Large-scale functional brain networks in human non-rapid eye movement sleep: Insights from combined electroencephalographic/functional magnetic resonance imaging studies

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 369, Issue 1952, 2011, Pages 3708-3729

  Spoormaker, Victor I ^a   Czisch, Michael ^a   Maquet, Pierre ^b   Jäncke, Lutz ^c  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Functional connectivity; Graph theory; Non rapid eye movement sleep; Plasticity; Small world; Spindle

Indexed keywords

BRAIN; DATA PROCESSING; FUNCTIONAL POLYMERS; GRAPH THEORY; MAGNETIC RESONANCE IMAGING; RESONANCE; SLEEP RESEARCH;

BODY OF KNOWLEDGE; BRAIN ACTIVITY; BRAIN NETWORKS; BRAIN PLASTICITY; EXPERIMENTAL STUDIES; FUNCTIONAL CONNECTIVITY; LOW FREQUENCY; MOTOR SKILLS; NEURAL CORRELATE; NON-RAPID EYE MOVEMENTS; SLEEP STAGE; SLOW WAVE; SMALL WORLDS; SPINDLE;

EYE MOVEMENTS;

BRAIN; ELECTROENCEPHALOGRAPHY; HISTOLOGY; HUMAN; METHODOLOGY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; REVIEW; SLEEP STAGE;

BRAIN; ELECTROENCEPHALOGRAPHY; HUMANS; MAGNETIC RESONANCE IMAGING; NERVE NET; NEURONAL PLASTICITY; SLEEP STAGES;

EID: 80054993916     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2011.0078     Document Type: Review

References (146)

1. Steriade, M. & McCarley, R. W. 2005 Brain control of wakefulness and sleep. New York, NY: Kluwer Academic.
2. Achermann, P. & Borbely, A. A. 2003 Mathematical models of sleep regulation. Front. Biosci. 8, S683-S693. (doi:10.2741/1064) (Pubitemid 39140188)
3. Dijk, D. J. & Lockley, S. W. 2002 Integration of human sleep-wake regulation and circadian rhythmicity. J. Appl. Physiol. 92, 852-862. (Pubitemid 34671057)
4. Massimini, M., Tononi, G. & Huber, R. 2009 Slow waves, synaptic plasticity and information processing: insights from transcranial magnetic stimulation and high-density EEG experiments. Eur. J. Neurosci. 29, 1761-1770. (doi:10.1111/j.1460-9568.2009.06720.x)
5. Czisch, M., Wehrle, R., Kaufmann, C., Wetter, T. C., Holsboer, F., Pollmächer, T. & Auer, D. P. 2004 Functional MRI during sleep: BOLD signal decreases and their electrophysiological correlates. Eur. J. Neurosci. 20, 566-574. (doi:10.1111/j.1460-9568.2004.03518.x) (Pubitemid 38969642)
6. Dang-Vu, T. T. et al. 2008 Spontaneous neural activity during human slow wave sleep. Proc. Natl Acad. Sci. USA 105, 15 160-15 165. (doi:10.1073/pnas. 0801819105)
7. Schabus, M. et al. 2007 Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl Acad. Sci. USA 104, 13 164-13 169. (doi:10.1073/pnas. 0703084104)
8. Manshanden, I., De Munck, J. C., Simon, N. R. & Lopes da Silva, F. H. 2002 Source localization of MEG sleep spindles and the relation to sources of alpha band rhythms. Clin. Neurophysiol. 113, 1937-1947. (doi:10.1016/S1388- 2457(02)00304-8) (Pubitemid 35441061)
9. Ioannides, A. A. et al. 2004 MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades. Cereb. Cortex 14, 56-72. (doi:10.1093/cercor/bhg091) (Pubitemid 38018054)
10. He, B. J., Snyder, A. Z., Zempel, J. M., Smyth, M. D. & Raichle, M. E. 2008 Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc. Natl Acad. Sci. USA 105, 16 039-16 044. (doi:10.1073/pnas.0807010105)
11. He, B. J., Zempel, J. M., Snyder, A. Z. & Raichle, M. E. 2010 The temporal structures and functional significance of scale-free brain activity. Neuron 66, 353-369. (doi:10.1016/j.neuron. 2010.04.020)
12. Watts, D. J. & Strogatz, S. H. 1998 Collective dynamics of 'small-world' networks. Nature 393, 440-442. (doi:10.1038/30918) (Pubitemid 28292183)
13. Steriade, M., Nunez, A. & Amzica, F. 1993 A novel slow (>1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252-3265. (Pubitemid 23241166)
14. Steriade, M., Timofeev, I. & Grenier, F. 2001 Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969-1985. (Pubitemid 32440676)
15. Steriade, M., Nunez, A. & Amzica, F. 1993 Intracellular analysis of relations between the slow (>1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266-3283. (Pubitemid 23241167)
16. Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T. J. & Steriade, M. 2000 Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10, 1185-1199. (doi:10.1093/cercor/10.12.1185)
17. Sanchez-Vives, M. V. & McCormick, D. A. 2000 Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034. (doi:10.1038/79848)
18. Crunelli, V. & Hughes, S. W. 2009 The slow (>1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci. 13, 9-17. (doi:10.1038/nn.2445)
19. Achermann, P. & Borbely, A. A. 1997 Low-frequency (>1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81, 213-222. (doi:10.1016/S0306-4522(97)00186-3) (Pubitemid 27373640)
20. Molle, M., Marshall, L., Gais, S. & Born, J. 2002 Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 22, 10 941-10 947.
