Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle

PLoS Computational Biology

Volumn 11, Issue 5, 2015, Pages

  Blanco, Wilfredo ^a,b   Pereira, Catia M ^c   Cota, Vinicius R ^a,d   Souza, Annie C ^a   Rennó Costa, César ^a   Santos, Sharlene ^a   Dias, Gabriella ^a   Guerreiro, Ana M G ^a   Tort, Adriano B L ^a   Neto, Adrião D ^a   Ribeiro, Sidarta ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^b DEPARTAMENTO DE FÍSICA   (Brazil)

^c Edmond and Lily Safra International Institute of Neuroscience of Natal   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO JOÃO DEL REI   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CALCIUM COMPOUNDS; EYE MOVEMENTS; SLEEP RESEARCH; WAKES;

EXCITATORY NEURONS; EXPOSED TO; LONG-TERM POTENTIATIONS; MEMORY CONSOLIDATION; RAPID EYE MOVEMENT; SLEEP-WAKE CYCLES; SLOW WAVE; SYNAPTIC HOMEOSTASIS; SYNAPTIC PLASTICITY; SYNAPTIC WEIGHT;

RATS;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; NERVE CELL NETWORK; NONHUMAN; RAT; REM SLEEP; SLEEP WAKING CYCLE; SPIKE WAVE; SYNAPSE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; ELECTROPHYSIOLOGY; MEMORY CONSOLIDATION; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; PSYCHOLOGICAL MODEL; SLEEP; WAKEFULNESS; WISTAR RAT;

ANIMALIA; RATTUS;

ACTION POTENTIALS; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; ELECTROPHYSIOLOGICAL PHENOMENA; HIPPOCAMPUS; HOMEOSTASIS; LONG-TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MODELS, NEUROLOGICAL; MODELS, PSYCHOLOGICAL; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SLEEP; SLEEP, REM; WAKEFULNESS;

EID: 84930608393     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004241     Document Type: Article

References (81)

