State-Dependent Variability of Neuronal Responses to Transcranial Magnetic Stimulation of the Visual Cortex

Neuron

Volumn 62, Issue 2, 2009, Pages 291-303

  Pasley, Brian N ^a,b   Allen, Elena A ^a,b   Freeman, Ralph D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Sysneuro

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; EXPERIMENTAL CAT; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; STIMULUS RESPONSE; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; BRAIN MAPPING; CATS; ELECTRIC STIMULATION; ELECTRODES; EVOKED POTENTIALS, VISUAL; NEURONS; PHOTIC STIMULATION; REACTION TIME; SPECTRUM ANALYSIS; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 65249183830     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.03.012     Document Type: Article

References (87)

1. Allen E.A., Pasley B.N., Duong T., and Freeman R.D. Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317 (2007) 1918-1921
2. Ambrosini A., de Noordhout A.M., Sandor P.S., and Schoenen J. Electrophysiological studies in migraine: a comprehensive review of their interest and limitations. Cephalalgia 23 Suppl 1 (2003) 13-31
3. Barker A.T., Jalinous R., and Freeston I.L. Non-invasive magnetic stimulation of human motor cortex. Lancet 1 (1985) 1106-1107
4. Belitski A., Gretton A., Magri C., Murayama Y., Montemurro M.A., Logothetis N.K., and Panzeri S. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 28 (2008) 5696-5709
5. Berardelli A., Inghilleri M., Rothwell J.C., Romeo S., Curra A., Gilio F., Modugno N., and Manfredi M. Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp. Brain Res. 122 (1998) 79-84
6. Bestmann S., Ruff C.C., Blakemore C., Driver J., and Thilo K.V. Spatial attention changes excitability of human visual cortex to direct stimulation. Curr. Biol. 17 (2007) 134-139
7. Bestmann S., Swayne O., Blankenburg F., Ruff C.C., Haggard P., Weiskopf N., Josephs O., Driver J., Rothwell J.C., and Ward N.S. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb. Cortex 18 (2008) 1281-1291
8. Bohning D.E., Shastri A., McConnell K.A., Nahas Z., Lorberbaum J.P., Roberts D.R., Teneback C., Vincent D.J., and George M.S. A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol. Psychiatry 45 (1999) 385-394
9. Brighina F., Piazza A., Daniele O., and Fierro B. Modulation of visual cortical excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp. Brain Res. 145 (2002) 177-181
10. Brighina F., Piazza A., Vitello G., Aloisio A., Palermo A., Daniele O., and Fierro B. rTMS of the prefrontal cortex in the treatment of chronic migraine: a pilot study. J. Neurol. Sci. 227 (2004) 67-71
11. Bruns A. Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches?. J. Neurosci. Methods 137 (2004) 321-332
12. Burt T., Lisanby S.H., and Sackeim H.A. Neuropsychiatric applications of transcranial magnetic stimulation: a meta analysis. Int. J. Neuropsychopharmacol. 5 (2002) 73-103
13. Buschman T.J., and Miller E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315 (2007) 1860-1862
14. Butefisch C.M., Davis B.C., Wise S.P., Sawaki L., Kopylev L., Classen J., and Cohen L.G. Mechanisms of use-dependent plasticity in the human motor cortex. Proc. Natl. Acad. Sci. USA 97 (2000) 3661-3665
15. Buzsaki G., and Draguhn A. Neuronal oscillations in cortical networks. Science 304 (2004) 1926-1929
16. Cahn S.D., Herzog A.G., and Pascual-Leone A. Paired-pulse transcranial magnetic stimulation: effects of hemispheric laterality, gender, and handedness in normal controls. J. Clin. Neurophysiol. 20 (2003) 371-374
17. Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., and Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313 (2006) 1626-1628
18. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M., and Cohen L.G. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48 (1997) 1398-1403
19. Cohen J., Cohen P., West S.G., and Aiken L.S. Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences (2003), Lawrence Erlbaum, Mahwah, NJ
20. Couturier J.L. Efficacy of rapid-rate repetitive transcranial magnetic stimulation in the treatment of depression: a systematic review and meta-analysis. J. Psychiatry Neurosci. 30 (2005) 83-90
21. de Labra C., Rivadulla C., Grieve K., Marino J., Espinosa N., and Cudeiro J. Changes in visual responses in the feline dLGN: selective thalamic suppression induced by transcranial magnetic stimulation of V1. Cereb. Cortex 17 (2007) 1376-1385
22. Destexhe A., Contreras D., and Steriade M. Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J. Neurosci. 19 (1999) 4595-4608
23. Efron B., and Tibshirani R. An Introduction to the Bootstrap (1994), Chapman & Hall, New York
24. Engel A.K., Fries P., and Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2 (2001) 704-716
