Optic tectal superficial interneurons detect motion in larval zebrafish

Detection of moving objects is an essential skill for animals to hunt prey, recognize conspecifics and avoid predators. The zebrafish, as a vertebrate model, primarily uses its elaborate visual system to distinguish moving objects against background scenes. The optic tectum (OT) receives and integrates inputs from various types of retinal ganglion cells (RGCs), including direction-selective (DS) RGCs and size-selective RGCs, and is required for both prey capture and predator avoidance. However, it remains largely unknown how motion information is processed within the OT. Here we performed in vivo whole-cell recording and calcium imaging to investigate the role of superficial interneurons (SINs), a specific type of optic tectal neurons, in motion detection of larval zebrafish. SINs mainly receive excitatory synaptic inputs, exhibit transient ON- or OFF-type of responses evoked by light flashes, and possess a large receptive field (RF). One fifth of SINs are DS and classified into two subsets with separate preferred directions. Furthermore, SINs show size-dependent responses to moving dots. They are efficiently activated by moving objects but not static ones, capable of showing sustained responses to moving objects and having less visual adaptation than periventricular neurons (PVNs), the principal tectal cells. Behaviorally, ablation of SINs impairs prey capture, which requires local motion detection, but not global looming-evoked escape. Finally, starvation enhances the gain of SINs’ motion responses while maintaining their size tuning and DS. These results indicate that SINs serve as a motion detector for sensing and localizing sized moving objects in the visual field. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s13238-018-0587-7) contains supplementary material, which is available to authorized users.