scholarly journals A consistent muscle activation strategy underlies crawling and swimming in Caenorhabditis elegans

2015 ◽  
Vol 12 (102) ◽  
pp. 20140963 ◽  
Author(s):  
Victoria J. Butler ◽  
Robyn Branicky ◽  
Eviatar Yemini ◽  
Jana F. Liewald ◽  
Alexander Gottschalk ◽  
...  

Although undulatory swimming is observed in many organisms, the neuromuscular basis for undulatory movement patterns is not well understood. To better understand the basis for the generation of these movement patterns, we studied muscle activity in the nematode Caenorhabditis elegans. Caenorhabditis elegans exhibits a range of locomotion patterns: in low viscosity fluids the undulation has a wavelength longer than the body and propagates rapidly, while in high viscosity fluids or on agar media the undulatory waves are shorter and slower. Theoretical treatment of observed behaviour has suggested a large change in force–posture relationships at different viscosities, but analysis of bend propagation suggests that short-range proprioceptive feedback is used to control and generate body bends. How muscles could be activated in a way consistent with both these results is unclear. We therefore combined automated worm tracking with calcium imaging to determine muscle activation strategy in a variety of external substrates. Remarkably, we observed that across locomotion patterns spanning a threefold change in wavelength, peak muscle activation occurs approximately 45° (1/8th of a cycle) ahead of peak midline curvature. Although the location of peak force is predicted to vary widely, the activation pattern is consistent with required force in a model incorporating putative length- and velocity-dependence of muscle strength. Furthermore, a linear combination of local curvature and velocity can match the pattern of activation. This suggests that proprioception can enable the worm to swim effectively while working within the limitations of muscle biomechanics and neural control.

1994 ◽  
Vol 192 (1) ◽  
pp. 129-145 ◽  
Author(s):  
J Long ◽  
M Mchenry ◽  
N Boetticher

We have developed an experimental procedure in which the in situ locomotor muscles of dead fishes can be electrically stimulated to generate swimming motions. This procedure gives the experimenter control of muscle activation and the mechanical properties of the body. Using pumpkinseed sunfish, Lepomis gibbosus, we investigated the mechanics of undulatory swimming by comparing the swimming kinematics of live sunfish with the kinematics of dead sunfish made to swim using electrical stimulation. In electrically stimulated sunfish, undulatory waves can be produced by alternating left­right contractions of either all the axial muscle or just the precaudal axial muscle. As judged by changes in swimming speed, most of the locomotor power is generated precaudally and transmitted to the caudal fin by way of the skin and axial skeleton. The form of the traveling undulatory wave ­ as measured by tail-beat amplitude, propulsive wavelength and maximal caudal curvature ­ can be modulated by experimental control of the body's passive stiffness, which is a property of the skin, connective tissue and axial skeleton.


1999 ◽  
Vol 202 (23) ◽  
pp. 3431-3438 ◽  
Author(s):  
T.J. Pedley ◽  
S.J. Hill

The load against which the swimming muscles contract, during the undulatory swimming of a fish, is composed principally of hydrodynamic pressure forces and body inertia. In the past this has been analysed, through an equation for bending moments, for small-amplitude swimming, using Lighthill's elongated-body theory and a ‘vortex-ring panel method’, respectively, to compute the hydrodynamic forces. Those models are outlined in this review, and a summary is given of recent work on large-amplitude swimming that has (a) extended the bending moment equation to large amplitude, which involves the introduction of a new (though probably usually small) term, and (b) developed a large-amplitude vortex-ring panel method. The latter requires computation of the wake, which rolls up into concentrated vortex rings and filaments, and has a significant effect on the pressure on the body. Application is principally made to the saithe (Pollachius virens). The calculations confirm that the wave of muscle activation travels down the fish much more rapidly than the wave of bending.


2018 ◽  
Vol 373 (1758) ◽  
pp. 20170376 ◽  
Author(s):  
Andrey Palyanov ◽  
Sergey Khayrulin ◽  
Stephen D. Larson

To better understand how a nervous system controls the movements of an organism, we have created a three-dimensional computational biomechanical model of the Caenorhabditis elegans body based on real anatomical structure. The body model is created with a particle system–based simulation engine known as Sibernetic, which implements the smoothed particle–hydrodynamics algorithm. The model includes an elastic body-wall cuticle subject to hydrostatic pressure. This cuticle is then driven by body-wall muscle cells that contract and relax, whose positions and shape are mapped from C. elegans anatomy, and determined from light microscopy and electron micrograph data. We show that by using different muscle activation patterns, this model is capable of producing C. elegans -like behaviours, including crawling and swimming locomotion in environments with different viscosities, while fitting multiple additional known biomechanical properties of the animal.  This article is part of a discussion meeting issue ‘Connectome to behaviour: modelling C. elegans at cellular resolution’.


2016 ◽  
Author(s):  
Mohamed Abdelhack

AbstractAdaptation in the sensory-mechanical loop during locomotion is a powerful mechanism that allows organisms to survive in different conditions and environments. Motile animals need to alter motion patterns in different environments. For example, crocodiles and other animals can walk on solid ground but switch to swimming in water beds. The nematode Caenorhabditis elegans also shows adaptability by employing thrashing behaviour in low viscosity media and crawling in high viscosity media. The mechanism that enables this adaptability is an active area of research. It has been attributed previously to neuro-modulation by dopamine and serotonin.The aim of this study is to physiologically investigate the neuronal mechanisms of modulation of locomotion by dopamine. The results suggest that the mechanosensory properties of the dopaminergic neurons PDE are not limited to touch sensation, but to surrounding environment resistance as well. The significance of such characterization is improving our understanding of dopamine gait switching which gets impaired in Parkinson’s disease.


