scholarly journals Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

2016 ◽  
Author(s):  
Kevin M. Collins ◽  
Addys Bode ◽  
Robert W. Fernandez ◽  
Jessica E. Tanis ◽  
Jacob Brewer ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Neural Circuit ◽  
Feedback Inhibition ◽  
Rhythmic Activity ◽  
Egg Laying ◽  
The Body ◽  
Active State ◽  
Neuroendocrine Cells ◽  
C Elegans ◽  
Discrete Signals

AbstractLike many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl− channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.

scholarly journals Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Kevin M Collins ◽  
Addys Bode ◽  
Robert W Fernandez ◽  
Jessica E Tanis ◽  
Jacob C Brewer ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Neural Circuit ◽  
Feedback Inhibition ◽  
Rhythmic Activity ◽  
Egg Laying ◽  
The Body ◽  
Active State ◽  
Neuroendocrine Cells ◽  
C Elegans ◽  
Discrete Signals

Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.

scholarly journals Release-dependent feedback inhibition by a presynaptically localized ligand-gated anion channel

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Seika Takayanagi-Kiya ◽  
Keming Zhou ◽  
Yishi Jin
Keyword(s):  
Motor Neurons ◽  
Neurotransmitter Release ◽  
Neural Circuit ◽  
Feedback Inhibition ◽  
Release Kinetics ◽  
Anion Channel ◽  
C Elegans ◽  
Release Of Acetylcholine ◽  
Presynaptic Release

Presynaptic ligand-gated ion channels (LGICs) have long been proposed to affect neurotransmitter release and to tune the neural circuit activity. However, the understanding of their in vivo physiological action remains limited, partly due to the complexity in channel types and scarcity of genetic models. Here we report that C. elegans LGC-46, a member of the Cys-loop acetylcholine (ACh)-gated chloride (ACC) channel family, localizes to presynaptic terminals of cholinergic motor neurons and regulates synaptic vesicle (SV) release kinetics upon evoked release of acetylcholine. Loss of lgc-46 prolongs evoked release, without altering spontaneous activity. Conversely, a gain-of-function mutation of lgc-46 shortens evoked release to reduce synaptic transmission. This inhibition of presynaptic release requires the anion selectivity of LGC-46, and can ameliorate cholinergic over-excitation in a C. elegans model of excitation-inhibition imbalance. These data demonstrate a novel mechanism of presynaptic negative feedback in which an anion-selective LGIC acts as an auto-receptor to inhibit SV release.

scholarly journals The female-specific VC neurons are mechanically activated, feed-forward motor neurons that facilitate serotonin-induced egg laying in C. elegans

2020 ◽  
Author(s):  
Richard J. Kopchock ◽  
Bhavya Ravi ◽  
Addys Bode ◽  
Kevin M. Collins
Keyword(s):  
Muscle Contraction ◽  
Motor Neurons ◽  
Neural Circuit ◽  
Egg Laying ◽  
Muscle Contractility ◽  
C Elegans ◽  
Optogenetic Stimulation ◽  
Vulval Muscle ◽  
Female Specific ◽  
Stimulation Of

AbstractSuccessful execution of behavior requires the coordinated activity and communication between multiple cell types. Studies using the relatively simple neural circuits of invertebrates have helped to uncover how conserved molecular and cellular signaling events shape animal behavior. To understand the mechanisms underlying neural circuit activity and behavior, we have been studying a simple circuit that drives egg-laying behavior in the nematode worm C. elegans. Here we show that the female-specific, Ventral C (VC) motoneurons are required for vulval muscle contractility and egg laying in response to serotonin. Ca2+ imaging experiments show the VCs are active during times of vulval muscle contraction and vulval opening, and optogenetic stimulation of the VCs promotes vulval muscle Ca2+ activity. However, while silencing of the VCs does not grossly affect steady-state egg-laying behavior, VC silencing does block egg laying in response to serotonin and increases the failure rate of egg-laying attempts. Signaling from the VCs facilitates full vulval muscle contraction and opening of the vulva for efficient egg laying. We also find the VCs are mechanically activated in response to vulval opening. Optogenetic stimulation of the vulval muscles is sufficient to drive VC Ca2+ activity and requires muscle contractility, showing the presynaptic VCs and the postsynaptic vulval muscles can mutually excite each other. Together, our results demonstrate that the VC neurons facilitate efficient execution of egg-laying behavior by coordinating postsynaptic muscle contractility in response to serotonin and mechanosensory feedback.

