Direction Selectivity and Receptive Fields of Zebrafish Tectal and Pretectal Neurons

Abstract

Optic flow processing by neurons in the diencephalic pretectum is essential for visually guided behaviours in vertebrates, such as the optokinetic and optomotor responses. Animals actively stabilize both their gaze and position relative to their surroundings when exposed to translational and rotational stimuli. Recently, pretectal neurons distinguishing these moving patterns have been identified in the zebrafish brain and they are thought to mediate downstream motor outputs. It is still unclear whether binocular stimulus motion in other planes besides the horizontal plane is also represented in the zebrafish brain. Furthermore, while receptive field sizes and centres of tectal neurons have been reported, those of zebrafish pretectal neurons remain mainly elusive. We elucidate these crucial features with in vivo calcium imaging. First, we find that both pretectal and tectal neurons are each tuned to one out of four (roughly equally spaced) preferred directions. No anatomical segregation of direction-selective tectal neurons was identified. Second, we identified neurons responding to specific translational or rotational whole-field patterns by presenting all possible binocular combinations of the four (monocularly) preferred stimulus directions to both eyes of the fish. These binocular selective neurons could – in principle – directly instruct appropriate compensatory eye and tail movements during optokinetic and optomotor behaviour, respectively. Furthermore, monocular receptive field mapping shows that the vast majority of tectal motion-sensitive neurons are tuned to small-size motion, many with reduced neural activities when the motion-covered region increases. The visual space of the small-size tectal receptive fields is over-represented in the nasal-dorsal visual field. In contrast, many pretectal neurons have large-sized receptive fields (> 60°x30°, in azimuth, and elevation) with centres of receptive fields in the ventral visual field. Finally, besides full-field motion, the larval zebrafish optomotor response was preferably evoked by binocular forward translational motion located in the ventral temporal visual field, which mainly overlaps with the receptive filed centres of the pretectal large-size receptive fields. Our study characterizes fundamental features of tectal and pretectal information processing and provides the basis for further investigations into visuomotor transformations in zebrafish.