scholarly journals Functionally asymmetric motor neurons coordinate locomotion of Caenorhabditis elegans

2018 ◽  
Author(s):  
Oleg Tolstenkov ◽  
Petrus Van der Auwera ◽  
Jana F. Liewald ◽  
Wagner Steuer Costa ◽  
Olga Bazhanova ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Gap Junctions ◽  
Motor Neurons ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Body Wave ◽  
Central Pattern Generators ◽  
Physiological Data ◽  
C Elegans ◽  
Pattern Generators

SummaryInvertebrate nervous systems are valuable models for fundamental principles of the control of behavior. Ventral nerve cord (VNC) motor neurons in Caenorhabditis elegans represent one of the best studied locomotor circuits, with known connectivity and functional information about most of the involved neuron classes. However, for one of those, the AS motor neurons (AS MNs), no physiological data is available. Combining specific expression and selective illumination, we precisely targeted AS MNs by optogenetics and addressed their role in the locomotion circuit. After photostimulation, AS MNs induce currents in post-synaptic body wall muscles (BWMs), exhibiting an initial asymmetry of excitatory output. This may facilitate complex regulatory motifs for adjusting direction during navigation. By behavioral and photo-inhibition experiments, we show that AS MNs contribute to propagation of the antero-posterior body wave during locomotion. By Ca2+-imaging in AS MNs and in their synaptic partners, we also reveal that AS MNs play a role in mediating forward and backward locomotion by integrating activity of premotor interneurons (PINs), as well as in coordination of the dorso-ventral body wave. AS MNs do not exhibit pacemaker properties, but potentially gate VNC central pattern generators (CPGs), as indicated by ceasing of locomotion when AS MNs are hyperpolarized. AS MNs provide positive feedback to the PIN AVA via gap junctions, a feature found also in other locomotion circuits. In sum, AS MNs have essential roles in coordinating locomotion, combining several functions, and emphasizing the compressed nature of the C. elegans nervous system in comparison to higher animals.HighlightsA class of motor neurons with unidentified function – AS cholinergic motor neurons - was characterized in C. elegans.AS neurons show asymmetry in both input and output and are specialized in coordination of dorso-ventral undulation bends.AS neurons mediate antero-posterior propagation of the undulatory body wave during locomotion.AS neurons integrate signals for forward and reverse locomotion from premotor interneurons and may gate ventral nerve cord central pattern generators (CPGs) via gap junctions.

scholarly journals A descending pathway facilitates undulatory wave propagation in Caenorhabditis elegans through gap junctions

2017 ◽  
Author(s):  
Tianqi Xu ◽  
Jing Huo ◽  
Shuai Shao ◽  
Michelle Po ◽  
Taizo Kawano ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Gap Junctions ◽  
Motor Neuron ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
The Body ◽  
C Elegans ◽  
Bending Waves ◽  
Forward Locomotion ◽  
Type Motor

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.

scholarly journals Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans

2018 ◽  
Vol 2 (3) ◽  
pp. 323-343 ◽  
Author(s):  
Erick O. Olivares ◽  
Eduardo J. Izquierdo ◽  
Randall D. Beer
Keyword(s):  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Computational Models ◽  
Neural Circuit ◽  
Central Pattern Generators ◽  
C Elegans ◽  
Segmentation Analysis ◽  
Pattern Generators ◽  
Neural Unit

C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circuit that supports intrinsic network oscillations. With a fully reconstructed connectome, the question of whether it is possible to have a CPG in the ventral nerve cord (VNC) of C. elegans can be answered through computational models. We modeled a repeating neural unit based on segmentation analysis of the connectome. We then used an evolutionary algorithm to determine the unknown physiological parameters of each neuron so as to match the features of the neural traces of the worm during forward and backward locomotion. We performed 1,000 evolutionary runs and consistently found configurations of the neural circuit that produced oscillations matching the main characteristic observed in experimental recordings. In addition to providing an existence proof for the possibility of a CPG in the VNC, we suggest a series of testable hypotheses about its operation. More generally, we show the feasibility and fruitfulness of a methodology to study behavior based on a connectome, in the absence of complete neurophysiological details.

scholarly journals Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Oleg Tolstenkov ◽  
Petrus Van der Auwera ◽  
Wagner Steuer Costa ◽  
Olga Bazhanova ◽  
Tim M Gemeinhardt ◽  
...  
Keyword(s):  
Wave Propagation ◽  
Caenorhabditis Elegans ◽  
Gap Junctions ◽  
Motor Neurons ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Muscle Activation ◽  
Functional Information ◽  
Nematode Caenorhabditis Elegans ◽  
Bending Wave

