Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in<i>Caenorhabditis elegans</i>

Olivares, Erick; Izquierdo, Eduardo J.; Beer, Randall D.

doi:10.1162/netn_a_00036

Cited by 30 publications

(40 citation statements)

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“…Recently, Olivares and co-workers [32] constructed a CPG model based on local network motifs along the ventral nerve cord; however, proposed biophysical mechanisms only partly agree with available experimental data; caveats remain that the direction of proposed CPG coupling is opposite to what has been discussed above.…”

Section: Towards a Full Mechanistic And Computational Model Of C Elementioning

confidence: 94%

“…Despite a deep understanding of anatomy [27][28][29][30][31] and theoretical studies [32][33][34], direct experimental evidence that addresses the potential existence and identity of C. elegans CPGs has been lacking. Obtaining a mechanistic understanding of the C. elegans motor rhythm has been difficult.…”

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

confidence: 99%

“…There have been continuous efforts to model C. elegans locomotion [33,34,[58][59][60][61]. Cohen and colleagues [32,62,63] developed proprioceptive coupling models for bending wave undulation, providing insights into gait adaptation [64][65][66].…”

Section: Towards a Full Mechanistic And Computational Model Of C Elementioning

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

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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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Section: Towards a Full Mechanistic And Computational Model Of C Elementioning

confidence: 94%

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

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

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“…Multiple CPGs can coordinate to produce forward locomotion in the worm 88 In previous work, we demonstrated the theoretical feasibility of a CPG in a small repeating subcircuit 89 of the ventral nerve cord without pacemaker neurons (Olivares et al, 2018). Can this repeating 90 circuit coordinate oscillations across the complete length of the worm to produce not just a 91 dorsoventral oscillation, but a propagating wave in the absence of stretch-receptor feedback?…”

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confidence: 99%

A neuromechanical model of multiple network rhythmic pattern generators for forward locomotion inC. elegans

Olivares

Izquierdo

Beer

2019

Preprint

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Multiple mechanisms contribute to the generation, propagation, and coordination of 8 rhythmic patterns necessary for locomotion in Caenorhabditis elegans. Current experiments have 9 focused on two possibilities: pacemaker neurons and stretch-receptor feedback. Here, we focus on 10 whether locomotion behavior can be produced by a chain of network oscillators in the ventral 11 nerve cord. We use a simulation model to demonstrate that a repeating neural circuit identified in 12 the worm's connectome can be chained together to drive forward locomotion on agar in a 13 neuromechanical model of the nematode, in the absence of pacemaker neurons or 14 stretch-receptor feedback. Systematic exploration of the space of possible solutions reveals that 15 there are multiple configurations that result in locomotion that match the kinematics of the worm 16 on agar. Analysis of the best solutions reveals that gap junctions between different classes of 17 motoneurons are likely to play key roles in coordinating oscillations along the ventral nerve cord. 18 19 40 1 of 24 Manuscript submitted to eLife that modulate C. elegans locomotion (Tavernarakis et al., 1997), as well as evidence of a direct 41 relationship between body curvature and neural activity (Wen et al., 2012). However, coordinated 42 rhythmic patterns can also be produced internally, while remaining open to modulation through 43 external contributions. Central pattern generators (CPGs) are known to be involved in a wide variety 44 of behaviors in a number of different organisms, including insect flight, swimming in molluscs, gut 45 movements in crustaceans, and swimming and respiration in vertebrates (Marder and Bucher, 2001; 46 Goulding, 2009; Katz, 2016; Arshavsky et al., 2016; Dasen, 2018; Minassian et al., 2017). In a CPG, 47 the rhythmic pattern can be generated through the intrinsic oscillatory properties of pacemaker 48 neurons or it can emerge from the interaction of networks of non-oscillatory neurons (Goulding, 49 2009). Recent experiments have provided support for the role of intrinsic oscillations in C. elegans 50 locomotion (Gao et al., 2018; Fouad et al., 2018; Xu et al., 2018). Although the work attributes the 51 source of these rhythm generators to pacemaker neurons, the evidence provided does not discard 52 the possibility of network oscillators (Wen et al., 2018). 53 It is increasingly acknowledged that simulation models play an important role in elucidating 54 how brain-body-environment systems produce behavior (Ijspeert, 2008; Abbott, 2008; Izquierdo, 55 2018). In C. elegans, there has been an surge of theoretical work focused on understanding the 56 neuromechanical basis of locomotion. Several computational models have demonstrated that 57 proprioception alone can be used to generate rhythmic patterns and propagate them along the 58 body (Niebur and Erdös, 1991; Karbowski et al., 2008; Boyle, 2009; Mailler et al., 2010; Wen et al., 59 2012; Izquierdo and Beer, 2018; Fieseler et al., 2018; Gleeson et al., 2018). There have also been a 60 number of m...