25. Fregni F., Simon D.K., Wu A., and Pascual-Leone A. Non-invasive brain stimulation for Parkinson's disease: a systematic review and meta-analysis of the literature. J. Neurol. Neurosurg. Psychiatry 76 (2005) 1614-1623
26. Fries P., Reynolds J.H., Rorie A.E., and Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291 (2001) 1560-1563
27. Fritsch G., and Hitzig E. Ueber die elektrishe Erregarkeit des Grosshirns (1870), Charles C. Thomas, Springfield, IL
28. George M.S., Wassermann E.M., and Post R.M. Transcranial magnetic stimulation: a neuropsychiatric tool for the 21st century. J. Neuropsychiatry Clin. Neurosci. 8 (1996) 373-382
29. Gross M., Nakamura L., Pascual-Leone A., and Fregni F. Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta-analysis comparing the recent vs. the earlier rTMS studies. Acta Psychiatr. Scand. 116 (2007) 165-173
30. Gur M., and Snodderly D.M. High response reliability of neurons in primary visual cortex (V1) of alert, trained monkeys. Cereb. Cortex 16 (2006) 888-895
31. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 55 (2007) 187-199
32. Heeger D.J., and Ress D. What does fMRI tell us about neuronal activity?. Nat. Rev. Neurosci. 3 (2002) 142-151
33. Henrie J.A., and Shapley R. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol. 94 (2005) 479-490
34. Holscher C., Anwyl R., and Rowan M.J. Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J. Neurosci. 17 (1997) 6470-6477
35. Horsley V., and Clarke R. The structure and functions of the cerebellum examined by a new method. Brain 31 (1908) 45-124
36. Houweling A.R., and Brecht M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451 (2008) 65-68
37. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., and Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 45 (2005) 201-206
38. Huber D., Petreanu L., Ghitani N., Ranade S., Hromadka T., Mainen Z., and Svoboda K. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451 (2008) 61-64
39. Izhikevich E.M. Bursting. Scholarpedia 1 (2006) 1300
40. Jarvis M.R., and Mitra P.P. Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput. 13 (2001) 717-749
41. Jing H., and Takigawa M. Observation of EEG coherence after repetitive transcranial magnetic stimulation. Clin. Neurophysiol. 111 (2000) 1620-1631
42. Kringelbach M.L., Jenkinson N., Owen S.L., and Aziz T.Z. Translational principles of deep brain stimulation. Nat. Rev. Neurosci. 8 (2007) 623-635
43. Lachaux J.P., Rodriguez E., Martinerie J., and Varela F.J. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8 (1999) 194-208
44. Lisanby S.H., and Belmaker R.H. Animal models of the mechanisms of action of repetitive transcranial magnetic stimulation (RTMS): comparisons with electroconvulsive shock (ECS). Depress. Anxiety 12 (2000) 178-187
45. Liu J., and Newsome W.T. Local field potential in cortical area MT: stimulus tuning and behavioral correlations. J. Neurosci. 26 (2006) 7779-7790
46. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 453 (2008) 869-878
47. Logothetis N.K., Kayser C., and Oeltermann A. In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron 55 (2007) 809-823
48. Manly C.F.J. Randomization and Monte-Carlo Methods in Biology (1991), Chapman & Hall, New York
49. Mantovani M., Van Velthoven V., Fuellgraf H., Feuerstein T.J., and Moser A. Neuronal electrical high frequency stimulation enhances GABA outflow from human neocortical slices. Neurochem. Int. 49 (2006) 347-350
50. Martin J.L., Barbanoj M.J., Schlaepfer T.E., Thompson E., Perez V., and Kulisevsky J. Repetitive transcranial magnetic stimulation for the treatment of depression. Systematic review and meta-analysis. Br. J. Psychiatry 182 (2003) 480-491
51. Massimini M., Ferrarelli F., Huber R., Esser S.K., Singh H., and Tononi G. Breakdown of cortical effective connectivity during sleep. Science 309 (2005) 2228-2232
52. Miller G. Neuroscience. Uncovering the magic in magnetic brain stimulation. Science 317 (2007) 1846
53. Mitra P.P., and Pesaran B. Analysis of dynamic brain imaging data. Biophys. J. 76 (1999) 691-708
54. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65 (1985) 37-100
55. Moliadze V., Zhao Y., Eysel U., and Funke K. Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J. Physiol. 553 (2003) 665-679
56. Moliadze V., Giannikopoulos D., Eysel U.T., and Funke K. Paired-pulse transcranial magnetic stimulation protocol applied to visual cortex of anaesthetized cat: effects on visually evoked single-unit activity. J. Physiol. 566 (2005) 955-965
57. Niessing J., Ebisch B., Schmidt K.E., Niessing M., Singer W., and Galuske R.A. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309 (2005) 948-951
