Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Abstract

Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of stochastic growth and retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

Neuron tracing and quantitative analyses of dendritic architecture reveal symmetrical three-way-junctions and phenotypes of git-1 in C. elegans

“…Morphological features of dendritic arbors, such as length, diameter, and orientation have been related to neuronal functions [4][5][6][7][8][9], while deformations of the dendritic architecture have been associated with diseases and disorders [10][11][12][13]. Dendritic morphology varies significantly across species and across neuronal classes, which are often associated with distinct characteristic shapes [1][2][3][14][15][16].…”

Drosophila Dendritic Arborisation Neurons: Fantastic Actin Dynamics and Where to Find Them

“…The lateral dendrites of c1da neurons run along the direction of contraction and are sequentially deformed within the consecutive segments during crawling. This branch orientation is thought to maximize membrane curvature during larval crawling and thereby tightly couples c1da dendrite morphology to the neurons' proprioceptive function [12,37]. The four c2da neurons also exhibit a simple dendritic morphology, but with longer branches than c1da neurons.…”

“…At that stage, da neurons are already polarized and extend their long main dendrites. A recent study investigated the embryonic stages of c1da neuron dendrite differentiation and revealed that the lateral branchlets of c1da neurons underwent repeated cycles of extensive dendritic branch formation and retraction [12]. This process temporarily gave rise to a much higher total number of lateral dendrites, as compared to the final c1da dendritic tree of a third instar larva, and led to the outgrowth of higher-order branches, which in the case of c1da neurons, are never found in the fully developed dendritic tree.…”

“…The mechanisms governing the outgrowth of the primary dendrites, their branching, and the stabilization of newly developed branches, all need to work coherently to achieve a fully functional dendritic tree. In recent years, with the continued support of modeling approaches, growth programs underlying the patterns of dendritic arborization and organization have been identified [11][12][13][14]. These models suggest deterministic and stochastic steps in a segmented/iterative growth program.…”

“…These models suggest deterministic and stochastic steps in a segmented/iterative growth program. Very recent studies even propose similar generalized growth programs for different neuron types [11][12][13]15]. Implementation of these programs is mediated by transcription factors [16][17][18][19] and other modulating stimuli such as external interaction cues [20][21][22].…”