Consideration of Individual Brain Geometry and Anisotropy on the Effect of tDCS

Document Type : Original Paper

Authors

1 Department of Psychology and Neuroscience, Leibniz Research Center, Dortmund, Germany

2 Department of Medical Physics, School of Medical Sciences, Tarbiat Modares University, Tehran, Iran.

3 Neurocognitive Laboratory, Iranian National Center for Addiction Studies (INCAS), Tehran University of Medical Sciences, Tehran, Iran

Abstract

Introduction: The response variability between subjects, which is one of the fundamental challenges facing transcranial direct current stimulation (tDCS), can be investigated by understanding how the current is distributed through the brain. This understanding can be obtained by means of computational methods utilizing finite element (FE) models.
Materials and Methods: In this study, the effect of realistic geometry and white matter anisotropy on the head electrical current density intensity (CDI) distribution was measured using a magnetic resonance imaging (MRI)-derived FE model at the whole brain, below electrodes, and cellular levels.
Results: The results revealed that on average, the real geometry changes the CDI in gray matter and the WM by 29% and 55%, respectively. In addition, WM anisotropy led to an 8% and 36% change of CDI across GM and WM, respectively. The results indicated that for this electrode configuration, the maximum CDI occurs not below the electrode, but somewhere between the electrodes, and its locus varies greatly between individuals.  In addition, by investigating the effect of current density components on cellular excitability, significant individual differences in the level of excitability were detected.
Conclusion: Accordingly, consideration of the real geometry in computational modeling is vital. In addition, WM anisotropy does not significantly influence the CDI on the gray matter surface, however, it alters the CDI inside the brain; therefore, it can be taken into account, especially, when stimulation of brain’s internal regions is proposed. Finally, to predict the outcome result of tDCS, the examination of its effect at the cellular level is of great importance.

