Patterned brain stimulation, what a framework with rhythmic and noisy components might tell us about recovery maximization

Frontiers in Human Neuroscience

Volumn , Issue JUN, 2013, Pages

  Schmidt, Sein ^a   Scholz, Michael ^a   Obermayer, Klaus ^a   Brandt, Stephan A ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN DEPTH STIMULATION; CEREBROVASCULAR ACCIDENT; CONVALESCENCE; EPILEPSY; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATHEMATICAL MODEL; MOTOR PERFORMANCE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NOISE; NON INVASIVE PROCEDURE; NONHUMAN; NONINVASIVE BRAIN STIMULATION; OSCILLATION; THERAPY EFFECT; TRANSCRANIAL ALTERNATING CURRENT STIMULATION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84933680057     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00325     Document Type: Article

References (138)

1. Abraham, W.C. (2008). Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 9, 387.
2. Ahissar, E., Vaadia, E., Ahissar, M., Bergman, H., Arieli, A., and Abeles, M. (1992). Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science 257, 1412-1415.
3. Antal, A., Boros, K., Poreisz, C., Chaieb, L., Terney, D., and Paulus, W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul 1, 97-105.
4. Antal, A., Terney, D., Poreisz, C., and Paulus, W. (2007). Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. Eur J Neurosci 26, 2687-2691.
5. Augustin, M., Ladenbauer, J., and Obermayer, K. (2013). How adaptation shapes spike rate oscillations in recurrent neuronal networks. Front Comput Neurosci 7, 9.
6. Baker, S.N. (2007). Oscillatory interactions between sensorimotor cortex and the periphery. Current opinion in neurobiology 17, 649-655.
7. Bascones, R., Garcia-Ojalvo, J., and Sancho, J.M. (2002). Pulse propagation sustained by noise in arrays of bistable electronic circuits. Phys Rev E Stat Nonlin Soft Matter Phys 65, 061108.
8. Bastani, A., and Jaberzadeh, S. (2012). Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: a systematic review and meta-analysis. Clin Neurophysiol 123, 644-657.
9. Benzi, R., Sutera, A., and Vulpiani, A. (1981). The mechanism of stochastic resonance. Journal of Physics A: Mathematical and General 14, L453-L457.
10. Berenyi, A., Belluscio, M., Mao, D., and Buzsaki, G. (2012). Closed-loop control of epilepsy by transcranial electrical stimulation. Science 337, 735-737.
11. Berger, H. (1929). Uber das elektrenkephalogramm des menschen. Arch. Psychiatr. Nervenkr 278.
12. Bezrukov, S.M., and Vodyanoy, I. (1995). Noise-induced enhancement of signal transduction across voltage-dependent ion channels. Nature 378, 362-364.
13. Bienenstock, E.L., Cooper, L.N., and Munro, P.W. (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2, 32-48.
14. Bindman, L.J., Lippold, O.C., and Redfearn, J.W. (1964). The Action of Brief Polarizing Currents on the Cerebral Cortex of the Rat (1) during Current Flow and (2) in the Production of Long-Lasting after-Effects. J Physiol 172, 369-382.
15. Brown, P. (2000). Cortical drives to human muscle: the Piper and related rhythms. Prog Neurobiol 60, 97-108.
16. Brown, P. (2003). Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov Disord 18, 357-363.
17. Brown, P., and Marsden, J.F. (2001). Cortical network resonance and motor activity in humans. Neuroscientist 7, 518-527.
18. Brunel, N., and Hansel, D. (2006). How noise affects the synchronization properties of recurrent networks of inhibitory neurons. Neural Comput 18, 1066-1110.
19. Bryant, H.L., and Segundo, J.P. (1976). Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260, 279-314.
20. Buzsaki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929.
21. Calvin, W.H., and Stevens, C.F. (1968). Synaptic noise and other sources of randomness in motoneuron interspike intervals. J Neurophysiol 31, 574-587.
22. Chaieb, L., Paulus, W., and Antal, A. (2011). Evaluating aftereffects of short-duration transcranial random noise stimulation on cortical excitability. Neural Plast 2011, 105927.
23. Chen, R., Cohen, L.G., and Hallett, M. (2002). Nervous system reorganization following injury. Neuroscience 111, 761-773.