58. Oliveri M., and Calvo G. Increased visual cortical excitability in ecstasy users: a transcranial magnetic stimulation study. J. Neurol. Neurosurg. Psychiatry 74 (2003) 1136-1138
59. Oliviero A., Strens L.H., Di Lazzaro V., Tonali P.A., and Brown P. Persistent effects of high frequency repetitive TMS on the coupling between motor areas in the human. Exp. Brain Res. 149 (2003) 107-113
60. Pascual-Leone A., Tormos J.M., Keenan J., Tarazona F., Canete C., and Catala M.D. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J. Clin. Neurophysiol. 15 (1998) 333-343
61. Pascual-Leone A., Walsh V., and Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Curr. Opin. Neurobiol. 10 (2000) 232-237
62. Patton H.D., and Amassian V.E. Single- and multiple-unit analysis of cortical stage of pyramidal tract activation. J. Neurophysiol. 17 (1954) 345-363
63. Paus T. Inferring causality in brain images: a perturbation approach. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360 (2005) 1109-1114
64. Pereda E., Quiroga R.Q., and Bhattacharya J. Nonlinear multivariate analysis of neurophysiological signals. Prog. Neurobiol. 77 (2005) 1-37
65. Pesaran B., Pezaris J.S., Sahani M., Mitra P.P., and Andersen R.A. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat. Neurosci. 5 (2002) 805-811
66. Reich D.S., Mechler F., Purpura K.P., and Victor J.D. Interspike intervals, receptive fields, and information encoding in primary visual cortex. J. Neurosci. 20 (2000) 1964-1974
67. Ridding M.C., and Rothwell J.C. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nat. Rev. Neurosci. 8 (2007) 559-567
68. Romei V., Brodbeck V., Michel C., Amedi A., Pascual-Leone A., and Thut G. Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cereb. Cortex 18 (2008) 2010-2018
69. Ruff C.C., Blankenburg F., Bjoertomt O., Bestmann S., Freeman E., Haynes J.D., Rees G., Josephs O., Deichmann R., and Driver J. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr. Biol. 16 (2006) 1479-1488
70. Saalmann Y.B., Pigarev I.N., and Vidyasagar T.R. Neural mechanisms of visual attention: how top-down feedback highlights relevant locations. Science 316 (2007) 1612-1615
71. Sack A.T., Kohler A., Bestmann S., Linden D.E., Dechent P., Goebel R., and Baudewig J. Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous fMRI, TMS, and behavioral studies. Cereb. Cortex 17 (2007) 2841-2852
72. Salinas F.S., Lancaster J.L., and Fox P.T. Detailed 3D models of the induced electric field of transcranial magnetic stimulation coils. Phys. Med. Biol. 52 (2007) 2879-2892
73. Sauseng P., Klimesch W., Gerloff C., and Hummel F.C. Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex. Neuropsychologia 47 (2009) 284-288
74. Siegel M., and Konig P. A functional gamma-band defined by stimulus-dependent synchronization in area 18 of awake behaving cats. J. Neurosci. 23 (2003) 4251-4260
75. Silvanto J., and Muggleton N.G. New light through old windows: moving beyond the "virtual lesion" approach to transcranial magnetic stimulation. Neuroimage 39 (2008) 549-552
76. Silvanto J., Muggleton N.G., Cowey A., and Walsh V. Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur. J. Neurosci. 25 (2007) 1874-1881
77. Skottun B.C., De Valois R.L., Grosof D.H., Movshon J.A., Albrecht D.G., and Bonds A.B. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31 (1991) 1079-1086
78. Stevens C.F., and Zador A.M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1 (1998) 210-217
79. Stewart L.M., Walsh V., and Rothwell J.C. Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study. Neuropsychologia 39 (2001) 415-419
80. Strens L.H., Oliviero A., Bloem B.R., Gerschlager W., Rothwell J.C., and Brown P. The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence. Clin. Neurophysiol. 113 (2002) 1279-1285
81. Tehovnik E.J., Tolias A.S., Sultan F., Slocum W.M., and Logothetis N.K. Direct and indirect activation of cortical neurons by electrical microstimulation. J. Neurophysiol. 96 (2006) 512-521
82. Terao Y., and Ugawa Y. Basic mechanisms of TMS. J. Clin. Neurophysiol. 19 (2002) 322-343
83. Theodore W.H. Transcranial magnetic stimulation in epilepsy. Epilepsy Curr. 3 (2003) 191-197
84. Thomson D.J. Spectrum estimation and harmonic analysis. Proc. IEEE 70 (1982) 1055-1096
85. Van Der Werf Y.D., Sadikot A.F., Strafella A.P., and Paus T. The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions. Exp. Brain Res. 175 (2006) 246-255
86. Wespatat V., Tennigkeit F., and Singer W. Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex. J. Neurosci. 24 (2004) 9067-9075
87. Ziemann U., Tam A., Butefisch C., and Cohen L.G. Dual modulating effects of amphetamine on neuronal excitability and stimulation-induced plasticity in human motor cortex. Clin. Neurophysiol. 113 (2002) 1308-1315