A Markovian dynamics for Caenorhabditis elegans behavior across scales

Author:

Costa Antonio C.1ORCID,Ahamed Tosif2ORCID,Jordan David3ORCID,Stephens Greg J.14ORCID

Affiliation:

1. Department of Physics and Astronomy, Vrije Universiteit Amsterdam, Amsterdam 1081HV, The Netherlands

2. Janelia Research Campus, HHMI, Ashburn, VA 20147

3. Department of Biochemistry, University of Cambridge, Cambridge CB2 1GA, United Kingdom

4. Biological Physics Theory Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa 904-0495, Japan

Abstract

How do we capture the breadth of behavior in animal movement, from rapid body twitches to aging? Using high-resolution videos of the nematode worm Caenorhabditis elegans , we show that a single dynamics connects posture-scale fluctuations with trajectory diffusion and longer-lived behavioral states. We take short posture sequences as an instantaneous behavioral measure, fixing the sequence length for maximal prediction. Within the space of posture sequences, we construct a fine-scale, maximum entropy partition so that transitions among microstates define a high-fidelity Markov model, which we also use as a means of principled coarse-graining. We translate these dynamics into movement using resistive force theory, capturing the statistical properties of foraging trajectories. Predictive across scales, we leverage the longest-lived eigenvectors of the inferred Markov chain to perform a top–down subdivision of the worm’s foraging behavior, revealing both “runs-and-pirouettes” as well as previously uncharacterized finer-scale behaviors. We use our model to investigate the relevance of these fine-scale behaviors for foraging success, recovering a trade-off between local and global search strategies.

Funder

Netherlands Organzation for Scientific Research

Netherlands Organization for Scientific Research

LabEx ENS-ICFP

Publisher

Proceedings of the National Academy of Sciences

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