Weak electric fields promote resonance in neuronal spiking activity: analytical results from two-compartment cell and network models

Abstract

Transcranial brain stimulation and evidence of ephaptic coupling have sparked strong interests in understanding the effects of weak electric fields on the dynamics of neuronal populations. While their influence on the subthreshold membrane voltage can be biophysically well explained using spatially extended neuron models, mechanistic analyses of neuronal spiking and network activity have remained a methodological challenge. More generally, this challenge applies to phenomena for which single-compartment (point) neuron models are oversimplified. Here we employ a pyramidal neuron model that comprises two compartments, allowing to distinguish basal-somatic from apical dendritic inputs and accounting for an extracellular field in a biophysically minimalistic way. Using an analytical approach we fit its parameters to reproduce the response properties of a canonical, spatial model neuron and dissect the stochastic spiking dynamics of single cells and large networks. We show that oscillatory weak fields effectively mimic anti-correlated inputs at the soma and dendrite and strongly modulate neuronal spiking activity in a rather narrow frequency band. This effect carries over to coupled populations of pyramidal cells and inhibitory interneurons, boosting network-induced resonance in the beta and gamma frequency bands. Our work contributes a useful theoretical framework for mechanistic analyses of population dynamics going beyond point neuron models, and provides insights on modulation effects of extracellular fields due to the morphology of pyramidal cells.\n\nAuthor SummaryThe elongated spatial structure of pyramidal neurons, which possess large apical dendrites, plays an important role for the integration of synaptic inputs and mediates sensitivity to weak extracellular electric fields. Modeling studies at the population level greatly contribute to our mechanistic understanding but face a methodological challenge because morphologically detailed neuron models are too complex for use in noisy, in-vivo like conditions and large networks in particular. Here we present an analytical approach based on a two-compartment spiking neuron model that can distinguish synaptic inputs at the apical dendrite from those at the somatic region and accounts for an extracellular field in a biophysically minimalistic way. We devised efficient methods to approximate the responses of a spatially more detailed pyramidal neuron model, and to study the spiking dynamics of single neurons and sparsely coupled large networks in the presence of fluctuating inputs. Using these methods we focused on how responses are affected by oscillatory weak fields. Our results suggest that ephaptic coupling may play a mechanistic role for oscillations of population activity and indicate the potential to entrain networks by weak electric stimulation.