1. Steriade M, McCormick DA, Sejnowski TJ, Thalamocortical oscillations in the sleeping and aroused brain. Science. 1993; 262: 679–85. 8235588
2. Noda H, Manohar S, Adey WR, Spontaneous activity of cat hippocampal neurons in sleep and wakefulness. Exp Neurol. 1969; 24: 217–31. 4306533
3. Hobson JA, McCarley RW, Cortical unit activity in sleep and waking. Electroencephalogr and Clin Neurophysiol; 1971; 30: 97–112. 4100287
4. Olcese U, Esser SK, Tononi G, Sleep and synaptic renormalization: a computational study. J Neurophysiol. 2010; 104: 3476–3493. doi: 10.1152/jn.00593.2010 20926617
5. Walker MP, Stickgold R, Sleep, Memory, and Plasticity. Ann Rev Psychol. 2006; 57: 139–166.
6. Diekelmann S, Born J, The memory function of sleep. Nat Rev Neurosci. 2010; 11: 114–126. doi: 10.1038/nrn2762 20046194
7. Tononi G, Cirelli C, Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull. 2003; 62: 143–150. 14638388
8. Vyazovskiy VV, Cirelli C, Tononi G, Tobler I, Cortical metabolic rates as measured by 2-deoxyglucose-uptake are increased after waking and decreased after sleep in mice. Brain Res Bull. 2008; 75: 591–597. doi: 10.1016/j.brainresbull.2007.10.040 18355635
9. Tononi G, Cirelli C, Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration. Neuron. 2014; 81: 12–34. doi: 10.1016/j.neuron.2013.12.025 24411729
10. Nere A, Hashmi A, Cirelli C, Tononi G. Sleep-dependent synaptic down-selection (I): modeling the benefits of sleep on memory consolidation and integration. Front Neurolog. 2013.
11. Hebb DO, The Organization of Behavior: A Neuropsychological Theory: John Wiley & Sons; 1949.
12. Ribeiro S, Nicolelis MAL, Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem. 2004; 11:686–696. 15576886
13. Poe GR, Walsh CM, Bjorness TE, Kerkhof GA, van Dongen HPA, Cognitive neuroscience of sleep. In: Elsevier; 2010. pp. 1–19.
14. Ribeiro S, Goyal V, Mello CV, Pavlides C, Brain gene expression during REM sleep depends on prior waking experience. Learn Mem. 1999; 6: 500–508. 10541470
15. Ribeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, Pavlides C, Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J Neurosci. 2002; 22: 10914–10923. 12486186
16. Ulloor J, Datta S, Spatio-temporal activation of cyclic AMP response element-binding protein, activity-regulated cytoskeletal-associated protein and brain-derived nerve growth factor: a mechanism for pontine-wave generator activation-dependent two-way active-avoidance memory processing in the rat. J Neurochem. 2005; 95: 418–428. 16190868
17. Jha SK, Jones BE, Coleman T, Steinmetz N, Law C-T, Griffin G, et al. Sleep-dependent plasticity requires cortical activity. J Neurosci. 2005; 25: 9266–9274. 16207886
18. Donlea JM, Thimgan MS, Suzuki Y, Gottschalk L, Shaw PJ, Inducing Sleep by Remote Control Facilitates Memory Consolidation in Drosophila. Science. 2011; 332: 1571–1576. doi: 10.1126/science.1202249 21700877
19. Chauvette S, Seigneur J, Timofeev I, Sleep Oscillations in the Thalamocortical System Induce Long-Term Neuronal Plasticity. Neuron. 2012; 75: 1105–1113. doi: 10.1016/j.neuron.2012.08.034 22998877
20. Ribeiro S, Shi X, Engelhard M, Zhou Y, Zhang H, Gervasoni D, et al. Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front Neurosci. 2007.
21. Yang G, Lai CSW, Cichon J, Ma L, Li W, Gan W-B, Sleep promotes branch-specific formation of dendritic spines after learning. Science. 2014; 344: 1173–1178. doi: 10.1126/science.1249098 24904169
22. Ravassard P, Pachoud B, Comte J-C, Mejia-Perez C, Scoté-Blachon C, Gay N, et al. 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: 227–240. 19238810
23. Tononi G, Cirelli C, Sleep function and synaptic homeostasis. Sleep Med Rev. 2006; 10: 49–62. 16376591
24. Bushey D, Tononi G, Cirelli C, Sleep and synaptic homeostasis: structural evidence in Drosophila. Science. 2011; 332: 1576–1581. doi: 10.1126/science.1202839 21700878
25. Grosmark AD, Mizuseki K, Pastalkova E, Diba K, Buzsáki G, REM sleep reorganizes hippocampal excitability. Neuron. 2012; 75: 1001–1007. doi: 10.1016/j.neuron.2012.08.015 22998869
26. Cirelli C, Gutierrez CM, Tononi G, Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron. 2004; 41: 35–43. 14715133
