, M. R.; Horvath, T. L.; Gao, X. B. Prolonged wakefulness induces experience-dependent synaptic plasticity in mouse hypocretin/orexin neurons. J. Clin. Invest., 2007, 117(12), 4022-4033.
43. Lu, B. BDNF and activity-dependent synaptic modulation. Learn. Mem., 2003, 10(2), 86-98.
44. Kossel, A. H.; Cambridge, S. B.; Wagner, U.; Bonhoeffer, T. A caged Ab reveals an immediate/instructive effect of BDNF during hippocampal synaptic potentiation. Proc. Natl. Acad. Sci. USA, 2001, 98(25), 14702-14707.
45. Messaoudi, E.; Bardsen, K.; Srebro, B.; Bramham, C. R. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J. Neurophysiol., 1998, 79(1), 496-499.
46. Messaoudi, E.; Ying, S. W.; Kanhema, T.; Croll, S. D.; Bramham, C. R. Brain-derived neurotrophic factor triggers transcriptiondependent, late phase long-term potentiation in vivo. J. Neurosci., 2002, 22(17), 7453-7461.
47. Akaneya, Y.; Tsumoto, T.; Kinoshita, S.; Hatanaka, H. Brainderived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci., 1997, 17(17), 6707-6716.
48. Jiang, B.; Akaneya, Y.; Hata, Y.; Tsumoto, T. Long-term depression is not induced by low-frequency stimulation in rat visual cortex in vivo: a possible preventing role of endogenous brain-derived neurotrophic factor. J. Neurosci., 2003, 23(9), 3761-3770.
49. Faraguna, U.; Vyazovskiy, V. V.; Nelson, A. B.; Tononi, G.; Cirelli, C. A causal role for brain-derived neurotrophic factor in the homeostatic regulation of sleep. J. Neurosci., 2008, 28(15), 4088-4095.
50. Huber, R.; Tononi, G.; Cirelli, C. Exploratory behavior, cortical BDNF expression, and sleep homeostasis. Sleep, 2007, 30(2), 129-139.
51. Hairston, I. S.; Peyron, C.; Denning, D. P.; Ruby, N. F.; Flores, J.; Sapolsky, R. M.; Heller, H. C.; O'Hara, B. F. Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J. Neurophysiol., 2004, 91(4), 1586-1595.
52. Rioult-Pedotti, M. S.; Friedman, D.; Hess, G.; Donoghue, J. P. Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci., 1998, 1(3), 230-234.
53. Rioult-Pedotti, M. S.; Friedman, D.; Donoghue, J. P. Learninginduced LTP in neocortex. Science, 2000, 290(5491), 533-536.
54. Monfils, M. H.; Teskey, G. C. Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation. Neuroscience, 2004, 125(2),329-336.
55. Greenough, W. T.; Larson, J. R.; Withers, G. S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav. Neural. Biol., 1985, 44(2), 301-314.
56. Withers, G. S.; Greenough, W. T. Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex. Neuropsychologia, 1989, 27(1), 61-69.
57. Harms, K. J.; Rioult-Pedotti, M. S.; Carter, D. R.; Dunaevsky, A. Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex. J. Neurosci., 2008, 28(22), 5686-5690.
58. Hanlon, E. C.; Faraguna, U.; Vyazovskiy, V. V.; Tononi, G.; Cirelli, C. Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep, 2009, 32(6), 719-729.
59. Esser, S. K.; Hill, S. L.; Tononi, G. Modeling the effects of transcranial magnetic stimulation on cortical circuits. J. Neurophysiol., 2005, 94(1), 622-639.
60. Huber, R.; Esser, S. K.; Ferrarelli, F.; Massimini, M.; Peterson, M. J.; Tononi, G. TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS ONE, 2007, 2(3), e276.
61. Huber, R.; Maatta, S.; Esser, S. K.; Sarasso, S.; Ferrarelli, F.; Watson, A.; Ferreri, F.; Peterson, M. J.; Tononi, G. Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J. Neurosci., 2008, 28(31), 7911-7918.
