Computer-based model of epidural motor cortex stimulation: Effects of electrode position and geometry on activation of cortical neurons

Clinical Neurophysiology

Volumn 123, Issue 1, 2012, Pages 160-172

  Wongsarnpigoon, Amorn ^a   Grill, Warren M ^a  

^a Duke University   (United States)

Author keywords

Finite element method; Motor cortex stimulation; Pyramidal cell

Indexed keywords

MYELIN;

ARTICLE; BRAIN NERVE CELL; CELL ACTIVATION; CELL POLARITY; COMPARTMENT MODEL; COMPUTER MODEL; DENDRITE; ELECTRODE; ELECTROSTIMULATION; EPIDURAL CORTICAL STIMULATION; GEOMETRY; MAXIMUM ALLOWABLE CONCENTRATION; MOTOR CORTEX; NERVE CELL EXCITABILITY; NERVE FIBER; NERVE POTENTIAL; NERVE STIMULATION; PERIKARYON; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SIMULATION;

DEEP BRAIN STIMULATION; ELECTRODES, IMPLANTED; HUMANS; MODELS, NEUROLOGICAL; MOTOR CORTEX; NEURONS;

EID: 84655169610     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2011.06.005     Document Type: Article

References (78)

1. Adkins D.L., Campos P., Quach D., Borromeo M., Schallert K., Jones T.A. Epidural cortical stimulation enhances motor function after sensorimotor cortical infarcts in rats. Exp Neurol 2006, 200:356-370.
2. Alo K.M., Holsheimer J. New trends in neuromodulation for the management of neuropathic pain. Neurosurgery 2002, 50:690-704.
3. Amaral D.G. The anatomical organization of the central nervous system. Principles of neural science 2000, McGraw-Hill, New York. E.R. Kandel, J.H. Schwartz, T.M. Jessell (Eds.).
4. Amassian V.E., Eberle L., Maccabee P.J., Cracco R.Q. Modelling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shaped volume conductor: the significance of fiber bending in excitation. Electroencephalogr Clin Neurophysiol 1992, 85:291-301.
5. Amassian V.E., Quirk G.J., Stewart M. A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. Electroencephalogr Clin Neurophysiol 1990, 77:390-401.
6. Anderson W.S., Kiyofuji S., Conway J.E., Busch C., North R.B., Garonzik I.M. Dysphagia and neuropathic facial pain treated with motor cortex stimulation: case report. Neurosurgery 2009, 65:E626. [Discussion E].
7. Bejjani B.P., Damier P., Arnulf I., Thivard L., Bonnet A.M., Dormont D., et al. Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med 1999, 340:1476-1480.
8. Berenstein C.K., Mens L.H., Mulder J.J., Vanpoucke F.J. Current steering and current focusing in cochlear implants: comparison of monopolar, tripolar, and virtual channel electrode configurations. Ear Hear 2008, 29:250-260.
9. Bonham B.H., Litvak L.M. Current focusing and steering: modeling, physiology, and psychophysics. Hear Res 2008, 242:141-153.
10. Boychuk J.A., Adkins D.L., Kleim J.A. Distributed versus focal cortical stimulation to enhance motor function and motor map plasticity in a rodent model of ischemia. Neurorehabil Neural Repair 2011, 25:88-97.
11. Brown J.A., Lutsep H., Cramer S.C., Weinand M. Motor cortex stimulation for enhancement of recovery after stroke: case report. Neurol Res 2003, 25:815-818.
12. Brown J.A., Lutsep H.L., Weinand M., Cramer S.C. Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery 2006, 58:464-473.
13. Butson C.R., Cooper S.E., Henderson J.M., McIntyre C.C. Patient-specific analysis of the volume of tissue activated during deep brain stimulation. NeuroImage 2007, 34:661-670.
14. Butson C.R., McIntyre C.C. Current steering to control the volume of tissue activated during deep brain stimulation. Brain Stimul 2008, 1:7-15.
15. Canavero S. Textbook of therapeutic cortical stimulation 2009, Nova Biomedical Books, New York.
