A physical theory of movement in small animals

Abstract

All animal movement must ultimately be governed by physical laws. As a basis for understanding the interactions between the nervous system, musculature, body mechanics and the environment that govern behaviour in the fruit fly larva, we here develop an effective theory for the physics of its motion in three dimensions. We start by defining a set of fields which quantify stretching, bending and twisting along the larva's anteroposterior (AP) axis. We then perform a search in the space of possible physical theories that could govern these fields, by using symmetry considerations, stability requirements and physical reasoning to rule out possible terms in our theory's Lagrangian (which governs its energy-conservative physics) and Rayleigh function (which governs its energy-dissipative physics). We restrict attention to the physics that dominates at long-wavelengths, which allows us to arrive at a unique, simple theory of the larval midline, governed by a minimum of phenomenological parameters that capture both purely biomechanical as well as neuromuscular effects. Owing to the simplicity of our theory, we are able to derive most of our results analytically. The model makes strong quantitative predictions for the dynamics of peristalsis, rolling, and self-righting, and also successfully predicts statistical properties of these behaviours and of unbiased substrate exploration.

Linking neural circuits to the mechanics of animal behavior in Drosophila larval locomotion

“…For instance, a mechanical model incorporating damped translational and torsional springs has demonstrated that local sensory-motor reflexes and long-range mutual inhibition between reflexes in distant segments are sufficient to generate crawling behavior ( Loveless et al, 2019 ). Additionally, an effective field theory with a quadratic Hamiltonian has been successful in describing larval movements, including crawling ( Loveless et al, 2021 ). These alternative theoretical approaches offer novel perspectives on larval locomotion and have the potential to uncover fundamental principles underlying it.…”

Optical mapping of ground reaction force dynamics in freely behaving Drosophila melanogaster larvae

“…The developmental and genetic origins of these structures have been extensively studied, but relatively little is known about how they are articulated during movement. While computational modelling and biomechanical measurements have provided an initial knowledgebase ( Loveless et al, 2019 ; Loveless et al, 2021 ; Gjorgjieva et al, 2013 ), data on biomechanical forces generated during substrate interactions in Drosophila larvae remain extremely limited ( Khare et al, 2015 ; Sun et al, 2022 ). Development of methods for measuring GRFs in this model organism would enable fully integrated neurogenetic-biomechanical approaches to understanding soft-bodied movement and fulfil calls from the modelling community for more biomechanics data ( Tytell et al, 2011 ).…”

Optical mapping of ground reaction force dynamics in freely behavingDrosophila melanogasterlarvae

“…The developmental and genetic origins of these structures have been extensively studied, but relatively little is known about how they are articulated during movement. While computational modelling and biomechanical measurements have provided an initial knowledgebase (34)(35)(36), data on biomechanical forces generated during substrate interactions in Drosophila larvae remain extremely limited (37,38). Development of methods for measuring GRFs in this model organism would enable fully integrated neurogenetic-biomechanical approaches to understanding soft-bodied movement and fulfil calls from the modelling community for more biomechanics data (39).…”