BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 2, Issue 4 , Pages 215-228.e3 , October 2009

Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro

  • Thomas Radman, PhD

      Affiliations

    • Department of Biomedical Engineering, City College of the City University of New York, New York, New York
  • ,
  • Raddy L. Ramos, PhD

      Affiliations

    • Department of Neuroscience, New York College of Osteopathic Medicine NYIT, Old Westbury, New York
    • Department of Psychology, Queens College, CUNY, Flushing, New York
  • ,
  • Joshua C. Brumberg, PhD

      Affiliations

    • Department of Psychology, Queens College, CUNY, Flushing, New York
  • ,
  • Marom Bikson, PhD

      Affiliations

    • Department of Biomedical Engineering, City College of the City University of New York, New York, New York
    • Corresponding Author InformationCorrespondence: Marom Bikson, PhD, 140th St and Convent Ave, CCNY BME, Steinman Hall Room T-463, New York, NY 10031.

Received 11 November 2008 ,Revised 21 March 2009 ,Accepted 27 March 2009.

References 

  1. Liebetanz D, Klinker F, Hering D, et al. Anticonvulsant effects of transcranial direct-current stimulation (tDCS) in the rat cortical ramp model of focal epilepsy. Epilepsia. 2006;47(7):1216–1224
  2. George MS, Lisanby SH, Sackeim HA. Transcranial magnetic stimulation: applications in neuropsychiatry. Arch Gen Psychiatry. 1999;56(4):300–311
  3. Avery DH, Holtzheimer PE, Fawaz W, et al. A controlled study of repetitive transcranial magnetic stimulation in medication-resistant major depression. Biol Psychiatry. 2006;59(2):187–194
  4. Boggio PS, Ferrucci R, Rigonatti SP, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J Neurol Sci. 2006;249(1):31–38
  5. Webster BR, Celnik PA, Cohen LG. Noninvasive brain stimulation in stroke rehabilitation. NeuroRx. 2006;3(4):474–481
  6. Fregni F, Boggio PS, Lima MC, et al. A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain. 2006;122(1-2):197–209
  7. Uy J, Ridding MC. Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation. J Neurosci Methods. 2003;127(2):193–197
  8. Marshall L, Helgadottir H, Molle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444(7119):610–613
  9. Fregni F, Boggio PS, Nitsche M, et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res. 2005;166(1):23–30
  10. Kincses TZ, Antal A, Nitsche NA, Bartfai O, Paulus W. Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human. Neuropsychologia. 2004;42(1):113–117
  11. Amassian VE, Eberle L, Maccabee PJ, Cracco RQ. 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(5):291–301
  12. Miranda PC, Lomarev M, Hallett M. Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol. 2006;117(7):1623–1629
  13. Krings T, Buchbinder BR, Butler WE, et al. Functional magnetic resonance imaging and transcranial magnetic stimulation: complementary approaches in the evaluation of cortical motor function. Neurology. 1997;48(5):1406–1416
  14. Wassermann EM, Wang B, Zeffiro TA, et al. Locating the motor cortex on the MRI with transcranial magnetic stimulation and PET. Neuroimage. 1996;3(1):1–9
  15. Komssi S, Savolainen P, Heiskala J, Kahkonen S. Excitation threshold of the motor cortex estimated with transcranial magnetic stimulation electroencephalography. Neuroreport. 2007;18(1):13–16
  16. Normann RA, Maynard EM, Rousche PJ, Warren DJ. A neural interface for a cortical vision prosthesis. Vision Res. 1999;39(15):2577–2587
  17. Badi AN, Hillman T, Shelton C, Normann RA. A technique for implantation of a 3-dimensional penetrating electrode array in the modiolar nerve of cats and humans. Arch Otolaryngol Head Neck Surg. 2002;128(9):1019–1025
  18. Esser SK, Hill SL, Tononi G. Modeling the effects of transcranial magnetic stimulation on cortical circuits. J Neurophysiol. 2005;94(1):622–639
  19. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117(Pt 4):847–858
  20. Takano B, Drzezga A, Peller M, et al. Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation. Neuroimage. 2004;23(3):849–859
  21. Maccabee PJ, Amassian VE, Eberle LP, Cracco RQ. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol. 1993;460:201–219
  22. Amassian VE, Maccabee PJ, Cracco RQ, et al. The polarity of the induced electric field influences magnetic coil inhibition of human visual cortex: implications for the site of excitation. Electroencephalogr Clin Neurophysiol. 1994;93(1):21–26
  23. Chan CY, Hounsgaard J, Nicholson C. Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. J Physiol. 1988;402:751–771
  24. Hern JE, Landgren S, Phillips CG, Procter R. Selective excitation of cortifgugal neurones by surfaceanodal stimulation of the baboon's motor cortex. J Physiol. 1962;161:73–90
