Extrasynaptic signaling enables an asymmetric juvenile motor circuit to produce a symmetric mature gait.

Bilaterians generate motor patterns with symmetries that correspond to their body plans. This is thought to arise from wiring symmetries in their motor circuitries. We show that juvenile C. elegans larva has an asymmetrically wired motor circuit, but they still generate bending pattern with dorsal-ventral symmetry. In this juvenile circuit, wiring between excitatory and inhibitory motor neurons drives and coordinates contraction of dorsal muscles with relaxation of ventral muscles, producing dorsal bends. Ventral bending is not driven by its own circuitry. Instead, ventral muscles are excited uniformly by premotor interneurons through extrasynaptic signaling, and ventral bends occur in entrainment to the activity of motor neurons for dorsal bends. During maturation, the juvenile motor circuit is replaced by two homologous motor circuits that separately generate dorsal and ventral bending. Our modeling reveals that the juvenile circuit configuration provides an adequate solution for an immature motor circuit to drive functional gait long before the animal matures.

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Distributed Rhythm Generators Underlie Caenorhabditis elegans Forward Locomotion

10.1101/141911 ◽

2017 ◽

Cited By ~ 1

Author(s):

Anthony D. Fouad ◽

Shelly Teng ◽

Julian R. Mark ◽

Alice Liu ◽

Pilar Alvarez-Illera ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Motor Neurons ◽

Animal Behavior ◽

Rhythm Generation ◽

Rhythmic Movements ◽

Neural Oscillators ◽

Motor Circuit ◽

C Elegans ◽

Body Regions ◽

Forward Locomotion

ABSTRACTCoordinated rhythmic movements are ubiquitous in animal behavior. In many organisms, chains of neural oscillators underlie the generation of these rhythms. In C. elegans, locomotor wave generation has been poorly understood; in particular, it is unclear where in the circuit rhythms are generated, and whether there exists more than one such generator. We used optogenetic and ablation experiments to probe the nature of rhythm generation in the locomotor circuit. We found that multiple sections of forward locomotor circuitry are capable of independently generating rhythms. By perturbing different components of the motor circuit, we localize the source of secondary rhythms to cholinergic motor neurons in the midbody. Using rhythmic optogenetic perturbation we demonstrate bidirectional entrainment of oscillations between different body regions. These results show that, as in many other vertebrates and invertebrates, the C. elegans motor circuit contains multiple oscillators that coordinate activity to generate behavior.

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

10.1101/2020.04.27.064550 ◽

2020 ◽

Author(s):

Shankar Ramachandran ◽

Navonil Banerjee ◽

Raja Bhattacharya ◽

Denis Touroutine ◽

Christopher M. Lambert ◽

...

Keyword(s):

Motor Neurons ◽

Adaptive Behavior ◽

Environmental Conditions ◽

Body Wall ◽

Behavioral Responses ◽

Physiological Changes ◽

C Elegans ◽

Motor Circuits ◽

Concerted Activity ◽

Stimulation Of

SUMMARYNeuromodulators 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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Interneuronal and motor patterns during crawling behavior of semi-intact leeches.

Journal of Experimental Biology ◽

10.1242/jeb.200.9.1369 ◽

1997 ◽

Vol 200 (9) ◽

pp. 1369-1381 ◽

Cited By ~ 2

Author(s):

A P Baader

Keyword(s):

Motor Neurons ◽

Behavior Pattern ◽

Activity Patterns ◽

Medicinal Leech ◽

Intracellular Recordings ◽

Motor Patterns ◽

Potential Oscillations ◽

Different Types ◽

Inhibitory Motor Neurons ◽

Membrane Potential Oscillations

Semi-intact tethered preparations were used to characterize neuronal activity patterns in midbody ganglia of the medicinal leech during crawling. Extra- and intracellular recordings were obtained from identified interneurons and from motor neurons of the longitudinal and circular muscles during crawling episodes. Coordinated activities of nine excitatory and inhibitory motor neurons of the longitudinal and circular muscles were recorded during the appropriate phases of crawling. Thus, during crawling, the leech uses motor output components known to contribute to other types of behavior, such as swimming or the shortening/local bending reflex. Interneurons with identified functions in these other types of behavior exhibit membrane potential oscillations that are in phase with the behavior pattern. Therefore, the recruitment of neuronal network elements during several types of behavior occurs not only at the motor neuron level but also involves interneurons. This applies even to some interneurons that were previously thought to have dedicated functions (such as cells 204 and 208 and the S cell). The function of neuronal circuitries in producing different types of behavior with a limited number of neurons is discussed.