16. Canavero S., Paolotti R. Extradural motor cortex stimulation for advanced Parkinson's disease: case report. Mov Disord 2000, 15:169-171.
17. Canavero S., Paolotti R., Bonicalzi V., Castellano G., Greco-Crasto S., Rizzo L., et al. Extradural motor cortex stimulation for advanced Parkinson disease. Report of two cases. J Neurosurg 2002, 97:1208-1211.
18. Chaturvedi A., Butson C.R., Lempka S.F., Cooper S.E., McIntyre C.C. Patient-specific models of deep brain stimulation: influence of field model complexity on neural activation predictions. Brain Stimul 2010, 3:65-67.
19. Cherney L.R., Erickson R.K., Small S.L. Epidural cortical stimulation as adjunctive treatment for non-fluent aphasia: preliminary findings. J Neurol Neurosurg Psychiatry 2010, 81:1014-1021.
20. De Ridder D., De Mulder G., Verstraeten E., Seidman M., Elisevich K., Sunaert S., et al. Auditory cortex stimulation for tinnitus. Acta Neurochir Suppl 2007, 97:451-462.
21. DeFelipe J., Alonso-Nanclares L., Arellano J.I. Microstructure of the neocortex: comparative aspects. J Neurocytol 2002, 31:299-316.
22. Dostrovsky J.O., Levy R., Wu J.P., Hutchison W.D., Tasker R.R., Lozano A.M. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol 2000, 84:570-574.
23. Drouot X., Oshino S., Jarraya B., Besret L., Kishima H., Remy P., et al. Functional recovery in a primate model of Parkinson's disease following motor cortex stimulation. Neuron 2004, 44:769-778.
24. Franzini A., Ferroli P., Dones I., Marras C., Broggi G. Chronic motor cortex stimulation for movement disorders: a promising perspective. Neurol Res 2003, 25:123-126.
25. Gorman A.L. Differential patterns of activation of the pyramidal system elicited by surface anodal and cathodal cortical stimulation. J Neurophysiol 1966, 29:547-564.
26. Grill W.M. Modeling the effects of electric fields on nerve fibers: influence of tissue electrical properties. IEEE Trans Biomed Eng 1999, 46:918-928.
27. Grill W.M., Mortimer J.T. Stimulus waveforms for selective neural stimulation. IEEE Eng Med Biol Mag 1995, 14:375-385.
28. Gustafsson B., Jankowska E. Direct and indirect activation of nerve cells by electrical pulses applied extracellularly. J Physiol 1976, 258:33-61.
29. Gutierrez J.C., Seijo F.J., Alvarez Vega M.A., Fernandez Gonzalez F., Lozano Aragoneses B., Blazquez M. Therapeutic extradural cortical stimulation for Parkinson's disease: report of six cases and review of the literature. Clin Neurol Neurosurg 2009, 111:703-707.
30. Hern J.E., Landgren S., Phillips C.G., Porter R. Selective excitation of corticofugal neurones by surface-anodal stimulation of the baboon's motor cortex. J Physiol 1962, 161:73-90.
31. Hestenes M.R., Stiefel E. Methods of conjugate gradients for solving linear systems. J Res Nat Bur Stand 1952, 49:409-436.
32. Hines M.L., Carnevale N.T. The NEURON simulation environment. Neural Comput 1997, 9:1179-1209.
33. Holsheimer J., Lefaucheur J.P., Buitenweg J.R., Goujon C., Nineb A., Nguyen J.P. The role of intra-operative motor evoked potentials in the optimization of chronic cortical stimulation for the treatment of neuropathic pain. Clin Neurophysiol 2007, 118:2287-2296.
34. Hosomi K., Saitoh Y., Kishima H., Oshino S., Hirata M., Tani N., et al. Electrical stimulation of primary motor cortex within the central sulcus for intractable neuropathic pain. Clin Neurophysiol 2008, 119:993-1001.
35. Houeto J.L., Mesnage V., Mallet L., Pillon B., Gargiulo M., du Moncel S.T., et al. Behavioural disorders, Parkinson's disease and subthalamic stimulation. J Neurol Neurosurg Psychiatry 2002, 72:701-707.