24. Clarke, P.G. (2012). The limits of brain determinacy. Proc Biol Sci 279, 1665-1674.
25. Cramer, S.C., Sur, M., Dobkin, B.H., O'brien, C., Sanger, T.D., Trojanowski, J.Q., Rumsey, J.M., Hicks, R., Cameron, J., Chen, D., Chen, W.G., Cohen, L.G., Decharms, C., Duffy, C.J., Eden, G.F., Fetz, E.E., Filart, R., Freund, M., Grant, S.J., Haber, S., Kalivas, P.W., Kolb, B., Kramer, A.F., Lynch, M., Mayberg, H.S., Mcquillen, P.S., Nitkin, R., Pascual-Leone, A., Reuter-Lorenz, P., Schiff, N., Sharma, A., Shekim, L., Stryker, M., Sullivan, E.V., and Vinogradov, S. (2011). Harnessing neuroplasticity for clinical applications. Brain 134, 1591-1609.
26. Creuzfeldt, O., and Struck, G. (1962). [Neurophysiology and morphology of the chronically isolated cortical islet in the cat: brain potentials and neuron activity of an isolated nerve cell population without afferent fibers.]. Arch.Psychiatr.Nervenkr.Z.Gesamte Neurol Psychiatr. 203, 708-731.
27. Debanne, D. (2004). Information processing in the axon. Nat Rev Neurosci 5, 304-316.
28. Deco, G., Jirsa, V., Mcintosh, A.R., Sporns, O., and Kotter, R. (2009). Key role of coupling, delay, and noise in resting brain fluctuations. Proc Natl Acad Sci U S A 106, 10302-10307.
29. Destexhe, A., and Contreras, D. (2006). Neuronal computations with stochastic network states. Science 314, 85-90.
30. Diba, K., Koch, C., and Segev, I. (2006). Spike propagation in dendrites with stochastic ion channels. J Comput Neurosci 20, 77-84.
31. Dimyan, M.A., and Cohen, L.G. (2011). Neuroplasticity in the context of motor rehabilitation after stroke. Nat Rev Neurol 7, 76-85.
32. Donner, T.H., and Siegel, M. (2011). A framework for local cortical oscillation patterns. Trends Cogn Sci 15, 191-199.
33. Durrant, S., Kang, Y., Stocks, N., and Feng, J. (2011). Suprathreshold stochastic resonance in neural processing tuned by correlation. Phys Rev E Stat Nonlin Soft Matter Phys 84, 011923.
34. Engel, A.K., and Fries, P. (2010). Beta-band oscillations--signalling the status quo? Current Opinion in Neurobiology 20, 156-165.
35. Engel, A.K., Fries, P., and Singer, W. (2001). Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2, 704-716.
36. Ermentrout, G.B., Galan, R.F., and Urban, N.N. (2008). Reliability, synchrony and noise. Trends Neurosci 31, 428-434.
37. European Registers of Stroke, I., Heuschmann, P.U., Di Carlo, A., Bejot, Y., Rastenyte, D., Ryglewicz, D., Sarti, C., Torrent, M., and Wolfe, C.D. (2009). Incidence of stroke in Europe at the beginning of the 21st century. Stroke 40, 1557-1563.
38. Faisal, A.A., Selen, L.P., and Wolpert, D.M. (2008). Noise in the nervous system. Nat Rev Neurosci 9, 292-303.
39. Fang, Y., Daly, J.J., Sun, J., Hvorat, K., Fredrickson, E., Pundik, S., Sahgal, V., and Yue, G.H. (2009). Functional corticomuscular connection during reaching is weakened following stroke. Clin Neurophysiol 120, 994-1002.
40. Farmer, S.F., Bremner, F.D., Halliday, D.M., Rosenberg, J.R., and Stephens, J.A. (1993). The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470, 127-155.
41. Fogelson, N., Kuhn, A.A., Silberstein, P., Limousin, P.D., Hariz, M., Trottenberg, T., Kupsch, A., and Brown, P. (2005). Frequency dependent effects of subthalamic nucleus stimulation in Parkinson's disease. Neurosci Lett 382, 5-9.
42. Fricke, K., Seeber, A.A., Thirugnanasambandam, N., Paulus, W., Nitsche, M.A., and Rothwell, J.C. (2011). Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J Neurophysiol 105, 1141-1149.
43. Friston, K.J. (1997). Another neural code? Neuroimage. 5, 213-220.
44. Gentner, R., Wankerl, K., Reinsberger, C., Zeller, D., and Classen, J. (2008). Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex 18, 2046-2053.
