Neuromodulation for brain disorders: Challenges and opportunities

IEEE Transactions on Biomedical Engineering

Volumn 60, Issue 3, 2013, Pages 610-624

  Johnson, Matthew D ^a   Lim, Hubert H ^a   Netoff, Theoden I ^a   Connolly, Allison T ^a   Johnson, Nessa ^a   Roy, Abhrajeet ^a   Holt, Abbey ^b   Lim, Kelvin O ^b   Carey, James R ^b   Vitek, Jerrold L ^b   He, Bin ^c  

^a University of Minnesota   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Deep brain stimulation (DBS); Intracranial cortical stimulation (ICS); Neuroengineering; Neuromodulation; Transcranial direct current stimulation (tDCS); Transcranial magnetic stimulation (TMS)

Indexed keywords

CORTICAL STIMULATION; DEEP BRAIN STIMULATION; DIRECT CURRENT; NEUROENGINEERING; NEUROMODULATION; TRANSCRANIAL MAGNETIC STIMULATION;

FUNCTIONAL ELECTRIC STIMULATION; INTELLIGENT CONTROL;

NEUROSURGERY;

ABLATION THERAPY; ACOUSTIC NERVE FIBER; ALGORITHM; BASAL GANGLION; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN DISEASE; CEREBROVASCULAR ACCIDENT; COCHLEA PROSTHESIS; DEPRESSION; DYSTONIA; ELECTRIC CURRENT; EPILEPSY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; IMPLANTABLE PULSE GENERATOR; INTRACRANIAL CORTICAL STIMULATION; INTRACTABLE EPILEPSY; LIMBIC CORTEX; MAGNETIC FIELD; MAJOR DEPRESSION; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NEUROMODULATION; OPTOGENETICS; PAIN; PARKINSON DISEASE; PERIAQUEDUCTAL GRAY MATTER; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SPIKE WAVE; SUBTHALAMIC NUCLEUS; TINNITUS; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; TREMOR; VIRAL GENE DELIVERY SYSTEM; WHITE MATTER;

ANIMALS; BIOMEDICAL RESEARCH; BRAIN DISEASES; DEEP BRAIN STIMULATION; HUMANS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84884660373     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2013.2244890     Document Type: Review

References (137)

1. E. S. Krames, P. H. Peckham, A. R. Rezai, and F. Aboelsaad, "What is Neuromodulation?" in Neuromodulation, E. S. Krames, P. H. Peckham, and A. R. Rezai, Eds. San Diego, CA, USA: Academic, 2009, pp. 3-8.
2. R. Hassler, T. Riechert, F. Mundinger, W. Umbach, and J. A. Ganglberger, "Physiological observations in stereotaxic operations in extrapyramidal motor disturbances," Brain, vol. 83, pp. 337-50, 1960.
3. C. C. McIntyre, W. M. Grill, D. L. Sherman, and N. V. Thakor, "Cellular effects of deep brain stimulation: Model-based analysis of activation and inhibition," J. Neurophysiol., vol. 91, no. 4, pp. 1457-1469, Apr. 2004.
4. T. Boraud, E. Bezard, B. Bioulac, and C. Gross, "High frequency stimulation of the internal Globus Pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey," Neurosci. Lett., vol. 215, no. 1, pp. 17-20, Aug. 30, 1996.
5. T. Hashimoto, C. M. Elder, M. S. Okun, S. K. Patrick, and J. L. Vitek, "Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons," J. Neurosci., vol. 23, no. 5, pp. 1916-1923, Mar. 1, 2003.
6. J. B. Ranck, Jr., "Which elements are excited in electrical stimulation of mammalian central nervous system: A review," Brain Res., vol. 98, no. 3, pp. 417-440, Nov. 21, 1975.
7. N. P. Stover, M. S. Okun, M. L. Evatt, D. V. Raju, R. A. Bakay, and J. L. Vitek, "Stimulation of the subthalamic nucleus in a patient with Parkinson disease and essential tremor," Arch. Neurol., vol. 62, no. 1, pp. 141-143, Jan. 2005.
8. S. Namba, T. Wani, Y. Shimizu, N. Fujiwara, Y. Namba, S. Nakamua, and A. Nishimoto, "Sensory and motor responses to deep brain stimulation. Correlation with anatomical structures," J. Neurosurg., vol. 63, no. 2, pp. 224-234, Aug. 1985. (Pubitemid 15246088)
9. W. M. Grill, A. N. Snyder, and S. Miocinovic, "Deep brain stimulation creates an informational lesion of the stimulated nucleus," Neuroreport, vol. 15, no. 7, pp. 1137-1140, May 19, 2004. (Pubitemid 38670068)
10. A. D. Dorval, A. M. Kuncel, M. J. Birdno, D. A. Turner, and W. M. Grill, "Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity," J. Neurophysiol., vol. 104, no. 2, pp. 911-921, Aug. 2010.
11. M. D. Johnson, J. L. Vitek, and C. C. McIntyre, "Pallidal stimulation that improves parkinsonian motor symptoms also modulates neuronal firing patterns in primary motor cortex in the MPTP-treated monkey," Exp. Neurol., vol. 219, no. 1, pp. 359-62, Sep. 2009.