36. Jankowska E., Padel Y., Tanaka R. The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol 1975, 249:617-636.
37. Jankowska E., Padel Y., Tanaka R. Projections of pyramidal tract cells to alpha-motoneurones innervating hind-limb muscles in the monkey. J Physiol 1975, 249:637-667.
38. Kaneko T., Cho R., Li Y., Nomura S., Mizuno N. Predominant information transfer from layer III pyramidal neurons to corticospinal neurons. J Comput Neurol 2000, 423:52-65.
39. Katayama Y., Oshima H., Fukaya C., Kawamata T., Yamamaoto T. Control of post-stroke movement disorders using chronic motor cortex stimulation. Acta Neurochir Suppl 2002, 79:89-92.
40. Katayama Y., Tsubokawa T., Maejima S., Hirayama T., Yamamoto T. Corticospinal direct response in humans: identification of the motor cortex during intracranial surgery under general anaesthesia. J Neurol Neurosurg Psychiatry 1988, 51:50-59.
41. Kleim J.A., Bruneau R., VandenBerg P., MacDonald E., Mulrooney R., Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol Res 2003, 25:789-793.
42. Kleiner-Fisman G., Fisman D.N., Kahn F.I., Sime E., Lozano A.M., Lang A.E. Motor cortical stimulation for parkinsonism in multiple system atrophy. Arch Neurol 2003, 60:1554-1558.
43. Landsberger D.M., Srinivasan A.G. Virtual channel discrimination is improved by current focusing in cochlear implant recipients. Hear Res 2009, 254:34-41.
44. Lefaucheur J.P., Drouot X., Cunin P., Bruckert R., Lepetit H., Creange A., et al. Motor cortex stimulation for the treatment of refractory peripheral neuropathic pain. Brain 2009, 132:1463-1471.
45. Levy R., Ruland S., Weinand M., Lowry D., Dafer R., Bakay R. Cortical stimulation for the rehabilitation of patients with hemiparetic stroke: a multicenter feasibility study of safety and efficacy. J Neurosurg 2008, 108:707-714.
46. Maccabee P.J., Amassian V.E., Eberle L.P., Cracco R.Q. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol 1993, 460:201-219.
47. Mainen Z.F., Sejnowski T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 1996, 382:363-366.
48. Manola L., Holsheimer J., Veltink P., Buitenweg J.R. Anodal vs cathodal stimulation of motor cortex: a modeling study. Clin Neurophysiol 2007, 118:464-474.
49. Manola L., Roelofsen B.H., Holsheimer J., Marani E., Geelen J. Modelling motor cortex stimulation for chronic pain control: electrical potential field, activating functions and responses of simple nerve fibre models. Med Biol Eng Comput 2005, 43:335-343.
50. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004, 5:793-807.
51. McIntyre C.C., Grill W.M. Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J Neurophysiol 2002, 88:1592-1604.
52. Miranda P.C., Correia L., Salvador R., Basser P.J. Tissue heterogeneity as a mechanism for localized neural stimulation by applied electric fields. Phys Med Biol 2007, 52:5603-5617.
53. Nahas Z., Anderson B.S., Borckardt J., Arana A.B., George M.S., Reeves S.T., et al. Bilateral epidural prefrontal cortical stimulation for treatment-resistant depression. Biol Psychiatry 2009, 9:9.
54. Nair D.R., Burgess R., McIntyre C.C., Luders H. Chronic subdural electrodes in the management of epilepsy. Clin Neurophysiol 2008, 119:11-28.
55. Nguyen J.P., Pollin B., Feve A., Geny C., Cesaro P. Improvement of action tremor by chronic cortical stimulation. Mov Disord 1998, 13:84-88.
56. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984, 307:462-465.
57. Pagni C.A., Albanese A., Bentivoglio A., Broggi G., Canavero S., Cioni B., et al. Results by motor cortex stimulation in treatment of focal dystonia, Parkinson's disease and post-ictal spasticity. The experience of the Italian study group of the Italian neurosurgical society. Acta Neurochir Suppl 2008, 101:13-21.
