A novel mechanism for volitional locomotion in larval zebrafish

Abstract

AbstractTo locomote stably, animals must coordinate volitional actions that change posture with opposing reflexes that hold posture constant [1–8]. These conflicting actions are thought to necessitate integrated control, in which reflexes are modulated to permit or even produce volitional movements [9–14]. Here we report that larval zebrafish (Danio rerio) utilize a simpler control scheme featuring independent volitional and reflexive movements. We present behavioral evidence that larvae swim in depth by appending destabilizing trunk rotations to steer with independent rotations to balance. When we manipulated buoyancy to deflect fish up or down, they redirected steering without coordinated changes to their balance reflex. As balance developed and increasingly opposed destabilization-mediated steering, larvae acquired compensatory use of their pectoral fins to steer. Removing the pectoral fins from older larvae impaired steering but preserved the strong balance reflex. Consequentially, older larvae without fins were strikingly less maneuverable — unable to revert to destabilization-mediated steering — revealing a rigidity inherent within the framework of independent volitional and reflexive control. Larval zebrafish therefore produce effective but inflexible locomotion by sequencing independent volitional and reflexive movements. These results reveal a simple control scheme, applicable for robotic design, that solves the general problem of coordinating volitional movements with the vital reflexes that oppose them.