Intracellular impedance measurements reveal non-ohmic properties of the extracellular medium around neurons

TL;DR

This study introduces a novel method to measure the impedance of neural tissue, revealing non-ohmic, frequency-dependent properties that challenge the traditional resistive models used in neuroscience.

Contribution

The paper presents a new in vivo and in vitro measurement technique that uncovers non-ohmic properties of the extracellular medium around neurons, contrasting with previous resistive assumptions.

Findings

Neural tissue exhibits non-ohmic, frequency-filtering impedance properties.

Traditional metal electrodes yield resistive impedance measurements.

Ionic diffusion contributes to the observed impedance characteristics.

Abstract

The electrical properties of extracellular space around neurons are important to understand the genesis of extracellular potentials, as well as for localizing neuronal activity from extracellular recordings. However, the exact nature of these extracellular properties is still uncertain. We introduce a method to measure the impedance of the tissue, and which preserves the intact cell-medium interface, using whole-cell patch-clamp recordings in vivo and in vitro. We find that neural tissue has marked non-ohmic and frequency-filtering properties, which are not consistent with a resistive (ohmic) medium, as often assumed. In contrast, using traditional metal electrodes provides very different results, more consistent with a resistive medium. The amplitude and phase profiles of the measured impedance are consistent with the contribution of ionic diffusion. We also show that the impact of such frequency-filtering properties is possibly important on the genesis of local field potentials, as well as on the cable properties of neurons. The present results show non-ohmic properties of the extracellular medium around neurons, and suggest that source estimation methods, as well as the cable properties of neurons, which all assume ohmic extracellular medium, may need to be re-evaluated.