  25. Bikson M, Inoue M, Akiyama H, et al. Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol. 2004;557(Pt 1):175–190
  26. Chan CY, Nicholson C. Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol. 1986;371:89–114
  27. Purpura DP, McMurtry JG. Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol. 1965;28:166–185
  28. Lopez L, Chan CY, Okada YC, Nicholson C. Multimodal characterization of population responses evoked by applied electric field in vitro: extracellular potential, magnetic evoked field, transmembrane potential, and current-source density analysis. J Neurosci. 1991;11(7):1998–2010
  29. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975;98(3):417–440
  30. Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9:527–565
  31. Gatter KC, Sloper JJ, Powell TP. The intrinsic connections of the cortex of area 4 of the monkey. Brain. 1978;101(3):513–541
  32. Miranda PC, Hallett M, Basser PJ. The electric field induced in the brain by magnetic stimulation: a 3-D finite-element analysis of the effect of tissue heterogeneity and anisotropy. IEEE Trans Biomed Eng. 2003;50(9):1074–1085
  33. Wagner T, Fregni F, Fecteau S, Grodzinsky A, Zahn M, Pascual-Leone A. Transcranial direct current stimulation: a computer-based human model study. Neuroimage. 2007;35(3):1113–1124
  34. Datta A, Elwassif M, Battaglia F, Bikson M. Transcranial current stimulation focality using disc and ring electrode configurations: FEM analysis. J Neural Eng. 2008;5(2):163–174
  35. Rattay F. Analysis of models for extracellular fiber stimulation. IEEE Trans Biomed Eng. 1989;36(7):676–682
  36. Nagarajan SS, Durand DM, Warman EN. Effects of induced electric fields on finite neuronal structures: a simulation study. IEEE Trans Biomed Eng. 1993;40(11):1175–1188
  37. Hause L. A mathematical model for transmembrane potentials secondary to extracellular fields. In:  Sances J,  Larson S editor. Electroanaesthesia: biomedical and biophysical studies. New York: Academic; 1975;p. 176–200
  38. Tranchina D, Nicholson C. A model for the polarization of neurons by extrinsically applied electric fields. Biophys J. 1986;50(6):1139–1156
  39. Svirskis G, Baginskas A, Hounsgaard J, Gutman A. Electrotonic measurements by electric field-induced polarization in neurons: theory and experimental estimation. Biophys J. 1997;73(6):3004–3015
  40. McIntyre CC, Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophys J. 1999;76(2):878–888
  41. Plonsey R, Barr RC. Electric field stimulation of excitable tissue. IEEE Eng Med Biol Mag. 1998;17(5):130–137
  42. Plonsey R, Altman KW. Electrical stimulation of excitable cells-a model approach. Proc IEEE. 1988;76(9):1122–1129
  43. Rotem A, Moses E. Magnetic stimulation of one-dimensional neuronal cultures. Biophys J. 2008;94(12):5065–5078
  44. Valero-Cabre A, Payne BR, Rushmore J, Lomber SG, Pascual-Leone A. Impact of repetitive transcranial magnetic stimulation of the parietal cortex on metabolic brain activity: a 14C-2DG tracing study in the cat. Exp Brain Res. 2005;163(1):1–12
  45. Durand DM. Suppression and control of epileptiform activity by electrical stimulation: a review. Proc IEEE. 2001;89:1065–1082
  46. Roth BJ. Mechanisms for electrical stimulation of excitable tissue. Crit Rev Biomed Eng. 1994;22(3-4):253–305
  47. Brumberg JC, Nowak LG, McCormick DA. Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci. 2000;20(13):4829–4843
  48. Radman T, Su Y, An JH, Parra LC, Bikson M. Spike timing amplifies the effect of electric fields on neurons: implications for endogenous field effects. J Neurosci. 2007;27(11):3030–3036
  49. Ramos RL, Tam DM, Brumberg JC. Physiology and morphology of callosal projection neurons in mouse. Neuroscience. 2008;153(3):654–663
  50. Yang CR, Seamans JK, Gorelova N. Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci. 1996;16(5):1904–1921
  51. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985;54(4):782–806
  52. Deans JK, Powell AD, Jefferys JG. Sensitivity of coherent oscillations in rat hippocampus to AC electric fields. J Physiol. 2007;583(Pt 2):555–565
  53. Ghai RS, Bikson K, Durand DM. Effects of applied electric fields on low- calcium epileptiform activity in the CA1 region of rat hippocampal slices. J Neurophysiol. 2000;84(1):274–280
  54. Francis JT, Gluckman BJ, Schiff SJ. Sensitivity of neurons to weak electric fields. J Neurosci. 2003;23(19):7255–7261
  55. Gluckman BJ, Neel EJ, Netoff TI, Ditto WL, Spano ML, Schiff SJ. Electric field suppression of epileptiform activity in hippocampal slices. J Neurophysiol. 1996;76(6):4202–4205