12. F. Agnesi, A. T. Connolly, K. B. Baker, J. L. Vitek, and M. D. Johnson, "Effects of pallidal DBS on the transmission of movementrelated activity in motor thalamus," Soc. Neurosci. Abs, p. 761.18, 2012.
13. C. Hauptmann and P. A. Tass, "Restoration of segregated, physiological neuronal connectivity by desynchronizing stimulation," J. Neural Eng., vol. 7, no. 5, p. 056008, Oct. 2010.
14. J. F. Atherton and M. D. Bevan, "Ionic mechanisms underlying autonomous action potential generation in the somata and dendrites of GABAergic substantia nigra pars reticulata neurons in vitro," J. Neurosci., vol. 25, no. 36, pp. 8272-8281, Sep. 7, 2005.
15. C. J. Wilson, B. Beverlin, 2nd, and T. Netoff, "Chaotic desynchronization as the therapeutic mechanism of deep brain stimulation," Front Syst. Neurosci., vol. 5, p. 50, 2011.
16. J. L. Vitek, T. Hashimoto, J. Peoples, M. R. DeLong, and R. A. Bakay, "Acute stimulation in the external segment of the globus pallidus improves parkinsonian motor signs," Mov Disord., vol. 19, no. 8, pp. 907-915, Aug. 2004. (Pubitemid 39199257)
17. J. Yianni, P. G. Bain, R. P. Gregory, D. Nandi, C. Joint, R. B. Scott, J. F. Stein, and T. Z. Aziz, "Post-operative progress of dystonia patients following globus pallidus internus deep brain stimulation," Eur. J. Neurol., vol. 10, no. 3, pp. 239-247, May 2003. (Pubitemid 36609478)
18. H. S. Mayberg, A. M. Lozano, V. Voon, H. E. McNeely, D. Seminowicz, C. Hamani, J. M. Schwalb, and S. H. Kennedy, "Deep brain stimulation for treatment-resistant depression," Neuron, vol. 45, no. 5, pp. 651-660, Mar. 3, 2005.
19. D. A. Malone, Jr., D. D. Dougherty, A. R. Rezai, L. L. Carpenter, G. M. Friehs, E. N. Eskandar, S. L. Rauch, S. A. Rasmussen, A. G. Machado, C. S. Kubu, A. R. Tyrka, L. H. Price, P. H. Stypulkowski, J. E. Giftakis, M. T. Rise, P. F. Malloy, S. P. Salloway, and B. D. Greenberg, "Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression," Biol. Psychiatry, vol. 65, no. 4, pp. 267-275, Feb. 15, 2009.
20. R. Fisher, V. Salanova, T. Witt, R. Worth, T. Henry, R. Gross, K. Oommen, I. Osorio, J. Nazzaro, D. Labar, M. Kaplitt, M. Sperling, E. Sandok, J. Neal, A. Handforth, J. Stern, A. DeSalles, S. Chung, A. Shetter, D. Bergen, R. Bakay, J. Henderson, J. French, G. Baltuch, W. Rosenfeld, A. Youkilis, W. Marks, P. Garcia, N. Barbaro, N. Fountain, C. Bazil, R. Goodman, G. McKhann, K. Babu Krishnamurthy, S. Papavassiliou, C. Epstein, J. Pollard, L. Tonder, J. Grebin, R. Coffey, and N. Graves, "Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy," Epilepsia, vol. 51, no. 5, pp. 899-908, May 2010.
21. A. W. Laxton, D. F. Tang-Wai, M. P. McAndrews, D. Zumsteg, R.Wennberg, R. Keren, J. Wherrett, G. Naglie, C. Hamani, G. S. Smith, and A. M. Lozano, "A phase I trial of deep brain stimulation of memory circuits in Alzheimer's disease," Ann. Neurol., vol. 68, no. 4, pp. 521-534, Oct. 2010.
22. J. Giacino, J. J. Fins, A. Machado, and N. D. Schiff, "Central thalamic deep brain stimulation to promote recovery from chronic posttraumatic minimally conscious state: Challenges and opportunities," Neuromodulation, vol. 15, no. 4, pp. 339-349, Jul. 2012.
23. S. L. Owen, A. L. Green, D. D. Nandi, R. G. Bittar, S. Wang, and T. Z. Aziz, "Deep brain stimulation for neuropathic pain," Acta Neurochir. Suppl., vol. 97, no. Pt 2, pp. 111-116, 2007.
24. G. C. McConnell, R. Q. So, J. D. Hilliard, P. Lopomo, and W. M. Grill, "Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns," J. Neurosci., vol. 32, no. 45, pp. 15657-15668, Nov. 7, 2012.
25. K. Deisseroth, "Optogenetics," Nat. Methods, vol. 8, no. 1, pp. 26-29, Jan. 2011.
26. V. Gradinaru, M. Mogri, K. R. Thompson, J. M. Henderson, and K. Deisseroth, "Optical deconstruction of parkinsonian neural circuitry," Science, vol. 324, no. 5925, pp. 354-359, Apr. 17, 2009.
