The Sleeping Cerebellum

Trends in Neurosciences

Volumn 40, Issue 5, 2017, Pages 309-323

  Canto, Cathrin B ^a   Onuki, Yoshiyuki ^a   Bruinsma, Bastiaan ^a   van der Werf, Ysbrand D ^a,b   De Zeeuw, Chris I ^a,c  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

cerebellum; consolidation; electrophysiology; memory; sleep; sleep disorders

Indexed keywords

CEREBELLUM; ELECTROENCEPHALOGRAM; FUNCTIONAL CONNECTIVITY; HUMAN; LEARNING; MEDICAL RESEARCH; MEMORY CONSOLIDATION; NONHUMAN; NONREM SLEEP; PRIORITY JOURNAL; PROCEDURAL MEMORY; REM SLEEP; REVIEW; SLEEP; SLEEP DISORDER; PHYSIOLOGY;

CEREBELLUM; HUMANS; LEARNING; SLEEP;

EID: 85017568283     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2017.03.001     Document Type: Review

References (156)

1. 1 Diekelmann, S., Born, J., The memory function of sleep. Nat. Rev. Neurosci. 11 (2010), 114–126.
2. 2 Diekelmann, S., Sleep for cognitive enhancement. Front. Syst. Neurosci., 8, 2014, 46.
3. 3 Saper, C.B., et al. Sleep state switching. Neuron 68 (2010), 1023–1042.
4. 4 Brown, R.E., et al. Control of sleep and wakefulness. Physiol. Rev. 92 (2012), 1087–1187.
5. 5 Berry, R., et al. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Technical Specifications Version 2.2. 2015, American Academy of Sleep Medicine.
6. 6 Krakauer, J.W., Shadmehr, R., Consolidation of motor memory. Trends Neurosci. 29 (2006), 58–64.
7. 7 De Zeeuw, C.I., et al. Spatiotemporal firing patterns in the cerebellum. Nat. Rev. Neurosci. 12 (2011), 327–344.
8. 8 Gao, Z., et al. Distributed synergistic plasticity and cerebellar learning. Nat. Rev. Neurosci. 13 (2012), 619–635.
9. 9 Cunchillos, J., De Andrés, I., Participation of the cerebellum in the regulation of the sleep-wakefulness cycle. Results in cerebellectomized cats. Electroencephalogr. Clin. Neurophysiol. 53 (1982), 549–558.
10. 10 de Andrés, I., et al. Functional anatomy of non-REM sleep. Front. Neurol., 2, 2011, 70.
11. 11 DelRosso, L.M., Hoque, R., The cerebellum and sleep. Neurol. Clin. 32 (2014), 893–900.
12. 12 Riedner, B.A., et al. Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. Prog. Brain Res. 193 (2011), 201–218.
13. 13 Marchesi, G.F., Strata, P., Climbing fibers of cat cerebellum: modulation of activity during sleep. Brain Res. 17 (1970), 145–148.
14. 14 Marchesi, G.F., Strata, P., Mossy and climbing fiber activity during phasic and tonic phenomena of sleep. Pflugers Arch. 323 (1971), 219–240.
15. 15 Schweighofer, N., et al. Cerebellar aminergic neuromodulation: towards a functional understanding. Brain Res. Rev. 44 (2004), 103–116.
16. 16 Steriade, M., et al. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13 (1993), 3252–3265.
17. 17 Steriade, M., et al. Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13 (1993), 3266–3283.
18. 18 Timofeev, I., et al. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10 (2000), 1185–1199.
19. 19 Timofeev, I., Steriade, M., Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76 (1996), 4152–4168.
20. 20 Steriade, M., et al. Thalamic Oscillations and Signaling. 1990, John Wiley & Sons.
21. 21 Niedermeyer, E., Uematsu, S., Electroencephalographic recordings from deep cerebellar structures in patients with uncontrolled epileptic seizures. Electroencephalogr. Clin. Neurophysiol. 37 (1974), 355–365.
22. 22 Zhou, H., et al. Cerebellar modules operate at different frequencies. Elife 2014 (2014), 1–18.