45. Ghosh, A., Rho, Y., Mcintosh, A.R., Kotter, R., and Jirsa, V.K. (2008). Noise during rest enables the exploration of the brain's dynamic repertoire. PLoS Comput Biol 4, e1000196.
46. Grefkes, C., and Fink, G.R. (2012). Disruption of motor network connectivity post-stroke and its noninvasive neuromodulation. Curr Opin Neurol 25, 670-675.
47. Grenier, F.O., Timofeev, I., and Steriade, M. (2001). Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J Neurophysiol 86, 1884-1898.
48. Gutkin, B.S., Jost, J., and Tuckwell, H.C. (2009). Inhibition of rhythmic neural spiking by noise: the occurrence of a minimum in activity with increasing noise. Naturwissenschaften 96, 1091-1097.
49. Hallett, M. (2005). Guest Editorial: Neuroplasticity and rehabilitation. J.Rehabil.Res.Dev. 42, xvii-xxii.
50. Halliday, D.M., Conway, B.A., Farmer, S.F., and Rosenberg, J.R. (1998). Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241, 5-8.
51. Hamada, M., Terao, Y., Hanajima, R., Shirota, Y., Nakatani-Enomoto, S., Furubayashi, T., Matsumoto, H., and Ugawa, Y. (2008). Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J Physiol 586, 3927-3947.
52. Hanggi, P. (2002). Stochastic resonance in biology. How noise can enhance detection of weak signals and help improve biological information processing. Chemphyschem 3, 285-290.
53. Harris, C.M., and Wolpert, D.M. (1998). Signal-dependent noise determines motor planning. Nature 394, 780-784.
54. Harris, J.A., Clifford, C.W., and Miniussi, C. (2008). The functional effect of transcranial magnetic stimulation: signal suppression or neural noise generation? J Cogn Neurosci 20, 734-740.
55. Hodgkin, A.L., and Huxley, A.F. (1990). A quantitative description of membrane current and its application to conduction and excitation in nerve. 1952. Bull Math Biol 52, 25-71; discussion 25-23.
56. Horsthemke, W., and Lefever, R. (1984). Noise-induced transitions: theory and applications in physics, chemistry, and biology. Springer Verlag.
57. Huang, Y.Z., Edwards, M.J., Rounis, E., Bhatia, K.P., and Rothwell, J.C. (2005). Theta burst stimulation of the human motor cortex. Neuron 45, 201-206.
58. Hummel, F.C., Celnik, P., Pascual-Leone, A., Fregni, F., Byblow, W.D., Buetefisch, C.M., Rothwell, J., Cohen, L.G., and Gerloff, C. (2008). Controversy: Noninvasive and invasive cortical stimulation show efficacy in treating stroke patients. Brain Stimul. 1, 370-382.
59. Hutcheon, B., and Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23, 216-222.
60. Jackson, A., and Zimmermann, J.B. (2012). Neural interfaces for the brain and spinal cord--restoring motor function. Nat Rev Neurol 8, 690-699.
61. Joundi, R.A., Jenkinson, N., Brittain, J.S., Aziz, T.Z., and Brown, P. (2012). Driving oscillatory activity in the human cortex enhances motor performance. Curr Biol 22, 403-407.
62. Jung, P., and Ziemann, U. (2009). Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J Neurosci 29, 5597-5604.
63. Kakuda, W., Abo, M., Shimizu, M., Sasanuma, J., Okamoto, T., Yokoi, A., Taguchi, K., Mitani, S., Harashima, H., Urushidani, N., Urashima, M., and Investigators, N. (2012). A multi-center study on low-frequency rTMS combined with intensive occupational therapy for upper limb hemiparesis in post-stroke patients. J Neuroeng Rehabil 9, 4.
64. Khedr, E.M., Rothwell, J.C., Ahmed, M.A., Shawky, O.A., and Farouk, M. (2007). Modulation of motor cortical excitability following rapid-rate transcranial magnetic stimulation. Clin Neurophysiol 118, 140-145.
65. Kim, D.Y., Lim, J.Y., Kang, E.K., You, D.S., Oh, M.K., Oh, B.M., and Paik, N.J. (2010). Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil 89, 879-886.
66. Kim, Y.H., You, S.H., Ko, M.H., Park, J.W., Lee, K.H., Jang, S.H., Yoo, W.K., and Hallett, M. (2006). Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 37, 1471-1476.
