Changes in postural syntax characterize sensory modulation and natural variation of C. elegans locomotion

Abstract

Locomotion is driven by shape changes coordinated by the nervous system through time; thus, enumerating an animals complete repertoire of shape transitions would provide a basis for a comprehensive understanding of locomotor behaviour. Here we introduce a discrete representation of behaviour in the nematode C. elegans. At each point in time, the worms posture is approximated by its closest matching template from a set of 90 postures and locomotion is represented as sequences of postures. The frequency distribution of postural sequences is heavy-tailed with a core of frequent behaviours and a much larger set of rarely used behaviours. Responses to optogenetic and environmental stimuli can be quantified as changes in postural syntax: worms show different preferences for different sequences of postures drawn from the same set of templates. A discrete representation of behaviour will enable the use of methods developed for other kinds of discrete data in bioinformatics and language processing to be harnessed for the study of behaviour.\n\nAuthor SummaryTechnology for recording neural activity is advancing rapidly and whole-brain imaging with single neuron resolution has already been demonstrated for smaller animals. To interpret such complex neural recordings, we need comprehensive characterizations of behaviour, which is the principal output of the brain. Animal tracking can increasingly be performed automatically but an outstanding challenge is finding ways to represent these behavioural data. We have focused on the movement of the nematode worm C. elegans to develop a quantitative representation of behaviour as a series of distinct postures. Each posture is analogous to a word in a language and so we can directly count the number of phrases that makes up the C. elegans behavioural repertoire. C. elegans has a very small nervous system but we find that its behavioural repertoire is still complex. As with human languages, there is a large number of possible phrases, but most are rarely used. When comparing different populations of worms or worms in different environments, we find that the difference between their behaviour is due to a subset of their entire repertoire. In the language analogy, these would correspond to idiomatic phrases that distinguish groups of speakers. A quantitative understanding of the nature of behavioural variation will inform research on the function and evolution of neural circuits.