Optimizing information transmission in neural induction constrains cell surface contacts of ascidian embryos

TL;DR

This study explores how the geometry of ascidian embryos influences neural induction by optimizing FGF signal transmission through cell surface contacts, revealing that natural contact areas are near optimal for information transfer.

Contribution

It demonstrates that embryo geometry constrains cell surface contacts to optimize FGF signaling, linking physical structure to neural fate determination.

Findings

Optimal cell surface contact areas match experimental observations.

Geometry influences the efficiency of FGF signal transmission.

Cell surface exposure variability regulates neural differentiation.

Abstract

The onset of neural induction in the anterior ectoderm of ascidian embryos is regulated at the extracellular level by FGF signaling molecules, which control the acquisition of neural fate through the activation of the ERK pathway. Among the anterior ectoderm cells exposed to FGF, only a fraction will acquire neural fate. The selection of neural precursors depends on the quasi-invariant geometry of the embryo, which imposes upon each ectoderm cell a precise area of cell surface contact with underlying FGF-expressing (mesendoderm) cells. Here, we investigate information transmission between FGF and activated ERK and how this depends on the geometry of the system. Optimizing information transmission with the constraint that the total FGF-emitting surface area is restricted, as in the embryo, we find that the surface contacts with FGF that maximize information transmission are close to those observed experimentally. This information optimal solution is compatible with the anterior ectoderm cells having different areas of cell surface exposure to FGF, allowing the embryo to use cell surface areas as a regulatory mechanism for differentiating the outcome of cells that sense a constant FGF concentration.