58. Phillips C.G., Porter R. Unifocal and bifocal stimulation of the motor cortex. J Physiol 1962, 162:532-538.
59. Plautz E.J., Barbay S., Frost S.B., Friel K.M., Dancause N., Zoubina E.V., et al. Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurol Res 2003, 25:801-810.
60. Radman T., Ramos R.L., Brumberg J.C., Bikson M. Role of cortical cell type and morphology in sub- and suprathreshold uniform electric field stimulation. Brain Stimulat 2009, 2:215-228.
61. Rasche D., Ruppolt M., Stippich C., Unterberg A., Tronnier V.M. Motor cortex stimulation for long-term relief of chronic neuropathic pain: a 10 year experience. Pain 2006, 121:43-52.
62. Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999, 89:335-346.
63. Rattay F. Current distance relations for fiber stimulation with pointsources. IEEE Trans Biomed Eng 2008, 55:1122-1127.
64. Romito L.M., Franzini A., Perani D., Carella F., Marras C., Capus L., et al. Fixed dystonia unresponsive to pallidal stimulation improved by motor cortex stimulation. Neurology 2007, 68:875-876.
65. Rubinstein J.T. Axon termination conditions for electrical stimulation. IEEE Trans Biomed Eng 1993, 40:654-663.
66. Sakas D.E., Flaskas T.N., Panourias I.G., Georgakoulias N. Bifocal cortical electrical stimulation for pain by interdural implantation of the electrodes. J Neurosurg 2010, 2010:2.
67. Salvador R., Silva S., Basser P.J., Miranda P.C. Determining which mechanisms lead to activation in the motor cortex: a modeling study of transcranial magnetic stimulation using realistic stimulus waveforms and sulcal geometry. Clin Neurophysiol 2010, 27:45.
68. Sloper J.J. An electron microscope study of the termination of afferent connections to the primate motor cortex. J Neurocytol 1973, 2:361-368.
69. Stoney S.D., Thompson W.D., Asanuma H. Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J Neurophysiol 1968, 31:659-669.
70. Tani N., Saitoh Y., Kishima H., Oshino S., Hatazawa J., Hashikawa K., et al. Motor cortex stimulation for levodopa-resistant akinesia: case report. Mov Disord 2007, 22:1645-1649.
71. Teskey G.C., Flynn C., Goertzen C.D., Monfils M.H., Young N.A. Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol Res 2003, 25:794-800.
72. Tsubokawa T., Katayama Y., Yamamoto T., Hirayama T., Koyama S. Chronic motor cortex stimulation for the treatment of central pain. Acta Neurochir Suppl (Wien) 1991, 52:137-139.
73. Tsubokawa T., Katayama Y., Yamamoto T., Hirayama T., Koyama S. Chronic motor cortex stimulation in patients with thalamic pain. J Neurosurg 1993, 78:393-401.
74. Velasco F., Carrillo-Ruiz J.D., Castro G., Arguelles C., Velasco A.L., Kassian A., et al. Motor cortex electrical stimulation applied to patients with complex regional pain syndrome. Pain 2009, 147:91-98.
75. Veraart C., Grill W.M., Mortimer J.T. Selective control of muscle activation with a multipolar nerve cuff electrode. IEEE Trans Biomed Eng 1993, 40:640-653.
76. Wongsarnpigoon A., Grill W.M. Computational modeling of epidural cortical stimulation. J Neural Eng 2008, 5:443-454.
77. Yamamoto T., Katayama Y., Obuchi T., Kano T., Kobayashi K., Oshima H., et al. Recording of corticospinal evoked potential for optimum placement of motor cortex stimulation electrodes in the treatment of post-stroke pain. Neurol Med Chir (Tokyo) 2007, 47:409-414.
78. Yousry T.A., Schmid U.D., Alkadhi H., Schmidt D., Peraud A., Buettner A., et al. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 1997, 120 (Pt 1):141-157.