21. Massimini, M., Huber, R., Ferrarelli, F., Hill, S. & Tononi, G. 2004 The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862-6870. (doi:10.1523/JNEUROSCI.1318-04.2004) (Pubitemid 39045442)
22. Borbely, A. A. 2001 From slow waves to sleep homeostasis: new perspectives. Arch. Ital. Biol. 139, 53-61. (Pubitemid 32158401)
23. Rechtschaffen, A. & Kales, A. 1968 A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. University of California, Los Angeles: Brain Information Service/Brain Research Institute.
24. Esser, S. K., Hill, S. L. & Tononi, G. 2007 Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 30, 1617-1630 (Pubitemid 350234741)
25. Vyazovskiy, V. V., Olcese, U., Lazimy, Y. M., Faraguna, U., Esser, S. K., Williams, J. C., Cirelli, C. & Tononi, G. 2009 Cortical firing and sleep homeostasis. Neuron 63, 865-878. (doi:10.1016/j.neuron.2009.08.024)
26. Finelli, L. A., Borbely, A. A. & Achermann, P. 2001 Functional topography of the human nonREM sleep electroencephalogram. Eur. J. Neurosci. 13, 2282-2290. (doi:10.1046/j.0953-816x.2001.01597.x) (Pubitemid 32664313)
27. Dang-Vu, T. T., Desseilles, M., Laureys, S., Degueldre, C., Perrin, F., Phillips, C., Maquet, P. & Peigneux, P. 2005 Cerebral correlates of delta waves during non-REM sleep revisited. Neuroimage 28, 14-21. (doi:10.1016/j. neuroimage.2005.05.028) (Pubitemid 41393883)
28. Mena-Segovia, J., Sims, H. M., Magill, P. J. & Bolam, J. P. 2008 Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol. 586, 2947-2960. (doi:10.1113/jphysiol.2008.153874) (Pubitemid 351837287)
29. Yeshenko, O., Moelle, M., Marshall, L., Born, J. & Sara, S. 2006 Locus coeruleus firing during SWS is time locked to slow oscillations: possible contribution of the noradrenergic system to off-line information processing in rats. J. Sleep Res. 15(Suppl. 1), 11.
30. Destexhe, A., Hughes, S. W., Rudolph, M. & Crunelli, V. 2007 Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci. 30, 334-342. (doi:10.1016/j.tins.2007.04.006) (Pubitemid 46991116)
31. Murphy, M., Riedner, B. A., Huber, R., Massimini, M., Ferrarelli, F. & Tononi, G. 2009 Source modeling sleep slow waves. Proc. Natl Acad. Sci. USA 106, 1608-1613. (doi:10.1073/pnas.0807933106)
32. De Gennaro, L. & Ferrara, M. 2003 Sleep spindles: an overview. Sleep Med. Rev. 7, 423-440. (doi:10.1053/smrv.2002.0252) (Pubitemid 37221986)
33. Bodizs, R., Kis, T., Lazar, A. S., Havran, L., Rigo, P., Clemens, Z. & Halász, P. 2005 Prediction of general mental ability based on neural oscillation measures of sleep. J. Sleep Res. 14, 285-292. (doi:10.1111/j.1365-2869.2005.00472.x) (Pubitemid 41291313)
