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.