27. M. Keane, S. Deyo, A. Abosch, J. A. Bajwa, and M. D. Johnson, "Improved spatial targeting with directionally segmented deep brain stimulation leads for treating essential tremor," J. Neural Eng., vol. 9, no. 4, p. 046005, Jun. 25, 2012.
28. D. McCreery, A. Lossinsky, V. Pikov, and X. Liu, "Microelectrode array for chronic deep-brain microstimulation and recording," IEEE Trans. Biomed. Eng., vol. 53, no. 4, pp. 726-737, Apr. 2006.
29. A. A. Kuhn, A. Kupsch, G. H. Schneider, and P. Brown, "Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease," Eur. J. Neurosci., vol. 23, no. 7, pp. 1956-1960, Apr. 2006.
30. A. A. Kuhn, F. Kempf, C. Brucke, L. Gaynor Doyle, I. Martinez-Torres, A. Pogosyan, T. Trottenberg, A. Kupsch, G. H. Schneider, M. I. Hariz, W. Vandenberghe, B. Nuttin, and P. Brown, "High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson's disease in parallel with improvement in motor performance," J. Neurosci., vol. 28, no. 24, pp. 6165-6173, Jun. 11, 2008.
31. M. Rosa, G. Giannicola, D. Servello, S. Marceglia, C. Pacchetti, M. Porta, M. Sassi, E. Scelzo, S. Barbieri, and A. Priori, "Subthalamic local field beta oscillations during ongoing deep brain stimulation in Parkinson's disease in hyperacute and chronic phases," Neurosignals, vol. 19, no. 3, pp. 151-162, 2011.
32. M. Kaminska, D. E. Lumsden, K. Ashkan, I. Malik, R. Selway, and J. P. Lin, "Rechargeable deep brain stimulators in the management of paediatric dystonia: Well tolerated with a low complication rate," Stereotact. Funct. Neurosurg., vol. 90, no. 4, pp. 233-239, 2012.
33. C. R. Butson, S. E. Cooper, J. M. Henderson, and C. C. McIntyre, "Patient-specific analysis of the volume of tissue activated during deep brain stimulation," Neuroimage, vol. 34, no. 2, pp. 661-670, Jan. 15, 2007.
34. G. Clark, "The multi-channel cochlear implant: Past, present and future perspectives," Cochlear Implants Int., vol. 10, no. Suppl 1, pp. 2-13, 2009.
35. A. L. Sampaio, M. F. Araujo, and C. A. Oliveira, "New criteria of indication and selection of patients to cochlear implant," Int. J. Otolaryngol., vol. 2011, art. no. 573968, 2011.
36. B. S. Wilson and M. F. Dorman, "Cochlear implants: A remarkable past and a brilliant future," Hear Res., vol. 242, no. 1-2, pp. 3-21, Aug. 2008.
37. B. H. Bonham and L. M. Litvak, "Current focusing and steering: Modeling, physiology, and psychophysics," Hear Res., vol. 242, no. 1-2, pp. 141-153, Aug. 2008.
38. J. F. Patrick, P. A. Busby, and P. J. Gibson, "The development of the Nucleus Freedom Cochlear implant system," Trends Amplif., vol. 10, no. 4, pp. 175-200, Dec. 2006.
39. L. Colletti, R. Shannon, and V. Colletti, "Auditory brainstem implants for neurofibromatosis type 2," Curr. Opin. Otolaryngol. Head Neck Surg., vol. 20, no. 5, pp. 353-357, Oct. 2012.
40. T. Lenarz, H. H. Lim, G. Reuter, J. F. Patrick, and M. Lenarz, "The auditory midbrain implant: A new auditory prosthesis for neural deafness-concept and device description," Otol. Neurotol., vol. 27, no. 6, pp. 838-843, Sep. 2006. (Pubitemid 44325516)
41. R. Behr, J. Muller, W. Shehata-Dieler, H. P. Schlake, J. Helms, K. Roosen, N. Klug, B. Holper, and A. Lorens, "The high rate CIS auditory brainstem implant for restoration of hearing in NF-2 Patients," Skull Base, vol. 17, no. 2, pp. 91-107, Mar. 2007.
42. T. Lenarz and H. H. Lim, "Auditory midbrain implant applications for tinnitus," presented at the NIH-NIDCD Workshop: Brain Stimulat. Treatment Tinnitus, Bethesda, MD, USA, 2009.
43. W. Penfield and H. Jasper, Epilepsy and the Functional Anatomy of the Human Brain. Boston, MA, USA: Little, Brown, 1954.
44. J. P. Lefaucheur, "Neurophysiology of cortical stimulation," Int. Rev. Neurobiol., vol. 107, pp. 57-85, 2012.
45. R. Levy, S. Ruland, M. Weinand, D. Lowry, R. Dafer, and R. Bakay, "Cortical stimulation for the rehabilitation of patients with hemiparetic stroke: A multicenter feasibility study of safety and efficacy," J. Neurosurg., vol. 108, no. 4, pp. 707-714, Apr. 2008. (Pubitemid 351498966)
46. D. De Ridder, S. Vanneste, S. Kovacs, S. Sunaert, T. Menovsky, P. van de Heyning, and A. Moller, "Transcranial magnetic stimulation and extradural electrodes implanted on secondary auditory cortex for tinnitus suppression," J. Neurosurg., vol. 114, no. 4, pp. 903-911, Apr. 2011.
