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Numerical Simulation of Concussive-Generated Cortical Spreading Depolarization to Optimize DC-EEG Electrode Spacing for Noninvasive Visual Detection

  • Cortical Spreading Depolarization
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Abstract

Background

Cortical spreading depolarization (SD) is a propagating depolarization wave of neurons and glial cells in the cerebral gray matter. SD occurs in all forms of severe acute brain injury, as documented by using invasive detection methods. Based on many experimental studies of mechanical brain deformation and concussion, the occurrence of SDs in human concussion has often been hypothesized. However, this hypothesis cannot be confirmed in humans, as SDs can only be detected with invasive detection methods that would require either a craniotomy or a burr hole to be performed on athletes. Typical electroencephalography electrodes, placed on the scalp, can help detect the possible presence of SD but have not been able to accurately and reliably identify SDs.

Methods

To explore the possibility of a noninvasive method to resolve this hurdle, we developed a finite element numerical model that simulates scalp voltage changes that are induced by a brain surface SD. We then compared our simulation results with retrospectively evaluated data in patients with aneurysmal subarachnoid hemorrhage from Drenckhahn et al. (Brain 135:853, 2012).

Results

The ratio of peak scalp to simulated peak cortical voltage, Vscalp/Vcortex, was 0.0735, whereas the ratio from the retrospectively evaluated data was 0.0316 (0.0221, 0.0527) (median [1st quartile, 3rd quartile], n = 161, p < 0.001, one sample Wilcoxon signed-rank test). These differing values provide validation because their differences can be attributed to differences in shape between concussive SDs and aneurysmal subarachnoid hemorrhage SDs, as well as the inherent limitations in human study voltage measurements. This simulated scalp surface potential was used to design a virtual scalp detection array. Error analysis and visual reconstruction showed that 1 cm is the optimal electrode spacing to visually identify the propagating scalp voltage from a cortical SD. Electrode spacings of 2 cm and above produce distorted images and high errors in the reconstructed image.

Conclusions

Our analysis suggests that concussive (and other) SDs can be detected from the scalp, which could confirm SD occurrence in human concussion, provide concussion diagnosis on the basis of an underlying physiological mechanism, and lead to noninvasive SD detection in the setting of severe acute brain injury

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Acknowledgements

We thank Thomas Ferguson, Richard Kraig, Douglas Smith, and Joel Greenberg for reading and commenting on the manuscript and Hiba Al-Ashtal for editorial services.

Funding

This project was conducted for CerebroScope, a medical device company developing a scalp direct current electroencephalography system for detecting SDs in severe acute brain injury, concussion, and migraine. This work was partially supported by grants from the United States Public Health Service National Institutes of Health; NS30839, NS30839-14S1, and NS66292 to the SCJ while at the Allegheny-Singer Research Institute; and 5R43NS092181 and 3R43NS092181-02S1 to SCJ for CerebroScope; Deutsche Forschungsgemeinschaft, German Research Council: DFG DR 323/5–1 and DFG DR 323/10–1 to JPD; and Bundesministerium fuer Bildung und Forschung (Era-Net Neuron EBio2), with funds from Bundesministerium fuer Bildung und Forschung (0101EW2004) to JPD.

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Authors and Affiliations

  1. CerebroScope, SciencePlusPlease LLC, Pittsburgh, PA, USA

    Samuel J. Hund, Benjamin R. Brown, Prahlad G. Menon & Stephen C. Jones

  2. SimulationSolutions, Pittsburgh, PA, USA

    Samuel J. Hund

  3. Center for Stroke Research, Charité, – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, Berlin, Germany

    Coline L. Lemale & Jens P. Dreier

  4. Department of Experimental Neurology, Charité, – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, Berlin, Germany

    Coline L. Lemale & Jens P. Dreier

  5. Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA

    Prahlad G. Menon

  6. Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, GA, USA

    Kirk A. Easley

  7. Department of Neurology, Charité, – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, Berlin, Germany

    Jens P. Dreier

  8. Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany

    Jens P. Dreier

  9. Einstein Center for Neurosciences Berlin, Berlin, Germany

    Jens P. Dreier

Authors
  1. Samuel J. Hund
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  2. Benjamin R. Brown
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  3. Coline L. Lemale
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  4. Prahlad G. Menon
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  5. Kirk A. Easley
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  7. Stephen C. Jones
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Contributions

SJH developed the code with input from SCJ and PGM and wrote the first draft. BRB contributed additional analysis. KAE conceived of and performed the statistical analysis. JPD and CLL supplied the comparison data. SCJ, SJH, BRB, and JPD edited the article. SCJ conceived of the project, provided supervision, and revised the article. The final manuscript was approved by all authors.

Corresponding author

Correspondence to Stephen C. Jones.

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Conflicts of interest

Samuel J. Hund, Prahlad G. Menon, and Stephen C. Jones are founding partners and shareholders of CerebroScope. Benjamin R. Brown is a consultant to and shareholder of CerebroScope.

Ethical Approval/Informed Consent

All ethical standards have been met. See section “Retrospective Evaluation of Human Data.”

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Hund, S.J., Brown, B.R., Lemale, C.L. et al. Numerical Simulation of Concussive-Generated Cortical Spreading Depolarization to Optimize DC-EEG Electrode Spacing for Noninvasive Visual Detection. Neurocrit Care 37 (Suppl 1), 67–82 (2022). https://doi.org/10.1007/s12028-021-01430-x

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