Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans

PLoS Comput Biol. 2021 Sep 10;17(9):e1009329. doi: 10.1371/journal.pcbi.1009329. eCollection 2021 Sep.

Abstract

Behavioral phenotyping of model organisms has played an important role in unravelling the complexities of animal behavior. Techniques for classifying behavior often rely on easily identified changes in posture and motion. However, such approaches are likely to miss complex behaviors that cannot be readily distinguished by eye (e.g., behaviors produced by high dimensional dynamics). To explore this issue, we focus on the model organism Caenorhabditis elegans, where behaviors have been extensively recorded and classified. Using a dynamical systems lens, we identify high dimensional, nonlinear causal relationships between four basic shapes that describe worm motion (eigenmodes, also called "eigenworms"). We find relationships between all pairs of eigenmodes, but the timescales of the interactions vary between pairs and across individuals. Using these varying timescales, we create "interaction profiles" to represent an individual's behavioral dynamics. As desired, these profiles are able to distinguish well-known behavioral states: i.e., the profiles for foraging individuals are distinct from those of individuals exhibiting an escape response. More importantly, we find that interaction profiles can distinguish high dimensional behaviors among divergent mutant strains that were previously classified as phenotypically similar. Specifically, we find it is able to detect phenotypic behavioral differences not previously identified in strains related to dysfunction of hermaphrodite-specific neurons.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Behavior, Animal / physiology
  • Caenorhabditis elegans / physiology*
  • Models, Biological*

Grants and funding

GS was supported by the DoD-Strategic Environmental Research and Development Program 15 RC-2509 (https://www.serdp-estcp.org/), NSF DEB-1655203, NSF ABI-1667584 (https://www.nsf.gov) and DOI USDI-NPS P20AC00527 (https://www.doi.gov/) and The McQuown Fund University of California, San Diego and The McQuown Chair in Natural Sciences, University of California, San Diego. SR was supported by NSF-IOS 1936674 (https://www.nsf.gov); TL was supported by The Scripps Institution of Oceanography Postdoctoral Fellowship. In all cases, the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.