67. Kurrer, C., and Schulten, K. (1995). Noise-induced synchronous neuronal oscillations. Phys Rev EStat Phys Plasmas Fluids Relat Interdiscip Topics 51, 6213-6218.
68. Laureys, S., Peigneux, P., Phillips, C., Fuchs, S., Degueldre, C., Aerts, J., Del Fiore, G., Petiau, C., Luxen, A., Van Der Linden, M., Cleeremans, A., Smith, C., and Maquet, P. (2001). Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 105, 521-525.
69. Leocani, L., Cohen, L.G., Wassermann, E.M., Ikoma, K., and Hallett, M. (2000). Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123 (Pt 6), 1161-1173.
70. Leocani, L., Toro, C., Manganotti, P., Zhuang, P., and Hallett, M. (1997). Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalogr Clin Neurophysiol 104, 199-206.
71. Lindenberg, R., Renga, V., Zhu, L.L., Nair, D., and Schlaug, G. (2010). Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75, 2176-2184.
72. Lindner, B. (2004). Effects of noise in excitable systems. Physics Reports 392, 321-424.
73. Llinas, R.R. (1988). The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242, 1654-1664.
74. Mackay, W.A. (1997). Synchronized neuronal oscillations and their role in motor processes. Trends Cogn Sci 1, 176-183.
75. Mainen, Z.F., and Sejnowski, T.J. (1995). Reliability of spike timing in neocortical neurons. Science 268, 1503-1506.
76. Manganotti, P., Gerloff, C., Toro, C., Katsuta, H., Sadato, N., Zhuang, P., Leocani, L., and Hallett, M. (1998). Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr Clin Neurophysiol 109, 50-62.
77. Mcdonnell, M.D., and Abbott, D. (2009). What is stochastic resonance? Definitions, misconceptions, debates, and its relevance to biology. PLoS Comput Biol 5, e1000348.
78. Mcdonnell, M.D., and Ward, L.M. (2011). The benefits of noise in neural systems: bridging theory and experiment. Nat Rev Neurosci 12, 415-426.
79. Mejias, J.F., and Torres, J.J. (2011). Emergence of resonances in neural systems: the interplay between adaptive threshold and short-term synaptic plasticity. PloS one 6, e17255.
80. Misic, B., Mills, T., Taylor, M.J., and Mcintosh, A.R. (2010). Brain noise is task dependent and region specific. J Neurophysiol 104, 2667-2676.
81. Moliadze, V., Antal, A., and Paulus, W. (2010a). Boosting brain excitability by transcranial high frequency stimulation in the ripple range. J Physiol 588, 4891-4904.
82. Moliadze, V., Antal, A., and Paulus, W. (2010b). Electrode-distance dependent after-effects of transcranial direct and random noise stimulation with extracephalic reference electrodes. Clin Neurophysiol 121, 2165-2171.
83. Moliadze, V., Atalay, D., Antal, A., and Paulus, W. (2012). Close to threshold transcranial electrical stimulation preferentially activates inhibitory networks before switching to excitation with higher intensities. Brain Stimul 5, 505-511.
84. Moss, F., Ward, L.M., and Sannita, W.G. (2004). Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol 115, 267-281.
85. Murase, N., Duque, J., Mazzocchio, R., and Cohen, L.G. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55, 400-409.
86. Neiman, A., Schimansky-Geier, L., Moss, F., Shulgin, B., and Collins, J.J. (1999). Synchronization of noisy systems by stochastic signals. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60, 284-292.
87. Nitsche, M.A., Cohen, L.G., Wassermann, E.M., Priori, A., Lang, N., Antal, A., Paulus, W., Hummel, F., Boggio, P.S., Fregni, F., and Pascual-Leone, A. (2008). Transcranial direct current stimulation: State of the art 2008. Brain Stimul 1, 206-223.
88. Nitsche, M.A., and Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527 Pt 3, 633-639.
89. Norrving, B., and Kissela, B. (2013). The global burden of stroke and need for a continuum of care. Neurology 80, S5-12.
90. Nowak, D.A., Bosl, K., Podubecka, J., and Carey, J.R. (2010). Noninvasive brain stimulation and motor recovery after stroke. Restor Neurol Neurosci 28, 531-544.
91. Ostojic, S., Brunel, N., and Hakim, V. (2009). Synchronization properties of networks of electrically coupled neurons in the presence of noise and heterogeneities. J Comput Neurosci 26, 369-392.