34. Schabus, M. 2009 Still missing some significant ingredients. Sleep 32, 291-293.
35. Doran, S. 2003 The dynamic topography of individual sleep spindles. Sleep Res. Online 5, 133-139. (Pubitemid 38972316)
36. Anderer, P., Klosch, G., Gruber, G., Trenker, E., Pascual-Marqui, R. D., Zeitlhofer, J., Barbanoj, M. J., Rappelsberger, P. & Saletu, B. 2001 Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 103, 581-592. (doi:10.1016/S0306-4522(01)00028-8) (Pubitemid 32239328)
37. Hofle, N., Paus, T., Reutens, D., Fiset, P., Gotman, J., Evans, A. C. & Jones, B. E. 1997 Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 17, 4800-4808. (Pubitemid 27246935)
38. Dehghani, N., Cash, S. S., Rossetti, A. O., Chen, C. C. & Halgren, E. 2010 Magnetoencephalography demonstrates multiple asynchronous generators during human sleep spindles. J. Neurophysiol. 104, 179-188. (doi:10.1152/jn. 00198.2010)
39. Fox, M. D. & Raichle, M. E. 2007 Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. (doi:10.1038/nrn2201) (Pubitemid 47283145)
40. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C. & Raichle, M. E. 2005 The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl Acad. Sci. USA 102, 9673-9678. (doi:10.1073/pnas.0504136102) (Pubitemid 40981739)
41. Biswal, B., Yetkin, F. Z., Haughton, V. M. & Hyde, J. S. 1995 Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. (doi:10.1002/mrm.1910340409)
42. Beckmann, C. F., DeLuca, M., Devlin, J. T. & Smith, S. M. 2005 Investigations into resting-state connectivity using independent component analysis. Phil. Trans. R. Soc. B 360, 1001-1013. (doi:10.1098/rstb.2005.1634) (Pubitemid 41672861)
43. Damoiseaux, J. S., Rombouts, S. A. R. B., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M. & Beckmann, C. F. 2006 Consistent resting-state networks across healthy subjects. Proc. Natl Acad. Sci. USA 103, 13848-13853. (doi:10.1073/pnas.0601417103) (Pubitemid 44413996)
44. Larson-Prior, L. J., Zempel, J. M., Nolan, T. S., Prior, F. W., Snyder, A. Z. & Raichle, M. E. 2009 Cortical network functional connectivity in the descent to sleep. Proc. Natl Acad. Sci. USA 106, 4489-4494. (doi:10.1073/pnas. 0900924106)
45. Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D. L. 2008 The brain's default network: anatomy, function, and relevance to disease. Ann. NY Acad. Sci. 1124, 1-38. (doi:10.1196/annals.1440.011) (Pubitemid 351506788)
46. Andrews-Hanna, J. R., Reidler, J. S., Huang, C. & Buckner, R. L. 2010 Evidence for the default network's role in spontaneous cognition. J. Neurophysiol. 104, 322-335. (doi:10.1152/jn.00830.2009)
47. Boly, M. et al. 2008 Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann. NY Acad. Sci. 1129, 119-129. (doi:10.1196/annals.1417.015) (Pubitemid 351990285)
48. Greicius, M. D., Flores, B. H., Menon, V., Glover, G. H., Solvason, H. B., Kenna, H., Reiss, A. L. & Schatzberg, A. F. 2007 Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 62, 429-437. (doi:10.1016/j.biopsych.2006.09.020) (Pubitemid 47284017)
49. Greicius, M. D., Srivastava, G., Reiss, A. L. & Menon, V. 2004 Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl Acad. Sci. USA 101, 4637-4642. (doi:10.1073/pnas.0308627101) (Pubitemid 38437463)
50. Horovitz, S. G., Fukunaga, M., de Zwart, J. A., van Gelderen, P., Fulton, S. C., Balkin, T. J. & Duyn, J. H. 2008 Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum. Brain Mapp. 29, 671-682. (doi:10.1002/hbm.20428) (Pubitemid 351794122)
51. Picchioni, D., Fukunaga, M., Carr, W. S., Braun, A. R., Balkin, T. J., Duyn, J. H. & Horovitz, S. G. 2008 fMRI differences between early and late stage-1 sleep. Neurosci. Lett. 441, 81-85. (doi:10.1016/j.neulet.2008.06.010)
52. Sämann, P. G., Wehrle, R., Hoehn, D., Spoormaker, V. I., Peters, H., Tully, C., Holsboer, F. & Czisch, M. In press. Development of the brain's default mode network from wakefulness to slow wave sleep. Cereb. Cortex. (doi:10.1093/cercor/bhq295)