62. De Gennaro, L.; Fratello, F.; Marzano, C.; Moroni, F.; Curcio, G.; Tempesta, D.; Pellicciari, M. C.; Pirulli, C.; Ferrara, M.; Rossini, P. M. Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. PLoS ONE, 2008, 3(6), e2483.
63. Bergmann, T. O.; Molle, 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., 2008, 27(9), 2241-2249.
64. Huber, R.; Ghilardi, M. F.; Massimini, M.; Tononi, G. Local sleep and learning. Nature, 2004, 430(6995), 78-81.
65. Huber, R.; Ghilardi, M. F.; Massimini, M.; Ferrarelli, F.; Riedner, B. A.; Peterson, M. J.; Tononi, G. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci., 2006, 9(9), 1169-1176.
66. Doeltgen, S. H.; Ridding, M. C. Behavioural exposure and sleep do not modify corticospinal and intracortical excitability in the human motor system. Clin. Neurophysiol., 2010, 121(3), 448-452.
67. Scalise, A.; Desiato, M. T.; Gigli, G. L.; Romigi, A.; Tombini, M.; Marciani, M. G.; Izzi, F.; Placidi, F. Increasing cortical excitability: a possible explanation for the proconvulsant role of sleep deprivation. Sleep, 2006, 29(12), 1595-1598.
68. Badawy, R. A.; Curatolo, J. M.; Newton, M.; Berkovic, S. F.; Macdonell, R. A. Sleep deprivation increases cortical excitability in epilepsy: syndrome-specific effects. Neurology, 2006, 67(6), 1018-1022.
69. Bellina, V.; Huber, R.; Rosanova, M.; Mariotti, M.; Tononi, G.; Massimini, M. Cortical excitability and sleep homeostasis in humans: a TMS/hd-EEG study. J. Sleep Res., 2008, 1(Suppl.1), 39.
70. Moruzzi, G. The functional significance of sleep with particular regard to the brain mechanisms underlying consciousness. In: Brain and Conscious Experience, Eccles, J. C., Ed.; Springer-Verlag: New York, 1966; pp. 345-388.
71. Steriade, M. Coherent oscillations and short-term plasticity in corticothalamic networks. Trends Neurosci., 1999, 22(8), 337-345.
72. Sejnowski, T. J.; Destexhe, A. Why do we sleep? Brain Res., 2000, 886(1/2), 208-223.
73. Datta, S. Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci., 2000, 20(22), 8607-8613.
74. Graves, L.; Pack, A.; Abel, T. Sleep and memory: a molecular perspective. Trends Neurosci., 2001, 24(4), 237-243.
75. Benington, J. H.; Frank, M. G. Cellular and molecular connections between sleep and synaptic plasticity. Prog. Neurobiol., 2003, 69(2), 71-101.
76. Walker, M. P. A refined model of sleep and the time course of memory formation. Behav. Brain Sci., 2005, 28(1), 51-64; discussion 64-104.
77. Stickgold, R. Sleep-dependent memory consolidation. Nature, 2005, 437(7063), 1272-8.
78. Kessels, H. W.; Malinow, R. Synaptic AMPA receptor plasticity and behavior. Neuron, 2009, 61(3), 340-50.
79. Turrigiano, G. G., The self-tuning neuron: synaptic scaling of excitatory synapses. Cell, 2008, 135(3), 422-435.
80. Jones, B. E. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol. Sci., 2005, 26(11), 578-586.
81. Cirelli, C.; Pompeiano, M.; Tononi, G. Neuronal gene expression in the waking state: A role for the locus coeruleus. Science, 1996, 274(5290), 1211-1215.
82. Seol, G. H.; Ziburkus, J.; Huang, S.; Song, L.; Kim, I. T.; Takamiya, K.; Huganir, R. L.; Lee, H. K.; Kirkwood, A. Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron, 2007, 55(6), 919-929.
83. Cirelli, C.; Tononi, G. Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J. Neurosci., 2000, 20(24), 9187-9194.
84. Steriade, M. The corticothalamic system in sleep. Front. Biosci., 2003, 8, D878-899.
85. Kemp, N.; Bashir, Z. I. Long-term depression: a cascade of induction and expression mechanisms. Prog. Neurobiol., 2001, 65(4), 339-365.
