Motor patterns during active electrosensory acquisition

Abstract

Motor patterns displayed during active electrosensory acquisition of information seem to be an essential part of a sensory strategy by which weakly electric fish actively generate and shape sensory flow. These active sensing strategies are expected to adaptively optimize ongoing behavior with respect to either motor efficiency or sensory information gained. The tight link between the motor domain and sensory perception in active electrolocation make weakly electric fish like Gnathonemus petersii an ideal system for studying sensory-motor interactions in the form of active sensing strategies. Analyzing the movements and electric signals of solitary fish during unrestrained exploration of objects in the dark, we here present the first formal quantification of motor patterns used by fish during electrolocation. Based on a cluster analysis of the kinematic values we categorized the basic units of motion. These were then analyzed for their associative grouping to identify and extract short coherent chains of behavior. This enabled the description of sensory behavior on different levels of complexity: from single movements, over short behaviors to more complex behavioral sequences during which the kinematics alter between different behaviors. We present detailed data for three classified patterns and provide evidence that these can be considered as motor components of active sensing strategies. In accordance with the idea of active sensing strategies, we found categorical motor patterns to be modified by the sensory context. In addition these motor patterns were linked with changes in the temporal sampling in form of differing electric organ discharge frequencies and differing spatial distributions. The ability to detect such strategies quantitatively will allow future research to investigate the impact of such behaviors on sensing.

Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip

“…The most common form of active sensing, found across animal taxa and behaviors, involves the generation of movements-e.g., whisking [4][5][6], touching [7,8], sniffing [9,10], and eye movements [11]. Active sensing movements profoundly affect the information carried by sensory feedback pathways [12][13][14][15] and are modulated by both top-down goals (e.g., measuring weight versus texture [1,16]) and bottom-up stimuli (e.g., lights on or off [12]), but it remains unclear whether and how these movements are controlled in relation to the ongoing feedback they generate. To investigate the control of movements for active sensing, we created an experimental apparatus for freely swimming weakly electric fish, Eigenmannia virescens, that modulates the gain of reafferent feedback by adjusting the position of a refuge based on real-time videographic measurements of fish position.…”

“…These movements create a dynamic difference between the position of the fish and the refuge, i.e., a sensory slip analogous to retinal slip [23,29], albeit mediated by the propagation of electricity in water [28]. Active swimming movements in electric fishes most likely prevent perceptual fading and enhance spatiotemporal patterns of sensory feedback [12,13,30], serving a similar role as small eye movements in vision [15,30,31].…”

Saccadic Movement Strategy in Common Cuttlefish (Sepia officinalis)

“…We clustered all classes between 2 and 20. For 20–50 classes, only every fifth class was analyzed because we rarely saw stable cluster combinations with these large numbers of classes (Geurten et al, 2010, 2014; Hofmann et al, 2014). To determine the number of classes that represent our data best, we used the quality and stability criteria described in Braun et al (2010).…”

Motion parallax in electric sensing

“…2C). Some of this variability will be due to differences in fish size and details of the electric field geometry, as well as differences in life history (6), neuronal processing (32,33), or kinematic abilities (20,30). As in visual depth perception (1,2), there are also multiple electrosensory cues that could be used in parallel during this centering task (15).…”

“…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).…”