53. Ferri, R., Rundo, F., Bruni, O., Terzano, M. G. & Stam, C. J. 2007 Small-world network organization of functional connectivity of EEG slow-wave activity during sleep. Clin. Neurophysiol. 118, 449-456. (doi:10.1016/j.clinph. 2006.10.021) (Pubitemid 46038825)
54. Ferri, R., Rundo, F., Bruni, O., Terzano, M. G. & Stam, C. J. 2008 The functional connectivity of different EEG bands moves towards small-world network organization during sleep. Clin. Neurophysiol. 119, 2026-2036. (doi:10.1016/j.clinph.2008.04.294)
55. Dimitriadis, S. I., Laskaris, N. A., Del Rio-Portilla, Y. & Koudounis, G. 2009 Characterizing dynamic functional connectivity across sleep stages from EEG. Brain Topogr. 22, 119-133. (doi:10.1007/s10548-008-0071-4)
56. Horovitz, S. G., Braun, A. R., Carr, W. S., Picchioni, D., Balkin, T. J., Fukunaga, M. & Duyn, J. H. 2009 Decoupling of the brain's default mode network during deep sleep. Proc. Natl Acad. Sci. USA 106, 11376-11 381. (doi:10.1073/pnas.0901435106)
57. Massimini, M., Ferrarelli, F., Huber, R., Esser, S. K., Singh, H. & Tononi, G. 2005 Breakdown of cortical effective connectivity during sleep. Science 309, 2228-2232. (doi:10.1126/science. 1117256) (Pubitemid 40941876)
58. Tononi, G. & Massimini, M. 2008 Why does consciousness fade in early sleep? Ann. NY Acad. Sci. 1129, 330-334. (doi:10.1196/annals.1417.024) (Pubitemid 351990293)
59. Tononi, G. 2004 An information integration theory of consciousness. BMC Neurosci. 5, 42. (doi:10.1186/1471-2202-5-42) (Pubitemid 40177039)
60. Achard, S., Salvador, R., Whitcher, B., Suckling, J. & Bullmore, E. 2006 A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26, 63-72. (doi:10.1523/JNEUROSCI.3874-05.2006) (Pubitemid 43090914)
61. Bullmore, E. & Sporns, O. 2009 Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186-198. (doi:10.1038/nrn2575)
62. Bassett, D. S. & Bullmore, E. 2006 Small-world brain networks. Neuroscientist 12, 512-523. (doi:10.1177/1073858406293182) (Pubitemid 44657966)
63. Sporns, O., Chialvo, D. R., Kaiser, M. & Hilgetag, C. C. 2004 Organization, development and function of complex brain networks. Trends Cogn. Sci. 8, 418-425. (doi:10.1016/j.tics. 2004.07.008) (Pubitemid 39179905)
64. Meunier, D., Achard, S., Morcom, A. & Bullmore, E. 2009 Age-related changes in modular organization of human brain functional networks. Neuroimage 44, 715-723. (doi:10.1016/j.neuroimage.2008.09.062)
65. Supekar, K., Musen, M. & Menon, V. 2009 Development of large-scale functional brain networks in children. PLoS Biol. 7, e1000157. (doi:10.1371/journal.pbio.1000157)
66. van den Heuvel, M. P., Stam, C. J., Kahn, R. S. & Hulshoff Pol, H. E. 2009 Efficiency of functional brain networks and intellectual performance. J. Neurosci. 29, 7619-7624. (doi:10.1523/JNEUROSCI.1443-09.2009)
67. Bassett, D. S., Bullmore, E., Verchinski, B. A., Mattay, V. S., Weinberger, D. R. & Meyer-Lindenberg, A. 2008 Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci. 28, 9239-9248. (doi:10.1523/JNEUROSCI.1929-08.2008)
68. Stam, C. J. et al. 2009 Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 132, 213-224. (doi:10.1093/brain/awn262)
69. Stam, C. J. 2009 Use of magnetoencephalography (MEG) to study functional brain networks in neurodegenerative disorders. J. Neurol. Sci. 289, 128-134. (doi:10.1016/j.jns.2009.08.028)
70. Spoormaker, V. I., Schröter, M. S., Gleiser, P. M., Andrade, K. C., Dresler, M., Wehrle, R., Sämann, P. G. & Czisch, M. 2010 Development of a large-scale functional brain network during human non-rapid eye movement sleep. J. Neurosci. 30, 11379-11 387. (doi:10.1523/JNEUROSCI.2015-10.2010)
71. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B. & Joliot, M. 2002 Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289. (doi:10.1006/nimg. 2001.0978) (Pubitemid 34852226)