86. Werk, C. M.; Chapman, C. A. Long-term potentiation of polysynaptic responses in layer V of the sensorimotor cortex induced by theta-patterned tetanization in the awake rat. Cereb. Cortex, 2003, 13(5), 500-507.
87. Birtoli, B.; Ulrich, D. Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J. Neurosci., 2004, 24(21), 4935-4940.
88. Rosanova, M.; Ulrich, D. Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci., 2005, 25(41), 9398-9405.
89. Werk, C. M.; Klein, H. S.; Nesbitt, C. E.; Chapman, C. A. Longterm depression in the sensorimotor cortex induced by repeated delivery of 10 Hz trains in vivo. Neuroscience, 2006, 140(1), 13-20.
90. Czarnecki, A.; Birtoli, B.; Ulrich, D. Cellular mechanisms of burst firing-mediated long-term depression in rat neocortical pyramidal cells. J. Physiol., 2007, 578(Pt 2), 471-479.
91. Lubenov, E. V.; Siapas, A. G. Decoupling through synchrony in neuronal circuits with propagation delays. Neuron, 2008, 58(1), 118-131.
92. Harley, C. Noradrenergic and locus coeruleus modulation of the perforant path-evoked potential in rat dentate gyrus supports a role for the locus coeruleus in attentional and memorial processes. Prog. Brain Res., 1991, 88, 307-321.
93. Stickgold, R.; Walker, M. P. Sleep-dependent memory consolidation and reconsolidation. Sleep Med., 2007, 8(4), 331-343.
94. Diekelmann, S.; Born, J. The memory function of sleep. Nat. Rev. Neurosci., 2010, 11(2), 114-126.
95. Hill, S.; Tononi, G.; Ghilardi, M. F. Sleep improves the variability of motor performance. Brain Res. Bull., 2008, 76(6), 605-611.
96. Olcese, U.; Esser, S. K.; Tononi, G. Sleep and synaptic renormalization: A computational study. J. Neurophysiol., 2010, 104(6),3476-3493.
97. Buzsaki, G. The hippocampo-neocortical dialogue. Cereb Cortex, 1996, 6(2), 81-92.
98. Buzsaki, G. Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res., 1998, 7(Suppl 1), 17-23.
99. Giocomo, L. M.; Hasselmo, M. E. Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol. Neurobiol., 2007, 36(2), 184-200.
100. Gais, S.; Born, J. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc. Natl. Acad. Sci. USA, 2004, 101(7), 2140-2144.
101. Rasch, B. H.; Born, J.; Gais, S. Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J. Cogn. Neurosci., 2006, 18(5), 793-802.
102. Louie, K.; Wilson, M. A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron, 2001, 29(1), 145-156.
103. Pennartz, C. M.; Lee, E.; Verheul, J.; Lipa, P.; Barnes, C. A.; McNaughton, B. L. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J. Neurosci., 2004, 24(29), 6446-6456.
104. Siapas, A. G.; Wilson, M. A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron, 1998, 21(5), 1123-1128.
105. Sirota, A.; Csicsvari, J.; Buhl, D.; Buzsaki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA, 2003, 100(4), 2065-2069.
106. Steriade, M.; Timofeev, I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron, 2003, 37(4), 563-576.
107. Ego-Stengel, V.; Wilson, M. A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus, 2010, 20(1), 1-10.
108. Girardeau, G.; Benchenane, K.; Wiener, S. I.; Buzsaki, G.; Zugaro, M. B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci., 2009, 12(10), 1222-1223.
109. Feinberg, I. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J. Psychiatr. Res., 1982, 17(4), 319-334.
110. Cowan, W. M.; Fawcett, J. W.; O'Leary, D. D.; Stanfield, B. B. Regressive events in neurogenesis. Science, 1984, 225(4668), 1258-1265.
111. Chugani, H. T. A critical period of brain development: studies of cerebral glucose utilization with PET. Prev. Med., 1998, 27(2), 184-188.
112. Carskadon, M. A.; Acebo, C.; Jenni, O. G. Regulation of adolescent sleep: implications for behavior. Ann. N. Y. Acad. Sci. USA, 2004, 1021, 276-291.
