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Electrical coupling between neurons is broadly present across brain areas and is typically assumed to synchronize network activity. However, intrinsic properties of the coupled cells can complicate this simple picture. Many cell types with electrical coupling show a diversity of post-spike subthreshold fluctuations, often linked to subthreshold resonance, which are transmitted through electrical synapses in addition to action potentials. Using the theory of weakly coupled oscillators, we explore the effect of both subthreshold and spike-mediated coupling on synchrony in small networks of electrically coupled resonate-and-fire neurons, a hybrid neuron model with damped subthreshold oscillations and a range of post-spike voltage dynamics. We calculate the phase response curve using an extension of the adjoint method that accounts for the discontinuous post-spike reset rule. We find that both spikes and subthreshold fluctuations can jointly promote synchronization. The subthreshold contribution is strongest when the voltage exhibits a significant post-spike elevation in voltage, or plateau potential. Additionally, we show that the geometry of trajectories approaching the spiking threshold causes a "reset-induced shear" effect that can oppose synchrony in the presence of network asymmetry, despite having no effect on the phase-locking of symmetrically coupled pairs.

Synchronization of Electrically Coupled Resonate-and-Fire Neurons