47. T. Tsubokawa, Y. Katayama, T. Yamamoto, T. Hirayama, and S. Koyama, "Chronicmotor cortex stimulation for the treatment of central pain," Acta Neurochir. Suppl. (Wien), vol. 52, pp. 137-139, 1991.
48. A. Wongsarnpigoon and W. M. Grill, "Computer-based model of epidural motor cortex stimulation: Effects of electrode position and geometry on activation of cortical neurons," Clin. Neurophysiol., vol. 123, no. 1, pp. 160-72, Jan. 2012.
49. L. R. Hochberg, M. D. Serruya, G. M. Friehs, J. A. Mukand, M. Saleh, A. H. Caplan, A. Branner, D. Chen, R. D. Penn, and J. P. Donoghue, "Neuronal ensemble control of prosthetic devices by a human with tetraplegia," Nature, vol. 442, no. 7099, pp. 164-171, Jul. 13, 2006.
50. E. M. Schmidt, M. J. Bak, F. T. Hambrecht, C. V. Kufta, D. K. O'Rourke, and P. Vallabhanath, "Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex," Brain, vol. 119, no. Pt 2, pp. 507-522, Apr. 1996.
51. M. H. Histed, V. Bonin, and R. C. Reid, "Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation," Neuron, vol. 63, no. 4, pp. 508-522, Aug. 27, 2009.
52. M. J. Morrell, "Responsive cortical stimulation for the treatment of medically intractable partial epilepsy," Neurology, vol. 77, no. 13, pp. 1295-1304, Sep. 27, 2011.
53. J. D. Rolston, S. A. Desai, N. G. Laxpati, and R. E. Gross, "Electrical stimulation for epilepsy: Experimental approaches," Neurosurg. Clin. N. Amer., vol. 22, no. 4, pp. 425-442, Oct. 2011.
54. A. J. Fenoy, M. A. Severson, I. O. Volkov, J. F. Brugge, and M. A. Howard, 3rd, "Hearing suppression induced by electrical stimulation of human auditory cortex," Brain Res., vol. 1118, no. 1, pp. 75-83, Nov. 6, 2006.
55. J. Zhang, "Auditory cortex stimulation to suppress tinnitus: Mechanisms and strategies," Hear Res., vol. 295, pp. 38-57, Jan. 2013.
56. J. J. Eggermont, "Hearing loss, hyperacusis, or tinnitus: What is modeled in animal research?," Hear Res., vol. 295, pp. 140-149, Jan. 2013.
57. J. G. Turner, "Behavioral measures of tinnitus in laboratory animals," Prog. Brain Res., vol. 166, pp. 147-156, 2007.
58. J. Ursick and H. Staecker, "An overview of animal models of tinnitus," B-ENT, vol. 3, no. Suppl 7, pp. 23-25, 2007.
59. C. P. Lanting, E. de Kleine, and P. van Dijk, "Neural activity underlying tinnitus generation: Results from PET and fMRI," Hear Res., vol. 255, no. 1-2, pp. 1-13, Sep. 2009.
60. B. Langguth, M. Schecklmann, A. Lehner, M. Landgrebe, T. B. Poeppl, P. M. Kreuzer, W. Schlee, N. Weisz, S. Vanneste, and D. De Ridder, "Neuroimaging and neuromodulation: Complementary approaches for identifying the neuronal correlates of tinnitus," Front Syst. Neurosci., vol. 6, art. no. 15, pp. 1-20, 2012.
61. N. Weisz, T. Hartmann, N. Muller, I. Lorenz, and J. Obleser, "Alpha rhythms in audition: Cognitive and clinical perspectives," Front Psychol., vol. 2, art. no. 73, pp. 1-15, 2011.
62. S. W. Cheung and P. S. Larson, "Tinnitus modulation by deep brain stimulation in locus of caudate neurons (area LC)," Neuroscience, vol. 169, no. 4, pp. 1768-1778, Sep. 15, 2010.
63. J. Viventi, D. H. Kim, L. Vigeland, E. S. Frechette, J. A. Blanco, Y. S. Kim, A. E. Avrin, V. R. Tiruvadi, S. W. Hwang, A. C. Vanleer, D. F. Wulsin, K. Davis, C. E. Gelber, L. Palmer, J. Van der Spiegel, J. Wu, J. Xiao, Y. Huang, D. Contreras, J. A. Rogers, and B. Litt, "Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo," Nat. Neurosci., vol. 14, no. 12, pp. 1599-1605, Dec. 2011.
