Title: Direction selectivity in the larval zebrafish optic tectum
Description: Larval zebrafish develop the ability to track moving prey within only five days of development, a behavior that relies on processing within the optic tectum. Since information about the direction of object motion is important for precise tracking, the encoding of direction by the tectum may be critical for this behavior. However, very little is known about the developmental and circuit mechanisms that mediate this computation. While the larval zebrafish tectum receives a single topographic projection from the contralateral retina, binocular animals have two topographically registered retinal projections and neurons that show matching direction selectivity for each eye. This functional alignment suggests that topographic inputs may be used to compute direction selectivity. To test this, we induced a de novo binocular retinal projection to the larval zebrafish optic tectum and examined the responses of populations of recipient neurons to moving stimuli using in vivo two-photon calcium imaging. Neurons in rewired fish were predominantly binocular with registered topographic mapping for each eye. They also showed matching direction selectivity for each eye, a computation that was dependent upon tectal inhibitory transmission. These data support a feed-back model whereby local tectal circuits compute direction selectivity using topographic information from the retina.

To further understand the local circuit mechanisms underlying tectal direction selective computation, we studied the contribution of recurrent excitation in the tectum. Using in vivo whole-cell recordings, we found that long latency excitatory inputs from recurrent connections contribute considerably to tectal receptive fields. Asymmetries in the magnitude of these recurrent inputs correlated with each direction selectivity. We found that differences between response magnitudes are amplified by nonlinear spike thresholding to produce direction selective firing and that asymmetric recurrent excitation can sculpt the temporal profile of moving stimuli. Global inhibition may further act to sharpen tuning. These findings suggest that tectal direction selectivity in the larval zebrafish relies predominantly on the processing of topographic inputs using feed-back rather than feed-forward mechanisms. This modularity and developmental plasticity may have been exploited to allow flexibility during brain evolution.