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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.

A crucial step in forming spatial representations of the environment involves the estimation of relative distance. Active sampling through specific movements is considered essential for optimizing the sensory flow that enables the extraction of distance cues. However, in electric sensing, direct evidence for the generation and exploitation of sensory flow is lacking. Weakly electric fish rely on a self-generated electric field to navigate and capture prey in the dark. This electric sense provides a blurred representation of the environment, making the exquisite sensory abilities of electric fish enigmatic. Stereotyped back-and-forth swimming patterns reminiscent of visual peering movements are suggestive of the active generation of sensory flow, but how motion contributes to the disambiguation of the electrosensory world remains unclear. Here, we show that a dipole-like electric field geometry coupled to motion provides the physical basis for a nonvisual parallax. We then show in a behavioral assay that this cue is used for electrosensory distance perception across phylogenetically distant taxa of weakly electric fish. Notably, these species electrically sample the environment in temporally distinct ways (using discrete pulses or quasisinusoidal waves), suggesting a ubiquitous role for parallax in electric sensing. Our results demonstrate that electrosensory information is extracted from sensory flow and used in a behaviorally relevant context. A better understanding of motion-based electric sensing will provide insight into the sensorimotor coordination required for active sensing in general and may lead to improved electric field-based imaging applications in a variety of contexts.