Topography of a Visuomotor Transformation

Abstract

The brain converts perceptual information into appropriate patterns of muscle activity depending on the categorization and localization of sensory cues. Sensorimotor information might either be encoded by distributed networks or by ''labeled lines'' connecting sensory channels to dedicated behavioral pathways. Here we investigate, in the context of natural behavior, how the tectum of larval zebrafish can inform downstream premotor areas. Optogenetic mapping revealed a tectal motor map underlying locomotor maneuvers for escape and approach. Single-cell reconstructions and high-resolution functional imaging showed that two spatially segregated and uncrossed descending axon tracts selectively transmit approach and escape signals to the hindbrain. Moreover, the approach pathway conveys information about retinotopic target coordinates to specific premotor ensembles via spatially ordered axonal projections. This topographic organization supports a tectum-generated space code sufficient to steer orienting movements. We conclude that specific labeled lines guide objectdirected behavior in the larval zebrafish brain.

Neuron types in the zebrafish optic tectum labeled by an id2b transgene

“…Based on previous studies it is most likely that the SM dendrite receives input from TL (Folgueira et al, ), while the SFGS dendrite most likely receives direct input from RGC axons. This finding also indicates tectal neurons postsynaptic to PyrNs contain dendrites spanning SGC, which includes the majority of tectal neurons with projections to preoptic regions of diencephalon, pretectum, and tegmentum (Helmbrecht et al, ).…”

“…Notably, DLT is a visually responsive structure reciprocally connected with optic tectum in goldfish (Niida & Ohono, ). In the larval zebrafish, a pan‐tectal transgenic gal4 line has been used to generate single cell labeling of tectobulbar neurons that innervate the mesencephalic and rhombencephalic premotor areas (Helmbrecht et al, ). However, the population examined in this study was comprised of multiple subtypes, as evidenced by variable innervation patterns and differential sensitivity to disruption of eph–ephrin signaling.…”

“…Optic tectum has also been implicated in sensorimotor processing (Barker & Baier, 2015;Bianco & Engert, 2015). Tectal influence over motor commands in teleost fish is mediated by descending outputs to mesencephalic and rhombencephalic premotor areas via the tectobulbar tract (Helmbrecht, Dal Maschio, Donovan, Koutsouli, & Baier, 2018). Ipsilaterally, two main visual output areas have been identified: nucleus of the DLT and lateral reticular formation (FRL).…”

“…Notably, DLT is a visually responsive structure reciprocally connected with optic tectum in goldfish (Niida & Ohono, 1984). In the larval zebrafish, a pan-tectal transgenic gal4 line has been used to generate single cell labeling of tectobulbar neurons that innervate the mesencephalic and rhombencephalic premotor areas (Helmbrecht et al, 2018).…”

Behavioral signatures of a developing neural code

“…These neurons then migrate anteriorly in the tectum and become tuned to more frontal stimuli , consistent with our results. Projections from the tectum to premotor areas have some topographic organization (Helmbrecht et al, 2018), suggesting that a simple topography-based code could provide the substrate for visuo-motor transformations. However due to the highly dynamic nature of the tectal map (for instance we found frontal shifts in tuning of around 50 • at each tectal position between 4 and 15 dpf ( Figure 2H)), such a topography-based code would presumably also require matched plasticity in downstream structures.…”