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Identification of multiple distinct neurogenic motor patterns that can occur simultaneously in the guinea pig distal colon

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.00256.2018 ◽

2019 ◽

Vol 316 (1) ◽

pp. G32-G44 ◽

Cited By ~ 6

Author(s):

Marcello Costa ◽

Lauren J. Keightley ◽

Lukasz Wiklendt ◽

Timothy J. Hibberd ◽

John W. Arkwright ◽

...

Keyword(s):

Guinea Pig ◽

Motor Neurons ◽

Distal Colon ◽

Intraluminal Pressure ◽

Afferent Neurons ◽

Motor Patterns ◽

Primary Afferent Neurons ◽

Primary Afferent ◽

Cholinergic Interneurons ◽

Inhibitory Motor Neurons

In the guinea pig distal colon, nonpropulsive neurally mediated motor patterns have been observed in different experimental conditions. Isolated segments of guinea pig distal colon were used to investigate these neural mechanisms by simultaneously recording wall motion, intraluminal pressure, and smooth muscle electrical activity in different conditions of constant distension and in response to pharmacological agents. Three distinct neurally dependent motor patterns were identified: transient neural events (TNEs), cyclic motor complexes (CMC), and distal colon migrating motor complexes (DCMMC). These could occur simultaneously and were distinguished by their electrophysiological, mechanical, and pharmacological features. TNEs occurred at irregular intervals of ~3s, with bursts of action potentials at 9 Hz. They propagated orally at 12 cm/s via assemblies of ascending cholinergic interneurons that activated final excitatory and inhibitory motor neurons, apparently without involvement of stretch-sensitive intrinsic primary afferent neurons. CMCs occurred during maintained distension and consisted of clusters of closely spaced TNEs, which fused to cause high-frequency action potential firing at 7 Hz lasting ~10 s. They generated periodic pressure peaks mediated by stretch-sensitive intrinsic primary afferent neurons and by cholinergic interneurons. DCMMCs were generated by ongoing activity in excitatory motor neurons without apparent involvement of stretch-sensitive neurons, cholinergic interneurons, or inhibitory motor neurons. In conclusion, we have identified three distinct motor patterns that can occur concurrently in the isolated guinea pig distal colon. The mechanisms underlying the generation of these neural patterns likely involve recruitment of different populations of enteric neurons with distinct temporal activation properties.

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Ebf Activates Expression of a Cholinergic Locus in a Multipolar Motor Ganglion Interneuron Subtype in Ciona

Frontiers in Neuroscience ◽

10.3389/fnins.2021.784649 ◽

2021 ◽

Vol 15 ◽

Author(s):

Sydney Popsuj ◽

Alberto Stolfi

Keyword(s):

Motor Neurons ◽

Terminal Differentiation ◽

Cholinergic Neuron ◽

Gene Products ◽

Exact Role ◽

C Elegans ◽

Motor Circuits ◽

Functional Identities ◽

Type Specification ◽

Differentiation Gene

Conserved transcription factors termed “terminal selectors” regulate neuronal sub-type specification and differentiation through combinatorial transcriptional regulation of terminal differentiation genes. The unique combinations of terminal differentiation gene products in turn contribute to the functional identities of each neuron. One well-characterized terminal selector is COE (Collier/Olf/Ebf), which has been shown to activate cholinergic gene batteries in C. elegans motor neurons. However, its functions in other metazoans, particularly chordates, is less clear. Here we show that the sole COE ortholog in the non-vertebrate chordate Ciona robusta, Ebf, controls the expression of the cholinergic locus VAChT/ChAT in a single dorsal interneuron of the larval Motor Ganglion, which is presumed to be homologous to the vertebrate spinal cord. We propose that, while the function of Ebf as a regulator of cholinergic neuron identity conserved across bilaterians, its exact role may have diverged in different cholinergic neuron subtypes (e.g., interneurons vs. motor neurons) in chordate-specific motor circuits.