72. Johnson, L. C., Hanson, K. & Bickford, R. G. 1976 Effect of flurazepam on sleep spindles and K-complexes. Electroencephalo Clin. Neurophysiol. 40, 67-77. (doi:10.1016/0013-4694(76)90180-2)
73. Ogilvie, R. D., Simons, I. A., Kuderian, R. H., MacDonald, T. & Rustenburg, J. 1991 Behavioral, event-related potential, and EEG/FFT changes at sleep onset. Psychophysiology 28, 54-64. (doi:10.1111/j.1469-8986.1991.tb03386. x)
74. Niiyama, Y., Fujiwara, R., Satoh, N. & Hishikawa, Y. 1994 Endogenous components of event-related potential appearing during NREM stage 1 and REM sleep in man. Int. J. Psychophysiol. 17, 165-174. (doi:10.1016/0167-8760(94) 90032-9) (Pubitemid 24244981)
75. Steriade, M., Contreras, D. & Amzica, F. 1994 Synchronized sleep oscillations and their paroxysmal developments. Trends Neurosci. 17, 199-208. (doi:10.1016/0166-2236(94)90104-X) (Pubitemid 24128463)
76. Boveroux, P. 2010 Breakdown of within-and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113, 1038-1053. (doi:10.1097/ALN. 0b013e3181f697f5)
77. Picchioni, D., Horovitz, S. G., Fukunaga, M., Carr, W. S., Meltzer, J. A., Balkin, T. J., Duyn, J. H. & Braun, A. R. 2010 Infraslow EEG oscillations organize large-scale cortical-subcortical interactions during sleep: a combined EEG/fMRI study. Brain Res. 1374, 63-72. (doi:10.1016/j. brainres.2010.12.035).
78. Weissenbacher, A., Kasess, C., Gerstl, F., Lanzenberger, R., Moser, E. & Windischberger, C. 2009 Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. Neuroimage 47, 1408-1416. (doi:10.1016/j.neuroimage.2009.05.005)
79. Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B. & Bandettini, P. A. 2009 The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44, 893-905. (doi:10.1016/j.neuroimage.2008.09.036)
80. Fox, M. D., Zhang, D., Snyder, A. Z. & Raichle, M. E. 2009 The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 101, 3270-3283. (doi:10.1152/jn.90777.2008)
81. Deco, G., Jirsa, V. K. & McIntosh, A. R. 2011 Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat. Rev. Neurosci. 12, 43-56. (doi:10.1038/nrn2961)
82. Magnin, M., Rey, M., Bastuji, H., Guillemant, P., Mauguiere, F. & Garcia-Larrea, L. 2010 Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc. Natl Acad. Sci. USA 107, 3829-3833. (doi:10.1073/pnas.0909710107)
83. Kaufmann, C., Wehrle, R., Wetter, T. C., Holsboer, F., Auer, D. P., Pollmächer, T. & Czisch, M. 2006 Brain activation and hypothalamic functional connectivity during humannon-rapid eye movement sleep: an EEG/fMRI study. Brain 129, 655-667. (doi:10.1093/brain/awh686) (Pubitemid 43278227)
84. He, B. J. & Raichle, M. E. 2009 The fMRI signal, slow cortical potential and consciousness. Trends Cogn. Sci. 13, 302-309. (doi:10.1016/j.tics. 2009.04.004)
85. Koch, C. 2009 The SCP is not specific enough to represent conscious content. Trends Cogn. Sci. 13, 367. (doi:10.1016/j.tics.2009.07.002)
86. Diekelmann, S. & Born, J. 2010 The memory function of sleep. Nat. Rev. Neurosci. 11, 114-126. (doi:10.1038/nrn2762)
87. Nofzinger, E. A. 2006 Neuroimaging of sleep and sleep disorders. Curr. Neurol. Neurosci. Rep. 6, 149-155. (doi:10.1007/s11910-996-0038-3)
88. Desseilles, M., Dang-Vu, T., Schabus, M., Sterpenich, V., Maquet, P. & Schwartz, S. 2008 Neuroimaging insights into the pathophysiology of sleep disorders. Sleep 31, 777-794. (Pubitemid 351810507)
89. Nofzinger, E. A., Nissen, C., Germain, A., Moul, D., Hall, M., Price, J. C., Miewald, J. M. & Buysse, D. J. 2006 Regional cerebral metabolic correlates of WASO during NREM sleep in insomnia. J. Clin. Sleep Med. 2, 316-322. (Pubitemid 44299556)
90. Riemann, D., Spiegelhalder, K., Espie, C., Pollmächer, T., Léger, D., Bassetti, C. & van Someren, E. 2010 Chronic insomnia: clinical and research challenges-an agenda. Pharmacopsychiatry 44, 1-14. (doi:10.1055/s-0030-1267978)
