Neuronal Dynamics Underlying Communication Signals in a Weakly Electric Fish: Implications for Connectivity in a Pacemaker Network

•An electrically coupled pacemaker network in electric fish sets the timing for its high-frequency electric organ discharge.•Synaptic inputs modulate the timing of this pacemaker on millisecond timescales to produce electrocommunication signals.•These synaptic inputs cause variable resetting of pacemaker neurons resulting in transient desynchronization at the network level.•Computational models illustrate how network connectivity can influence the temporal features of pacemaker resetting.•Differences in pacemaker network connectivity may underlie diversity in communication signals across species. Neuronal networks can produce stable oscillations and synchrony that are under tight control yet flexible enough to rapidly switch between dynamical states. The pacemaker nucleus in the weakly electric fish comprises a network of electrically coupled neurons that fire synchronously at high frequency. This activity sets the timing for an oscillating electric organ discharge with the lowest cycle-to-cycle variability of all known biological oscillators. Despite this high temporal precision, pacemaker activity is behaviorally modulated on millisecond time-scales for the generation of electrocommunication signals. The network mechanisms that allow for this combination of stability and flexibility are not well understood. In this study, we use an in vitro pacemaker preparation from Apteronotus leptorhynchus to characterize the neural responses elicited by the synaptic inputs underlying electrocommunication. These responses involve a variable increase in firing frequency and a prominent desynchronization of neurons that recovers within 5 oscillation cycles. Using a previously developed computational model of the pacemaker network, we show that the frequency changes and rapid resynchronization observed experimentally are most easily explained when model neurons are interconnected more densely and with higher coupling strengths than suggested by published data. We suggest that the pacemaker network achieves both stability and flexibility by balancing coupling strength with interconnectivity and that variation in these network features may provide a substrate for species-specific evolution of electrocommunication signals.