Direction selectivity in the visual system of the zebrafish larva

Abstract

Neural circuits in the vertebrate retina extract the direction of object motion from visual scenes and convey this information to sensory brain areas, including the optic tectum. It is unclear how computational layers beyond the retina process directional inputs. Recent developmental and functional studies in the zebrafish larva, using minimally invasive optical imaging techniques, indicate that direction selectivity might be a genetically hardwired property of the zebrafish brain. Axons from specific direction-selective (DS) retinal ganglion cells appear to converge on distinct laminae in the superficial tectal neuropil where they serve as inputs to DS postsynaptic neurons of matching specificity. In addition, inhibitory recurrent circuits in the tectum might strengthen the DS response of tectal output neurons. Here we review these recent findings and discuss some controversies with a particular focus on the zebrafish tectum's role in extracting directional features from moving visual scenes.

Keywords: direction selectivity; neural circuits; optic tectum; visual system; zebrafish.

FIGURE 1

Mechanisms for direction selectivity computation in the zebrafish larva tectum. (A) Direction information from a moving stimulus is extracted by retinal circuits and transferred by RGC axons, which are specific for the stimulus direction (small red or blue arrows), to distinct laminae in the tectal neuropil. The retinal arbors are then targeted by the distal arbors of PVNs in their respective laminae thus acquiring direction specificity themselves. Heterotypic connections between proximal PVN arbors might lead to reciprocal inhibition thus sharpening DS PVN response to a moving stimulus in a specific direction (large red or blue arrows). (B) A DS PVN (blue) receives excitatory inputs from one or more non-DS RGCs in the tectal neuropil. In addition, it receives intratectal inhibitory input from an interneuron (red) that is retinotopically positioned on the side of the DS PVN facing the preferred stimulus direction. Thus, a moving stimulus in the preferred direction (black pointed arrow) elicits excitatory currents in the retina that excite DS PVNs. Currents from the inhibitory interneurons arrive later and do not interfere with the PVNs activity state. Moving stimuli in the null-direction, however, elicit inhibitory currents in the tectal interneuron, which arrive first at the DS PVN thus blocking any subsequent excitatory currents the DS PVN might receive from the retina. DS, direction-selective; RGC, retinal ganglion cell; PVN, periventricular neuron; SAC, stratum album centrale; SFGS (B-F), sublaminae of stratum fibrosum et griseum superficiale; SGC, stratum griseum centrale; SO, stratum opticum; SPV, stratum periventriculare.