Three‐dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern

Abstract

We are interested in the generation of endogenous electric fields associated with ionic currents driven through the vertebrate embryo by the transepithelial potential of its surface ectoderm. Using a non‐invasive vibrating electrode for the measurement of ionic current, we have provided measurements of currents traversing amphibian embryos, and a preliminary report of the internal, extracellular voltage gradient under the neural plate which polarizes the embryo in the rostral/caudal axis (Metcalf et al. [1994] J. Exp. Zool. 268:307–322). Here we complete a description of this gradient in electrical potential (ca. 10 mV/mm, caudally negative), describe a simultaneous gradient organized in the medial/lateral axis (ca. 5–18 mV/mm, negative at the margins of the neural folds), and describe their appearance and disappearance during ontogeny of the axolotl embryo. Both voltage gradients are not expressed until neurulation, and disappear at its climax. This appearance and disappearance correlates with the shunting of current out of the lateral margins of the neural folds in rostral regions of the embryo beginning at stage 15, and is not associated with a more substantial current leak from the blastopore which appears at gastrulation. A steady blastopore current is still present after neural tube formation when intra‐embryonic electric fields have been extinguished. We discuss the direct experimental tests supporting the hypothesis that these extracellular electric fields both polarize the early vertebrate embryo and serve as cues for morphogenesis and pattern. © 1995 Wiley‐Liss, Inc.