Motion parallax in electric sensing

Abstract

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.