92. Pascual-Leone, A., Valls-Sole, J., Wassermann, E.M., and Hallett, M. (1994). Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117 (Pt 4), 847-858.
93. Paulus, W. (2005). Toward establishing a therapeutic window for rTMS by theta burst stimulation. Neuron 45, 181-183.
94. Paulus, W. (2011). Transcranial electrical stimulation (tES -tDCS; tRNS, tACS) methods. Neuropsychol Rehabil 21, 602-617.
95. Pell, G.S., Roth, Y., and Zangen, A. (2011). Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol 93, 59-98.
96. Pfurtscheller, G., Graimann, B., Huggins, J.E., Levine, S.P., and Schuh, L.A. (2003). Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114, 1226-1236.
97. Plow, E.B., Carey, J.R., Nudo, R.J., and Pascual-Leone, A. (2009). Invasive cortical stimulation to promote recovery of function after stroke: a critical appraisal. Stroke 40, 1926-1931.
98. Polania, R., Nitsche, M.A., Korman, C., Batsikadze, G., and Paulus, W. (2012). The importance of timing in segregated theta phase-coupling for cognitive performance. Curr Biol 22, 1314-1318.
99. Ponomarenko, A.A., Li, J.S., Korotkova, T.M., Huston, J.P., and Haas, H.L. (2008). Frequency of network synchronization in the hippocampus marks learning. Eur J Neurosci 27, 3035-3042.
100. Postnov, D.E., Setsinskii, D.V., and Sosnovtseva, O.V. (2001). Stochastic synchronization and the growth in regularity of the noise-induced oscillations. Technical Physics Letters 27, 463-466.
101. Rothkegel, H., Sommer, M., and Paulus, W. (2010). Breaks during 5Hz rTMS are essential for facilitatory after effects. Clin Neurophysiol 121, 426-430.
102. Salenius, S., and Hari, R. (2003). Synchronous cortical oscillatory activity during motor action. Curr Opin Neurobiol 13, 678-684.
103. Schmidt, R., and Lee, T. (2005). Motor control and learning: a behavorial emphasis.
104. Schmidt, S., Mante, A., Ronnefarth, M., Fleischmann, R., Gall, C., and Brandt, S.A. (2013). Progressive enhancement of alpha activity and visual function in patients with optic neuropathy: a two-week repeated session alternating current stimulation study. Brain Stimul 6, 87-93.
105. Schneidman, E., Freedman, B., and Segev, I. (1998). Ion channel stochasticity may be critical in determining the reliability and precision of spike timing. Neural Comput 10, 1679-1703.
106. Schoen, I., and Fromherz, P. (2008). Extracellular stimulation of mammalian neurons through repetitive activation of Na+ channels by weak capacitive currents on a silicon chip. J Neurophysiol 100, 346-357.
107. Schoffelen, J.M., Oostenveld, R., and Fries, P. (2005). Neuronal coherence as a mechanism of effective corticospinal interaction. Science (New York, N.Y.) 308, 111-113.
108. Schulz, R., Gerloff, C., and Hummel, F.C. (2013). Non-invasive brain stimulation in neurological diseases. Neuropharmacology 64, 579-587.
109. Schwarzkopf, D.S., Silvanto, J., and Rees, G. (2011). Stochastic resonance effects reveal the neural mechanisms of transcranial magnetic stimulation. J Neurosci 31, 3143-3147.
110. Sejnowski, T.J., and Paulsen, O. (2006). Network oscillations: emerging computational principles. J Neurosci 26, 1673-1676.
111. Shadlen, M.N., and Newsome, W.T. (1994). Noise, neural codes and cortical organization. Curr Opin Neurobiol 4, 569-579.
112. Siebner, H.R., Hartwigsen, G., Kassuba, T., and Rothwell, J. (2010). How does transcranial magnetic stimulation modify neuronal activity in the brain? -Implications for studies of cognition. Cortex 45, 1035-1042.
113. Sosnovtseva, O.V., Fomin, A.I., Postnov, D.E., and Anishchenko, V.S. (2001). Clustering of noise-induced oscillations. Phys Rev E Stat Nonlin Soft Matter Phys 64, 026204.
114. Sporns, O., Chialvo, D.R., Kaiser, M., and Hilgetag, C.C. (2004). Organization, development and function of complex brain networks. Trends Cogn Sci 8, 418-425.