23. 23 Teixeira, M.J., et al. Deep brain stimulation of the dentate nucleus improves cerebellar ataxia after cerebellar stroke. Neurology 85 (2015), 2075–2076.
24. 24 Kros, L., et al. Controlling cerebellar output to treat refractory epilepsy. Trends Neurosci. 38 (2015), 787–799.
25. 25 Dalal, S.S., et al. Oscillatory activity of the human cerebellum: the intracranial electrocerebellogram revisited. Neurosci. Biobehav. Rev. 37 (2013), 585–593.
26. 26 Muthukumaraswamy, S.D., High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front. Hum. Neurosci., 7, 2013, 138.
27. 27 Grech, R., et al. Review on solving the inverse problem in EEG source analysis. J. Neuroeng. Rehabil., 5, 2008, 25.
28. 28 Diedrichsen, J., et al. Advances in functional imaging of the human cerebellum. Curr. Opin. Neurol. 23 (2010), 382–387.
29. 29 Kaufmann, C., et al. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study. Brain 129 (2006), 655–667.
30. 30 Braun, A., Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 120 (1997), 1173–1197.
31. 31 Kajimura, N., et al. Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J. Neurosci. 19 (1999), 10065–10073.
32. 32 Hofle, N., et al. Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 17 (1997), 4800–4808.
33. 33 Hiroki, M., Cerebral white matter blood flow is constant during human non-rapid eye movement sleep: a positron emission tomographic study. J. Appl. Physiol. 98 (2005), 1846–1854.
34. 34 Kjaer, T.W., et al. Regional cerebral blood flow during light sleep – a H(2)(15)O-PET study. J. Sleep Res. 11 (2002), 201–207.
35. 35 Jahnke, K., et al. To wake or not to wake? The two-sided nature of the human K-complex. Neuroimage 59 (2012), 1631–1638.
36. 36 Schabus, M., et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 13164–13169.
37. 37 Dang-Vu, T.T., et al. Spontaneous neural activity during human slow wave sleep. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 15160–15165.
38. 38 Saletin, J.M., et al. Structural brain correlates of human sleep oscillations. Neuroimage 83 (2013), 658–668.
39. 39 Mano, N., Changes of simple and complex spike activity of cerebellar purkinje cells with sleep and waking. Science 170 (1970), 1325–1327.
40. 40 Schonewille, M., et al. Purkinje cells in awake behaving animals operate at the upstate membrane potential. Nat. Neurosci. 9 (2006), 459–461.
41. 41 McCarley, R.W., Hobson, J.A., Simple spike firing patterns of cat cerebellar Purkinje cells in sleep and waking. Electroencephalogr. Clin. Neurophysiol. 33 (1972), 471–483.
42. 42 Oldfield, C.S., et al. Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 13153–13158.
43. 43 Loewenstein, Y., et al. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat. Neurosci. 8 (2005), 202–211.
44. 44 Ros, H., et al. Neocortical networks entrain neuronal circuits in cerebellar cortex. J. Neurosci. 29 (2009), 10309–10320.
45. 45 Nir, Y., Tononi, G., Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn. Sci. 14 (2010), 88–100.
46. 46 Hong, C.C.-H., et al. fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Hum. Brain Mapp. 30 (2009), 1705–1722.
47. 47 Miyauchi, S., et al. Human brain activity time-locked to rapid eye movements during REM sleep. Exp. Brain Res. 192 (2009), 657–667.
48. 48 Hobson, J.A., McCarley, R.W., Spontaneous discharge rates of cat cerebellar Purkinje cells in sleep and waking. Electroencephalogr. Clin. Neurophysiol. 33 (1972), 457–469.
49. 49 Palmer, C., Interpositus and fastigial unit activity during sleep and waking in the cat. Electroencephalogr. Clin. Neurophysiol. 46 (1979), 357–370.
50. 50 Velluti, R., et al. Spontaneous cerebellar nuclei PGO-like waves in natural paradoxical sleep and under reserpine. Electroencephalogr. Clin. Neurophysiol. 60 (1985), 243–248.
51. 51 Sokoloff, G., et al. Twitch-related and rhythmic activation of the developing cerebellar cortex. J. Neurophysiol. 114 (2015), 1746–1756.