Keywords

Main Subjects


  1. Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA. Partially non‐linear stimulation intensity‐dependent effects of direct current stimulation on motor cortex excitability in humans. The Journal of physiology. 2013 Apr 1;591(7):1987-2000. DOI: 10.1113/jphysiol.2012.249730.
  2. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, et al. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain stimulation. 2013 May 31;6(3):424-32. DOI: 10.1016/j.brs.2012.04.011.
  3. Nitsche MA, Doemkes S, Karakoese T, Antal A, Liebetanz D, Lang N, et al. Shaping the effects of transcranial direct current stimulation of the human motor cortex. Journal of neurophysiology. 2007 Apr 1;97(4):3109-17. DOI: 10.1152/jn.01312.2006.
  4. Kuo HI, Bikson M, Datta A, Minhas P, Paulus W, Kuo MF, et al. Comparing cortical plasticity induced by conventional and high-definition 4× 1 ring tDCS: a neurophysiological study. Brain stimulation. 2013 Jul 31;6(4):644-8. DOI: 10.1016/j.brs.2012.09.010.
  5. Ho KA, Taylor JL, Chew T, Gálvez V, Alonzo A, Bai S, et al. The effect of transcranial direct current stimulation (tDCS) electrode size and current intensity on motor cortical excitability: evidence from single and repeated sessions. Brain stimulation. 2016 Feb 29;9(1):1-7. DOI: 10.1016/j.brs.2015.08.003.
  6. Ferrucci R, Mameli F, Guidi I, Mrakic-Sposta S, Vergari M, Marceglia SE, et al. Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology. 2008 Aug 12;71(7):493-8. DOI: 10.1212/01.wnl.0000317060.43722.a3.
  7. Marceglia S, Mrakic-Sposta S, Rosa M, Ferrucci R, Mameli F, Vergari M, et al. Transcranial direct current stimulation modulates cortical neuronal activity in Alzheimer's disease. Frontiers in neuroscience. 2016;10. DOI: 10.3389/fnins.2016.00134.
  8. Doruk D, Gray Z, Bravo GL, Pascual-Leone A, Fregni F. Effects of tDCS on executive function in Parkinson's disease. Neuroscience letters. 2014 Oct 17; 582:27-31. DOI: 10.1016/j.neulet.2014.08.043.
  9. Fregni F, Boggio PS, Santos MC, Lima M, Vieira AL, Rigonatti SP, et al. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson's disease. Movement disorders. 2006 Oct 1;21(10):1693-702. DOI: 10.1002/mds.21012.
  10. Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke?. The Lancet Neurology. 2006 Aug 31;5(8):708-12. DOI: 10.1016/S1474-4422(06)70525-7.
  11.  Boggio PS, Nunes A, Rigonatti SP, Nitsche MA, Pascual-Leone A, Fregni F. Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restorative neurology and neuroscience. 2007 Jan 1;25(2):123-9.
  12. Boggio PS, Rigonatti SP, Ribeiro RB, Myczkowski ML, Nitsche MA, Pascual-Leone A, et al. A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. International Journal of Neuropsychopharmacology. 2008 Mar 1;11(2):249-54. DOI: 10.1017/S1461145707007833.
  13. Fregni F, Boggio PS, Nitsche MA, Marcolin MA, Rigonatti SP, Pascual‐Leone A. Treatment of major depression with transcranial direct current stimulation. Bipolar disorders. 2006 Apr 1;8(2):203-4. DOI: 10.1111/j.1399-5618.2006.00291.x.
  14. Fregni F, Freedman S, Pascual-Leone A. Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques. The Lancet Neurology. 2007 Feb 28;6(2):188-91. DOI: 10.1016/S1474-4422(07)70032-7.
  15. Fregni F, Liguori P, Fecteau S, Nitsche MA, Pascual-Leone A, Boggio PS. Cortical stimulation of the prefrontal cortex with transcranial direct current stimulation reduces cue-provoked smoking craving: a randomized, sham-controlled study. Journal of Clinical Psychiatry. 2008 Jan 1;69(1):32-40.
  16. Fregni F, Orsati F, Pedrosa W, Fecteau S, Tome FA, Nitsche MA, et al. Transcranial direct current stimulation of the prefrontal cortex modulates the desire for specific foods. Appetite. 2008 Jul 31;51(1):34-41. DOI: 10.1016/j.appet.2007.09.016.
  17. Krause B, Kadosh RC. Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation. Frontiers in systems neuroscience. 2014;8. DOI: 10.3389/fnsys.2014.00025.
  18. Terney D, Antal A, Paulus W. Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. Brain Stimulation. 2008 Jul 31;1(3):255-6. DOI: 10.1111/j.1460-9568.2007.05896.x.
  19. Bikson M, Rahman A, Datta A. Computational models of transcranial direct current stimulation. Clinical EEG and Neuroscience. 2012 Jul;43(3):176-83. DOI: 10.1177/1550059412445138.
