Abstract

Complex dendritic trees are a distinctive feature of neurons. Alterations to dendritic morphology are associated with developmental, behavioral and neurodegenerative changes. The highly-arborized PVD neuron of C. elegans serves as a model to study dendritic patterning; however, quantitative, objective and automated analyses of PVD morphology are missing. Here, we present a method for neuronal feature extraction, based on deep-learning and fitting algorithms. The extracted neuronal architecture is represented by a database of structural elements for abstracted analysis. We obtain excellent automatic tracing of PVD trees and uncover that dendritic junctions are unevenly distributed. Surprisingly, these junctions are three-way-symmetrical on average, while dendritic processes are arranged orthogonally. We quantify the effect of mutation in git-1, a regulator of dendritic spine formation, on PVD morphology and discover a localized reduction in junctions. Our findings shed new light on PVD architecture, demonstrating the effectiveness of our objective analyses of dendritic morphology and suggest molecular control mechanisms.

Highlights

  • The link between the information processing function of neurons and the intricate shapes of their dendritic processes has been the subject of over a century of extensive study [1,2,3]

  • We present an algorithmic approach for detection and classification of the treelike dendrites of the PVD neuron in C. elegans worms

  • We have found that the junctions connecting branched dendrites have a three-way-symmetry, the dendrites are arranged in a crosshatch pattern, and that the distribution of junctions varies across distinct sub-classes of the PVD’s dendritic tree

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Summary

Introduction

The link between the information processing function of neurons and the intricate shapes of their dendritic processes has been the subject of over a century of extensive study [1,2,3]. The C. elegans bilateral PVD neuron has become a powerful model to study dendritic patterning, owing greatly to its stereotypical, highly ordered structure in the fourth larval stage and young adult (Fig 1A) [17]. By late L4 (typically within ~30 hours at 20 ̊C), their complex dendritic arbor of repeating candelabra-shaped units extends almost the entire surface area of the worm [17,18]. This highly organized structure is made of tubular processes with diameters ranging between 35–60 nm [17,18,20]. The relatively complex and high-order arborization of the PVD makes it an excellent model for studying the connection between structure and function in the nervous system [9,17,18,26,27,28]

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