52. 52 Del Rio-Bermudez, C., Spontaneous activity and functional connectivity in the developing cerebellorubral system. J. Neurophysiol. 116 (2016), 1316–1327.
53. 53 De Zeeuw, C.I., et al. Causes and consequences of oscillations in the cerebellar cortex. Neuron 58 (2008), 655–658.
54. 54 Andre, P., Arrighi, P., Hipnic modulation of cerebellar information processing: implications for the cerebro-cerebellar dialogue. Cerebellum 2 (2003), 84–95.
55. 55 Popa, D., et al. Functional role of the cerebellum in gamma-band synchronization of the sensory and motor cortices. J. Neurosci. 33 (2013), 6552–6556.
56. 56 Steriade, M., et al. Clustered firing in the cerebello-thalamic pathway during synchronized sleep. Brain Res. 26 (1971), 425–432.
57. 57 Steriade, M., et al. Control of unitary activities in cerebellothalamic pathway during wakefulness and synchronized sleep. J. Neurophysiol. 34 (1971), 389–413.
58. 58 Tagliazucchi, E., Laufs, H., Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82 (2014), 695–708.
59. 59 Tagliazucchi, E., et al. Large-scale brain functional modularity is reflected in slow electroencephalographic rhythms across the human non-rapid eye movement sleep cycle. Neuroimage 70 (2013), 327–339.
60. 60 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. 110 (2013), 10300–10305.
61. 61 Soteropoulos, D.S., Baker, S.N., Cortico-cerebellar coherence during a precision grip task in the monkey. J. Neurophysiol. 95 (2006), 1194–1206.
62. 62 Gross, J., et al. The neural basis of intermittent motor control in humans. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 2299–2302.
63. 63 Rowland, N.C., et al. Cortico-cerebellar coherence and causal connectivity during slow-wave activity. Neuroscience 166 (2010), 698–711.
64. 64 Altmann, A., et al. Validation of non-REM sleep stage decoding from resting state fMRI using linear support vector machines. Neuroimage 125 (2016), 544–555.
65. 65 Macey, P.M., et al. Brain structural changes in obstructive sleep apnea. Sleep 31 (2008), 967–977.
66. 66 Desseilles, M., et al. Neuroimaging insights into the pathophysiology of sleep disorders. Sleep 31 (2008), 777–794.
67. 67 Boucetta, S., et al. Structural brain alterations associated with rapid eye movement sleep behavior disorder in Parkinson's disease. Sci. Rep., 6, 2016, 26782.
68. 68 Hanyu, H., et al. Voxel-based magnetic resonance imaging study of structural brain changes in patients with idiopathic REM sleep behavior disorder. Parkinsonism Relat. Disord. 18 (2012), 136–139.
69. 69 Pedroso, J.L., et al. Sleep disorders in machado-joseph disease: frequency, discriminative thresholds, predictive values, and correlation with ataxia-related motor and non-motor features. Cerebellum 10 (2011), 291–295.
70. 70 Pedroso, J.L., et al. Sleep disorders in cerebellar ataxias. Arq. Neuropsiquiatr. 69 (2011), 253–257.
71. 71 Mehta, L.R., et al. Sporadic fatal insomnia masquerading as a paraneoplastic cerebellar syndrome. Arch. Neurol. 65 (2008), 971–973.
72. 72 Sonni, A., et al. The effects of sleep dysfunction on cognition, affect, and quality of life in individuals with cerebellar ataxia. J. Clin. Sleep Med. 10 (2014), 535–543.
73. 73 Garrido Zinn, C., et al. Major neurotransmitter systems in dorsal hippocampus and basolateral amygdala control social recognition memory. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E4914–E4919.
74. 74 Silva, G.M.F., et al. NREM-related parasomnias in Machado-Joseph disease: clinical and polysomnographic evaluation. J. Sleep Res. 25 (2016), 11–15.
75. 75 Martinez, A.R., et al. Fatigue and its associated factors in spinocerebellar ataxia type 3/Machado-Joseph disease. Cerebellum 16 (2017), 118–121.
