A neuromechanical model forDrosophilalarval crawling based on physical measurements

Abstract

Animal locomotion requires dynamic interactions between neural circuits, muscles, and surrounding environments. In contrast to intensive studies on neural circuits, the neuromechanical basis for animal behaviour remains unclear due to the lack of information on the physical properties of animals. Here, taking Drosophila larvae as a model system, we proposed an integrated neuromechanical model based on physical measurements. The physical parameters were obtained by a stress-relaxation assay, and the neural circuit motif was extracted from a chain of excitatory and inhibitory interneurons, which was identified previously by connectomics. Based on the model, we systematically performed perturbation analyses on the parameters in the model to study their kinematic effects on locomotion performance. We found that modification of most of the parameters in the simulation could increase the speed of locomotion. Our physical measurement and modelling would provide a new framework for neural circuit studies and soft robot engineering.

Interspecies variation of larval locomotion kinematics in the genusDrosophilaand its relation to habitat temperature

“…Furthermore, kinematics of the larval locomotion have been measured and investigated quantitatively in detail (Gepner et al, 2015;Gershow et al, 2012;Gomez-Marin et al, 2011;Gomez-Marin & Louis, 2014;Heckscher et al, 2012;Hernandez-Nunez et al, 2015;Lahiri et al, 2011;Luo et al, 2010) and analysed by mathematical modelling (Gjorgjieva et al, 2013;Loveless et al, 2019;Loveless & Webb, 2018;Pehlevan et al, 2016;Sun et al, 2020).…”

“…Proprioceptive feedback and neuromodulation are both important for the normal crawling speed (Fox et al, 2006; Hughes & Thomas, 2007). Furthermore, kinematics of the larval locomotion have been measured and investigated quantitatively in detail (Gepner et al, 2015; Gershow et al, 2012; Gomez-Marin et al, 2011; Gomez-Marin & Louis, 2014; Heckscher et al, 2012; Hernandez-Nunez et al, 2015; Lahiri et al, 2011; Luo et al, 2010) and analysed by mathematical modelling (Gjorgjieva et al, 2013; Loveless et al, 2019; Loveless & Webb, 2018; Pehlevan et al, 2016; Sun et al, 2020). Regarding temperature sensing, neuronal and molecular mechanisms on temperature-guided behaviour have been clarified (Dillon et al, 2009; Klein et al, 2015; Kwon et al, 2008, 2010; Liu et al, 2003; Ni et al, 2016; Rosenzweig et al, 2005b, 2008; Shen et al, 2011).…”

A physical theory of movement in small animals

“…As well as extensive behavioural data, there is currently a concerted effort to map the neural connectome of the larva, and to link observed neural anatomy and dynamics to behaviour [16][17][18][19][20][21][22][23][24][25][26][27]. Moreover, recent modelling studies have already explored the importance of biomechanics in understanding the animal's crawling (in 1 spatial dimension) [28][29][30][31] and substrate exploration/taxis behaviours (in 2 spatial dimensions) [30,32,33], emphasising the crucial role that sensory feedback, which conveys some measurement of the physical state of the animal to its nervous system, plays during behaviour [28][29][30][31]33]. Cutting-edge research is beginning to experimentally probe the physics of the animal's body [31].…”

“…Moreover, recent modelling studies have already explored the importance of biomechanics in understanding the animal's crawling (in 1 spatial dimension) [28][29][30][31] and substrate exploration/taxis behaviours (in 2 spatial dimensions) [30,32,33], emphasising the crucial role that sensory feedback, which conveys some measurement of the physical state of the animal to its nervous system, plays during behaviour [28][29][30][31]33]. Cutting-edge research is beginning to experimentally probe the physics of the animal's body [31]. The larva thus offers a number of advantages as a model system for studying the physics of behaviour.…”

“…Correspondingly, Drosophila larvae are able to perform a wide repertoire of behaviours under experimental conditions [20], including: peristaltic crawling [21], rolling [22–24], self-righting [16, 25, 26], rearing [20], hunching [23], and digging [27–30]. Recent modelling studies have exploited this system to explore the importance of biomechanics in understanding the animal’s crawling (in one spatial dimension, 1D) [19, 31–33] and substrate exploration/taxis behaviours (in two spatial dimensions, 2D) [18, 19, 34]. Additionally, the larva provides a prototypical example of the bilaterally-symmetric, slender, soft, segmented body physics that are common to many animals, and that are increasingly being exploited in the design of robotic systems [4, 5].…”