Sensory Flow as a Basis for a Novel Distance Cue in Freely Behaving Electric Fish

Abstract

The sensory input that an animal receives is directly linked to its motor activity. Behavior thus enables animals to influence their sensory input, a concept referred to as active sensing. How such behavior can serve as a scaffold for generating sensory information is of general scientific interest. In this article, we investigate how behavior can shape sensory information by using some unique features of the sensorimotor system of the weakly electric fish. Based on quantitative behavioral characterizations and computational reconstruction of sensory input, we show how electrosensory flow is actively created during highly patterned, spontaneous behavior in Gnathonemus petersii. The spatiotemporal structure of the sensory input provides information for the computation of a novel distance cue, which allows for a continuous estimation of distance. This has significant advantages over previously known nondynamic distance estimators as determined from electric image blur. Our investigation of the sensorimotor interactions in pulsatile electrolocation shows, for the first time, that the electrosensory flow contains behaviorally relevant information accessible only through active behavior. As patterned sensory behaviors are a shared feature of (active) sensory systems, our results have general implications for the understanding of (active) sensing, with the proposed sensory flow-based measure being potentially pertinent to a broad range of sensory modalities. <b>SIGNIFICANCE STATEMENT</b> Acquisition of sensory information depends on motion, as either an animal or its sensors move. Behavior can thus actively influence the sensory flow; and in this way, behavior can be seen as a manifestation of the brain9s integrative functions. The properties of the active pulsatile electrolocation system in Gnathonemus petersii allow for the sensory input to be computationally reconstructed, enabling us to link the informational content of spatiotemporal sensory dynamics to behavior. Our study reveals a novel sensory cue for estimating depth that is actively generated by the fishes9 behavior. The physical and behavioral similarities between electrolocation and other active sensory systems suggest that this may be a mechanism shared by (active) sensory systems.