64. X. Han, "Optogenetics in the nonhuman primate," Prog. Brain Res., vol. 196, pp. 215-233, 2012.
65. F. J. Seijo, M. A. Alvarez-Vega, J. C. Gutierrez, F. Fdez-Glez, and B. Lozano, "Complications in subthalamic nucleus stimulation surgery for treatment of Parkinson's disease. Review of 272 procedures," Acta Neurochir (Wien), vol. 149, no. 9, pp. 867-875, 2007. (Pubitemid 47319154)
66. M. A. Nitsche, L. G. Cohen, E. M. Wassermann, A. Priori, N. Lang, A. Antal, W. Paulus, F. Hummel, P. S. Boggio, F. Fregni, and A. Pascual-Leone, "Transcranial direct current stimulation: State of the art 2008," Brain Stimul., vol. 1, no. 3, pp. 206-223, Jul. 2008.
67. A. Datta, V. Bansal, J. Diaz, J. Patel, D. Reato, and M. Bikson, "Gyriprecise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad," Brain Stimul., vol. 2, no. 4, pp. 201-207, 207 e1, Oct. 2009.
68. M. Parazzini, S. Fiocchi, E. Rossi, A. Paglialonga, and P. Ravazzani, "Transcranial direct current stimulation: Estimation of the electric field and of the current density in an anatomical human head model," IEEE Trans. Biomed. Eng., vol. 58, no. 6, pp. 1773-1780, Jun. 2011.
69. V. P. Clark, B. A. Coffman, A. R. Mayer, M. P. Weisend, T. D. Lane, V. D. Calhoun, E. M. Raybourn, C. M. Garcia, and E. M. Wassermann, "TDCS guided using fMRI significantly accelerates learning to identify concealed objects," Neuroimage, vol. 59, no. 1, pp. 117-128, Jan. 2, 2012.
70. S. Zaghi, M. Acar, B. Hultgren, P. S. Boggio, and F. Fregni, "Noninvasive brain stimulation with low-intensity electrical currents: Putative mechanisms of action for direct and alternating current stimulation," Neuroscientist, vol. 16, no. 3, pp. 285-307, Jun. 2010.
71. A. R. Brunoni, M. A. Nitsche, N. Bolognini, M. Bikson, T. Wagner, L. Merabet, D. J. Edwards, A. Valero-Cabre, A. Rotenberg, A. Pascual-Leone, R. Ferrucci, A. Priori, P. S. Boggio, and F. Fregni, "Clinical research with transcranial direct current stimulation (tDCS): Challenges and future directions," Brain Stimul., vol. 5, no. 3, pp. 175-195, Jul. 2012.
72. C. Y. Chan and C. Nicholson, "Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum," J. Physiol., vol. 371, pp. 89-114, Feb. 1986. (Pubitemid 16139407)
73. B. J. Gluckman, E. J. Neel, T. I. Netoff, W. L. Ditto, M. L. Spano, and S. J. Schiff, "Electric field suppression of epileptiform activity in hippocampal slices," J. Neurophysiol., vol. 76, no. 6, pp. 4202-4205, Dec. 1996.
74. M. Bikson, M. Inoue, H. Akiyama, J. K. Deans, J. E. Fox, H. Miyakawa, and J. G. Jefferys, "Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro," J. Physiol., vol. 557, no. Pt 1, pp. 175-190, May 15, 2004.
75. J. G. Jefferys, J. Deans, M. Bikson, and J. Fox, "Effects of weak electric fields on the activity of neurons and neuronal networks," Radiat. Prot Dosimetry, vol. 106, no. 4, pp. 321-323, 2003. (Pubitemid 37540479)
76. M. A. Nitsche and W. Paulus, "Excitability changes induced in the human motor cortex byweak transcranial direct current stimulation," J. Physiol., vol. 527, no. Pt 3, pp. 633-639, Sep. 15, 2000.
77. A. R. Brunoni, J. Amadera, B. Berbel, M. S. Volz, B. G. Rizzerio, and F. Fregni, "A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation," Int. J. Neuropsychopharmacol., vol. 14, no. 8, pp. 1133-1145, Sep. 2011.
78. L. Jacobson, A. Ezra, U. Berger, and M. Lavidor, "Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation," Clin. Neurophysiol., vol. 123, no. 5, pp. 979-984, May. 2012.
79. J. Matsumoto, T. Fujiwara, O. Takahashi, M. Liu, A. Kimura, and J. Ushiba, "Modulation of mu rhythm desynchronization during motor imagery by transcranial direct current stimulation," J. Neuroeng. Rehabil., vol. 7, pp. 1-5, 2010.
80. R. Polania, M. A. Nitsche, and W. Paulus, "Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation," Hum Brain Mapp., vol. 32, no. 8, pp. 1236-1249, Aug. 2011.
81. T. Zaehle, P. Sandmann, J. D. Thorne, L. Jancke, and C. S. Herrmann, "Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: Combined behavioural and electrophysiological evidence," BMC Neurosci., vol. 12, pp. 1-11, 2011.
82. M. L. Joy, V. P. Lebedev, and J. S. Gati, "Imaging of current density and current pathways in rabbit brain during transcranial electrostimulation," IEEE Trans. Biomed. Eng., vol. 46, no. 9, pp. 1139-1149, Sep. 1999.