76. 76 De Andres, I., Reinoso-Suarez, F., Participation of the cerebellum in the regulation of the sleep-wakefulness cycle through the superior cerebellar peduncle. Arch. Ital. Biol. 117 (1979), 140–163.
77. 77 Grube, M., et al. Dissociation of duration-based and beat-based auditory timing in cerebellar degeneration. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 11597–11601.
78. 78 Walker, M.P., et al. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35 (2002), 205–211.
79. 79 Debas, K., et al. Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 17839–17844.
80. 80 Barakat, M., et al. Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. 217 (2011), 117–121.
81. 81 Stoodley, C.J., The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 11 (2012), 352–365.
82. 82 De Zeeuw, C.I., Ten Brinke, M.M., Motor learning and the cerebellum. Cold Spring Harb. Perspect. Biol., 7, 2015, a021683.
83. 83 Verweij, I.M., et al. Sleep to the beat: a nap favours consolidation of timing. Behav. Neurosci. 130 (2016), 298–304.
84. 84 Lewis, P.A., et al. Keeping time in your sleep: overnight consolidation of temporal rhythm. Neuropsychologia 49 (2011), 115–123.
85. 85 Barakat, M., et al. Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum. Brain Mapp. 34 (2013), 2918–2928.
86. 86 Fogel, S., et al. Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation. Neurobiol. Aging 49 (2017), 154–164.
87. 87 Cousins, J.N., et al. Cued reactivation of motor learning during sleep leads to overnight changes in functional brain activity and connectivity. PLoS Biol., 14, 2016, e1002451.
88. 88 Fischer, S., et al. Sleep forms memory for finger skills. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 11987–11991.
89. 89 Maquet, P., et al. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 3 (2000), 831–836.
90. 90 Ohno, H., et al. REM sleep deprivation suppresses acquisition of classical eyeblink conditioning. Sleep 25 (2002), 877–881.
91. 91 Maquet, P., et al. Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging. J. Neurosci. 23 (2003), 1432–1440.
92. 92 Boele, H.-J., et al. Axonal sprouting and formation of terminals in the adult cerebellum during associative motor learning. J. Neurosci. 33 (2013), 17897–17907.
93. 93 Gao, Z., et al. Excitatory cerebellar nucleocortical circuit provides internal amplification during associative conditioning. Neuron 89 (2016), 645–657.
94. 94 Yamazaki, T., et al. Modeling memory consolidation during posttraining periods in cerebellovestibular learning. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3541–3546.
95. 95 Kassardjian, C.D., The site of a motor memory shifts with consolidation. J. Neurosci. 25 (2005), 7979–7985.
96. 96 Shutoh, F., et al. Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139 (2006), 767–777.
97. 97 Anzai, M., et al. Effects of reversible pharmacological shutdown of cerebellar flocculus on the memory of long-term horizontal vestibulo-ocular reflex adaptation in monkeys. Neurosci. Res. 68 (2010), 191–198.
98. 98 Okamoto, T., et al. Role of cerebellar cortical protein synthesis in transfer of memory trace of cerebellum-dependent motor learning. J. Neurosci. 31 (2011), 8958–8966.
99. 99 Fogel, S.M., et al. How to become an expert: a new perspective on the role of sleep in the mastery of procedural skills. Neurobiol. Learn. Mem. 125 (2015), 236–248.
100. 100 van Dongen, E.V., et al. Memory stabilization with targeted reactivation during human slow-wave sleep. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 10575–10580.
101. 101 Fifer, W.P., et al. Newborn infants learn during sleep. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 10320–10323.
102. 102 Barik, S., De Beaurepaire, R., Dopamine D3 modulation of locomotor activity and sleep in the nucleus accumbens and in lobules 9 and 10 of the cerebellum in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 29 (2005), 718–726.
103. 103 Silva-Marques, B., Intracerebellar vermis histamine facilitates memory consolidation in the elevated T maze model. Neurosci. Lett. 620 (2016), 33–37.
104. 104 van Neerven, J., et al. Injections of β-noradrenergic substances in the flocculus of rabbits affect adaptation of the VOR gain. Exp. Brain Res., 141, 1990, 537.
