A framework to reconcile frequency scaling measurements, from intracellular recordings, local-field potentials, up to EEG and MEG signals

TL;DR

This paper proposes a comprehensive framework to reconcile conflicting measurements of brain tissue's electric properties, emphasizing ionic diffusion and shunt effects, to better interpret neural signals across multiple scales.

Contribution

It introduces a novel explanation involving ionic diffusion and shunt currents to unify diverse experimental findings on brain tissue conductivity.

Findings

Ionic diffusion explains the observed frequency scaling in brain signals.

Shunt currents can distort electrode measurements, causing discrepancies.

A new measurement method is proposed to avoid shunting effects.

Abstract

In this viewpoint article, we discuss the electric properties of the medium around neurons, which are important to correctly interpret extracellular potentials or electric field effects in neural tissue. We focus on how these electric properties shape the frequency scaling of brain signals at different scales, such as intracellular recordings, the local field potential (LFP), the electroencephalogram (EEG) or the magnetoencephalogram (MEG). These signals display frequency-scaling properties which are not consistent with resistive media. The medium appears to exert a frequency filtering scaling as $1/\sqrt{f}$, which is the typical frequency scaling of ionic diffusion. Such a scaling was also found recently by impedance measurements in physiological conditions. Ionic diffusion appears to be the only possible explanation to reconcile these measurements and the frequency-scaling properties found in different brain signals. However, other measurements suggest that the extracellular medium is essentially resistive. To resolve this discrepancy, we show new evidence that metal-electrode measurements can be perturbed by shunt currents going through the surface of the brain. Such a shunt may explain the contradictory measurements, and together with ionic diffusion, provides a framework where all observations can be reconciled. Finally, we propose a method to perform measurements avoiding shunting effects, thus enabling to test the predictions of this framework.