The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators (original) (raw)

References

1. Metherate, R., Cox, C.L. & Ashe, J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701–4711 (1992).
   Article CAS PubMed PubMed Central Google Scholar
2. Steriade, M., Nuñez, A. & Amzica, F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3253–3265 (1993).
   Google Scholar
3. Steriade, M., Nuñez, A. & Amzica, F. Intracellular analysis between slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266–3283 (1993).
   CAS PubMed PubMed Central Google Scholar
4. Steriade, M., Contreras, D., Curró Dossi, R. & Nuñez, A. The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J. Neurosci. 13, 3284–3299 (1993).
   CAS PubMed PubMed Central Google Scholar
5. Achermann, P. & Borbély, A. Low-frequency (<1 Hz) oscillations in the human sleep EEG. Neuroscience 81, 213–222 (1997).
   CAS PubMed Google Scholar
6. Cash, S.S. et al. The human K-complex represents an isolated cortical down-state. Science 324, 1084–1087 (2009).
   CAS PubMed PubMed Central Google Scholar
7. Greenberg, D.S., Houweling, A.R. & Kerr, J.N.D. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 11, 749–751 (2008).
   CAS PubMed Google Scholar
8. Kerr, J.N.D., Greenberg, D. & Helmchen, F. Imaging input and output of neocortical networks in vivo. Proc. Natl. Acad. Sci. USA 102, 14063–14068 (2005).
   CAS PubMed PubMed Central Google Scholar
9. Luczak, A., Barthó, P., Marguet, S.L., Buzsáki, G. & Harris, K.D. Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl. Acad. Sci. USA 104, 347–352 (2007).
   CAS PubMed Google Scholar
10. Massimini, M., Huber, R., Ferrarelli, F., Hill, S. & Tononi, G. The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862–6870 (2004).
    CAS PubMed PubMed Central Google Scholar
11. Petersen, C.C.H., Hahn, T.T.G., Mehta, M., Grinvald, A. & Sakmann, B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. USA 100, 13638–13643 (2003).
    Article CAS PubMed PubMed Central Google Scholar
12. Puig, M.V., Ushimaru, M. & Kawaguchi, Y. Two distinct activity patterns of fast-spiking interneurons during neocortical UP states. Proc. Natl. Acad. Sci. USA 105, 8428–8433 (2008).
    CAS PubMed PubMed Central Google Scholar
13. Simon, N.R., Kemp, B., Manshanden, I. & Lopes da Silva, F.H. Whole-head measures of sleep from MEG signals and the ubiquitous “slow oscillation”. Sleep Res. Online 5, 105–113 (2003).
    Google Scholar
14. Volgushev, M., Chauvette, S., Mukovski, M. & Timofeev, I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave sleep. J. Neurosci. 26, 5665–5672 (2006).
    CAS PubMed PubMed Central Google Scholar
15. Blethyn, K.L., Hughes, S.W., Tóth, T.I., Cope, D.W. & Crunelli, V. Neuronal basis of the slow (<1Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J. Neurosci. 26, 2474–2486 (2006).
    CAS PubMed PubMed Central Google Scholar
16. Cossart, R., Aronov, D. & Yuste, R. Attractor dynamics of network UP states in the neocortex. Nature 423, 283–288 (2003).
    CAS PubMed Google Scholar
17. Dang-Vu, T.T. et al. Spontaneous neural activity during human slow wave sleep. Proc. Natl. Acad. Sci. USA 105, 15160–15165 (2008).
    PubMed PubMed Central Google Scholar
18. Hughes, S.W., Cope, D.W., Blethyn, K.L. & Crunelli, V. Cellular mechanisms of the slow (<1 Hz) oscillation in thalamocortical neurons in vitro. Neuron 33, 947–958 (2002).
    CAS PubMed Google Scholar
19. MacLean, J.N., Watson, B.O., Aaron, G.B. & Yuste, R. Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48, 811–823 (2005).
    CAS PubMed Google Scholar
20. Rigas, P. & Castro-Alamancos, M.A. Thalamocortical Up states: different effects of intrinsic and extrinsic cortical inputs on persistent activity. J. Neurosci. 27, 4261–4272 (2007).
    CAS PubMed PubMed Central Google Scholar
21. Reig, R., Gallego, R., Nowak, L.G. & Sanchez-Vives, M.V. Impact of cortical network activity on short-term synaptic depression. Cereb. Cortex 16, 688–695 (2006).
    PubMed Google Scholar
22. Sanchez-Vives, M.V. & McCormick, D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).
    CAS PubMed Google Scholar
23. Shu, Y., Hasenstaub, A. & McCormick, D.A. Turning on and off recurrent balanced cortical activity. Nature 423, 288–293 (2003).