91. Jäncke, L. 2009 The plastic human brain. Restor. Neurol. Neurosci. 27, 521-538.
92. Münte, T. F., Altenmüller, E. & Jäncke, L. 2002 The musician's brain as a model of neuroplasticity. Nat. Rev. Neurosci. 3, 473-478. (doi:10.1038/nrm866) (Pubitemid 135711803)
93. Jäncke, L., Koeneke, S., Hoppe, A., Rominger, C. & Haenggi, J. 2009 The architecture of the golfer's brain. PLoS ONE 4, e4785. (doi:10.1371/journal.pone.0004785)
94. Aydin, K., Ucar, A., Oguz, K. K., Okur, O. O., Agayev, A., Unal, Z., Yilmaz, S. & Ozturk, C. 2007 Increased gray matter density in the parietal cortex of mathematicians: a voxel-based morphometry study. Am. J. Neuroradiol. 28, 1859-1864. (doi:10.3174/ajnr.A0696) (Pubitemid 350174723)
95. Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S. & Frith, C. D. 2000 Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl Acad. Sci. USA 97, 4398-4403. (doi:10.1073/pnas.070039597) (Pubitemid 30226144)
96. Mechelli, A., Crinion, J. T., Noppeney, U., O'Doherty, J., Ashburner, J., Frackowiak, R. S. & Price, C. J. 2004 Neurolinguistics: structural plasticity in the bilingual brain. Nature 431, 757. (doi:10.1038/431757a) (Pubitemid 39434062)
97. Cannonieri, G. C., Bonilha, L., Fernandes, P. T., Cendes, F. & Li, L. M. 2007 Practice and perfect: length of training and structural brain changes in experienced typists. Neuroreport 18, 1063-1066. (doi:10.1097/WNR. 0b013e3281a030e5) (Pubitemid 46905185)
98. Bengtsson, S. L., Nagy, Z., Skare, S., Forsman, L., Forssberg, H. & Ullén, F. 2005 Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 8, 1148-1150. (doi:10.1038/nn1516) (Pubitemid 43348132)
99. Imfeld, A., Oechslin, M. S., Meyer, M., Loenneker, T. & Jäncke, L. 2009 White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage 46, 600-607. (doi:10.1016/j. neuroimage.2009.02.025)
100. Oechslin, M. S., Imfeld, A., Loenneker, T., Meyer, M. & Jäncke, L. 2010 The plasticity of the superior longitudinal fasciculus as a function of musical expertise: a diffusion tensor imaging study. Front. Hum. Neurosci. 3, 76. (doi:10.3389/neuro.09.076.2009).