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“…In line with previous models [35, 38, 39], the model assumes electrical synapses can be modeled as bidirectional ohmic resistances. As we have shown previously [40], this neural model has the capacity to reproduce qualitatively a wide range of electrophysiological properties observed in C. elegans neurons [32, 33]. The model can reproduce the passive activity that has been observed in some neurons, like for example, AVA.…”

Section: Modelmentioning

confidence: 58%

From head to tail: A neuromechanical model of forward locomotion in C. elegans

Izquierdo

Beer

2018

Preprint

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Introduction 1Behavior is grounded in the interaction between an organism's brain, its body, and its 2 environment. How simple neuronal circuits interact with their muscles and mechanical bodies 3 to generate behavior is not yet well understood. With 302 neurons and a near complete 4 reconstruction of the neural and muscle anatomy at the cellular level [1], C. elegans is an ideal 5 candidate organism to understand the neuromechanical basis of behavior. 6 Locomotion is essential to most living organisms. Since nearly the entire behavioral repertoire 7 of C. elegans is expressed through movement, understanding the neuromechanical basis of 8 locomotion is especially critical as a foundation upon which analyses of all other behaviors 9 must build. C. elegans locomotes in an undulatory fashion, generating thrust by propagating 10 dorsoventral bends along its body. Movement is generated by body wall muscles arranged 11 in staggered pairs along four bundles [2]. The anterior-most muscles are driven by a head 12 motorneuron circuit and the rest of the muscles are driven by motorneurons in the ventral 13 nerve cord (VNC). Although the nematode is not segmented, a statistical analysis of the VNC 14 motorneurons in relation to the position of the muscles they innervate revealed a repeating neural 15 unit [3]. Interestingly, while the repeating neural units in the VNC are inter-connected via a set of 16 chemical and electrical synapses, the head circuit is largely disconnected from the rest of the VNC 17 neural units. Motorneurons in both the head and the VNC circuit have been long postulated to 18 be mechanosensitive to stretch [1, 4, 5], and evidence in support of this has been shown recently 19 for the VNC [6]. Despite all of this anatomical knowledge, how the rhythmic pattern is generated 20 and propagated along the body during forward locomotion on agar is not yet well understood. 21A number of computational models of C. elegans locomotion have been proposed (see 22 reviews [7, 8, 9]). The model described in this paper differs from previous models in four 23 main ways. First, our model of the VNC incorporates the recent analysis of its repeating 24 structure [3]. Second, our model of stretch-receptors feedback takes into consideration recent 25 findings regarding the range and directionality of local body curvature on motoneurons [6]. Third, 26 our model takes into consideration the head motorneuron circuit, which had been largely ignored 27 in most models of locomotion, by either replicating an additional VNC unit or adding an oscillator 28 in the head. Finally, all current models have assumed specific mechanisms for how the rhythmic 29 movement is generated and propagated, with little systematic exploration of the possibilities. 30Here we present a model of forward locomotion grounded in the neurobiology, anatomy, and 31 physics of the worm. The model integrates a head motorneuron circuit based on hypotheses 32 postulated in the original "Mind of the Worm" paper [1] with a model of a repeating neural 33 unit in ...

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

Cited by 30 publications

References 54 publications

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

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

A neuromechanical model of multiple network rhythmic pattern generators for forward locomotion inC. elegans

From head to tail: A neuromechanical model of forward locomotion in C. elegans

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