2012 ◽  
Vol 107 (12) ◽  
pp. 3385-3396 ◽  
Author(s):  
Karen Jansen ◽  
Friedl De Groote ◽  
Firas Massaad ◽  
Pieter Meyns ◽  
Jacques Duysens ◽  
...  

Leg kinematics during backward walking (BW) are very similar to the time-reversed kinematics during forward walking (FW). This suggests that the underlying muscle activation pattern could originate from a simple time reversal, as well. Experimental electromyography studies have confirmed that this is the case for some muscles. Furthermore, it has been hypothesized that muscles showing a time reversal should also exhibit a reversal in function [from accelerating the body center of mass (COM) to decelerating]. However, this has not yet been verified in simulation studies. In the present study, forward simulations were used to study the effects of muscles on the acceleration of COM in FW and BW. We found that a reversal in function was indeed present in the muscle control of the horizontal movement of COM (e.g., tibialis anterior and gastrocnemius). In contrast, muscles' antigravity contributions maintained their function for both directions of movement. An important outcome of the present study is therefore that similar muscles can be used to achieve opposite functional demands at the level of control of the COM when walking direction is reversed. However, some muscles showed direction-specific contributions (i.e., dorsiflexors). We concluded that the changes in muscle contributions imply that a simple time reversal would be insufficient to produce BW from FW. We therefore propose that BW utilizes extra elements, presumably supraspinal, in addition to a common spinal drive. These additions are needed for propulsion and require a partial reconfiguration of lower level common networks.


Author(s):  
Jason J. Kutch ◽  
Francisco J. Valero-Cuevas

One of the main goals of neuromuscular modeling is to establish the range of feasible muscle activations for a given mechanical output of the body. This is not a trivial problem because there are typically infinitely many combinations of muscle activations that will generate the same joint torques, as most joints are actuated by more muscles than rotational degrees of freedom. Here we show that well-established geometric methods easily provide a complete description of the set of muscle activations that generate a desired set of joint torques or endpoint forces. In contrast to iterative linear programming optimizations, geometric methods provide a set of solutions in muscle activation space simply by converting between the geometric representations of neural and mechanical constraints. As an example, we use geometric methods to find the feasible set of activations that produce fingertip forces in a set of directions. These results show that for a given set of fingertip forces, the range of feasible activation for each muscle can differ with the choice of mechanical constraints. Thus, the mechanical constraints of the task play an important role governing the options the nervous system has when controlling redundant muscles.


1999 ◽  
Vol 202 (23) ◽  
pp. 3397-3403 ◽  
Author(s):  
J.D. Altringham ◽  
D.J. Ellerby

Undulatory swimming in fish is powered by the segmental body musculature of the myotomes. Power generated by this muscle and the interactions between the fish and the water generate a backward-travelling wave of lateral displacement of the body and caudal fin. The body and tail push against the water, generating forward thrust. The muscle activation and strain patterns that underlie body bending and thrust generation have been described for a number of species and show considerable variation. This suggests that muscle function may also vary among species. This variation must be due in large part to the complex interactions between muscle mechanical properties, fish body form, swimming mode, swimming speed and phylogenetic relationships. Recent work in several laboratories has been directed at studying patterns of muscle power output in vitro under simulated swimming conditions. This work suggests that the way that fish generate muscle power and convert it into thrust through the body and caudal fin does indeed vary. However, despite the differences, several features appear to be common to virtually all species studied and suggest where future effort should be directed if muscle function in swimming fish is to be better understood.


2018 ◽  
Vol 373 (1758) ◽  
pp. 20180208 ◽  
Author(s):  
Jack E. Denham ◽  
Thomas Ranner ◽  
Netta Cohen

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 Caenorhabditis elegans , 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 C. elegans at cellular resolution’.


BIO-PROTOCOL ◽  
2012 ◽  
Vol 2 (17) ◽  
Author(s):  
Mikiro Nawa ◽  
Masaaki Matsuoka

Genetics ◽  
1994 ◽  
Vol 137 (2) ◽  
pp. 483-498
Author(s):  
J Ahnn ◽  
A Fire

Abstract We have used available chromosomal deficiencies to screen for genetic loci whose zygotic expression is required for formation of body-wall muscle cells during embryogenesis in Caenorhabditis elegans. To test for muscle cell differentiation we have assayed for both contractile function and the expression of muscle-specific structural proteins. Monoclonal antibodies directed against two myosin heavy chain isoforms, the products of the unc-54 and myo-3 genes, were used to detect body-wall muscle differentiation. We have screened 77 deficiencies, covering approximately 72% of the genome. Deficiency homozygotes in most cases stain with antibodies to the body-wall muscle myosins and in many cases muscle contractile function is observed. We have identified two regions showing distinct defects in myosin heavy chain gene expression. Embryos homozygous for deficiencies removing the left tip of chromosome V fail to accumulate the myo-3 and unc-54 products, but express antigens characteristic of hypodermal, pharyngeal and neural development. Embryos lacking a large region on chromosome III accumulate the unc-54 product but not the myo-3 product. We conclude that there exist only a small number of loci whose zygotic expression is uniquely required for adoption of a muscle cell fate.


Sign in / Sign up

Export Citation Format

Share Document