    CAS PubMed Google Scholar
24. 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. 11, 200–208 (2008).
    CAS PubMed Google Scholar
25. Wolansky, T., Clement, E.A., Peters, S.R., Palczak, M.A. & Dickson, C.T. Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J. Neurosci. 26, 6213–6229 (2006).
    CAS PubMed PubMed Central Google Scholar
26. De Gennaro, L. et al. Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. PLoS One 3, e2483 (2008).
    PubMed PubMed Central Google Scholar
27. Huber, R., Ghilardi, M.F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78–81 (2004).
    CAS PubMed Google Scholar
28. Huber, R. et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci. 9, 1169–1176 (2006).
    CAS PubMed Google Scholar
29. Ji, D. & Wilson, M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100–107 (2007).
    CAS PubMed Google Scholar
30. Marshall, L., Helgadóttir, H., Mölle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006).
    CAS PubMed Google Scholar
31. Massimini, M., Rosanova, M. & Mariotti, M. EEG slow (approximately 1 Hz) waves are associated with nonstationarity of thalamo-cortical sensory processing in the sleeping human. J. Neurophysiol. 89, 1205–1213 (2003).
    PubMed Google Scholar
32. Mölle, M., Marshall, L., Gais, S. & Born, J. Learning increases human electro-encephalographic coherence during subsequent slow sleep oscillations. Proc. Natl. Acad. Sci. USA 101, 13963–13968 (2004).
    PubMed PubMed Central Google Scholar
33. Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535–545 (2004).
    CAS PubMed Google Scholar
34. Contreras, D. & Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 15, 604–622 (1995).
    CAS PubMed PubMed Central Google Scholar
35. Doi, A. et al. Slow oscillation of membrane currents mediated by glutamatergic inputs of rat somatosensory cortical neurons: in vivo patch-clamp analysis. Eur. J. Neurosci. 26, 2565–2575 (2007).
    PubMed Google Scholar
36. Hughes, S.W., Cope, D.W., Tóth, T.I., Williams, S.R. & Crunelli, V. All thalamocortical neurones possess a T-type Ca2+ 'window' current that enables the expression of bistability-mediated activities. J. Physiol. (Lond.) 517, 805–815 (1999).
    CAS Google Scholar
37. Zhu, L. et al. Nucleus- and species-specific properties of the slow (<1 Hz) sleep oscillation in thalamocortical neurons. Neuroscience 141, 621–636 (2006).
    CAS PubMed Google Scholar
38. Amzica, F. & Steriade, M. The functional significance of K-complexes. Sleep Med. Rev. 6, 139–149 (2002).
    PubMed Google Scholar
39. De Gennaro, L. & Ferrara, M. Sleep spindles: an overview. Sleep Med. Rev. 7, 423–440 (2003).
    PubMed Google Scholar
40. Hoffman, K.L. et al. The upshot of Up states in the neocortex: from slow oscillations to memory formation. J. Neurosci. 27, 11838–11841 (2007).
    CAS PubMed PubMed Central Google Scholar
41. Mehta, M.R. Cortico-hippocampal interation during up-down states and memory consolidation. Nat. Neurosci. 10, 13–15 (2007).
    CAS PubMed Google Scholar
42. Tononi, G., Massimini, M. & Riedner, B.A. Sleepy dialogues between cortex and hippocampus: who talks to whom? Neuron 52, 748–749 (2006).
    CAS PubMed Google Scholar
43. Yuste, R., MacLean, J.N., Smith, J. & Lansner, A. The cortex as a central pattern generator. Nat. Rev. Neurosci. 6, 477–483 (2005).
    CAS PubMed Google Scholar
44. Simon, N.R., Manshanden, I. & Lopes da Silva, F.H.A. MEG study of sleep. Brain Res. 860, 64–76 (2000).
    CAS PubMed Google Scholar
45. Amzica, F. & Steriade, M. The K-complex: its slow rhythmicity and relation to delta waves. Neurology 49, 952–959 (1997).
    CAS PubMed Google Scholar
46. Mölle, M., Marshall, L., Gais, S. & Born, J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 22, 10941–10947 (2002).
    PubMed PubMed Central Google Scholar
47. Amzica, F. & Steriade, M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience 82, 671–686 (1998).
    CAS PubMed Google Scholar
48. 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. 19, 4595–4608 (1999).
    CAS PubMed PubMed Central Google Scholar
49. Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985 (2001).
