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Electrical Stimulation of the Human Cerebral Cortex by Extracranial Muscle Activity: Effect Quantification With Intracranial EEG and FEM Simulations

Open Access
Abstract:
Objective: Electric fields (EF) of approx. 0.2 V/m have been shown to be sufficiently strong to both modulate neuronal activity in the cerebral cortex and have measurable effects on cognitive performance. We hypothesized that the EF caused by the electrical activity of extracranial muscles during natural chewing may reach similar strength in the cerebral cortex and hence might act as an endogenous modality of brain stimulation. Here, we present first steps toward validating this hypothesis. Methods: Using a realistic volume conductor head model of an epilepsy patient having undergone intracranial electrode placement and utilizing simultaneous intracranial and extracranial electrical recordings during chewing, we derive predictions about the chewing-related cortical EF strength to be expected in healthy individuals. Results: We find that in the region of the temporal poles, the expected EF strength may reach amplitudes in the order of 0.1–1 V/m. Conclusion: The cortical EF caused by natural chewing could be large enough to modulate ongoing neural activity in the cerebral cortex and influence cognitive performance. Significance: The present study lends first support for the assumption that extracranial muscle activity might represent an endogenous source of electrical brain stimulation. This offers a new potential explanation for the puzzling effects of gum chewing on cognition, which have been repeatedly reported in the literature.
Published in: IEEE Transactions on Biomedical Engineering ( Volume: 63, Issue: 12, Dec. 2016 )
Page(s): 2552 - 2563
Date of Publication: 19 July 2016
ISSN Information:
PubMed ID: 27448334

