Spatiotemporal structure of intracranial electric fields induced by transcranial electric stimulation in human and nonhuman primates

Transcranial electric stimulation (TES) is an emerging technique, developed to non-invasively modulate brain function. However, the spatiotemporal distribution of the intracranial electric fields induced by TES remains poorly understood. In particular, it is unclear how much current actually reaches the brain, and how it distributes across the brain. Lack of this basic information precludes a firm mechanistic understanding of TES effects. In this study we directly measure the spatial and temporal characteristics of the electric field generated by TES using stereotactic EEG (s-EEG) electrode arrays implanted in cebus monkeys and surgical epilepsy patients. We found a small frequency dependent decrease (10%) in magnitudes of TES induced potentials and negligible phase shifts over space. Electric field strengths were strongest in superficial brain regions with maximum values of about 0.5 mV/mm. Our results provide crucial information for the interpretation of human TES studies and the optimization and design of TES stimulation protocols. In addition, our findings have broad implications concerning electric field propagation in non-invasive recording techniques such as EEG/MEG.

[1]  Yuzhuo Su,et al.  Spike Timing Amplifies the Effect of Electric Fields on Neurons: Implications for Endogenous Field Effects , 2007, The Journal of Neuroscience.

[2]  D. McCormick,et al.  Endogenous Electric Fields May Guide Neocortical Network Activity , 2010, Neuron.

[3]  P. Miranda,et al.  Physics of effects of transcranial brain stimulation. , 2013, Handbook of clinical neurology.

[4]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[5]  D. A. Driscoll,et al.  EEG electrode sensitivity--an application of reciprocity. , 1969, IEEE transactions on bio-medical engineering.

[6]  W. Pritchard,et al.  The brain in fractal time: 1/f-like power spectrum scaling of the human electroencephalogram. , 1992, The International journal of neuroscience.

[7]  W. Paulus Transcranial electrical stimulation (tES – tDCS; tRNS, tACS) methods , 2011, Neuropsychological rehabilitation.

[8]  Claude Bédard,et al.  Evidence for frequency-dependent extracellular impedance from the transfer function between extracellular and intracellular potentials , 2009, Journal of Computational Neuroscience.

[9]  L. Bindman,et al.  Long-lasting Changes in the Level of the Electrical Activity of the Cerebral Cortex produced by Polarizing Currents , 1962, Nature.

[10]  D. Reato,et al.  Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad , 2009, Brain Stimulation.

[11]  R. W. Lau,et al.  The dielectric properties of biological tissues: II. Measurements in the frequency range 10 Hz to 20 GHz. , 1996, Physics in medicine and biology.

[12]  J. Rothwell,et al.  Variability in Response to Transcranial Direct Current Stimulation of the Motor Cortex , 2014, Brain Stimulation.

[13]  D. B. Heppner,et al.  Considerations of quasi-stationarity in electrophysiological systems. , 1967, The Bulletin of mathematical biophysics.

[14]  F. Fröhlich,et al.  Transcranial Alternating Current Stimulation Modulates Large-Scale Cortical Network Activity by Network Resonance , 2013, The Journal of Neuroscience.

[15]  Joseph R. Madsen,et al.  Individualized localization and cortical surface-based registration of intracranial electrodes , 2012, NeuroImage.

[16]  L. Parra,et al.  Low-Intensity Electrical Stimulation Affects Network Dynamics by Modulating Population Rate and Spike Timing , 2010, The Journal of Neuroscience.

[17]  Alexander Opitz,et al.  Determinants of the electric field during transcranial direct current stimulation , 2015, NeuroImage.

[18]  C. Koch,et al.  Transcranial Electric Stimulation Entrains Cortical Neuronal Populations in Rats , 2010, The Journal of Neuroscience.

[19]  M. Grueschow,et al.  The precision of value-based choices depends causally on fronto-parietal phase coupling , 2015, Nature Communications.

[20]  Gregor Thut,et al.  Alpha Power Increase After Transcranial Alternating Current Stimulation at Alpha Frequency (α-tACS) Reflects Plastic Changes Rather Than Entrainment , 2015, Brain Stimulation.

[21]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[22]  B. Cheeran,et al.  Inter-individual Variability in Response to Non-invasive Brain Stimulation Paradigms , 2014, Brain Stimulation.

[23]  Markus Zahn,et al.  Impact of brain tissue filtering on neurostimulation fields: A modeling study , 2013, NeuroImage.

[24]  Richard G. Lyons,et al.  Reducing FFT Scalloping Loss Errors Without Multiplication [DSP Tips and Tricks] , 2011, IEEE Signal Processing Magazine.

[25]  C. Gabriel,et al.  Electrical conductivity of tissue at frequencies below 1 MHz , 2009, Physics in medicine and biology.

[26]  Á. Pascual-Leone,et al.  Noninvasive human brain stimulation. , 2007, Annual review of biomedical engineering.

[27]  J. Jefferys,et al.  Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro , 2004, The Journal of physiology.

[28]  R PLONSEY,et al.  RECIPROCITY APPLIED TO VOLUME CONDUCTORS AND THE ECG. , 1963, IEEE transactions on bio-medical engineering.

[29]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[30]  N. Logothetis,et al.  In Vivo Measurement of Cortical Impedance Spectrum in Monkeys: Implications for Signal Propagation , 2007, Neuron.

[31]  C. Bédard,et al.  Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. , 2003, Biophysical journal.

[32]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[33]  C Gabriel,et al.  The dielectric properties of biological tissues: I. Literature survey. , 1996, Physics in medicine and biology.

[34]  L. Parra,et al.  Optimized multi-electrode stimulation increases focality and intensity at target , 2011, Journal of neural engineering.

[35]  Walter Paulus,et al.  Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases , 2014, NeuroImage.

[36]  Christof Koch,et al.  Ephaptic coupling of cortical neurons , 2011, Nature Neuroscience.

[37]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[38]  M. Bikson,et al.  Methods for extra-low voltage transcranial direct current stimulation: Current and time dependent impedance decreases , 2013, Clinical Neurophysiology.

[39]  Raja Parasuraman,et al.  Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation , 2014, NeuroImage.

[40]  Giulio Ruffini,et al.  The electric field in the cortex during transcranial current stimulation , 2013, NeuroImage.

[41]  Ashesh D. Mehta,et al.  Dominant frequencies of resting human brain activity as measured by the electrocorticogram , 2013, NeuroImage.

[42]  M. Belluscio,et al.  Closed-Loop Control of Epilepsy by Transcranial Electrical Stimulation , 2012, Science.

[43]  Sung Chan Jun,et al.  Validation of Computational Studies for Electrical Brain Stimulation With Phantom Head Experiments , 2015, Brain Stimulation.