105. 105 Tan, H.S., et al. Effects of alpha-noradrenergic substances on the optokinetic and vestibulo-ocular responses in the rabbit: a study with systemic and intrafloccular injections. Brain Res. 562 (1991), 207–215.
106. 106 Eban-Rothschild, A., VTA dopaminergic neurons regulate ethologically relevant sleep-wake behaviors. Nat. Neurosci. 19 (2016), 1356–1366.
107. 107 Barmack, N.H., et al. Cholinergic innervation of the cerebellum of the rat by secondary vestibular afferents. Ann. N. Y. Acad. Sci. 656 (1992), 566–579.
108. 108 Jaarsma, D., et al. Cholinergic innervation and receptors in the cerebellum. Prog. Brain Res. 114 (1997), 67–96.
109. 109 Freedman, R., et al. Noradrenaline modulation of the responses of the cerebellar Purkinje cell to afferent synaptic activity. Br. J. Pharmacol. 57 (1976), 603–605.
110. 110 Hoffer, B.J., et al. Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. II. Sensitivity of Purkinje cells to norepinephrine and related substances administered by microiontophoresis. Brain Res. 25 (1971), 523–534.
111. 111 Hökfelt, T., Fuxe, K., Cerebellar monoamine nerve terminals, a new type of afferent fibers to the cortex cerebelli. Exp. Brain Res. 9 (1969), 63–72.
112. 112 Olson, L., Fuxe, K., On the projections from the locus coeruleus noradrenaline neurons: the cerebellar innervation. Brain Res. 28 (1971), 165–171.
113. 113 Geurts, F.J., et al. Localization of 5-HT2A, 5-HT3, 5-HT5A and 5-HT7 receptor-like immunoreactivity in the rat cerebellum. J. Chem. Neuroanat. 24 (2002), 65–74.
114. 114 Bloom, F.E., et al. Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. I. Localization of the fibers and their synapses. Brain Res. 25 (1971), 501–521.
115. 115 Bishop, G., Ho, R., The distribution and origin of serotonin immunoreactivity in the rat cerebellum. Brain Res. 331 (1985), 195–207.
116. 116 Kerr, C.W., Bishop, G.A., Topographical organization in the origin of serotoninergic projections to different regions of the cat cerebellar cortex. J. Comp. Neurol. 304 (1991), 502–515.
117. 117 Kitzman, P.H., Bishop, G.A., The physiological effects of serotonin on spontaneous and amino acid- induced activation of cerebellar nuclear cells: an in vivo study in the cat. Prog. Brain Res. 114 (1997), 209–223.
118. 118 Kitzman, P.H., Bishop, G.A., The origin of serotoninergic afferents to the cats cerebellar nuclei. J. Comp. Neurol. 340 (1994), 541–550.
119. 119 Shen, B., et al. Excitatory effects of histamine on cerebellar interpositus nuclear cells of rats through H(2) receptors in vitro. Brain Res. 948 (2002), 64–71.
120. 120 Tian, L., et al. Histamine excites rat cerebellar Purkinje cells via H2 receptors in vitro. Neurosci. Res. 36 (2000), 61–66.
121. 121 Panula, P., et al. Histamine-containing nerve fibers innervate human cerebellum. Neurosci. Lett. 160 (1993), 53–56.
122. 122 Airaksinen, M.S., Histaminergic system in the tree shrew brain. J. Comp. Neurol. 286 (1989), 289–310.
123. 123 Airaksinen, M.S., Panula, P., The histaminergic system in the guinea pig central nervous system: an immunocytochemical mapping study using an antiserum against histamine. J. Comp. Neurol. 273 (1988), 163–186.
124. 124 Inagaki, N., et al. Organization of histaminergic fibers in the rat brain. J. Comp. Neurol. 273 (1988), 283–300.
125. 125 Nambu, T., et al. Distribution of orexin neurons in the adult rat brain. Brain Res. 827 (1999), 243–260.
126. 126 Peyron, C., et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18 (1998), 9996–10015.
127. 127 Ciriello, J., Caverson, M.M., Hypothalamic orexin-A (hypocretin-1) neuronal projections to the vestibular complex and cerebellum in the rat. Brain Res. 1579 (2014), 20–34.