83. S. H. Jang, S. H. Ahn, W. M. Byun, C. S. Kim, M. Y. Lee, and Y. H. Kwon, "The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: An fMRI study," Neurosci. Lett., vol. 460, no. 2, pp. 117-120, Aug. 28, 2009.
84. C. R. Kim, D. Y. Kim, L. S. Kim, M. H. Chun, S. J. Kim, and C. H. Park, "Modulation of cortical activity after anodal transcranial direct current stimulation of the lower limb motor cortex: A functional MRI study," Brain Stimul., vol. 5, no. 4, pp. 462-467, Oct. 2012.
85. R. Polania, W. Paulus, and M. A. Nitsche, "Reorganizing the intrinsic functional architecture of the human primary motor cortex during rest with non-invasive cortical stimulation," PLoS One, vol. 7, no. 1, e30971, pp. 1-10, 2012.
86. C. Pena-Gomez, R. Sala-Lonch, C. Junque, I. C. Clemente, D. Vidal, N. Bargallo, C. Falcon, J. Valls-Sole, A. Pascual-Leone, and D. Bartres-Faz, "Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI," Brain Stimul., vol. 5, no. 3, pp. 252-263, Jul. 2012.
87. D. Keeser, T. Meindl, J. Bor, U. Palm, O. Pogarell, C. Mulert, J. Brunelin, H. J. Moller, M. Reiser, and F. Padberg, "Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI," J. Neurosci., vol. 31, no. 43, pp. 15284-15293, Oct. 26, 2011.
88. J. Brunelin, M. Mondino, L. Gassab, F. Haesebaert, L. Gaha, M. F. Suaud-Chagny, M. Saoud, A. Mechri, and E. Poulet, "Examining transcranial direct-current stimulation (tDCS) as a treatment for hallucinations in schizophrenia," Amer. J. Psychiatry, vol. 169, no. 7, pp. 719-724, Jul. 1, 2012.
89. A. Vercammen, J. A. Rushby, C. Loo, B. Short, C. S. Weickert, and T. W. Weickert, "Transcranial direct current stimulation influences probabilistic association learning in schizophrenia," Schizophr Res., vol. 131, no. 1-3, pp. 198-205, Sep. 2011.
90. S. Fecteau, A. Pascual-Leone, D. H. Zald, P. Liguori, H. Theoret, P. S. Boggio, and F. Fregni, "Activation of prefrontal cortex by transcranial direct current stimulation reduces appetite for risk during ambiguous decision making," J. Neurosci., vol. 27, no. 23, pp. 6212-6218, Jun. 6, 2007.
91. S. Fecteau, D. Knoch, F. Fregni, N. Sultani, P. Boggio, and A. Pascual-Leone, "Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: A direct current stimulation study," J. Neurosci., vol. 27, no. 46, pp. 12500-12505, Nov. 14, 2007.
92. A. Demirtas-Tatlidede, A. M. Vahabzadeh-Hagh, and A. Pascual-Leone, "Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders?," Neuropharmacology, vol. 64, pp. 566-578, Jan. 2013.
93. J. P. Dmochowski, A. Datta, M. Bikson, Y. Su, and L. C. Parra, "Optimized multi-electrode stimulation increases focality and intensity at target," J. Neural Eng., vol. 8, no. 4, p. 046011, Aug. 2011.
94. R. J. Sadleir, T. D. Vannorsdall, D. J. Schretlen, and B. Gordon, "Target optimization in transcranial direct current stimulation," Front Psychiatry, vol. 3, p. 90, 2012.
95. P. Faria, F. Fregni, F. Sebastiao, A. I. Dias, and A. Leal, "Feasibility of focal transcranial DC polarization with simultaneous EEG recording: Preliminary assessment in healthy subjects and human epilepsy," Epilepsy Behav., vol. 25, no. 3, pp. 417-425, Nov. 2012.
96. A. Antal, M. Bikson, A. Datta, B. Lafon, P. Dechent, L. C. Parra, and W. Paulus, "Imaging artifacts induced by electrical stimulation during conventional fMRI of the brain," Neuroimage, Oct. 23, 2012, Available: http://www.sciencedirect.com/science/article/pii/S1053811912010294
97. A. Berenyi, M. Belluscio, D. Mao, and G. Buzsaki, "Closed-loop control of epilepsy by transcranial electrical stimulation," Science, vol. 337, no. 6095, pp. 735-737, Aug. 10, 2012.
98. A. T. Barker, I. L. Freeston, R. Jalinous, and J. A. Jarratt, "Magnetic stimulation of the human brain and peripheral nervous system: An introduction and the results of an initial clinical evaluation," Neurosurgery, vol. 20, no. 1, pp. 100-109, Jan. 1987.
99. L. G. Cohen, B. J. Roth, J. Nilsson, N. Dang, M. Panizza, S. Bandinelli, W. Friauf, and M. Hallett, "Effects of coil design on delivery of focal magnetic stimulation. Technical considerations," Electroencephalogr. Clin. Neurophysiol., vol. 75, no. 4, pp. 350-357, Apr. 1990. (Pubitemid 20111472)
100. S. Ueno, T. Tashiro, and K. Harada, "Localized stimulation of neural tissues in the brain by means of a paired configuration of time-varying magnetic-fields," J. Appl. Phys., vol. 64, no. 10, pp. 5862-5864, Nov. 15, 1988.
