scholarly journals Signatures of proprioceptive control in Caenorhabditis elegans locomotion

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’.

2018 ◽  
Author(s):  
Jack E. Denham ◽  
Thomas Ranner ◽  
Netta Cohen

Animal locomotion describes the coordinated self-propelled movement of a body, subject to the combined effects of internal muscle forcing and external forces. Here we use an integrated neuromechanical computational model to study the combined effects of neural modulation, mechanical modulation and modulation of the external environments on undulatory forward locomotion in the nematode C. elegans. In particular we use a proprioceptively driven neural control circuit to consider the effects of proprioception, body elasticity and environmental drag on the waveform, frequency and speed of undulations. We find qualitative differences in the frequency-wavelength relationship obtained under extrinsic modulation of the environmental fluid or body elasticity versus intrinsic modulation due to changes in the sensorimotor control. We consider possible targets of modulation by the worm and implications of our results for our understanding of the neural control of locomotion in this system.


2018 ◽  
Vol 373 (1758) ◽  
pp. 20170374 ◽  
Author(s):  
Eduardo J. Izquierdo ◽  
Randall D. Beer

With 302 neurons and a near-complete reconstruction of the neural and muscle anatomy at the cellular level, Caenorhabditis elegans is an ideal candidate organism to study the neuromechanical basis of behaviour. Yet despite the breadth of knowledge about the neurobiology, anatomy and physics of C. elegans , there are still a number of unanswered questions about one of its most basic and fundamental behaviours: forward locomotion. How the rhythmic pattern is generated and propagated along the body is not yet well understood. We report on the development and analysis of a model of forward locomotion that integrates the neuroanatomy, neurophysiology and body mechanics of the worm. Our model is motivated by experimental analysis of the structure of the ventral cord circuitry and the effect of local body curvature on nearby motoneurons. We developed a neuroanatomically grounded model of the head motoneuron circuit and the ventral nerve cord circuit. We integrated the neural model with an existing biomechanical model of the worm's body, with updated musculature and stretch receptors. Unknown parameters were evolved using an evolutionary algorithm to match the speed of the worm on agar. We performed 100 evolutionary runs and consistently found electrophysiological configurations that reproduced realistic control of forward movement. The ensemble of successful solutions reproduced key experimental observations that they were not designed to fit, including the wavelength and frequency of the propagating wave. Analysis of the ensemble revealed that head motoneurons SMD and RMD are sufficient to drive dorsoventral undulations in the head and neck and that short-range posteriorly directed proprioceptive feedback is sufficient to propagate the wave along the rest of the body. This article is part of a discussion meeting issue ‘Connectome to behaviour: modelling C. elegans at cellular resolution’.


2017 ◽  
Author(s):  
Tianqi Xu ◽  
Jing Huo ◽  
Shuai Shao ◽  
Michelle Po ◽  
Taizo Kawano ◽  
...  

Descending signals from the brain play critical roles in controlling and modulating locomotion kinematics. In the Caenorhabditis elegans nervous system, descending AVB premotor interneurons exclusively form gap junctions with B-type motor neurons that drive forward locomotion. We combined genetic analysis, optogenetic manipulation, and computational modeling to elucidate the function of AVB-B gap junctions during forward locomotion. First, we found that some B-type motor neurons generated intrinsic rhythmic activity, constituting distributed central pattern generators. Second, AVB premotor interneurons drove bifurcation of B-type motor neuron dynamics, triggering their transition from stationary to oscillatory activity. Third, proprioceptive couplings between neighboring B-type motor neurons entrained the frequency of body oscillators, forcing coherent propagation of bending waves. Despite substantial anatomical differences between the worm motor circuit and those in higher model organisms, we uncovered converging principles that govern coordinated locomotion.Significance StatementA deep understanding of the neural basis of motor behavior must integrate neuromuscular dynamics, mechanosensory feedback, as well as global command signals, to predict behavioral dynamics. Here, we report on an integrative approach to defining the circuit logic underlying coordinated locomotion in C. elegans. Our combined experimental and computational analysis revealed that (1) motor neurons in C. elegans could function as intrinsic oscillators; (2) Descending inputs and proprioceptive couplings work synergistically to facilitate the sequential activation of motor neuron activities, allowing bending waves to propagate efficiently along the body. Our work thus represents a key step towards an integrative view of animal locomotion.


