Schoppik, D. | Search bioRxiv

bioRxiv2017

A novel mechanism for volitional locomotion in larval zebrafish

To 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.

neuroscience↗

bioRxiv2017

Gaze-stabilizing central vestibular neurons project asymmetrically to extraocular motoneuron pools

Within reflex circuits, specific anatomical projections allow central neurons to relay sensations to effectors that generate movements. A major challenge is to relate anatomical features of central neural populations -- such as asymmetric connectivity -- to the computations the populations perform. To address this problem, we mapped the anatomy, modeled the function, and discovered a new behavioral role for a genetically-defined population of central vestibular neurons in rhombomeres 5-7 of larval zebrafish. First, we found that neurons within this central population project preferentially to motoneurons that move the eyes downward. Concor-dantly, when the entire population of asymmetrically-projecting neurons was stimulated collectively, only downward eye rotations were observed, demonstrating a functional correlate of the anatomical bias. When these neurons are ablated, fish failed to rotate their eyes following either nose-up or nose-down body tilts. This asymmetrically-projecting central population thus participates in both up and downward gaze stabilization. In addition to projecting to motoneurons, central vestibular neurons also receive direct sensory input from peripheral afferents. To infer whether asymmetric projections can facilitate sensory encoding or motor output, we modeled differentially-projecting sets of central vestibular neurons. Whereas motor command strength was independent of projection allocation, asymmetric projections enabled more accurate representation of nose-up stimuli. The model shows how asymmetric connectivity could enhance the representation of imbalance during nose-up postures while preserving gaze-stabilization performance. Finally, we found that central vestibular neurons were necessary for a vital behavior requiring maintenance of a nose-up posture: swim bladder inflation. These observations suggest that asymmetric connectivity in the vestibular system facilitates representation of ethologically-relevant stimuli without compromising reflexive behavior.\n\nSignificance StatementInterneuron populations use specific anatomical projections to transform sensations into reflexive actions. Here we examined how the anatomical composition of a genetically-defined population of balance interneurons in the larval zebrafish relates to the computations it performs. First, we found that the population of interneurons that stabilize gaze preferentially project to motoneurons that move the eyes downward. Next, we discovered through modeling that such projection patterns can enhance the encoding of nose-up sensations without compromising gaze stabilization. Finally we found that loss of these interneurons impairs a vital behavior, swim bladder inflation, that relies on maintaining a nose-up posture. These observations suggest that anatomical specialization permits neural circuits to represent relevant features of the environment without compromising behavior.

neuroscience↗