101. S. Rossi, M. Hallett, P. M. Rossini, and A. Pascual-Leone, "Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research," Clin. Neurophysiol., vol. 120, no. 12, pp. 2008-2039, Dec. 2009.
102. A. T. Barker, R. Jalinous, and I. L. Freeston, "Non-invasive magnetic stimulation of human motor cortex," Lancet, vol. 1, no. 8437, pp. 1106-1107, May 11, 1985. (Pubitemid 15075547)
103. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone, "Noninvasive human brain stimulation," Annu. Rev. Biomed. Eng., vol. 9, pp. 527-565, 2007.
104. W. C. Drevets, "Neuroimaging and neuropathological studies of depression: Implications for the cognitive-emotional features of mood disorders," Curr. Opin. Neurobiol., vol. 11, no. 2, pp. 240-249, Apr. 2001.
105. P. B. Fitzgerald, T. J. Oxley, A. R. Laird, J. Kulkarni, G. F. Egan, and Z. J. Daskalakis, "An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression," Psychiatry Res., vol. 148, no. 1, pp. 33-45, Nov. 22, 2006.
106. J. M. Leppanen, "Emotional information processing in mood disorders: A review of behavioral and neuroimaging findings," Curr. Opin. Psychiatry, vol. 19, no. 1, pp. 34-39, Jan. 2006.
107. A. Pascual-Leone, B. Rubio, F. Pallardo, and M. D. Catala, "Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression," Lancet, vol. 348, no. 9022, pp. 233-237, Jul. 27, 1996.
108. P. B. Fitzgerald, K. Hoy, Z. J. Daskalakis, and J. Kulkarni, "A randomized trial of the anti-depressant effects of low- and high-frequency transcranial magnetic stimulation in treatment-resistant depression," Depress Anxiety, vol. 26, no. 3, pp. 229-234, 2009.
109. F. A. Kozel and M. S. George, "Meta-analysis of left prefrontal repetitive transcranial magnetic stimulation (rTMS) to treat depression," J. Psychiatry Pract., vol. 8, no. 5, pp. 270-275, Sep. 2002.
110. J. L. Couturier, "Efficacy of rapid-rate repetitive transcranial magnetic stimulation in the treatment of depression: A systematic review and meta-analysis," J. Psychiatry Neurosci., vol. 30, no. 2, pp. 83-90, Mar. 2005.
111. C. Schonfeldt-Lecuona, L. Cardenas-Morales, R. W. Freudenmann, T. Kammer, and U. Herwig, "Transcranial magnetic stimulation in depression - Lessons from the multicentre trials," Restor Neurol. Neurosci., vol. 28, no. 4, pp. 569-576, 2010.
112. J. P. O'Reardon, H. B. Solvason, P. G. Janicak, S. Sampson, K. E. Isenberg, Z. Nahas, W. M. McDonald, D. Avery, P. B. Fitzgerald, C. Loo, M. A. Demitrack, M. S. George, and H. A. Sackeim, "Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: A multisite randomized controlled trial," Biol. Psychiatry, vol. 62, no. 11, pp. 1208-1216, Dec. 1, 2007.
113. U. Herwig, L. Cardenas-Morales, B. J. Connemann, T. Kammer, and C. Schonfeldt-Lecuona, "Sham or real-post hoc estimation of stimulation condition in a randomized transcranial magnetic stimulation trial," Neurosci. Lett., vol. 471, no. 1, pp. 30-33, Feb. 26, 2010.
114. M. T. Berlim, F. Van den Eynde, and Z. J. Daskalakis, "A systematic review and meta-analysis on the efficacy and acceptability of bilateral repetitive transcranial magnetic stimulation (rTMS) for treating major depression," Psychol. Med., pp. 1-10, Dec. 3, 2012.
115. M. D. Fox, R. L. Buckner, M. P. White, M. D. Greicius, and A. Pascual-Leone, "Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate," Biol. Psychiatry, vol. 72, no. 7, pp. 595-603, Oct. 1, 2012.
116. M. C. Ridding and J. C. Rothwell, "Is there a future for therapeutic use of transcranial magnetic stimulation?" Nat. Rev. Neurosci., vol. 8, no. 7, pp. 559-567, Jul. 2007.
117. C. G. Mansur, F. Fregni, P. S. Boggio, M. Riberto, J. Gallucci-Neto, C. M. Santos, T. Wagner, S. P. Rigonatti, M. A. Marcolin, and A. Pascual-Leone, "A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients," Neurology, vol. 64, no. 10, pp. 1802-1804, May 24, 2005. (Pubitemid 40695826)
118. F. Fregni, P. S. Boggio, A. C. Valle, R. R. Rocha, J. Duarte, M. J. Ferreira, T. Wagner, S. Fecteau, S. P. Rigonatti, M. Riberto, S. D. Freedman, and A. Pascual-Leone, "Asham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients," Stroke, vol. 37, no. 8, pp. 2115-2122, Aug. 2006. (Pubitemid 44309913)
119. Y. H. Kim, S. H. You, M. H. Ko, J. W. Park, K. H. Lee, S. H. Jang, W. K. Yoo, and M. Hallett, "Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke," Stroke, vol. 37, no. 6, pp. 1471-1476, Jun. 2006. (Pubitemid 44305728)
120. W. H. Chang, Y. H. Kim, O. Y. Bang, S. T. Kim,Y. H. Park, and P. K. Lee, "Long-term effects of rTMS on motor recovery in patients after subacute stroke," J. Rehabil. Med., vol. 42, no. 8, pp. 758-764, Sep. 2010.
