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.

Motion parallax in electric sensing

“…In summary, although the lateral position of the shuttle walls was constant, changing their longitudinal speed caused the fish to move toward the slower side. While these shifts are small (<1 cm), they are behaviorally relevant, as prey detection and the inspection of larger objects occur on similar spatial scales (11,21).…”

“…When a fish scans an object, the spatial aspects of the electric image are transformed into a local temporal pattern of input to the skin electroreceptors (the temporal electric image). Closer objects, with narrower images, lead to higher rates of change in this temporal input (19,21). Importantly, the temporal electric image and motion parallax cues are inseparable, due to their mutual dependence on electric field geometry: motion parallax increases the speed of image translation for closer objects and thus increases the rate of change of the temporal electric image.…”

“…Both lineages exhibit similar stereotypical swimming movements (e.g., va-et-vient scanning) during electrosensory-based behaviors (11,17,18,20,22). Such motion will generate the electrosensory flow that leads to motion parallax (19,21,22), but how the electric fish brain controls the necessary movements remains unknown. The neural coding of image shape and motion is very different between pulse-type Mormyrid (Gnathonemus) and wave-type Gymnotiform (Apteronotus and Eigenmannia) fish; the sensory encoding stage primarily involves a latency code in the former and a rate code in the latter (35).…”

“…1 and Figs. S1 and S2 were calculated using the boundary element method (BEM) (10,21,41); the electric images were calculated as described for the experimental data (modulation of perturbed vs. unperturbed condition). To calculate the electric images produced by the Perspex shuttle (Supporting Information and Fig.…”

“…A number of static cues related to the electric image have been linked to electrosensory distance perception (12,14,15), but how fish use motion-based sensory flow is not clear. Indeed, the stereotyped "va-et-vient" swimming resembling visual peering movements (16)(17)(18) strongly suggests that dynamic cues are extracted through the generation of sensory flow (19)(20)(21)(22). In addition, electrosensory neurons encode a wide range of spatiotemporally varying stimuli that could arise from sensory flow (23)(24)(25).…”