128. 128 Ikai, Y., et al. Dopaminergic and non-dopaminergic neurons in the ventral tegmental area of the rat project, respectively, to the cerebellar cortex and deep cerebellar nuclei. Neuroscience 51 (1992), 719–728.
129. 129 Melchitzky, D.S., Lewis, D.A., Tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in the primate cerebellum. Evidence for a lobular- and laminar-specific dopamine innervation. Neuropsychopharmacology 22 (2000), 466–472.
130. 130 Panagopoulos, N.T., Dopaminergic innervation and binding in the rat cerebellum. Neurosci. Lett. 130 (1991), 208–212.
131. 131 Hurley, M.J., et al. Markers for dopaminergic neurotransmission in the cerebellum in normal individuals and patients with Parkinson's disease examined by RT-PCR. Eur. J. Neurosci. 18 (2003), 2668–2672.
132. 132 Rath, M.F., et al. Circadian oscillators in the mouse brain: molecular clock components in the neocortex and cerebellar cortex. Cell Tissue Res. 357 (2014), 743–755.
133. 133 Honma, S., et al. Circadian oscillation of BMAL1, a partner of a mammalian clock gene clock, in rat suprachiasmatic nucleus. Biochem. Biophys. Res. Commun. 250 (1998), 83–87.
134. 134 Rath, M.F., et al. Circadian oscillations of molecular clock components in the cerebellar cortex of the rat. Chronobiol. Int. 29 (2012), 1289–1299.
135. 135 Mendoza, J., et al. The cerebellum harbors a circadian oscillator involved in food anticipation. J. Neurosci. 30 (2010), 1894–1904.
136. 136 Mordel, J., et al. The output signal of Purkinje cells of the cerebellum and circadian rhythmicity. PLoS One, 8, 2013, e58457.
137. 137 Cirelli, C., et al. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41 (2004), 35–43.
138. 138 Hasselmo, M.E., Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3 (1999), 351–359.
139. 139 Oudiette, D., Paller, K.A., Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn. Sci. 17 (2013), 142–149.
140. 140 Ji, D., Wilson, M.A., Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10 (2007), 100–107.
141. 141 Nádasdy, Z., et al. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19 (1999), 9497–9507.
142. 142 Yang, G., et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344 (2014), 1173–1178.
143. 143 Nagai, H., et al. Sleep Consolidates Motor Learning of Complex Movement Sequences in Mice. Sleep 40 (2017), 367–377.
144. 144 Tononi, G., Cirelli, C., Sleep function and synaptic homeostasis. Sleep Med. Rev. 10 (2006), 49–62.
145. 145 Nere, A., et al. Sleep-dependent synaptic down-selection (I): modeling the benefits of sleep on memory consolidation and integration. Front. Neurol., 4, 2013, 143.
146. 146 Tononi, G., Cirelli, C., Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81 (2014), 12–34.
147. 147 Vyazovskiy, V.V., et al. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 11 (2008), 200–208.
148. 148 de Vivo, L., et al. Ultrastructural evidence for synaptic scaling across the wake/sleep cycle. Science 355 (2017), 507–510.
149. 149 Gilestro, G.F., et al. Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324 (2009), 109–112.
150. 150 Wolpert, D.M., et al. Internal models in the cerebellum. Trends Cogn. Sci. 2 (1998), 338–347.
151. 151 Imamizu, H., et al. Cerebellar internal models: implications for the dexterous use of tools. Cerebellum 11 (2012), 325–335.
152. 152 Fischer, S., Motor memory consolidation in sleep shapes more effective neuronal representations. J. Neurosci. 25 (2005), 11248–11255.
153. 153 Passot, J.-B., et al. Coupling internal cerebellar models enhances online adaptation and supports offline consolidation in sensorimotor tasks. Front. Comput. Neurosci., 7, 2013, 95.
154. 154 Gray-Edwards, H.L., et al. High resolution MRI anatomy of the cat brain at 3Tesla. J. Neurosci. Methods 227 (2014), 10–17.
155. 155 Diedrichsen, J., et al. A probabilistic MR atlas of the human cerebellum. Neuroimage 46 (2009), 39–46.
156. 156 Walker, M.P., et al. Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133 (2005), 911–917.