Mechanics of exploration inDrosophila melanogaster

Abstract

The Drosophila larva executes a stereotypical exploratory routine that appears to consist of stochastic alternation between straight peristaltic crawling and reorientation events through lateral bending. We present a model of larval mechanics for axial and transverse motion over a planar substrate, and use it to develop a simple, reflexive neuromuscular model from physical principles. In the absence of damping and driving, the mechanics of the body produces axial travelling waves, lateral oscillations, and unpredictable, chaotic deformations. The neuromuscular system counteracts friction to recover these motion patterns, giving rise to forward and backward peristalsis in addition to turning. The model produces spontaneous exploration, even though the model nervous system has no intrinsic pattern generating or decision making ability, and neither senses nor drives bending motions. Ultimately, our model suggests a novel view of larval exploration as a deterministic superdiffusion process which is mechanistically grounded in the chaotic mechanics of the body. 7 Drosophila larva executes a stereotypical exploratory routine [1] which appears to 8 consist of a series of straight runs punctuated by reorientation events [2]. Straight runs 9 are produced by laterally symmetric peristaltic compression waves, which propagate 10 along the larval body in the same direction as overall motion (i.e. posterior-anterior 11 waves carry the larva forwards relative to the substrate, anterior-posterior waves carry 12 the larva backwards) [3]. Reorientation is brought about by laterally asymmetric 13 compression and expansion of the most anterior body segments of the larva, which 14 causes the body axis of the larva to bend [2].15Peristaltic crawling and reorientation are commonly thought to constitute discrete 16 behavioural states, driven by distinct motor programs [2]. In exploration, it is assumed, 17 alternation between these states occurs stochastically, allowing the larva to search its 18 environment through an unbiased random walk [1,[4][5][6]. The state transitions or 19 direction and magnitude of turns can be biased by sensory input to produce taxis 20 PLOS 1/27 behaviours [4, 5, 7-13]. The neural circuits involved in producing the larval exploratory 21 routine potentially lie within the ventral nerve cord (VNC), since silencing the synaptic 22 communication within the brain and subesophageal ganglia (SOG) does not prevent 23 substrate exploration [1]. Electrophysiological and optogenetic observations of fictive 24 locomotion patterns within the isolated VNC [14, 15] support the prevailing hypothesis 25 that the exploratory routine is primarily a result of a centrally generated motor pattern. 26 As such, much recent work has focused on identifying and characterising the cells and 27 circuits within the larval VNC [16-32]. However, behaviour rarely arises entirely from 28 central mechanisms; sensory feedback and biomechanics often play a key role [33, 34] 29including the potential introduction of stochasticity. Indeed, thermog...

ADrosophilalarval premotor/motor neuron connectome generating two behaviors via distinct spatio-temporal muscle activity

“…Here we focus on forward and backward locomotion. Forward crawling behavior in larvae involves a peristaltic contraction wave from posterior to anterior segments; backward crawling entails a posterior propagation of the contraction wave (Crisp et al 2008; Dixit et al 2008; Berni et al 2012; Gjorgjieva et al 2013; Heckscher et al 2015; Pulver et al 2015; Loveless et al 2018).…”