Signatures of proprioceptive control inCaenorhabditis eleganslocomotion

Abstract

Animal neuromechanics describes the coordinated self-propelled movement of a body, subject to the combined effects of internal neural control and mechanical forces. Here we use a computational model to identify effects of neural and mechanical modulation on undulatory forward locomotion of , with a focus on proprioceptively driven neural control. We reveal a fundamental relationship between body elasticity and environmental drag in determining the dynamics of the body and demonstrate the manifestation of this relationship in the context of proprioceptively driven control. By considering characteristics unique to proprioceptive neurons, we predict the signatures of internal gait modulation that contrast with the known signatures of externally or biomechanically modulated gait. We further show that proprioceptive feedback can suppress neuromechanical phase lags during undulatory locomotion, contrasting with well studied advancing phase lags that have long been a signature of centrally generated, feed-forward control.This article is part of a discussion meeting issue 'Connectome to behaviour: modelling at cellular resolution'.

Inhibition underlies fast undulatory locomotion inC. elegans

“…In C. elegans, proprioceptive control of forward locomotion is mediated by B-type excitatory motoneurons (Wen et al, 2012;Fouad et al, 2018). Based on the neural circuitry, anatomy and ablation results (Chalfie et al, 1985;White et al, 1985;Chen et al, 2006) and consistent with previous models of forward locomotion (Niebur and Erdös, 1991; Cohen and Boyle 2010; Bryden and Cohen 2008;Boyle et al, 2012) in our model, B-type motoneurons receive a descending locomotion command input and local inhibitory input; internally, they are driven by a spatially extended proprioceptive input (Denham et al, 2018). For an in depth discussion of this class of models, see relevant reviews (Cohen and Boyle, 2010;Cohen and Sanders, 2014;Cohen and Denham, 2019).…”

“…To probe different hypotheses about neural control and test their consequences in different fluid environments, we use an integrated neuromechanical model. Our model nematode consists of a smooth, continuous mechanical body, driven by neuromuscular activation, and subject to fluid drag forces (Denham et al, 2018). Our models aim to address the phenotypes of GABA transmission mutants during forward or backward locomotion, rather than directional changes or the shrinker phenotype.…”

“…Specifically we focus on our results showing suppressed undulation frequencies in GABA mutants and suggesting that this phenotype is caused by defects in the ventral nerve cord circuitry, rather than by defects in premotor interneurons. To this end, we adapted an existing model of forward locomotion control (Denham et al, 2018). In particular, we explored two different paradigms of neural control: a proprioceptively driven model and a feedforward model, mimicking CPG control (Denham et al, 2018).…”

“…To this end, we adapted an existing model of forward locomotion control (Denham et al, 2018). In particular, we explored two different paradigms of neural control: a proprioceptively driven model and a feedforward model, mimicking CPG control (Denham et al, 2018). We subjected each model to different perturbations and explored the behavior generated in our neuromechanical framework in virtual liquid and agar-like conditions.…”

“…Paradigm 1: CPG control. Following Denham et al (2018) and in the absence of detailed CPG mechanisms, we model the essential feature of feedforward control, namely the existence of endogenous, central pattern generation that produces neural oscillations at a characteristic frequency and is embedded in a biomechanical body. We therefore model the neural activation by a retrograde traveling sine wave of unit amplitude with period, ܶ , and wavelength, ߣ , that activates the muscles continuously along the body.…”