  20. Truong DQ, Magerowski G, Blackburn GL, Bikson M, Alonso-Alonso M. Computational modeling of transcranial direct current stimulation (tDCS) in obesity: impact of head fat and dose guidelines. NeuroImage: Clinical. 2013 Dec 31;2: 759-66. DOI: 10.1016/j.nicl.2013.05.011.
  21. Shahid S, Wen P, Ahfock T. Numerical investigation of white matter anisotropic conductivity in defining current distribution under tDCS. Computer methods and programs in biomedicine. 2013 Jan 31;109(1):48-64. DOI: 10.1016/j.cmpb.2012.09.001.
  22. Wiethoff S, Hamada M, Rothwell JC. Variability in response to transcranial direct current stimulation of the motor cortex. Brain stimulation. 2014 Jun 30;7(3):468-75. DOI: 10.1016/j.brs.2014.02.003.
  23. López-Alonso V, Cheeran B, Río-Rodríguez D, Fernández-del-Olmo M. Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain stimulation. 2014 Jun 30;7(3):372-80. DOI: 10.1016/j.brs.2014.02.004.
  24. Dyke K, Kim S, Jackson GM, Jackson SR. Intra-subject consistency and reliability of response following 2 mA transcranial direct current stimulation. Brain stimulation. 2016 Dec 31;9(6):819-25. DOI: 10.1016/j.brs.2016.06.052.
  25. Jacobson L, Koslowsky M, Lavidor M. tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Experimental brain research. 2012 Jan 1;216(1):1-0. DOI: 10.1007/s00221-011-2891-9.
  26.  Dmochowski JP, Bikson M, Datta A, Richardson J, Fridriksson J, Parra LC. On the role of electric field orientation in optimal design of transcranial current stimulation. InEngineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE 2012 Aug 28 (pp. 6426-6429). IEEE.
  27. Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M. Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain stimulation. 2009 Oct 31;2(4):201-7. DOI: 10.1016/j.brs.2009.03.005.
  28. Rush S, Driscoll DA. Current distribution in the brain from surface electrodes. Anesthesia & Analgesia. 1968 Nov 1;47(6):717-23.
  29.  Ruffini G, Wendling F, Merlet I, Molaee-Ardekani B, Mekonnen A, Salvador R, et al. Transcranial current brain stimulation (tCS): models and technologies. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2013 May;21(3):333-45. DOI: 10.1109/TNSRE.2012.2200046.
  30. Salvador R, Mekonnen A, Ruffini G, Miranda PC. Modeling the electric field induced in a high resolution realistic head model during transcranial current stimulation. InEngineering in Medicine and Biology Society (EMBC), 2010 Annual International Conference of the IEEE 2010 Aug 31 (pp. 2073-2076). IEEE. DOI: 10.1109/IEMBS.2010.5626315.
  31. Suh HS, Lee WH, Cho YS, Kim JH, Kim TS. Reduced spatial focality of electrical field in tDCS with ring electrodes due to tissue anisotropy. InEngineering in Medicine and Biology Society (EMBC), 2010 Annual International Conference of the IEEE 2010 Aug 31 (pp. 2053-2056). IEEE. DOI: 10.1109/IEMBS.2010.5626502.
  32. Opitz A, Paulus W, Will S, Antunes A, Thielscher A. Determinants of the electric field during transcranial direct current stimulation. Neuroimage. 2015 Apr 1;109:140-50. DOI: 10.1016/j.neuroimage.2015.01.033.
  33. Halko MA, Datta A, Plow EB, Scaturro J, Bikson M, Merabet LB. Neuroplastic changes following rehabilitative training correlate with regional electrical field induced with tDCS. Neuroimage. 2011 Aug 1;57(3):885-91. DOI: 10.1016/j.neuroimage.2011.05.026.
  34. Arlotti M, Rahman A, Minhas P, Bikson M. Axon terminal polarization induced by weak uniform DC electric fields: a modeling study. InEngineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE 2012 Aug 28 (pp. 4575-4578). IEEE. DOI: 10.1109/EMBC.2012.6346985.
  35. Laakso I, Tanaka S, Koyama S, De Santis V, Hirata A. Inter-subject variability in electric fields of motor cortical tDCS. Brain stimulation. 2015 Oct 31;8(5):906-13. DOI: 10.1016/j.brs.2015.05.002.
  36. Shahid SS, Bikson M, Salman H, Wen P, Ahfock T. The value and cost of complexity in predictive modelling: role of tissue anisotropic conductivity and fibre tracts in neuromodulation. Journal of neural engineering. 2014 Apr 16;11(3):036002. DOI: 10.1088/1741-2560/11/3/036002.
  37. Suh HS, Lee WH, Kim TS. Influence of anisotropic conductivity in the skull and white matter on transcranial direct current stimulation via an anatomically realistic finite element head model. Physics in Medicine and Biology. 2012 Oct 9;57(21):6961. DOI: 10.1088/0031-9155/57/21/6961.
