Abstract

Author SummaryThe vertebrate brain contains a point-to-point representation of sensory input from the eye. This visual map forms during embryonic development, by neuronal cells of the retina sending targeted axon projections to the brain. Since the projection needs to wire up neighboring cell positions in the retina to neighboring target areas in the brain, all retinal cells must harbor a defined spatial coordinate as prerequisite for map formation. How such a retinal coordinate system is established and maintained in the dynamically evolving embryo is a fundamental, but unresolved, question. By combining genetic analysis and in vivo imaging in zebrafish embryos, we have tracked the developmental origin of cell coordinates in the retina. We find that three related Fgf signals emanating from outside the eye define relative cell positions in the retina very early, already at the onset of its formation. But the absolute position of retinal cells relative to the body axes is greatly rearranged during subsequent development. In this phase, surprisingly, the same Fgf signals that at first defined retinal cell positions now balance asymmetric cell movements and cell shape changes, which are required for harmonic retinal growth and the final alignment of cell coordinates in the eye.

Highlights

  • Map-like representation of sensory information is an evolutionary conserved principle of brain organization and function [1]

  • By in vivo imaging GFP-tagged retinal progenitor cells, we find that subsequent eye morphogenesis requires gradual tissue compaction in the nasal half and directed cell movements into the temporal half of the retina

  • Retinotopic mapping occurs as a function of retinal ganglion cell (RGC) position along molecular gradients within a coordinate system set by the major retinal axes

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Summary

Introduction

Map-like representation of sensory information is an evolutionary conserved principle of brain organization and function [1]. Guidance molecule expression along the nasaltemporal retina axis is regulated by the nasal- and temporalspecific transcription factors Foxg, Foxd, SOHo, and GH6 [9,10,11,12]. Retinotopic mapping occurs as a function of RGC position along molecular gradients within a coordinate system set by the major retinal axes. This suggests that axis formation and mapping are intimately connected developmental processes, but the nature and timing of the signals that establish cell positional identities in this coordinate system are largely unknown

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