Membrane potential resonance frequency directly influences network frequency through electrical coupling

Oscillatory networks often include neurons with membrane potential resonance, exhibiting a peak in the voltage amplitude as a function of current input at a nonzero (resonance) frequency (f_res). Although f_res has been correlated to the network frequency (f_net) in a variety of systems, a causal relationship between the two has not been established. We examine the hypothesis that combinations of biophysical parameters that shift f_res, without changing other attributes of the impedance profile, also shift f_net in the same direction. We test this hypothesis, computationally and experimentally, in an electrically coupled network consisting of intrinsic oscillator (O) and resonator (R) neurons. We use a two-cell model of such a network to show that increasing f_res of R directly increases f_net and that this effect becomes more prominent if the amplitude of resonance is increased. Notably, the effect of f_res on f_net is independent of the parameters that define the oscillator or the combination of parameters in R that produce the shift in f_res, as long as this combination produces the same impedance vs. frequency relationship. We use the dynamic clamp technique to experimentally verify the model predictions by connecting a model resonator to the pacemaker pyloric dilator neurons of the crab Cancer borealis pyloric network using electrical synapses and show that the pyloric network frequency can be shifted by changing f_res in the resonator. Our results provide compelling evidence that f_res and resonance amplitude strongly influence f_net, and therefore, modulators may target these attributes to modify rhythmic activity.