  38.  Metwally MK, Han SM, Kim TS. The effect of tissue anisotropy on the radial and tangential components of the electric field in transcranial direct current stimulation. Medical & biological engineering & computing. 2015 Oct 1;53(10):1085-101. DOI: 10.1007/s11517-015-1301-z.
  39. Huang Y, Dmochowski JP, Su Y, Datta A, Rorden C, Parra LC. Automated MRI segmentation for individualized modeling of current flow in the human head. Journal of neural engineering. 2013 Oct 8;10(6):066004. DOI: 10.1088/1741-2560/10/6/066004.
  40. Plonsey R, Heppner DB. Considerations of quasi-stationarity in electrophysiological systems. Bulletin of mathematical Biology. 1967 Dec 1;29(4):657-64.
  41. Miranda PC, Pajevic S, Pierpoali C, Hallett M, Basser P. The distribution of currents induced in the brain by magnetic stimulation: a finite element analysis incorporating DT-MRI-derived conductivity data. InProceedings of the International Society for Magnetic Resonance in Medicine 2001 (Vol. 9).
  42. Kim S, Kim TS, Zhou Y, Singh M. Influence of conductivity tensors in the finite element model of the head on the forward solution of EEG. InNuclear Science Symposium Conference Record, 2001 IEEE 2001 (Vol. 4, pp. 1892-1896). IEEE. DOI: 10.1109/NSSMIC.2001.1009193.
  43. Abascal JF, Arridge SR, Atkinson D, Horesh R, Fabrizi L, De Lucia M, et al. Use of anisotropic modelling in electrical impedance tomography; description of method and preliminary assessment of utility in imaging brain function in the adult human head. Neuroimage. 2008 Nov 1;43(2):258-68. DOI: 10.1016/j.neuroimage.2008.07.023.
  44. Purpura DP, McMurtry JG. Intracellular activities and evoked potential changes during polarization of motor cortex. Journal of neurophysiology. 1965 Jan 1;28(1):166-85.
  45. Gluckman BJ, Neel EJ, Netoff TI, Ditto WL, Spano ML, Schiff SJ. Electric field suppression of epileptiform activity in hippocampal slices. Journal of Neurophysiology. 1996 Dec 1;76(6):4202-5.
  46. Radman T, Ramos RL, Brumberg JC, Bikson M. Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain stimulation. 2009 Oct 31;2(4):215-28. DOI: 10.1016/j.brs.2009.03.007.
  47. Rattay F. Analysis of models for external stimulation of axons. IEEE transactions on biomedical engineering. 1986 Oct(10):974-7. DOI: 10.1109/TBME.1986.325670.
  48.  Datta A, Truong D, Minhas P, Parra LC, Bikson M. Inter-individual variation during transcranial direct current stimulation and normalization of dose using MRI-derived computational models. Frontiers in psychiatry. 2012;3. DOI: 10.3389/fpsyt.2012.00091.
  49. Ferdjallah M, Bostick FX, Barr RE. Potential and current density distributions of cranial electrotherapy stimulation (CES) in a four-concentric-spheres model. IEEE Transactions on Biomedical Engineering. 1996 Sep;43(9):939-43. DOI: 10.1109/10.532128.
  50. Li LM, Uehara K, Hanakawa T. The contribution of interindividual factors to variability of response in transcranial direct current stimulation studies. Frontiers in cellular neuroscience. 2015;9. DOI: 10.3389/fncel.2015.00181.
  51. Bikson M, Rahman A, Datta A, Fregni F, Merabet L. High‐Resolution Modeling Assisted Design of Customized and Individualized Transcranial Direct Current Stimulation Protocols. Neuromodulation: Technology at the Neural Interface. 2012 Jul 1;15(4):306-15.
  52.  Wagner S, Rampersad SM, Aydin Ü, Vorwerk J, Oostendorp TF, Neuling T, et al. Investigation of tDCS volume conduction effects in a highly realistic head model. Journal of neural engineering. 2013 Dec 5;11(1):016002. DOI: 10.1088/1741-2560/11/1/016002.
  53. Datta A, Baker JM, Bikson M, Fridriksson J. Individualized model predicts brain current flow during transcranial direct-current stimulation treatment in responsive stroke patient. Brain stimulation. 2011 Jul 31;4(3):169-74. DOI: 10.1016/j.brs.2010.11.001.
  54.  Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain?. European Journal of Neuroscience. 2005 Jul 1;22(2):495-504. DOI: 10.1111/j.1460-9568.2005.04233.x.
  55. Sadleir RJ, Vannorsdall TD, Schretlen DJ, Gordon B. Transcranial direct current stimulation (tDCS) in a realistic head model. Neuroimage. 2010 Jul 15;51(4):1310-8. DOI: 10.1016/j.neuroimage.2010.03.052.
