The effect of ionic diffusion on extracellular potentials in neural tissue

Abstract

In computational neuroscience, it is common to use the simplifying assumption that diffusive currents are negligible compared to Ohmic currents. However, endured periods of intense neural signaling may cause local ion concentration changes in the millimolar range. Theoretical studies have identified scenarios where steep concentration gradients give rise to diffusive currents that are of comparable magnitude with Ohmic currents, and where the simplifying assumption that diffusion can be neglected does not hold. We here propose a novel formalism for computing (1) the ion concentration dynamics and (2) the electrical potential in the extracellular space surrounding multi-compartmental neuron models or networks of such (e.g., the Blue-Brain simulator). We use this formalism to explore the effects that diffusive currents can have on the extracellular (ECS) potential surrounding a small population of active cortical neurons. Our key findings are: (i) Sustained periods of neuronal output (simulations were run for 84 s) could change local ECS ion concentrations by several mM, as observed experimentally. (ii) For large, but realistic, concentration gradients, diffusive currents in the ECS were of the same magnitude as Ohmic currents. (iii) Neuronal current sources could induce local changes in the ECS potential by a few mV, whereas diffusive currents could could induce local changes in the ECS potential by a few tens of a mV. Diffusive currents could thus have a quite significant impact on ECS potentials. (v) Potential variations caused by diffusive currents were quite slow, but could influence the comparable to those induced by Ohmic currents up to frequencies as high as 7Hz.

27 pages, 8 figures

References in corpus (11)

• Does the 1/f frequency-scaling of brain signals reflect self-organized critical states?
• Macroscopic models of local field potentials and the apparent 1/f noise in brain activity
• Frequency dependence of signal power and spatial reach of the local field potential
• Electrodiffusive model for astrocytic and neuronal ion concentration dynamics
• On 1/f^alpha power laws originating from linear neuronal cable theory: power spectral densities of the soma potential, transmembrane current and single-neuron contribution to the EEG
• Intracellular impedance measurements reveal non-ohmic properties of the extracellular medium around neurons
• Generalized cable theory for neurons in complex and heterogeneous media
• A new open source software for the calculation of the liquid junction potential between two solutions according to the stationary Nernst-Planck equation
• From Three-Dimensional Electrophysiology to the Cable Model: an Asymptotic Study
• Generalized cable formalism to calculate the magnetic field of single neurons and neuronal populations
• How the active and diffusional nature of brain tissues can generate monopole signals at micrometer sized measures

Cited by in corpus (3)

• Finite element simulation of ionicelectrodiffusion in cellular geometries
• Spatio-temporal modeling of saltatory conduction in neurons using Poisson-Nernst-Planck treatment and estimation of conduction velocity
• Accurate numerical simulation of electrodiffusion and water movement in brain tissue