Stimulus predictability mediates a switch in locomotor smooth pursuit performance for Eigenmannia virescens

Abstract

SUMMARYThe weakly electric glass knifefish, Eigenmannia virescens, will swim forward and backward, using propulsion from an anal ribbon fin, in response to motion of a computer-controlled moving refuge. Fish were recorded performing a refuge-tracking behavior for sinusoidal (predictable) and sum-of-sines (pseudo-random) refuge trajectories. For all trials, we observed high coherence between refuge and fish trajectories, suggesting linearity of the tracking dynamics. But superposition failed: we observed categorical differences in tracking between the predictable single-sine stimuli and the unpredictable sum-of-sines stimuli. This nonlinearity suggests a stimulus-mediated adaptation. At all frequencies tested, fish demonstrated reduced tracking error when tracking single-sine trajectories and this was typically accompanied by a reduction in overall movement. Most notably, fish demonstrated reduced phase lag when tracking single-sine trajectories. These data support the hypothesis that fish generate an internal dynamical model of the stimulus motion, hence improving tracking of predictable trajectories (relative to unpredictable ones) despite similar or reduced motor cost. Similar predictive mechanisms based on the dynamics of stimulus movement have been proposed recently, but almost exclusively for nonlocomotor tasks by humans, such as oculomotor target tracking and posture control. These data suggest that such mechanisms might be common across taxa and behaviors.

Mutually opposing forces during locomotion can eliminate the tradeoff between maneuverability and stability

“…Note that we only examined forward swimming for experimental convenience, because the fish often tend to reorient themselves into the flow. However, the fish readily swim both forward and backward when tracking a refuge (8,9), and when they do swim backward, the nodal point shifts rostral to its zero position as expected (Movie S3).…”

“…This may seem surprising because these antagonistic forces do not contribute to the cycle-averaged movement of the center of mass of the animal. Such antagonistic forces are not only present during forward locomotion but in hovering for animals such as hummingbirds, hawkmoths, and electric fish; these animals produce large antagonistic forces and exhibit extraordinary maneuverability during station keeping (6)(7)(8)(9). In this study, we demonstrate that active generation and differential control of such antagonistic forces can eliminate the tradeoff between stability and maneuverability during locomotion.…”

“…We designed a linear quadratic tracking controller (33) to track a reference trajectory along the longitudinal axis. This is similar to the natural tracking behavior of electric knifefish (7)(8)(9). Control inputs to the robot were chosen to be either nodal point shift ðΔLÞ for the counterpropagating wave strategy of thrust modulation or frequency (f) for the unidirectional traveling wave strategy.…”

Active sensing via movement shapes spatiotemporal patterns of sensory feedback

“…For each experiment, an individual fish was transferred to a testing tank equipped with a computer-controlled moving refuge and a highspeed video camera [see fig.1 in Roth et al (Roth et al, 2011)]. Animals were allowed to acclimate to the test tank and refuge for 2-24h prior to any experimental trials.…”

“…The experimental setup was similar to that used in previous reports ( Fig.1B) (Cowan and Fortune, 2007;Roth et al, 2011). For these experiments, the refuge (or 'shuttle') was machined from a 15cm segment of 2ϫ2inch gray rectangular PVC tubing.…”