Extending Integrate-and-Fire Model Neurons to Account for the Effects of Weak Electric Fields and Input Filtering Mediated by the Dendrite

Abstract

Transcranial brain stimulation and evidence of ephaptic coupling have recently sparked strong interests in understanding the effects of weak electric fields on the dynamics of brain networks and of coupled populations of neurons. The collective dynamics of large neuronal populations can be efficiently studied using single-compartment (point) model neurons of the integrate-and-fire (IF) type as their elements. These models, however, lack the dendritic morphology required to biophysically describe the effect of an extracellular electric field on the neuronal membrane voltage. Here, we extend the IF point neuron models to accurately reflect morphology dependent electric field effects extracted from a canonical spatial “ball-and-stick” (BS) neuron model. Even in the absence of an extracellular field, neuronal morphology by itself strongly affects the cellular response properties. We, therefore, derive additional components for leaky and nonlinear IF neuron models to reproduce the subthreshold voltage and spiking dynamics of the BS model exposed to both fluctuating somatic and dendritic inputs and an extracellular electric field. We show that an oscillatory electric field causes spike rate resonance, or equivalently, pronounced spike to field coherence. Its resonance frequency depends on the location of the synaptic background inputs. For somatic inputs the resonance appears in the beta and gamma frequency range, whereas for distal dendritic inputs it is shifted to even higher frequencies. Irrespective of an external electric field, the presence of a dendritic cable attenuates the subthreshold response at the soma to slowly-varying somatic inputs while implementing a low-pass filter for distal dendritic inputs. Our point neuron model extension is straightforward to implement and is computationally much more efficient compared to the original BS model. It is well suited for studying the dynamics of large populations of neurons with heterogeneous dendritic morphology with (and without) the influence of weak external electric fields.