h-type membrane current shapes the local field potential from populations of pyramidal neurons

Abstract

In cortex, the local field potential (LFP) is thought to mainly stem from correlated synaptic input to populations of geometrically aligned neurons. Computer models of single cortical pyramidal neurons showed that subthreshold voltage-dependent membrane conductances can also shape the LFP signal, in particular the hyperpolarization-activated cation current (Ih; h-type). This ion channel is prominent in various types of pyramidal neurons, typically showing an increasing density gradient along the apical dendrites. Here, we investigate how Ih affects the LFP generated by a model of a population of cortical pyramidal neurons. We find that the LFP from populations of neurons that receive uncorrelated synaptic input can be well predicted by the LFP from single neurons. In this case, when input impinges on the distal dendrites, where most h-type channels are located, a strong resonance in the LFP was measured near the soma, whereas the opposite configuration does not reveal an Ih contribution to the LFP. Introducing correlations in the synaptic inputs to the pyramidal cells strongly amplifies the LFP, while maintaining the differential effects of Ih for distal dendritic versus perisomatic input. Previous theoretical work showed that input correlations do not amplify LFP power when neurons receive synaptic input uniformly across the cell. We find that this crucially depends on the membrane conductance distribution: the asymmetric distribution of Ih results in a strong amplification of the LFP when synaptic inputs to the cell population are correlated. In conclusion, we find that the h-type current is particularly suited to shape the LFP signal in cortical populations.