Descending pathway facilitates undulatory wave propagation in
            <i>Caenorhabditis elegans</i>
            through gap junctions

Xu, Tianqi; Huo, Jing; Shao, Shimiao; Po, Michelle D.; Kawano, Taizo; Lu, Yangning; Wu, Min; Zhen, Mei; Wen, Quan

doi:10.1073/pnas.1717022115

Cited by 60 publications

(116 citation statements)

References 61 publications

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“…Furthermore, we demonstrate a methodology to systematically explore different mechanisms that match behaviour given biological assumptions. Further work will involve matching the behaviour of the integrated neuromechanical model to the effect produced from optogenetic and physical manipulations reported in recent experiments [57,58]. Ultimately, improving our understanding of forward locomotion will allow us to study more complex behaviours that may require contributions from additional neural circuits.…”

Section: Discussionmentioning

confidence: 99%

From head to tail: a neuromechanical model of forward locomotion inCaenorhabditis elegans

Izquierdo¹,

Beer²

2018

Phil. Trans. R. Soc. B

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With 302 neurons and a near-complete reconstruction of the neural and muscle anatomy at the cellular level, 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, 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 at cellular resolution'.

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Section: Discussionmentioning

confidence: 99%

From head to tail: a neuromechanical model of forward locomotion inCaenorhabditis elegans

Izquierdo¹,

Beer²

2018

Phil. Trans. R. Soc. B

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“…Among them, the A-and some B-class excitatory motor neurons are main executors of body undulation during backward and forward movement, respectively. Recent studies reveal that these motor neurons function as the respective CPGs for backward and forward movements [38][39][40]. The A-class motor neurons exhibited intrinsic oscillatory activities (figure 1a) that were sufficient to execute slow backward movements without premotor interneurons (figure 1b).…”

Section: Cpgs For Body Bending Reside In the C Elegans Ventral Nervementioning

confidence: 99%

“…Mechanisms must be in place to coordinate CPGs' activities distributed along the C. elegans body to form a cohesive propagating bending wave [34]. During forward movements in microfluidic devices, local and directional proprioceptive coupling between the adjacent body regions plays a critical role in the propagation of undulation [40,41]. When the mid-body region was trapped in a microfluidic channel with a defined curvature, the unrestrained posterior body region exhibited the same curvature in the same direction (figure 3b).…”

Section: Proprioception Entrains and Coordinates Cpgdriven Body Undulmentioning

confidence: 99%

“…The bendsensitivity of B-class motor neurons allows the curvature change in an anterior body to define the curvature of the Optogenetic experiments reveal that proprioception entrains the B-class motor neuron's oscillation. When proprioceptive signal from the most anterior body region was eliminated by either optogenetically inhibiting the head muscles or anterior B-type motor neurons, the mid-body generated rhythmic bending activity, with a higher frequency than normal undulation [38,40] (figure 3c). Hence, the B-class motor neurons situated in the anterior and posterior body region may operate at different intrinsic frequencies, but directional proprioceptive coupling entrains their activities to generate coherent body undulation ( figure 3c,d).…”

Section: Proprioception Entrains and Coordinates Cpgdriven Body Undulmentioning

confidence: 99%

“…Upon hyperpolarization, they use electrical synapses to facilitate efficient inhibition of all A-class motor neuron activities [39,53]. Similarly, the depolarization and hyperpolarization of the AVB premotor interneurons could potentiate and halt forward locomotion, respectively, through their electrical coupling with the B-class motor neurons [40].…”

Section: Descending Pathways By the Projectionpremotor Interneurons Cmentioning

confidence: 99%

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

Wen

Gao

Zhen

2018

Phil. Trans. R. Soc. B

Self Cite

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The intrinsic oscillatory activity of central pattern generators underlies motor rhythm. We review and discuss recent findings that address the origin of 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 sensorimotor system. 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. 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 at cellular resolution'.

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Fast whole‐body motor neuron calcium imaging of freely moving Caenorhabditis elegans without coverslip pressed

Fang

Zhai

et al. 2021

Cytometry Pt A

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Caenorhabditis elegans (C. elegans) is an ideal model organism for studying neuronal functions at the system level. This article develops a customized system for wholebody motor neuron calcium imaging of freely moving C. elegans without the coverslip pressed. Firstly, we proposed a fast centerline localization algorithm that could deal with most topology-variant cases costing only 6 ms for one frame, not only benefits for real-time localization but also for post-analysis. Secondly, we implemented a fulltime two-axis synchronized motion strategy by adaptively adjusting the motion parameters of two motors in every short-term motion step (~50 ms). Following the above motion tracking configuration, the tracking performance of our system has been demonstrated to completely support the high spatiotemporal resolution calcium imaging on whole-body motor neurons of wild-type (N2) worms as well as two mutants (unc-2, unc-9), even the instantaneous speed of worm moving without coverslip pressed was extremely up to 400 μm/s.

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Descending pathway facilitates undulatory wave propagation in Caenorhabditis elegans through gap junctions

Cited by 60 publications

References 61 publications

From head to tail: a neuromechanical model of forward locomotion inCaenorhabditis elegans

From head to tail: a neuromechanical model of forward locomotion inCaenorhabditis elegans

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

Fast whole‐body motor neuron calcium imaging of freely moving Caenorhabditis elegans without coverslip pressed

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