  56. Gluckman BJ, Nguyen H, Weinstein SL, Schiff SJ. Adaptive electric field control of epileptic seizures. J Neurosci. 2001;21(2):590–600
  57. Brumberg JC, Hamzei-Sichani F, Yuste R. Morphological and physiological characterization of layer VI corticofugal neurons of mouse primary visual cortex. J Neurophysiol. 2003;89(5):2854–2867
  58. Rocco MM, Brumberg JC. The sensorimotor slice. J Neurosci Methods. 2007;162(1-2):139–147
  59. Ramos RL, Smith PT, DeCola C, Tam D, Corzo O, Brumberg JC. Cytoarchitecture and transcriptional profiles of neocortical malformations in inbred mice. Cereb Cortex. 2008;18(11):2614–2628
  60. Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res. 1998;118(4):477–488
  61. Bostock H. The strength-duration relationship for excitation of myelinated nerve: computed dependence on membrane parameters. J Physiol. 1983;341:59–74
  62. Meyer G. Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol. 1987;262(3):402–428
  63. Jefferys JG. Influence of electric fields on the excitability of granule cells in guinea-pig hippocampal slices. J Physiol. 1981;319:143–152
  64. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol. 2005;94(3):1904–1911
  65. Parra LC, Bikson M. Model of the effect of extracellular fields on spike time coherence. Conf Proc IEEE Eng Med Biol Soc. 2004;6:4584–4587
  66. Delgado-Lezama R, Perrier JF, Hounsgaard J. Local facilitation of plateau potentials in dendrites of turtle motoneurones by synaptic activation of metabotropic receptors. J Physiol. 1999;515(Pt 1):203–207
  67. Terzuolo CA, Bullock TH. Measurement of imposed voltage gradient adequate to modulate neuronal firing. Proc Natl Acad Sci U S A. 1956;42(9):687–694
  68. McIntyre CC, Grill WM. Selective microstimulation of central nervous system neurons. Ann Biomed Eng. 2000;28(3):219–233
  69. Izhikevich E. Dynamical systems in neuroscience: geometry of excitability and bursting. Cambridge (MA): MIT Press; 2005;
  70. Lesica NA, Stanley GB. Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. J Neurosci. 2004;24(47):10731–10740
  71. Lu SM, Guido W, Sherman SM. Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. J Neurophysiol. 1992;68(6):2185–2198
  72. Larkman AU, Major G, Stratford KJ, Jack JJ. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: IV, electrical geometry. J Comp Neurol. 1992;323(2):137–152
  73. Brocke J, Irlbacher K, Hauptmann B, Voss M, Brandt SA. Transcranial magnetic and electrical stimulation compared: does TES activate intracortical neuronal circuits?. Clin Neurophysiol. 2005;116(12):2748–2756
  74. Patton HD, Amassian VE. Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J Neurophysiol. 1954;17(4):345–363
  75. Rothwell J, Burke D, Hicks R, Stephen J, Woodforth I, Crawford M. Transcranial electrical stimulation of the motor cortex in man: further evidence for the site of activation. J Physiol. 1994;481(Pt 1):243–250
  76. Nakamura H, Kitigawa H, Kawaguchi Y, Tsuji H. Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol. 1997;498(Pt 3):817–823
  77. Sommer M, Lang N, Tergau F, Paulus W. Neuronal tissue polarization induced by repetitive transcranial magnetic stimulation ? Neuroreport. 2002;13(6):809–811
  78. Epstein CM, Schwartzberg DG, Davey KR, Sudderth DB. Localizing the site of magnetic brain stimulation in humans. Neurology. 1990;40(4):666–670
  79. Rudiak D, Marg E. Finding the depth of magnetic brain stimulation: a re-evaluation. Electroencephalogr Clin Neurophysiol. 1994;93(5):358–371
  80. Thielscher A, Kammer T. Linking physics with physiology in TMS: a sphere field model to determine the cortical stimulation site in TMS. Neuroimage. 2002;17(3):1117–1130
  81. Peterchev AV, Jalinous R, Lisanby SH. A transcranial magnetic stimulator inducing near-rectangular pulses with controllable pulse width (cTMS). IEEE Trans Biomed Eng. 2008;55(1):257–266
  82. Tehovnik EJ, Tolias AS, Sultan F, Slocum WM, Logothetis NK. Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol. 2006;96(2):512–521
  83. Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W. Modulation of cortical excitability by weak direct current stimulation—technical, safety and functional aspects. Suppl Clin Neurophysiol. 2003;56:255–276
  84. Nitsche MA, Fricke K, Henschke U, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol. 2003;553(Pt 1):293–301
  85. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(Pt 3):633–639

 This work was supported in part by the NIH NS058758 to J.C.B, NS054783-01A1 S06GMOO8168 to MB, the Andy Grove Foundation, and PSC-CUNY.

PII: S1935-861X(09)00042-4

doi: 10.1016/j.brs.2009.03.007

BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 2, Issue 4 , Pages 215-228.e3 , October 2009