101. Koeneke, S., Lutz, K., Herwig, U., Ziemann, U. & Jäncke, L. 2006 Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp. Brain Res. 174, 199-209. (doi:10.1007/s00221- 006-0440-8) (Pubitemid 44421098)
102. Jäncke, L., Gaab, N., Wüstenberg, T., Scheich, H. & Heinze, H. J. 2001 Short-term functional plasticity in the human auditory cortex: an fMRI study. Brain Res. Cogn. Brain Res. 12, 479-485. (doi:10.1016/S0926-6410(01) 00092-1) (Pubitemid 33022703)
103. Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S. & Passingham, R. E. 1994 Motor sequence learning: a study with positron emission tomography. J. Neurosci. 14, 3775-3790. (Pubitemid 24174123)
104. Gaab, N., Gaser, C. & Schlaug, G. 2006 Improvement-related functional plasticity following pitch memory training. Neuroimage 31, 255-263. (doi:10.1016/j.neuroimage.2005.11.046) (Pubitemid 44250878)
105. Kempermann, G., Kuhn, H. G. & Gage, F. H. 1997 More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495. (doi:10.1038/386493a0) (Pubitemid 27164074)
106. Tost, H., Braus, D. F., Hakimi, S., Ruf, M., Vollmert, C., Hohn, F. & Meyer-Lindenberg, A. 2010 Acute D2 receptor blockade induces rapid, reversible remodeling in human cortical-striatal circuits. Nat. Neurosci. 13, 920-922. (doi:10.1038/nn.2572)
107. Walker, M. P. & Stickgold, R. 2004 Sleep-dependent learning and memory consolidation. Neuron 44, 121-133. (doi:10.1016/j.neuron.2004.08.031) (Pubitemid 39348835)
108. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. 2002 Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205-211. (doi:10.1016/S0896-6273(02)00746-8) (Pubitemid 34804334)
109. Walker, M. P., Stickgold, R., Alsop, D., Gaab, N. & Schlaug, G. 2005 Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133, 911-917. (doi:10.1016/j. neuroscience.2005.04.007) (Pubitemid 40814599)
110. Korman, M., Doyon, J., Doljansky, J., Carrier, J., Dagan, Y. & Karni, A. 2007 Daytime sleep condenses the time course of motor memory consolidation. Nat. Neurosci. 10, 1206-1213. (doi:10.1038/nn1959) (Pubitemid 47339956)
111. Korman, M., Raz, N., Flash, T. & Karni, A. 2003 Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance. Proc. Natl Acad. Sci. USA 100, 12 492-12 497. (doi:10.1073/pnas. 2035019100) (Pubitemid 37271587)
112. Fischer, S., Nitschke, M. F., Melchert, U. H., Erdmann, C. & Born, J. 2005 Motor memory consolidation in sleep shapes more effective neuronal representations. J. Neurosci. 25, 11 248-11 255. (doi:10.1523/JNEUROSCI.1743-05. 2005) (Pubitemid 43083699)
113. Hotermans, C., Peigneux, P., Maertens de Noordhout, A., Moonen, G. & Maquet, P. 2006 Early boost and slow consolidation in motor skill learning. Learn. Mem. 13, 580-583. (doi:10.1101/lm.239406) (Pubitemid 44498409)
114. Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. 2002 Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987-11 991. (doi:10.1073/pnas.182178199) (Pubitemid 34994511)
115. Rieth, C. A., Cai, D. J., McDevitt, E. A. & Mednick, S. C. 2010 The role of sleep and practice in implicit and explicit motor learning. Behav. Brain Res. 214, 470-474. (doi:10.1016/j.bbr.2010.05.052)
116. Cai, D. J. & Rickard, T. C. 2009 Reconsidering the role of sleep for motor memory. Behav. Neurosci. 123, 1153-1157. (doi:10.1037/a0017672)
117. Brawn, T. P., Fenn, K. M., Nusbaum, H. C. & Margoliash, D. 2010 Consolidating the effects of waking and sleep on motor-sequence learning. J. Neurosci. 30, 13977-13 982. (doi:10.1523/JNEUROSCI.3295-10.2010)
118. Tononi, G. & Cirelli, C. 2003 Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull 62, 143-150. (doi:10.1016/j.brainresbull.2003.09. 004) (Pubitemid 37443660)
119. Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., Lehéricy, S. & Benali, H. 2009 Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61-75. (doi:10.1016/j.bbr.2008.11.012)
120. Maquet, P. et al. 2000 Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 3, 831-836. (doi:10.1038/77744) (Pubitemid 30485710)
121. Peigneux, P. et al. 2003 Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage 20, 125-134. (doi:10.1016/S1053-8119(03)00278-7) (Pubitemid 37188504)
122. Blanke, O., Ortigue, S., Landis, T. & Seeck, M. 2002 Stimulating illusory own-body perceptions. Nature 419, 269-270. (doi:10.1038/419269a)
123. Seitz, R. J. & Roland, P. E. 1992 Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study. Eur. J. Neurosci. 4, 154-165. (doi:10.1111/j.1460-9568.1992.tb00862.x)
124. Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. 2004 Local sleep and learning. Nature 430, 78-81. (doi:10.1038/nature02663) (Pubitemid 38915227)
125. Molle, M., Eschenko, O., Gais, S., Sara, S. J. & Born, J. 2009 The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci. 29, 1071-1081. (doi:10.1111/j.1460-9568.2009.06654.x)
126. Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klösch, G., Anderer, P., Klimesch, W., Saletu, B. & Zeitlhofer, J. 2004 Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479-1485. (Pubitemid 40041615)
127. Schmidt, C., Peigneux, P., Muto, V., Schenkel, M., Knoblauch, V., Münch, M., de Quervain, D. J.-F., Wirz-Justice, A. & Cajochen, C. 2006 Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J. Neurosci. 26, 8976-8982. (doi:10.1523/JNEUROSCI.2464-06.2006) (Pubitemid 44319386)
128. Gais, S., Molle, M., Helms, K. & Born, J. 2002 Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830-6834. (Pubitemid 35386440)
129. Clemens, Z., Fabo, D. & Halasz, P. 2005 Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529-535. (doi:10.1016/j.neuroscience.2005.01.011) (Pubitemid 40417924)
130. Clemens, Z., Fabo, D. & Halasz, P. 2006 Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 403, 52-56. (doi:10.1016/j.neulet.2006.04.035) (Pubitemid 43977792)
131. Fogel, S. M. & Smith, C. T. 2006 Learning-dependent changes in sleep spindles and stage 2 sleep. J. Sleep Res. 15, 250-255. (doi:10.1111/j.1365-2869. 2006.00522.x) (Pubitemid 44215541)
132. Fogel, S. M., Smith, C. T. & Cote, K. A. 2007 Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav. Brain Res. 180, 48-61. (doi:10.1016/j.bbr. 2007.02.037) (Pubitemid 46661013)
133. Morin, A. et al. 2008 Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 31, 1149-1156.
134. Tamaki, M., Matsuoka, T., Nittono, H. & Hori, T. 2009 Activation of fast sleep spindles at the premotor cortex and parietal areas contributes to motor learning: a study using sLORETA. Clin. Neurophysiol. 120, 878-886. (doi:10.1016/j.clinph.2009.03.006)
135. Nishida, M. & Walker, M. P. 2007 Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2, e341. (doi:10.1371/journal.pone.0000341)
136. Genzel, L., Dresler, M., Wehrle, R., Grözinger, M. & Steiger, A. 2009 Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep 32, 302-310.
137. Moroni, F. et al. 2008 Procedural learning and sleep hippocampal low frequencies in humans. Neuroimage 42, 911-918. (doi:10.1016/j.neuroimage.2008. 05.027)
138. Koeneke, S., Lutz, K., Herwig, U., Ziemann, U. & Jancke, L. 2006 Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp. Brain Res. 174, 199-209. (doi:10.1007/s00221- 006-0440-8) (Pubitemid 44421098)
139. Rosenthal, C. R., Roche-Kelly, E. E., Husain, M. & Kennard, C. 2009 Response-dependent contributions of human primary motor cortex and angular gyrus to manual and perceptual sequence learning. J. Neurosci. 29, 15 115-15 125. (doi:10.1523/JNEUROSCI.2603-09.2009)
140. Jäncke, L., Loose, R., Lutz, K., Specht, K. & Shah, N. J. 2000 Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli. Brain Res. Cogn. Brain Res. 10, 51-66. (doi:10.1016/S0926- 6410(00)00022-7)
141. Gheysen, F., Van Opstal, F., Roggeman, C., Van Waelvelde, H. & Fias, W. 2010 Hippocampal contribution to early and later stages of implicit motor sequence learning. Exp. Brain Res. 202, 795-807. (doi:10.1007/s00221-010-2186-6)
142. Praeg, E., Esslen, M., Lutz, K. & Jäncke, L. 2006 Neuronal modifications during visuomotor association learning assessed by electric brain tomography. Brain Topogr. 19, 61-75. (doi:10.1007/s10548-006-0013-y) (Pubitemid 44924073)
143. Blum, J., Lutz, K. & Jäncke, L. 2007 Coherence and phase locking of intracerebral activation during visuo-and audio-motor learning of continuous tracking movements. Exp. Brain Res. 182, 59-69. (doi:10.1007/s00221-007-0963-7) (Pubitemid 47318246)
144. Doyon, J. & Benali, H. 2005 Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 15, 161-167. (doi:10.1016/j.conb.2005.03.004) (Pubitemid 41569264)
145. Doyon, J., Penhune, V., Ungerleider, L. G. 2003 Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41, 252-262. (doi:10.1016/S0028-3932(02)00158-6) (Pubitemid 35365955)
146. Koeneke, S., Lutz, K., Wustenberg, T. & Jäncke, L. 2004 Bimanual versus unimanual coordination: what makes the difference? Neuroimage 22, 1336-1350. (doi:10.1016/j. neuroimage.2004.03.012) (Pubitemid 38829223)