Thermal effects on neurons during stimulation of the brain

Tae Ken Kim, Herve Kadji, Andrew J. Whalen, Arian Ashourvan, Eugene Freeman, Shelley I. Fried, Srinivas Tadigadapa, Steven J. Schiff

Research output: Contribution to journalArticlepeer-review

12 Scopus citations

Abstract

All electric and magnetic stimulation of the brain deposits thermal energy in the brain. This occurs through either Joule heating of the conductors carrying current through electrodes and magnetic coils, or through dissipation of energy in the conductive brain. Objective. Although electrical interaction with brain tissue is inseparable from thermal effects when electrodes are used, magnetic induction enables us to separate Joule heating from induction effects by contrasting AC and DC driving of magnetic coils using the same energy deposition within the conductors. Since mammalian cortical neurons have no known sensitivity to static magnetic fields, and if there is no evidence of effect on spike timing to oscillating magnetic fields, we can presume that the induced electrical currents within the brain are below the molecular shot noise where any interaction with tissue is purely thermal. Approach. In this study, we examined a range of frequencies produced from micromagnetic coils operating below the molecular shot noise threshold for electrical interaction with single neurons. Main results. We found that small temperature increases and decreases of 1 °C caused consistent transient suppression and excitation of neurons during temperature change. Numerical modeling of the biophysics demonstrated that the Na-K pump, and to a lesser extent the Nernst potential, could account for these transient effects. Such effects are dependent upon compartmental ion fluxes and the rate of temperature change. Significance. A new bifurcation is described in the model dynamics that accounts for the transient suppression and excitation; in addition, we note the remarkable similarity of this bifurcation's rate dependency with other thermal rate-dependent tipping points in planetary warming dynamics. These experimental and theoretical findings demonstrate that stimulation of the brain must take into account small thermal effects that are ubiquitously present in electrical and magnetic stimulation. More sophisticated models of electrical current interaction with neurons combined with thermal effects will lead to more accurate modulation of neuronal activity.

Original languageEnglish (US)
Article number056029
JournalJournal of neural engineering
Volume19
Issue number5
DOIs
StatePublished - Oct 1 2022

All Science Journal Classification (ASJC) codes

  • Biomedical Engineering
  • Cellular and Molecular Neuroscience

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