115. Stein, R.B., Gossen, E.R., and Jones, K.E. (2005). Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6, 389-397.
116. Strens, L.H., Asselman, P., Pogosyan, A., Loukas, C., Thompson, A.J., and Brown, P. (2004). Corticocortical coupling in chronic stroke: its relevance to recovery. Neurology 63, 475-484.
117. Strogatz, S.H., and Mirollo, R.E. (1991). Stability of incoherence in a population of coupled oscillators. Journal of Statistical Physics 63, 613-635.
118. Swayne, O.B., Rothwell, J.C., Ward, N.S., and Greenwood, R.J. (2008). Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 18, 1909-1922.
119. Talelli, P., and Rothwell, J. (2006). Does brain stimulation after stroke have a future? Curr Opin Neurol 19, 543-550.
120. Talelli, P., Wallace, A., Dileone, M., Hoad, D., Cheeran, B., Oliver, R., Vandenbos, M., Hammerbeck, U., Barratt, K., Gillini, C., Musumeci, G., Boudrias, M.H., Cloud, G.C., Ball, J., Marsden, J.F., Ward, N.S., Di Lazzaro, V., Greenwood, R.G., and Rothwell, J.C. (2012). Theta burst stimulation in the rehabilitation of the upper limb: a semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil Neural Repair 26, 976-987.
121. Terney, D., Chaieb, L., Moliadze, V., Antal, A., and Paulus, W. (2008). Increasing human brain excitability by transcranial high-frequency random noise stimulation. J Neurosci 28, 14147-14155.
122. Thut, G., Miniussi, C., and Gross, J. (2012). The functional importance of rhythmic activity in the brain. Curr Biol 22, R658-663.
123. Thut, G., and Pascual-Leone, A. (2010). A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr 22, 219-232.
124. Thut, G., Veniero, D., Romei, V., Miniussi, C., Schyns, P., and Gross, J. (2011). Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 21, 1176-1185.
125. Timme, M., Wolf, F., and Geisel, T. (2002). Coexistance of regular and irregular dynamics in complex networks of pulse-coupled oscillators. Physical review letters.
126. Torres, J.J., Marro, J., and Mejias, J.F. (2011). Can intrinsic noise induce various resonant peaks? New Journal of Physics 13, 053014.
127. Toschke, A.M., Tilling, K., Cox, A.M., Rudd, A.G., Heuschmann, P.U., and Wolfe, C.D. (2010). Patient-specific recovery patterns over time measured by dependence in activities of daily living after stroke and post-stroke care: the South London Stroke Register (SLSR). Eur J Neurol 17, 219-225.
128. Van Wijk, B.C., Beek, P.J., and Daffertshofer, A. (2012). Neural synchrony within the motor system: what have we learned so far? Front Hum Neurosci 6, 252.
129. Varela, F., Lachaux, J.P., Rodriguez, E., and Martinerie, J. (2001). The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2, 229-239.
130. Ward, L.M., Maclean, S.E., and Kirschner, A. (2010). Stochastic resonance modulates neural synchronization within and between cortical sources. PloS one 5, e14371.
131. Watts, D.J., and Strogatz, S.H. (1998). Collective dynamics of 'small-world' networks. Nature 393, 440-442.
132. White, J.A., Rubinstein, J.T., and Kay, A.R. (2000). Channel noise in neurons. Trends Neurosci 23, 131-137.
133. Wolfe, C.D., Crichton, S.L., Heuschmann, P.U., Mckevitt, C.J., Toschke, A.M., Grieve, A.P., and Rudd, A.G. (2011). Estimates of outcomes up to ten years after stroke: analysis from the prospective South London Stroke Register. PLoS Med 8, e1001033.
134. Yarom, Y., and Hounsgaard, J. (2011). Voltage fluctuations in neurons: signal or noise? Physiol Rev 91, 917-929.
135. Yu, S., Huang, D., Singer, W., and Nikolic, D. (2008). A small world of neuronal synchrony. Cereb Cortex 18, 2891-2901.
136. Zaehle, T., Rach, S., and Herrmann, C.S. (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PloS one 5, e13766.
137. Zhou, C., Kurths, J., and Hu, B. (2003). Frequency and phase locking of noise-sustained oscillations in coupled excitable systems: array-enhanced resonances. Phys Rev EStat Nonlin Soft Matter Phys 67, 030101.
138. Ziemann, U., and Siebner, H.R. (2008). Modifying motor learning through gating and homeostatic metaplasticity, in: Brain Stimul.).