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Distributed rhythm generators underlie Caenorhabditis elegans forward locomotion

eLife ◽

10.7554/elife.29913 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 24

Author(s):

Anthony D Fouad ◽

Shelly Teng ◽

Julian R Mark ◽

Alice Liu ◽

Pilar Alvarez-Illera ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Motor Neurons ◽

Animal Behavior ◽

Rhythm Generation ◽

Rhythmic Movements ◽

Neural Oscillators ◽

Motor Circuit ◽

C Elegans ◽

Body Regions ◽

Forward Locomotion

Coordinated rhythmic movements are ubiquitous in animal behavior. In many organisms, chains of neural oscillators underlie the generation of these rhythms. In C. elegans, locomotor wave generation has been poorly understood; in particular, it is unclear where in the circuit rhythms are generated, and whether there exists more than one such generator. We used optogenetic and ablation experiments to probe the nature of rhythm generation in the locomotor circuit. We found that multiple sections of forward locomotor circuitry are capable of independently generating rhythms. By perturbing different components of the motor circuit, we localize the source of secondary rhythms to cholinergic motor neurons in the midbody. Using rhythmic optogenetic perturbation, we demonstrate bidirectional entrainment of oscillations between different body regions. These results show that, as in many other vertebrates and invertebrates, the C. elegans motor circuit contains multiple oscillators that coordinate activity to generate behavior.

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

eLife ◽

10.7554/elife.71747 ◽

2021 ◽

Vol 10 ◽

Author(s):

Shankar Ramachandran ◽

Navonil Banerjee ◽

Raja Bhattacharya ◽

Michele L Lemons ◽

Jeremy Florman ◽

...

Keyword(s):

Food Availability ◽

Motor Neurons ◽

Body Wall ◽

Neuron Activity ◽

C Elegans ◽

Motor Circuits ◽

Neuron Activation ◽

Concerted Activity ◽

G Protein Coupled ◽

Stimulation Of

Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.

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The Caenorhabditis elegans odr-2 Gene Encodes a Novel Ly-6-Related Protein Required for Olfaction

Genetics ◽

10.1093/genetics/157.1.211 ◽

2001 ◽

Vol 157 (1) ◽

pp. 211-224 ◽

Cited By ~ 1

Author(s):

Joseph H Chou ◽

Cornelia I Bargmann ◽

Piali Sengupta

Keyword(s):

Caenorhabditis Elegans ◽

Motor Neurons ◽

Amino Terminus ◽

Signaling Proteins ◽

Related Protein ◽

Olfactory Neurons ◽

Unique Role ◽

C Elegans ◽

Founding Member ◽

High Concentrations

Abstract Caenorhabditis elegans odr-2 mutants are defective in the ability to chemotax to odorants that are recognized by the two AWC olfactory neurons. Like many other olfactory mutants, they retain responses to high concentrations of AWC-sensed odors; we show here that these residual responses are caused by the ability of other olfactory neurons (the AWA neurons) to be recruited at high odor concentrations. odr-2 encodes a membrane-associated protein related to the Ly-6 superfamily of GPI-linked signaling proteins and is the founding member of a C. elegans gene family with at least seven other members. Alternative splicing of odr-2 yields three predicted proteins that differ only at the extreme amino terminus. The three isoforms have different promoters, and one isoform may have a unique role in olfaction. An epitope-tagged ODR-2 protein is expressed at high levels in sensory neurons, motor neurons, and interneurons and is enriched in axons. The AWC neurons are superficially normal in their development and structure in odr-2 mutants, but their function is impaired. Our results suggest that ODR-2 may regulate AWC signaling within the neuronal network required for chemotaxis.

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