    CAS PubMed Google Scholar
50. Krueger, J.M. et al. Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9, 910–919 (2008).
    CAS PubMed PubMed Central Google Scholar
51. Siegel, J.M. Do all animals sleep? Trends Neurosci. 31, 208–213 (2008).
    CAS PubMed PubMed Central Google Scholar
52. Bokor, H. et al. Selective GABAergic control of higher-order thalamic relays. Neuron 45, 929–940 (2005).
    CAS PubMed Google Scholar
53. Contreras, D. & Steriade, M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J. Physiol. (Lond.) 490, 159–179 (1996).
    CAS Google Scholar
54. Contreras, D. & Steriade, M. Synchronization of low-frequency rhythms in corticothalamic networks. Neuroscience 76, 11–24 (1997).
    CAS PubMed Google Scholar
55. Contreras, D. & Steriade, M. State-dependent fluctuations of low-frequency rhythms in corticothalamic networks. Neuroscience 76, 25–38 (1997).
    CAS PubMed Google Scholar
56. Haider, B., Duque, A., Hasenstaub, A.R. & McCormick, D.A. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26, 4535–4545 (2006).
    CAS PubMed PubMed Central Google Scholar
57. Rudolph, M., Pospischil, M., Timofeev, I. & Destexhe, A. Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J. Neurosci. 27, 5280–5290 (2007).
    CAS PubMed PubMed Central Google Scholar
58. Steriade, M. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb. Cortex 7, 583–604 (1997).
    CAS PubMed Google Scholar
59. Steriade, M. Cellular substrates of brain rhythms. in Electroencephalography: Basic Principles, Clinical Applications, and Related Fields (eds, E. Niedermeyer & F. Lopes da Silva) 27–62 (Williams and Wilkins, Baltimore, 1993).
60. Timofeev, I. & Steriade, M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76, 4152–4168 (1996).
    CAS PubMed Google Scholar
61. Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T.J. & Steriade, M. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10, 1185–1199 (2000).
    CAS PubMed Google Scholar
62. Amzica, F. & Steriade, M. Disconnection of synaptic linkages disrupts synchronization of a slow oscillation. J. Neurosci. 15, 4658–4677 (1995).
    CAS PubMed PubMed Central Google Scholar
63. Bazhenov, M., Timofeev, I., Steriade, M. & Sejnowski, T.J. Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22, 8691–8704 (2002).
    CAS PubMed PubMed Central Google Scholar
64. Compte, A., Sanchez-Vives, M.V., McCormick, D.A. & Wang, X.-J. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J. Neurophysiol. 89, 2707–2725 (2003).
    PubMed Google Scholar
65. Hill, S. & Tononi, G. Modeling sleep and wakefulness in the thalamocortical system. J. Neurophysiol. 93, 1671–1698 (2005).
    PubMed Google Scholar
66. Le Bon-Jego, M. & Yuste, R. Persistently active, pacemaker-like neurons in neocortex. Front. Neurosci. 1, 123–129 (2007).
    PubMed PubMed Central Google Scholar
67. Cunningham, M.O. et al. Neuronal metabolism governs cortical network response state. Proc. Natl. Acad. Sci. USA 103, 5597–5601 (2006).
    CAS PubMed PubMed Central Google Scholar
68. Steriade, M., Timofeev, I., Grenier, F. & Dürmüller, N. Role of thalamic and cortical neurons in augmenting responses and self-sustained activity: dual intracellular recordings in vivo. J. Neurosci. 18, 6425–6443 (1998).
    CAS PubMed PubMed Central Google Scholar
69. Swadlow, H.A. & Gusev, A.G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat. Neurosci. 4, 402–408 (2001).
    CAS PubMed Google Scholar
70. Williams, S.R., Turner, J.P., Tóth, T.I., Hughes, S.W. & Crunelli, V. The 'window' component of the low threshold Ca2+ current produces input signal amplification and bistability in cat and rat thalamocortical neurones. J. Physiol. (Lond.) 505, 689–705 (1997).
    CAS Google Scholar
71. Sherman, S.M. & Guillery, R.W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).
    CAS PubMed Google Scholar
72. Llinás, R.R. & Steriade, M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297–3308 (2006).
    PubMed Google Scholar
73. Godwin, D.W., Van Horn, S.C., Sesma, M., Romano, C. & Sherman, S.M. Ultrastructural localization suggests that retinal and cortical inputs access different metabotropic glutamate receptors in the lateral geniculate nucleus. J. Neurosci. 16, 8181–8192 (1996).
    CAS PubMed PubMed Central Google Scholar
74. Turner, J.P. & Salt, T.E. Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurones in vitro. J. Physiol. (Lond.) 510, 829–843 (1998).
