Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization

PLoS Comput Biol. 2020 Jan 2;16(1):e1007602. doi: 10.1371/journal.pcbi.1007602. eCollection 2020 Jan.

Abstract

A central problem of neuroscience involves uncovering the principles governing the organization of nervous systems which ensure robustness in brain development. The nematode Caenorhabditis elegans provides us with a model organism for studying this question. In this paper, we focus on the invariant connection structure and spatial arrangement of the neurons comprising the somatic neuronal network of this organism to understand the key developmental constraints underlying its design. We observe that neurons with certain shared characteristics-such as, neural process lengths, birth time cohort, lineage and bilateral symmetry-exhibit a preference for connecting to each other. Recognizing the existence of such homophily and their relative degree of importance in determining connection probability within neurons (for example, in synapses, symmetric pairing is the most dominant factor followed by birth time cohort, process length and lineage) helps in connecting specific neuronal attributes to the topological organization of the network. Further, the functional identities of neurons appear to dictate the temporal hierarchy of their appearance during the course of development. Providing crucial insights into principles that may be common across many organisms, our study shows how the trajectory in the developmental landscape constrains the structural organization of a nervous system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / growth & development*
  • Caenorhabditis elegans / physiology*
  • Computational Biology
  • Models, Neurological*
  • Nervous System / growth & development*
  • Neurogenesis / physiology*
  • Neurons / physiology

Grants and funding

This work was partially supported by grant BT/PR14055/Med/30/350/2010 of Dept. of Biotechnology, Govt. of India [http://dbtindia.gov.in/] (NC and SS) and IMSc Complex Systems Project (XI Plan) funded by Dept. of Atomic Energy, Govt. of India [http://www.dae.nic.in/] (AP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.