Control of Turning Behaviors by Spinal Projection Neurons in the Larval Zebrafish

Abstract

This thesis aims to examine how hindbrain spinal projection neurons (SPNs), namely RoV3, MiV1 and MiV2 control tail undulations during turning behaviors. I find that phototaxic turns differ from forward swims by an increased tail bend and a prolonged cycle period during the first undulation, while the later undulations are largely identical. Interestingly, laser ablation of RoV3, MiV1 and MiV2 neurons specifically affects the first undulation cycle by reducing the tail bend and the cycle period. Thus fish without the SPNs mainly perform forward swims in response to the turn-inducing phototaxic cues. These results suggest that the descending motor command that generates turns in larval zebrafish are composed of two pathways: one generates symmetric tail undulations, and the other, mediated by RoV3, MiV1 and MiV2 neurons, provides a brief and biased effect that modulates the first cycle of tail movement. Furthermore, fish whose unilateral SPNs are ablated are unable to perform turns toward the ablated side during the phototaxis, the optomotor response, the dark-flash response, and spontaneous swims, indicating the universal role of the SPNs in controlling visually-induced and spontaneous turns. Simultaneous two-photon calcium imaging and motor nerve recording in paralyzed fish show that RoV3, MiV2 and most MiV1 neurons on the turning side are active during turns, and that these activities are linearly correlated to the vigor of the intended turns. However, some MiV1 neurons are broadly tuned for all swimming directions. Computer simulations suggest that unilateral descending innervations to a specific type of spinal interneurons, namely commissural inhibitory interneurons, can generate a two-fold increase in the spinal network’s cycle period. This suggests that the SPNs could potentially innervate two types of spinal interneurons, namely \(CoBL_{gly}\) and CoLo, in order to control the rhythm during turns. An additional chapter of this thesis examines the ontogeny of operant and classical learning behaviors in zebrafish. Using strategically positioned visual cues paired with electroshocks, I find that both learning behaviors are expressed reliably around week 3, and reach adult performance levels at week 6. These memories are behaviorally expressed in adults for 6 hours and retrievable for 12 hours.