113. Campbell, I. G.; Feinberg, I. Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc. Natl. Acad. Sci. USA, 2009, 106(13), 5177-5180.
114. Heynen, A. J.; Yoon, B. J.; Liu, C. H.; Chung, H. J.; Huganir, R. L.; Bear, M. F. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat. Neurosci., 2003, 6(8), 854-862.
115. Miyamoto, H.; Katagiri, H.; Hensch, T. Experience-dependent slow-wave sleep development. Nat. Neurosci., 2003, 6(6), 553-554.
116. Feinberg, I. Effects of maturation and aging on slow-wave sleep in man: Implications for neurobiology. In: Slow Wave Sleep: Physiological, Pathophysiological and Functional Aspects. Wauquier A, D. C., Radulovacki M., Ed.; Raven Press: New York, 1989.
117. Feinberg, I.; Thode, H. C., Jr.; Chugani, H. T.; March, J. D. Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. J. Theor. Biol., 1990, 142(2), 149-161.
118. Huttenlocher, P. R.; Dabholkar, A. S. Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol., 1997, 387(2), 167-178.
119. Sowell, E. R.; Thompson, P. M.; Tessner, K. D.; Toga, A. W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. J. Neurosci., 2001, 21(22), 8819-8829.
120. Frank, M. G.; Issa, N. P.; Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron, 2001, 30(1), 275-287.
121. Dadvand, L.; Stryker, M. P.; Frank, M. G. Sleep does not enhance the recovery of deprived eye responses in developing visual cortex. Neuroscience, 2006, 143(3), 815-826.
122. Aton, S. J.; Seibt, J.; Dumoulin, M.; Jha, S. K.; Steinmetz, N.; Coleman, T.; Naidoo, N.; Frank, M. G. Mechanisms of sleepdependent consolidation of cortical plasticity. Neuron, 2009, 61(3), 454-466.
123. McDermott, C. M.; LaHoste, G. J.; Chen, C.; Musto, A.; Bazan, N. G.; Magee, J. C. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J. Neurosci., 2003, 23(29), 9687-9995.
124. Kopp, C.; Longordo, F.; Nicholson, J. R.; Luthi, A. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J. Neurosci., 2006, 26(48), 12456-12465.
125. Tartar, J. L.; Ward, C. P.; McKenna, J. T.; Thakkar, M.; Arrigoni, E.; McCarley, R. W.; Brown, R. E.; Strecker, R. E. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur. J. Neurosci., 2006, 23(10), 2739-2748.
126. Ravassard, P.; Pachoud, B.; Comte, J. C.; Mejia-Perez, C.; Scote-Blachon, C.; Gay, N.; Claustrat, B.; Touret, M.; Luppi, P. H.; Salin, P. A. Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. Sleep, 2009, 32(2), 227-240.
127. Shaffery, J. P.; Sinton, C. M.; Bissette, G.; Roffwarg, H. P.; Marks, G. A. Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience, 2002, 110(3), 431-443.
128. Shaffery, J. P.; Lopez, J.; Bissette, G.; Roffwarg, H. P. Rapid eye movement sleep deprivation in post-critical period, adolescent rats alters the balance between inhibitory and excitatory mechanisms in visual cortex. Neurosci. Lett., 2006, 393(2-3), 131-135.
129. Gilestro, G. F.; Tononi, G.; Cirelli, C. Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science, 2009, 324(5923), 109-112.
130. Donlea, J. M.; Ramanan, N.; Shaw, P. J. Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science, 2009, 324(5923), 105-108.
131. Sagaspe, P.; Taillard, J.; Chaumet, G.; Moore, N.B.B.; Philip, P. Aging and Nocturnal Driving: Better with Coffee or a Nap? A Randomized Study. Sleep, 2007, 30(12), 1808-1813.
132. Blatter, K.; Opwis, K.; Munch, M.; Wirz-Justice, A.; Cajochen, C. Sleep loss-related decrements in plan ning performance in healthy elderly depend on task difficulty. J. Sleep Res., 2005, 14(4), 409-417.