Locomotion circuits developed in simple animals, and circuit motifs further evolved in higher animals. To understand locomotion circuit motifs, they must be characterized in many models. The nematode Caenorhabditis elegans possesses one of the best-studied circuits for undulatory movement. Yet, for 1/6th of the cholinergic motor neurons (MNs), the AS MNs, functional information is unavailable. Ventral nerve cord (VNC) MNs coordinate undulations, in small circuits of complementary neurons innervating opposing muscles. AS MNs differ, as they innervate muscles and other MNs asymmetrically, without complementary partners. We characterized AS MNs by optogenetic, behavioral and imaging analyses. They generate asymmetric muscle activation, enabling navigation, and contribute to coordination of dorso-ventral undulation as well as anterio-posterior bending wave propagation. AS MN activity correlated with forward and backward locomotion, and they functionally connect to premotor interneurons (PINs) for both locomotion regimes. Electrical feedback from AS MNs via gap junctions may affect only backward PINs.

scholarly journals Caenorhabditis elegans excitatory ventral cord motor neurons derive rhythm for body undulation

2018 ◽  
Vol 373 (1758) ◽  
pp. 20170370 ◽  
Author(s):  
Quan Wen ◽  
Shangbang Gao ◽  
Mei Zhen
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
Oscillatory Activity ◽  
C Elegans ◽  
Ventral Cord ◽  
Small Neuron ◽  
Motor Rhythm ◽  
Pattern Generators

The intrinsic oscillatory activity of central pattern generators underlies motor rhythm. We review and discuss recent findings that address the origin of Caenorhabditis elegans motor rhythm. These studies propose that the A- and mid-body B-class excitatory motor neurons at the ventral cord function as non-bursting intrinsic oscillators to underlie body undulation during reversal and forward movements, respectively. Proprioception entrains their intrinsic activities, allows phase-coupling between members of the same class motor neurons, and thereby facilitates directional propagation of undulations. Distinct pools of premotor interneurons project along the ventral nerve cord to innervate all members of the A- and B-class motor neurons, modulating their oscillations, as well as promoting their bi-directional coupling. The two motor sub-circuits, which consist of oscillators and descending inputs with distinct properties, form the structural base of dynamic rhythmicity and flexible partition of the forward and backward motor states. These results contribute to a continuous effort to establish a mechanistic and dynamic model of the C. elegans sensorimotor system. C. elegans exhibits rich sensorimotor functions despite a small neuron number. These findings implicate a circuit-level functional compression. By integrating the role of rhythm generation and proprioception into motor neurons, and the role of descending regulation of oscillators into premotor interneurons, this numerically simple nervous system can achieve a circuit infrastructure analogous to that of anatomically complex systems. C. elegans has manifested itself as a compact model to search for general principles of sensorimotor behaviours. This article is part of a discussion meeting issue ‘Connectome to behaviour: modelling C. elegans at cellular resolution’.

scholarly journals Mutations Affecting Nerve Attachment of Caenorhabditis elegans

Genetics ◽  
2001 ◽  
Vol 157 (4) ◽  
pp. 1611-1622 ◽  
Author(s):  
Go Shioi ◽  
Michinari Shoji ◽  
Masashi Nakamura ◽  
Takeshi Ishihara ◽  
Isao Katsura ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Body Wall ◽  
The Body ◽  
Genetic Loci ◽  
Muscle Attachment ◽  
C Elegans ◽  
Ventral Cord ◽  
Excretory Canal

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.

scholarly journals A neuromechanical model of multiple network rhythmic pattern generators for forward locomotion in C. elegans

2019 ◽  
Author(s):  
Erick Olivares ◽  
Eduardo J. Izquierdo ◽  
Randall D. Beer
Keyword(s):  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Stretch Receptor ◽  
Rhythmic Pattern ◽  
Pacemaker Neurons ◽  
C Elegans ◽  
Forward Locomotion ◽  
Pattern Generators ◽  
Multiple Network ◽  
A Chain

AbstractMultiple mechanisms contribute to the generation, propagation, and coordination of the rhythmic patterns necessary for locomotion in Caenorhabditis elegans. Current experiments have focused on two possibilities: pacemaker neurons and stretch-receptor feedback. Here, we focus on whether it is possible that a chain of multiple network rhythmic pattern generators in the ventral nerve cord also contribute to locomotion. We use a simulation model to search for electrophysiological parameters of the anatomically constrained ventral nerve cord circuit that, when embodied and situated, can drive forward locomotion on agar, in the absence of pacemaker neurons or stretch-receptor feedback. Systematic exploration of the space of possible solutions reveals that there are multiple configurations that result in locomotion that is consistent with certain aspects of the kinematics of worm locomotion on agar. Analysis of the best solutions reveals that gap junctions between different classes of motorneurons in the ventral nerve cord can play key roles in coordinating the multiple rhythmic pattern generators.

Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae

Development ◽  
1982 ◽  
Vol 67 (1) ◽  
pp. 89-100
Author(s):  
Alison M. G. Robertson ◽  
J. N. Thomson
Keyword(s):  
Cell Death ◽  
Caenorhabditis Elegans ◽  
Programmed Cell Death ◽  
Ultrastructural Study ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Condensed Chromatin ◽  
C Elegans ◽  
Programmed Death ◽  
Selection Of

In the nematode C. elegans, cells undergoing programmed death in the developing ventral nerve cord were identified by Nomarski optics and prepared for ultrastructural study at various times after their birth in mitosis. The sequence of changes observed suggests that the hypodermis recognizes the dying cell before completion of telophase. The dying cell is engulfed and digestion then occurs until all that remains within the hypodermal cytoplasm is a collection of membranous whorls interspersed with condensed chromatin-like remnants. The process shares several features with apoptosis, the mode of programmed cell death observed in vertebrates and insects. The selection of cells for programmed death appears not to involve competition for peripheral targets.

Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans

Development ◽  
1993 ◽  
Vol 117 (3) ◽  
pp. 1071-1087 ◽  
Author(s):  
G. Garriga ◽  
C. Desai ◽  
H.R. Horvitz
Keyword(s):  
Caenorhabditis Elegans ◽  
Epithelial Cells ◽  
Motor Neurons ◽  
Growth Cone ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Egg Laying ◽  
Axonal Guidance ◽  
Nematode Caenorhabditis Elegans ◽  
Vulval Precursor Cells

The two serotonergic HSN motor neurons of the nematode Caenorhabditis elegans innervate the vulval muscles and stimulate egg laying by hermaphrodites. By analyzing mutant and laser-operated animals, we find that both epithelial cells of the developing vulva and axons of the ventral nerve cord are required for HSN axonal guidance. Vulval precursor cells help guide the growth cone of the emerging HSN axon to the ventral nerve cord. Vulval cells also cause the two HSN axons to join the ventral nerve cord in two separate fascicles and to defasciculate from the ventral nerve cord and branch at the vulva. The axons of either the PVP or PVQ neurons are also necessary for the HSN axons to run in two separate fascicles within the ventral nerve cord. Our observations indicate that the outgrowth of the HSN axon is controlled in multiple ways by both neuronal and nonneuronal cells.

scholarly journals A terminal selector prevents a Hox transcriptional switch to safeguard motor neuron identity throughout life

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Weidong Feng ◽  
Yinan Li ◽  
Pauline Dao ◽  
Jihad Aburas ◽  
Priota Islam ◽  
...  
Keyword(s):  
Ion Channels ◽  
Motor Neurons ◽  
General Principle ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Neurotransmitter Receptors ◽  
Dual Function ◽  
C Elegans ◽  
Neuronal Identity ◽  
Transcriptional Switch

To become and remain functional, individual neuron types must select during development and maintain throughout life their distinct terminal identity features, such as expression of specific neurotransmitter receptors, ion channels and neuropeptides. Here, we report a molecular mechanism that enables cholinergic motor neurons (MNs) in the C. elegans ventral nerve cord to select and maintain their unique terminal identity. This mechanism relies on the dual function of the conserved terminal selector UNC-3 (Collier/Ebf). UNC-3 synergizes with LIN-39 (Scr/Dfd/Hox4-5) to directly co-activate multiple terminal identity traits specific to cholinergic MNs, but also antagonizes LIN-39’s ability to activate terminal features of alternative neuronal identities. Loss of unc-3 causes a switch in the transcriptional targets of LIN-39, thereby alternative, not cholinergic MN-specific, terminal features become activated and locomotion defects occur. The strategy of a terminal selector preventing a transcriptional switch may constitute a general principle for safeguarding neuronal identity throughout life.

scholarly journals Excitatory Motor Neurons are Local Central Pattern Generators in an Anatomically Compressed Motor Circuit for Reverse Locomotion

2017 ◽  
Author(s):  
Shangbang Gao ◽  
Sihui Asuka Guan ◽  
Anthony D. Fouad ◽  
Jun Meng ◽  
Taizo Kawano ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Calcium Imaging ◽  
Central Pattern Generators ◽  
Oscillatory Activity ◽  
Intrinsic Activity ◽  
C Elegans ◽  
Class A ◽  
Cell Ablation ◽  
Pattern Generators

AbstractCentral pattern generators are cell‐ or network-driven oscillators that underlie motor rhythmicity. The existence and identity of C. elegans CPGs remain unknown. Through cell ablation, electrophysiology, and calcium imaging, we identified oscillators for reverse locomotion. We show that the cholinergic and excitatory class A motor neurons exhibit intrinsic and oscillatory activity, and such an activity can drive reverse locomotion without premotor interneurons. Regulation of their oscillatory activity, either through effecting an endogenous constituent of oscillation, the P/Q/N high voltage-activated calcium channel UNC-2, or, via dual regulation – inhibition and activation ‐ by the descending premotor interneurons AVA, determines the propensity, velocity, and sustention of reverse locomotion. Thus, the reversal motor executors themselves serve as oscillators; regulation of their intrinsic activity controls the reversal motor state. These findings exemplify anatomic and functional compression: motor executors integrate the role of rhythm generation in a locomotor network that is constrained by small cell numbers.

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