How do neural systems process sensory information to control locomotion? The weakly electric knifefish Eigenmannia, an ideal model for studying sensorimotor control, swims to stabilize the sensory image of a sinusoidally moving refuge. Tracking performance is best at stimulus frequencies less than approximately 1 Hz. Kinematic analysis, which is widely used in the study of neural control of movement, predicts commensurately low-pass sensory processing for control. The inclusion of Newtonian mechanics in the analysis of the behavior, however, categorically shifts the prediction: this analysis predicts that sensory processing is high pass. The counterintuitive prediction that a low-pass behavior is controlled by a high-pass neural filter nevertheless matches previously reported but poorly understood high-pass filtering seen in electrosensory afferents and downstream neurons. Furthermore, a model incorporating the high-pass controller matches animal behavior, whereas the model with the low-pass controller does not and is unstable. Because locomotor mechanics are similar in a wide array of animals, these data suggest that such high-pass sensory filters may be a general mechanism used for task-level locomotion control. Furthermore, these data highlight the critical role of mechanical analyses in addition to widely used kinematic analyses in the study of neural control systems.
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