Regulated neurite tension as a mechanism for determination of neuronal arbor geometries in vivo

Abstract

Transection and displacement experiments on isolated neurons in culture have shown that their neurites are under tension [1,2]. Such tensile forces might be important in determining the structures of neuronal arbors in vivo[1]. It has also been proposed that tension mechanisms generate the global folding patterns of the brain [3]. It has been difficult to determine whether tension is important in vivo, however, because most neuronal arbors have complex three-dimensional structures that cannot be perturbed in a controlled manner. Here we describe a situation in which tension can be demonstrated and perturbed in an intact central nervous system (CNS). In the embryonic CNS neuropil of the grasshopper Schistocerca americana, the axon of a local serotonergic interneuron known as s1 [4] forms a characteristic bifurcation. The geometry of this bifurcation node is highly conserved between embryos and held constant during development. Current models for the development of such geometries usually propose that they are created and maintained by neurite adhesion to localized substrates. Here we show that the structure of the s1 bifurcation node is likely to be determined by balanced tension between three fixed points. This was revealed by selectively transecting each of the branches that intersect at the node. Transections are followed by a rapid restructuring (‘snapping’) of the node geometry.