Authors

Author image of Lukas Dominique Josef Fiederer
Intracranial EEG and Brain Imaging Lab, Epilepsy Center, Medical Center – University of Freiburg, Freiburg, Germany
Lukas Dominique Josef Fiederer was born in Meyrin, Switzerland, in 1988. He received the Dipl. Biol. degree in biology from the University of Freiburg, Freiburg, Germany, in 2012. He is currently working toward the doctoral thesis (Dr. rer. nat.) at the University Medical Center Freiburg, Freiburg, Germany.
Since 2013, he is also in charge of the EEG laboratory of the Intracranial EEG and Brain Imaging Lab, Epilepsy Center, University Medical Center Freiburg, Freiburg, Germany. His main research interests include human electrophysiology, in particular surface EEG and invasive EEG, their measurement, analysis and simulation/reconstruction using highly detailed and individualized FEM head models.
Author image of Jacob Lahr
Intracranial EEG and Brain Imaging Lab, Epilepsy Center, Medical Center – University of Freiburg, Freiburg, Germany
Jacob Lahr received the M.D. degree from Albert-Ludwigs University, Freiburg, Germany, in 2011.
He is currently a Resident in the Department of Psychiatry, University Medical Center of Freiburg, Freiburg, Germany. His research fields include signal quality in intracranial electroencephalography and noninvasive brain stimulation.
Author image of Johannes Vorwerk
Institute for Biomagnetism and Biosignalanalysis, University of Münster, Münster, Germany
Johannes Vorwerk received the M.Sc. degree in mathematics with a minor in physics from the University of Münster, Münster, Germany, in 2011 and the PhD degree in Mathematics from the University of Münster in 2016. In April 2016, he joined the Scientific Computing and Imaging (SCI) Institute at the University of Utah, Salt Lake City, USA as a Postdoctoral Fellow.
His research interests include EEG/MEG source localization with a focus on solving the EEG/MEG forward problem using FE methods and tCS optimization.
Author image of Felix Lucka
Center for Medical Image Computing, University College London, London, England
Felix Lucka received the Ph.D. degree in mathematics from the University of Münster, Münster, Germany, supervised by Martin Burger, the Head of the working group “Imaging,” Institute for Applied Mathematics, and by Carsten H. Wolters, the Head of the working group “Methods in bioelectromagnetism,” Institute for Biomagnetism and Biosignalanalysis.
In September 2014, he joined the “Center for Medical Image Computing” (CMIC) at the UCL, U.K., as a Research Associate to work with Simon Arridge. His research interests include inverse problems, Bayesian inference, and mathematical modeling applied to biomedical imaging and brain research.
Author image of Ad Aertsen
Neurobiology and Biophysics, Faculty of Biology, University of Freiburg
Ad Aertsen received the M.Sc. degree in physics from the University of Utrecht, The Netherlands, in 1973. He also studied applied mathematics from the same institute. He received the Ph.D. degree in physics in P. Johannesma and J. Eggermont's Neurophysics Laboratory, University of Nijmegen, The Netherlands, in 1981. He pursued his postdoctoral studies in physiology with G. Gerstein at the University of Pennsylvania, Philadelphia, PA, USA.
He is a Professor of neurobiology and biophysics, Faculty of Biology, University of Freiburg, Freiburg, Germany. He is a Founding Director of the Bernstein Center Freiburg. He was a Research Group Leader with V. Braitenberg at the Max-Planck-Institute for Biological Cybernetics in Tu¨bingen, Germany, a Visiting Professor with E. Vaadia and M. Abeles, Hebrew University, Jerusalem, Israel, a Research Group Leader with W. von Seelen, Ruhr-University, Bochum, Germany, and an Associate Professor at the Weizmann Institute of Science, Rehovot, Israel, working with A. Arieli and A. Grinvald. He moved to Freiburg University, Germany, in 1996. There, his research interests include the recording, analysis, and modelingof neuronal assembly activity in cortical networks, on the improvement of computational neuroscience methods, and on the development of brain–machine interfaces, including neuronal motor prostheses.
Carsten Hermann Wolters received the M.Sc. degree in mathematics with a minor in medicine from the RWTH Aachen, Aachen, Germany, the Ph.D. degree in mathematics from the University of Leipzig, Leipzig, Germany, and the Habilitation in mathematics from the University of Münster, Münster, Germany, in 1997, 2003, and 2008, respectively.
From 1997 to 2004, he was with the Max Planck Institutes for Human Cognitive and Brain Sciences and Mathematics in the Sciences, Leipzig, Germany. In 2004, he joined the Scientific Computing and Imaging Institute, University of Utah, Salt Lake City, UT, USA. Since 2005, he has been a Research Associate with the Institute for Biomagnetism and Biosignalanalysis (IBB), University of Münster, Münster, Germany. Since 2008, he has been heading the research group “Methods in Bioelectromagnetism” at IBB. His research interests include the field of neuroscience with a focus on reconstructing and manipulating neuronal networks in the human brain.
Author image of Andreas Schulze-Bonhage
Epilepsy Center, Medical Center–University of Freiburg, Freiburg, Germany
Andreas Schulze-Bonhage received the M.D. degree in medicine from the University of Münster, Münster, Germany, in 1998. He was habilitated by the University of Freiburg in 2004.
He is the Head of the Epilepsy Center, University Medical Center Freiburg, Freiburg, Germany and a Professor of neurology and clinical neurophysiology.
Dr. Schulze-Bonhage is a Member of the board of directors, University Medical Center, Freiburg, a Member of the Bernstein Center Freiburg, and a Principal Investigator in the Excellence Cluster BrainLinks-BrainTools. Furthermore, he is a Member of the editorial boards of Epilepsia, Seizure, Frontiers in Epilepsy, Epilepsy Research and Treatment, and Zeitschrift für Epileptologie . He has authored more than 240 publications in peer reviewed journals.
Author image of Tonio Ball
Intracranial EEG and Brain Imaging Lab, Epilepsy Center, Medical Center – University of Freiburg, Freiburg, Germany
Tonio Ball received the M.D. degree in medicine from the University of Freiburg, Freiburg, Germany.
He has a permanent position as a Research Group Leader of the Intracranial EEG and Brain Imaging Lab, Epilepsy Center, University Medical Center Freiburg, Freiburg, Germany. His main research interests include recording, analysis, and modeling of cortical neuronal population activity across multiple spatial scales, from microECoG to EEG and fMRI, and the application of such measurements in clinical neurotechnology.
Dr. Ball is a Member of the executive board and a Principal Investigator in the Excellence Cluster BrainLinks-BrainTools at the University of Freiburg. He is a Founding Member of the Bernstein Center Freiburg.