121. E. M. Khedr, M. R. Abdel-Fadeil, A. Farghali, and M. Qaid, "Role of 1 and 3 Hz repetitive transcranial magnetic stimulation onmotor function recovery after acute ischaemic stroke," Eur. J. Neurol., vol. 16, no. 12, pp. 1323-1330, Dec. 2009.
122. N. Takeuchi, T. Tada, M. Toshima, Y. Matsuo, and K. Ikoma, "Repetitive transcranial magnetic stimulation over bilateral hemispheres enhances motor function and training effect of paretic hand in patients after stroke," J. Rehabil. Med., vol. 41, no. 13, pp. 1049-1054, Nov. 2009.
123. P. Jung and U. Ziemann, "Homeostatic and nonhomeostatic modulation of learning in human motor cortex," J. Neurosci., vol. 29, no. 17, pp. 5597-5604, Apr. 29, 2009.
124. E. L. Bienenstock, L. N. Cooper, and P. W. Munro, "Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex," J. Neurosci., vol. 2, no. 1, pp. 32-48, Jan. 1982.
125. K. Fricke, A. A. Seeber, N. Thirugnanasambandam, W. Paulus, M. A. Nitsche, and J. C. Rothwell, "Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex," J. Neurophysiol., vol. 105, no. 3, pp. 1141-1149, Mar. 2011.
126. W. C. Abraham and M. F. Bear, "Metaplasticity: The plasticity of synaptic plasticity," Trends Neurosci., vol. 19, no. 4, pp. 126-130, Apr. 1996.
127. M. B. Iyer, N. Schleper, and E. M. Wassermann, "Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation," J. Neurosci., vol. 23, no. 34, pp. 10867-10872, Nov. 26, 2003.
128. S. Nouri and S. C. Cramer, "Anatomy and physiology predict response to motor cortex stimulation after stroke," Neurology, vol. 77, no. 11, pp. 1076-1083, Sep. 13, 2011.
129. B. Cheeran, P. Talelli, F. Mori, G. Koch, A. Suppa, M. Edwards, H. Houlden, K. Bhatia, R. Greenwood, and J. C. Rothwell, "A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS," J. Physiol., vol. 586, no. Pt 23, pp. 5717-5725, Dec. 1, 2008.
130. A. V. Peterchev, R. Jalinous, and S. H. Lisanby, "A transcranial magnetic stimulator inducing near-rectangular pulses with controllable pulse width (cTMS)," IEEE Trans. Biomed. Eng., vol. 55, no. 1, pp. 257-266, Jan. 2008. (Pubitemid 350308413)
131. N. Gattinger, G. Moessnang, and B. Gleich, "flexTMS - a novel repetitive transcranial magnetic stimulation device with freely programmable stimulus currents," IEEE Trans. Biomed. Eng., vol. 59, no. 7, pp. 1962-1970, Jul. 2012.
132. M. Chen and D. J. Mogul, "Using increased structural detail of the cortex to improve the accuracy of modeling the effects of transcranial magnetic stimulation on neocortical activation," IEEE Trans. Biomed. Eng., vol. 57, no. 5, pp. 1216-1226, May 2010.
133. Y. Roth, A. Zangen, and M. Hallett, "A coil design for transcranial magnetic stimulation of deep brain regions," J. Clin. Neurophysiol., vol. 19, no. 4, pp. 361-370, Aug. 2002. (Pubitemid 35304369)
134. A. Zangen, Y. Roth, B. Voller, and M. Hallett, "Transcranial magnetic stimulation of deep brain regions: Evidence for efficacy of the H-coil," Clin. Neurophysiol., vol. 116, no. 4, pp. 775-779, Apr. 2005. (Pubitemid 40431994)
135. E. A. Fridman, T. Hanakawa, M. Chung, F. Hummel, R. C. Leiguarda, and L. G. Cohen, "Reorganization of the human ipsilesional premotor cortex after stroke," Brain, vol. 127, no. Pt 4, pp. 747-758, Apr. 2004.
136. R. Martuzzi, M. M. Murray, P. P. Maeder, E. Fornari, J. Thiran, S. Clarke, C. M. Michel, and R. A. Meuli, "Visuo-motor pathways in humans revealed by event-related fMRI," Exp. Brain Res., vol. 170, no. 4, pp. 472-487, Apr. 2006.
137. W. Y. Hsu, C. H. Cheng, K. K. Liao, I. H. Lee, and Y. Y. Lin, "Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: A meta-analysis," Stroke, vol. 43, no. 7, pp. 1849-1857, Jul. 2012.