Modeling extracellular field potentials and the frequency-filtering properties of extracellular space

Extracellular local field potentials are usually modeled as arising from a set of current sources embedded in a homogeneous extracellular medium. Although this formalism can successfully model several properties of extracellular local field potentials, it does not account for their frequency-dependent attenuation with distance, a property essential to correctly model extracellular spikes. Here we derive expressions for the extracellular potential that include this frequency-dependent attenuation. We first show that, if the extracellular conductivity is nonhomogeneous, there is induction of nonhomogeneous charge densities that may result in a low-pass filter. We next derive a simplified model consisting of a punctual (or spherical) current source with spherically symmetric conductivity/permittivity gradients around the source. We analyze the effect of different radial profiles of conductivity and permittivity on the frequency-filtering behavior of this model. We show that this simple model generally displays low-pass filtering behavior, in which fast electrical events (such as Na(+)-mediated action potentials) attenuate very steeply with distance, whereas slower (K(+)-mediated) events propagate over larger distances in extracellular space, in qualitative agreement with experimental observations. This simple model can be used to obtain frequency-dependent extracellular field potentials without taking into account explicitly the complex folding of extracellular space.