2018 ◽  
Vol 115 (16) ◽  
pp. E3616-E3625 ◽  
Author(s):  
Alejandro Bilbao ◽  
Amar K. Patel ◽  
Mizanur Rahman ◽  
Siva A. Vanapalli ◽  
Jerzy Blawzdziewicz

Locomotion of the nematode Caenorhabditis elegans is a key observable used in investigations ranging from behavior to neuroscience to aging. However, while the natural environment of this model organism is 3D, quantitative investigations of its locomotion have been mostly limited to 2D motion. Here, we present a quantitative analysis of how the nematode reorients itself in 3D media. We identify a unique behavioral state of C. elegans—a roll maneuver—which is an essential component of 3D locomotion in burrowing and swimming. The rolls, associated with nonzero torsion of the nematode body, result in rotation of the plane of dorsoventral body undulations about the symmetry axis of the trajectory. When combined with planar turns in a new undulation plane, the rolls allow the nematode to reorient its body in any direction, thus enabling complete exploration of 3D space. The rolls observed in swimming are much faster than the ones in burrowing; we show that this difference stems from a purely hydrodynamic enhancement mechanism and not from a gait change or an increase in the body torsion. This result demonstrates that hydrodynamic viscous forces can enhance 3D reorientation in undulatory locomotion, in contrast to known hydrodynamic hindrance of both forward motion and planar turns.


2018 ◽  
Author(s):  
Jack E. Denham ◽  
Thomas Ranner ◽  
Netta Cohen

In all animals, the successful orchestration of motor programs hinges on appropriate coupling between components of the system, from neural circuit dynamics, through muscles and body properties to the physical environment. We study this coupling in undulatory locomotion, with a view to better understanding the relative roles of central and reflex-driven control. We ask how the coupling between neural control and body mechanics is affected by sensory inputs during undulatory locomotion in C. elegans. To address this question, we use a biomechanical simulation framework, within which we separately model feed forward and feedback controlled undulations. We characterize neuromechanical phase lag and locomotion speed using body stiffness as a control parameter. We show that sensory entrainment can suppress neuromechanical phase lag, that would otherwise emerge under centrally generated feed forward control.


Genetics ◽  
2001 ◽  
Vol 157 (4) ◽  
pp. 1611-1622 ◽  
Author(s):  
Go Shioi ◽  
Michinari Shoji ◽  
Masashi Nakamura ◽  
Takeshi Ishihara ◽  
Isao Katsura ◽  
...  

Abstract Using a pan-neuronal GFP marker, a morphological screen was performed to detect Caenorhabditis elegans larval lethal mutants with severely disorganized major nerve cords. We recovered and characterized 21 mutants that displayed displacement or detachment of the ventral nerve cord from the body wall (Ven: ventral cord abnormal). Six mutations defined three novel genetic loci: ven-1, ven-2, and ven-3. Fifteen mutations proved to be alleles of previously identified muscle attachment/positioning genes, mup-4, mua-1, mua-5, and mua-6. All the mutants also displayed muscle attachment/positioning defects characteristic of mua/mup mutants. The pan-neuronal GFP marker also revealed that mutants of other mua/mup loci, such as mup-1, mup-2, and mua-2, exhibited the Ven defect. The hypodermis, the excretory canal, and the gonad were morphologically abnormal in some of the mutants. The pleiotropic nature of the defects indicates that ven and mua/mup genes are required generally for the maintenance of attachment of tissues to the body wall in C. elegans.


2004 ◽  
Vol 9 (2) ◽  
pp. 147-152 ◽  
Author(s):  
Brenda R. Ellerbrock ◽  
Eileen M. Coscarelli ◽  
Mark E. Gurney ◽  
Timothy G. Geary

Caenorhabditis elegans contains 3 homologs of presenilin genes that are associated with Alzheimer s disease. Loss-of-function mutations in C. elegans genes cause a defect in egg laying. In humans, loss of presenilin-1 (PS1) function reduces amyloid-beta peptide processing from the amyloid protein precursor. Worms were screened for compounds that block egg laying, phenocopying presenilin loss of function. To accommodate even relatively high throughput screening, a semi-automated method to quantify egg laying was devised by measuring the chitinase released into the culture medium. Chitinase is released by hatching eggs, but little is shed into the medium from the body cavity of a hermaphrodite with an egg laying deficient ( egl) phenotype. Assay validation involved measuring chitinase release from wild-type C. elegans (N2 strain), sel-12 presenilin loss-of-function mutants, and 2 strains of C. elegans with mutations in the egl-36K+ channel gene. Failure to find specific presenilin inhibitors in this collection likely reflects the small number of compounds tested, rather than a flaw in screening strategy. Absent defined biochemical pathways for presenilin, this screening method, which takes advantage of the genetic system available in C. elegans and its historical use for anthelminthic screening, permits an entry into mechanism-based discovery of drugs for Alzheimer s disease. ( Journal of Biomolecular Screening 2004:147-152)