    CAS Google Scholar
75. Steriade, M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087–1106 (2006).
    CAS PubMed Google Scholar
76. Hughes, S.W. et al. Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. Neuron 42, 253–268 (2004).
    CAS PubMed Google Scholar
77. Cox, C.L., Reichova, I. & Sherman, S.M. Functional synaptic contacts by intranuclear axon collaterals of thalamic relay neurons. J. Neurosci. 23, 7642–7646 (2003).
    CAS PubMed PubMed Central Google Scholar
78. Cox, C.L. & Sherman, S.M. Control of dendritic outputs of inhibitory interneurons in the lateral geniculate nucleus. Neuron. 27, 597–610 (2000).
    CAS PubMed Google Scholar
79. Soltesz, I. & Crunelli, V. A role for low-frequency, rhythmic synaptic potentials in the synchronization of cat thalamocortical cells. J. Physiol. (Lond.) 457, 257–276 (1992).
    CAS Google Scholar
80. Lõrincz, M.L., Kékesi, K.A., Juhász, G., Crunelli, V. & Hughes, S.W. Temporal framing of thalamic relay-mode firing by phasic inhibition during the alpha rhythm. Neuron 63, 683–696 (2009).
    PubMed PubMed Central Google Scholar
81. Hughes, S.W., Blethyn, K.L., Cope, D.W. & Crunelli, V. Properties and origin of spikelets in thalamocortical neurones in vitro. Neuroscience 110, 395–401 (2002).
    CAS PubMed Google Scholar
82. Tóth, T.I., Hughes, S.W. & Crunelli, V. Analysis and biophysical interpretation of bistable behaviour in thalamocortical neurons. Neuroscience 87, 519–523 (1998).
    PubMed Google Scholar
83. Crunelli, V., Tóth, T.I., Cope, D.W., Blethyn, K. & Hughes, S.W. The 'window' T-type calcium current in brain dynamics of different behavioral states. J. Physiol. (Lond.) 562, 121–129 (2005).
    CAS Google Scholar
84. Crunelli, V., Cope, D.W. & Hughes, S.W. Thalamic T-type Ca2+ channels and NREM sleep. Cell Calcium 40, 175–190 (2006).
    CAS PubMed PubMed Central Google Scholar
85. McCormick, D.A. & von Krosigk, M. Corticothalamic activation modulates thalamic firing through glutamate 'metabotropic' receptors. Proc. Natl. Acad. Sci. USA 89, 2774–2778 (1992).
    CAS PubMed PubMed Central Google Scholar
86. Turner, J.P. & Salt, T.E. Synaptic activation of the group I metabotropic glutamate receptor mGlu1 on the thalamocortical neurons of the rat dorsal lateral geniculate nucleus in vitro. Neuroscience 100, 493–505 (2000).
    CAS PubMed Google Scholar
87. Beierlein, M., Fall, C.P., Rinzel, J. & Yuste, R. Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J. Neurosci. 22, 9885–9894 (2002).
    CAS PubMed PubMed Central Google Scholar
88. McCormick, D.A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39, 337–388 (1992).
    CAS PubMed Google Scholar
89. Destexhe, A., Hughes, S.W., Rudolph, M. & Crunelli, V. Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci. 30, 334–342 (2007).
    CAS PubMed PubMed Central Google Scholar
90. Isomura, Y. et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52, 871–882 (2006).
    CAS PubMed Google Scholar
91. Lee, A.K. & Wilson, M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).
    CAS PubMed Google Scholar
92. Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J. & Buzsáki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).
    PubMed PubMed Central Google Scholar
93. Sirota, A., Csicsvari, J., Buhl, D. & Buzsáki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA 100, 2065–2069 (2003).
    CAS PubMed PubMed Central Google Scholar
94. Jones, E.G. The Thalamus (Plenum Press, New York, 2008).
95. Cueni, L. et al. T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat. Neurosci. 11, 683–692 (2008).
    CAS PubMed Google Scholar
96. Czarnecki, A., Birtoli, B. & Ulrich, D. Cellular mechanisms of burst firing–mediated long-term depression in rat neocortical pyramidal cells. J. Physiol. (Lond.) 578, 471–479 (2007).
    CAS Google Scholar
97. Stern, E.A., Kincaid, A.E. & Wilson, C.J. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697–1715 (1997).
    CAS PubMed Google Scholar
98. Mena-Segovia, J., Sims, H.M., Magill, P.J. & Bolam, J.P. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol. (Lond.) 586, 2947–2960 (2008).
    CAS Google Scholar
99. Jones, B.E. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol. Sci. 26, 578–586 (2005).
    CAS PubMed Google Scholar
100. Steriade, M., Contreras, D., Amzica, F. & Timofeev, I. Synchronization of fast (30–40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J. Neurosci. 16, 2788–2808 (1996).
     CAS PubMed PubMed Central Google Scholar

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