An extrasynaptic GABAergic signal modulates a pattern of forward movement in Caenorhabditis elegans

Song, Yu; Wen, Quan; He, Liu; Zhong, Connie S.; Qin, Yuqi; Harris, Graham P.; Kawano, Taizo; Wu, Min; Xu, Tianqi; Samuel, Aravinthan D. T.; Zhang, Yun

doi:10.7554/elife.14197

Cited by 50 publications

(59 citation statements)

References 72 publications

(145 reference statements)

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“…They have been previously implicated in directional head bending and steering. [37][38][39][40] To better define the behavioral effects of SMD modulation, we more closely examined body bending in animals overexpressing ckr-1 under control of the odr-2 (16) promoter, and also using a second promoter, flp-22∆4, that was recently shown to drive selective expression in the SMD neurons 41 (Fig. 6A).…”

Section: Ckr-1 Functions In the Smd Head Motor Neurons To Modulate Bomentioning

confidence: 99%

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

Ramachandran

Banerjee

Bhattacharya

et al. 2020

Preprint

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Neuromodulators promote adaptive behaviors in response to either environmental or internal physiological changes. These responses are often complex and may involve concerted activity changes across circuits that are not physically connected. It is not well understood how neuromodulatory systems act across circuits to elicit complex behavioral responses. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by selectively modulating the activity of head and body wall motor neurons. NLP-12 modulation of the head and body wall motor circuits is generated through conditional involvement of alternate GPCR targets. The CKR-1 GPCR is highly expressed in the head motor circuit, and functions to enhance head bending and increase trajectory reorientations during local food searching, primarily through stimulatory actions on SMD head motor neurons. In contrast, NLP-12 activation of CKR-1 and CKR-2 GPCRs regulates body bending under basal conditions, primarily through actions on body wall motor neurons. Thus, locomotor responses to changing environmental conditions emerge from conditional NLP-12 stimulation of head or body wall motor neuron targets.

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Section: Ckr-1 Functions In the Smd Head Motor Neurons To Modulate Bomentioning

confidence: 99%

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

Ramachandran

Banerjee

Bhattacharya

et al. 2020

Preprint

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“…Models for other motor primitives, including head oscillation, head casting and body turning [58,[67][68][69][70] may be similarly constructed. With an understanding of individual modules, we are better positioned to use the connectome [28] as a road map to model how they are coordinated, such as the interaction between head oscillation and body undulation during forward and backward movements (figure 6a).…”

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

confidence: 99%

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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“…By contrast, the two merged lateral octant end plate regions on each side have significant differences from the dorso/ ventral octants: there are three additional classes of bilaterally symmetrical neurons (RMG, RMF and RMH), but no SMD or SMB neurons, which are four-way symmetrical. Other hints that the lateral endplate regions may have functions other than generating the predominantly dorso/ventral movements of EHMs comes from the observation that ablation of the dorsal and ventral RMEs increases the amplitude of EHMs, whereas ablation of the lateral RME neurons does not [31]. These observations suggest that it might be valid to simplify the study of circuitry that generates EHMs by focusing on the motor neurons in the two ventral and two dorsal octants and ignoring the four lateral octants.…”

Section: Circuits Most Likely To Be Involved In Generating Exploratormentioning

confidence: 99%

Clues to basis of exploratory behaviour of theC. eleganssnout from head somatotropy

White

2018

Phil. Trans. R. Soc. B

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Wave propagation during locomotory movements of is constrained to a single dorso/ventral plane. By contrast, the tip of the head (snout) can make rapid exploratory movements in all directions relative to the body axis. These extra degrees of freedom are probably important for animals to seek and identify desirable passages in the interstices of the three-dimensional matrix of soil particles, their usual habitat. The differences in degrees of freedom of movement between snout and body are reflected in the innervation of the musculature. Along the length of the body, the two quadrants of dorsal muscle receive common innervation as do the two quadrants of ventral muscle. By contrast, muscles in the snout have an octagonal arrangement of innervation. It is likely that the exploratory behaviour of the snout is mediated by octant-specific motor and sensory neurons, together with their associated interneurons. The well-defined anatomical structure and neural circuitry of the snout together with behavioural observations should facilitate the implementation of models of the neural basis of exploratory movements, which could lead to an understanding of the basis of this relatively complex behaviour, a behaviour that has similarities to foraging in some vertebrates.This article is part of a discussion meeting issue 'Connectome to behaviour: modelling at cellular resolution'.

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An extrasynaptic GABAergic signal modulates a pattern of forward movement in Caenorhabditis elegans

Cited by 50 publications

References 72 publications

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

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

Clues to basis of exploratory behaviour of theC. eleganssnout from head somatotropy

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