1991 ◽  
Vol 98 (4) ◽  
pp. 491-496
Author(s):  
R. Nave ◽  
D. Furst ◽  
U. Vinkemeier ◽  
K. Weber

We have isolated mini-titin from the nematodes Ascaris lumbricoides and Caenorhabditis elegans under native conditions using a modification in the procedure to prepare this protein from insect muscle. The proteins have an apparent molecular weight of 600,000 and appear in oriented specimens as flexible thin rods with a length around 240–250 nm. The circular dichroism spectrum of the Ascaris protein is dominated by beta-structure. The proteins react with antibodies to insect mini-titin and also with antibodies raised against peptides contained in the sequence predicted for twitchin, the product of the Caenorhabditis elegans unc-22 gene. Antibodies to insect mini-titin decorate the body musculature as well as the pharynx of wild-type C. elegans in immunofluorescence microscopy. In the twitchin mutant E66 only the pharynx is decorated. We conclude that the mini-titins of invertebrate muscles defined earlier by ultrastructural criteria are very likely to be twitchins, i.e. molecules necessary for normal muscle contraction. We discuss the molecular properties of the proteins in the light of the sequence established for twitchin.


1993 ◽  
Vol 4 (9) ◽  
pp. 941-952 ◽  
Author(s):  
J E Schwarzbauer ◽  
C S Spencer

The extracellular matrix-associated protein, SPARC (osteonectin [Secreted Protein Acidic and Rich in Cysteine]), modulates cell adhesion and induces a change in cell morphology. SPARC expression in mammals is developmentally regulated and is highest at sites of extracellular matrix assembly and remodeling such as parietal endoderm and bone. We have isolated cDNA and genomic DNA clones encoding the Caenorhabditis elegans homologue of SPARC. The gene organization is highly conserved, and the proteins encoded by mouse, human, and nematode genes are about 38% identical. SPARC consists of four domains (I-IV) based on predicted secondary structure. Using bacterial fusion proteins containing nematode domain I or the domain IV EF-hand motif, we show that, like the mammalian proteins, both domains bind calcium. In transgenic nematodes expressing a SPARC-lacZ fusion gene, beta-galactosidase staining accumulated in a striated pattern in the more heavily stained muscle cells along the body. Comparison of the pattern of transgene expression to unc-54-lacZ animals demonstrated that SPARC is expressed by body wall and sex muscle cells. Appropriate levels of SPARC are essential for normal C. elegans development and muscle function. Transgenic nematodes overexpressing the wild-type SPARC gene were abnormal. Embryos were deformed, and adult hermaphrodites had vulval protrusions and an uncoordinated (Unc) phenotype with reduced mobility and paralysis.


2020 ◽  
Author(s):  
Heather Archer ◽  
Selina Deiparine ◽  
Erik C. Andersen

ABSTRACTPhoresy is a behavior in which an organism, the phoront, travels from one location to another by ‘hitching a ride’ on the body of a host as it disperses. Some phoronts are generalists, taking advantage of any available host. Others are specialists and travel only when specific hosts are located using chemical cues to identify and move (chemotax) toward the preferred host. Free-living nematodes, like Caenorhabditis elegans, are often found in natural environments that contain terrestrial isopods and other invertebrates. Additionally, the C. elegans wild strain PB306 was isolated associated with the isopod Porcellio scaber. However, it is currently unclear if C. elegans is a phoront of terrestrial isopods, and if so, whether it is a specialist, generalist, or developmental stage-specific combination of both strategies. Because the relevant chemical stimuli might be secreted compounds or volatile odorants, we used different types of chemotaxis assays across diverse extractions of compounds or odorants to test whether C. elegans is attracted to P. scaber. We show that two different strains – the wild isolate PB306 and the laboratory-adapted strain N2 – are not attracted to P. scaber during either the dauer or adult life stages. Our results indicate that C. elegans was not attracted to chemical compounds or volatile odorants from P. scaber, providing valuable empirical evidence to suggest that any associations between these two species are likely opportunistic rather than specific phoresy.


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