27. Giuditta A, Ambrosini MV, Montagnese P, Mandile P, Cotugno M, Zucconi GG, et al. The sequential hypothesis of the function of sleep. Behav Brain Res. 1995; 69: 157–166. 7546307
28. Walker R, Russo V, Memory consolidation and forgetting during sleep: A neural network model. Neural Proc Lett. 2004; 19: 147–156.
29. Abraham WC, Robins A, Memory retention-the synaptic stability versus plasticity dilemma. Trends Neurosci. 2005; 28: 73–78. 15667929
30. Sejnowski TJ, Destexhe A, Why do we sleep? Brain Res. 2000; 886:208–23. 11119697
31. Ribeiro S, Gervasoni D, Soares ES, Zhou Y, Lin S-C, Pantoja J, et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2004; e24.
32. Calais JB, Ojopi EB, Morya E, Sameshima K, Ribeiro S, Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobio Learn Mem. 2015; 1: 002. http://dx.doi.org/10.1016/j.nlm.2015.01.002.
33. Ravassard P, Hamieh AM, Malleret G, Salin P-A, Paradoxical sleep: A vigilance state to gate long-term brain plasticity? Neurobio Learn Mem. 2014; 11: 013. http://dx.doi.org/10.1016/j.nlm.2014.11.013.
34. Silva AJ, Stevens CF, Tonegawa S, Wang Y, Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science. 1992; 257: 201–206. 1378648
35. Mayford M, Bach ME, Huang Y-Y, Wang L, Hawkins RD, Kandel ER, Control of memory formation through regulated expression of a CaMKII transgene. Science. 1996; 274: 1678–1683. 8939850
36. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R, Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 2009; 458: 299–304. doi: 10.1038/nature07842 19295602
37. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci. 2001; 4: 289–296. 11224546
38. Guzowski JF, Setlow B, Wagner EK, McGaugh JL, Experience-Dependent Gene Expression in the Rat Hippocampus after Spatial Learning: A Comparison of the Immediate-Early GenesArc, c-fos, and zif268. J Neurosci. 2001; 21: 5089–5098. 11438584
39. Gervasoni D, Lin SC, Ribeiro S, Soares ES, Pantoja J, Nicolelis MAL, Global forebrain dynamics predict rat behavioral states and their transitions. J Neurosci. 2004; 24: 11137–11147. 15590930
40. Vasconcelos N, Pantoja J, Belchior H, Caixeta FV, Faber J, Freire MAM, et al. Cross-modal responses in the primary visual cortex encode complex objects and correlate with tactile discrimination. PNAS USA. 2011; 108:15408–15413. doi: 10.1073/pnas.1102780108 21876148
41. Ribeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, Pavlides C, Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J Neurosci. 2002; 22: 10914–10923. 12486186
42. De Gennaro L, Ferrara M, Sleep spindles: an overview. Sleep Med Rev. 2003; 7: 423–440. 14573378
43. Gottesmann C, The transition from slow-wave sleep to paradoxical sleep: evolving facts and concepts of the neurophysiological processes underlying the intermediate stage of sleep. Neurosci & Biobehav Rev. 1996; 20: 367–387.
44. Ackley DH, Hinton GE, Sejnowski TJ, A learning algorithm for boltzmann machines. Cog Sci. 1985; 9: 147–169.
45. van Rossum MC, Bi GQ, Turrigiano GG, Stable Hebbian learning from spike timing-dependent plasticity. J Neurosci. 2000; 20: 8812–8821. 11102489
46. Debanne D, Gahwiler BH, Thompson SM, Synaptic and non-synaptic plasticity between individual pyramidal cells in the rat hippocampus in vitro. J Physiol-Paris. 1996; 90: 307–309. 9089497
47. Bi G-q, Poo M-m, Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type. J Neurosci. 1998; 18: 10464–10472. 9852584
48. Mello CV, Clayton DF, Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci. 1994; 14: 6652–6666. 7965067
49. Guzowski JF, McNaughton BL, Barnes CA, Worley PF, Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci. 1999; 2: 1120–1124. 10570490
50. de Almeida L, Idiart M, Lisman JE, A second function of gamma frequency oscillations: an E%-max winner-take-all mechanism selects which cells fire. J Neurosci. 2009; 29: 7497–7503. doi: 10.1523/JNEUROSCI.6044-08.2009 19515917
51. Rennó-Costa C, Lisman JE, Verschure PF, The mechanism of rate remapping in the dentate gyrus. Neuron. 2010; 68: 1051–1058. doi: 10.1016/j.neuron.2010.11.024 21172608
52. Rennó-Costa C, Lisman J, Verschure P, A Signature of Attractor Dynamics in the CA3 Region of the Hippocampus. PLoS Comp Biol. 2014; 10: e1003641. doi: 10.1371/journal.pcbi.1003641 24854425