  56.  Metwally MK, Cho YS, Park HJ, Kim TS. Investigation of the electric field components of tDCS via anisotropically conductive gyri-specific finite element head models. InEngineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE 2012 Aug 28 (pp. 5514-5517). IEEE. DOI: 10.1109/EMBC.2012.6347243.
  57. Russell MJ, Goodman T, Pierson R, Shepherd S, Wang Q, Groshong B, Wiley DF. Individual differences in transcranial electrical stimulation current density. Journal of biomedical research. 2013 Nov;27(6):495. DOI: 10.7555/JBR.27.20130074.
  58. Holdefer RN, Sadleir R, Russell MJ. Predicted current densities in the brain during transcranial electrical stimulation. Clinical neurophysiology. 2006 Jun 30;117(6):1388-97. DOI: 10.1016/j.clinph.2006.02.020.
  59. Oostendorp TF, Hengeveld YA, Wolters CH, Stinstra J, van Elswijk G, Stegeman DF. Modeling transcranial DC stimulation. InEngineering in Medicine and Biology Society, 2008. EMBS 2008. 30th Annual International Conference of the IEEE 2008 Aug 20 (pp. 4226-4229). IEEE. DOI: 10.1109/IEMBS.2008.4650142.
  60. Suh HS, Kim SH, Lee WH, Kim TS. Realistic simulation of transcranial direct current stimulation via 3-D high-resolution finite element analysis: effect of tissue anisotropy. InEngineering in Medicine and Biology Society, 2009. EMBC 2009. Annual International Conference of the IEEE 2009 Sep 3 (pp. 638-641). IEEE. DOI: 10.1109/IEMBS.2009.5333686.
  61. Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, et al. Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. The Journal of physiology. 2013 May 1;591(10):2563-78. DOI: 10.1113/jphysiol.2012.247171.
  62. Kabakov AY, Muller PA, Pascual-Leone A, Jensen FE, Rotenberg A. Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. Journal of neurophysiology. 2012 Apr 1;107(7):1881-9. DOI: 10.1152/jn.00715.2011.
  63. Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, et al. Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. The Journal of physiology. 2004 May 1;557(1):175-90. DOI: 10.1113/jphysiol.2003.055772.
  64. Ono M, Kubik S, Abernathey CD. Atlas of the cerebral sulci. Tps; 1990.
  65. Fischl B, Sereno MI, Tootell RB, Dale AM. High-resolution intersubject averaging and a coordinate system for the cortical surface. Human brain mapping. 1999 Jan 1;8(4):272-84.
  66. Shahid S, Wen P, Ahfock T. Effect of fat and muscle tissue conductivity on cortical currents-a tDCS study. InComplex Medical Engineering (CME), 2011 IEEE/ICME International Conference on 2011 May 22 (pp. 211-215). IEEE. DOI: 10.1109/ICCME.2011.5876735.
  67. Truong DQ, Magerowski G, Pascual-Leone A, Alonso-Alonso M, Bikson M. Finite element study of skin and fat delineation in an obese subject for transcranial direct current stimulation. InEngineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE 2012 Aug 28 (pp. 6587-6590). IEEE. DOI: 10.1109/EMBC.2012.6347504.
  68. Parazzini M, Fiocchi S, Rossi E, Paglialonga A, Ravazzani P. Transcranial direct current stimulation: estimation of the electric field and of the current density in an anatomical human head model. IEEE Transactions on Biomedical Engineering. 2011 Jun;58(6):1773-80. DOI: 10.1109/TBME.2011.2116019.
  69.  Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. Journal of magnetic resonance imaging. 2001 Apr 1;13(4):534-46.
  70. D.S. Tuch, Q‐ball imaging, Magnetic resonance in medicine, 52 (2004) 1358-1372.
  71.  Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, et al. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage. 2008 Jul 15;41(4):1267-77. DOI: 10.1016/j.neuroimage.2008.03.036.
  72. Tuch DS, Reese TG, Wiegell MR, Makris N, Belliveau JW, Wedeen VJ. High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magnetic resonance in medicine. 2002 Oct 1;48(4):577-82. DOI: 10.1002/mrm.10268.
  73. Jog MV, Smith RX, Jann K, Dunn W, Lafon B, Truong D, et al. In-vivo imaging of magnetic fields induced by transcranial direct current stimulation (tDCS) in human brain using MRI. Scientific reports. 2016;6. DOI: 10.1038/srep34385.
  74. Kwon OI, Sajib SZ, Sersa I, Oh TI, Jeong WC, Kim HJ, et al. Current Density Imaging during Transcranial Direct Current Stimulation (tDCS) using DT-MRI and MREIT: Algorithm Development and Numerical Simulations. IEEE Trans. on Biomedical Engineering. 2015;22. DOI: 10.1109/TBME.2015.2448555.