53. Davis S, Bozon B, Laroche S, How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res. 2003; 142: 17–30. 12798262
54. Markram H, Lübke J, Frotscher M, Sakmann B, Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 1997; 275: 213–215. 8985014
55. Nádasdy Z, Hirase H, Czurkó A, Csicsvari J, Buzsáki G, Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999; 19: 9497–9507. 10531452
56. Karlsson MP, Frank LM, Awake replay of remote experiences in the hippocampus. Nat Neurosci. 2009; 12: 913–918. doi: 10.1038/nn.2344 19525943
57. Wilson MA, McNaughton BL, Reactivation of hippocampal ensemble memories during sleep. Science. 1994; 265: 676–679. 8036517
58. Steriade M, Timofeev I, Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron. 2003; 37: 563–576. 12597855
59. Lisman JE, A mechanism for memory storage insensitive to molecular turnover: a bistable autophosphorylating kinase. PNAS USA. 1985; 82: 3055–3057. 2986148
60. Lisman J, A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. PNAS USA. 1989; 86: 9574–9578. 2556718
61. Wang JH, Kelly PT, The balance between postsynaptic Ca (2+)-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn Mem. 1996; 3: 170–181. 10456087
62. Lisman J, Schulman H, Cline H, The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 2002; 3: 175–190. 11994750
63. Murakoshi H, Yasuda R, Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci. 2012; 35: 135–143. doi: 10.1016/j.tins.2011.12.002 22222350
64. Murakoshi H, Wang H, Yasuda R, Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature. 2011; 472: 100–104. doi: 10.1038/nature09823 21423166
65. Siapas AG, Wilson MA, Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron. 1998; 21: 1123–1128. 9856467
66. Gais S, Mölle M, Helms K, Born J, Learning-dependent increases in sleep spindle density. J Neurosci. 2002; 22: 6830–6834. 12151563
67. Mölle M, Marshall L, Gais S, Born J, Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. PNAS USA. 2004; 101: 13963–13968. 15356341
68. Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G, et al. Sleep spindle‐related activity in the human EEG and its relation to general cognitive and learning abilities. Euro J Neurosci. 2006; 23: 1738–17346. 16623830
69. Sirota A, Csicsvari J, Buhl D, Buzsáki G, Communication between neocortex and hippocampus during sleep in rodents. PNAS USA. 2003; 100: 2065–2069. 12576550
70. Stickgold R, Scott L, Rittenhouse C, Hobson JA, Sleep-Induced Changes in Associative Memory. J Cog Neurosci. 1999; 11: 182–193.
71. Stickgold R, Sleep-dependent memory consolidation. Nature. 2005; 437: 1272–1278. 16251952
72. Born J, Rasch B, Gais S, Sleep to remember. Neuroscientist. 2006; 12: 410–424. 16957003
73. Rasch B, Buchel C, Gais S, Born J, Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007; 315: 1426–1429. 17347444
74. Wagner U, Gais S, Born J, Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem. 2001; 8: 112–119 11274257
75. Payne JD, Stickgold R, Swanberg K, Kensinger EA, Sleep preferentially enhances memory for emotional components of scenes. Psychol Sci. 2008; 19: 781–788. doi: 10.1111/j.1467-9280.2008.02157.x 18816285
76. Hu P, Stylos-Allan M, Walker MP, Sleep facilitates consolidation of emotional declarative memory. Psychol Sci. 2006; 17: 891–898. 17100790
77. Wagner U, Gais S, Haider H, Verleger R, Born J, Sleep inspires insight. Nature. 2004; 427: 352–355. 14737168
78. Wilhelm I, Diekelmann S, Molzow I, Ayoub A, Molle M, Born J, Sleep selectively enhances memory expected to be of future relevance. J Neurosci. 2011; 31: 1563–1569. doi: 10.1523/JNEUROSCI.3575-10.2011 21289163
79. Saletin JM, Goldstein AN, Walker MP, The role of sleep in directed forgetting and remembering of human memories. Cereb Cortex. 2011; 21: 2534–2541. doi: 10.1093/cercor/bhr034 21459838
80. Hashmi A, Nere A, Tononi G, Sleep-dependent synaptic down-selection (II): Single-neuron level benefits for matching, selectivity, and specificity. Front Neurol. 2013; 4: 148. doi: 10.3389/fneur.2013.00148 24151486
81. McDevitt EA, Duggan KA, Mednick SC, REM sleep rescues learning from interference. Neurobio Learn Mem. 2014. 11: 015 http://dx.doi.org/10.1016/j.nlm.2014.11.015.