scholarly journals Screening for Presenilin Inhibitors Using the Free-Living Nematode, Caenorhabditis elegans

2004 ◽  
Vol 9 (2) ◽  
pp. 147-152 ◽  
Author(s):  
Brenda R. Ellerbrock ◽  
Eileen M. Coscarelli ◽  
Mark E. Gurney ◽  
Timothy G. Geary
Keyword(s):  
Caenorhabditis Elegans ◽  
High Throughput Screening ◽  
Screening Method ◽  
Genetic System ◽  
Body Cavity ◽  
Egg Laying ◽  
The Body ◽  
Loss Of Function ◽  
C Elegans ◽  
Automated Method

Caenorhabditis elegans contains 3 homologs of presenilin genes that are associated with Alzheimer s disease. Loss-of-function mutations in C. elegans genes cause a defect in egg laying. In humans, loss of presenilin-1 (PS1) function reduces amyloid-beta peptide processing from the amyloid protein precursor. Worms were screened for compounds that block egg laying, phenocopying presenilin loss of function. To accommodate even relatively high throughput screening, a semi-automated method to quantify egg laying was devised by measuring the chitinase released into the culture medium. Chitinase is released by hatching eggs, but little is shed into the medium from the body cavity of a hermaphrodite with an egg laying deficient ( egl) phenotype. Assay validation involved measuring chitinase release from wild-type C. elegans (N2 strain), sel-12 presenilin loss-of-function mutants, and 2 strains of C. elegans with mutations in the egl-36K+ channel gene. Failure to find specific presenilin inhibitors in this collection likely reflects the small number of compounds tested, rather than a flaw in screening strategy. Absent defined biochemical pathways for presenilin, this screening method, which takes advantage of the genetic system available in C. elegans and its historical use for anthelminthic screening, permits an entry into mechanism-based discovery of drugs for Alzheimer s disease. ( Journal of Biomolecular Screening 2004:147-152)

scholarly journals GABAergic motor neurons bias locomotor decision-making in C. elegans

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Ping Liu ◽  
Bojun Chen ◽  
Zhao-Wen Wang
Keyword(s):  
Decision Making ◽  
Motor Neurons ◽  
Gaba Receptor ◽  
Single Neuron ◽  
Neural Circuit ◽  
Electrical Coupling ◽  
C Elegans ◽  
Sensory Modalities ◽  
Motor Information ◽  
Molecular Bases

Abstract Proper threat-reward decision-making is critical to animal survival. Emerging evidence indicates that the motor system may participate in decision-making but the neural circuit and molecular bases for these functions are little known. We found in C. elegans that GABAergic motor neurons (D-MNs) bias toward the reward behavior in threat-reward decision-making by retrogradely inhibiting a pair of premotor command interneurons, AVA, that control cholinergic motor neurons in the avoidance neural circuit. This function of D-MNs is mediated by a specific ionotropic GABA receptor (UNC-49) in AVA, and depends on electrical coupling between the two AVA interneurons. Our results suggest that AVA are hub neurons where sensory inputs from threat and reward sensory modalities and motor information from D-MNs are integrated. This study demonstrates at single-neuron resolution how motor neurons may help shape threat-reward choice behaviors through interacting with other neurons.

scholarly journals Electric Egg-Laying: Effect of Electric Field in a Microchannel on C. elegans Egg-Laying Behavior

2020 ◽  
Author(s):  
Khaled Youssef ◽  
Daphne Archonta ◽  
Terrance J. Kubiseski ◽  
Anurag Tandon ◽  
Pouya Rezai
Keyword(s):  
Electric Field ◽  
Neural Circuit ◽  
Response Duration ◽  
Egg Laying ◽  
Fluorescent Imaging ◽  
The Novel ◽  
Neural Basis ◽  
C Elegans ◽  
Intracellular Calcium Dynamics ◽  
Reduced Rate

ABSTRACTIn this paper, the novel effect of electric field (EF) on adult C. elegans egg-laying in a microchannel is discovered and correlated with neural and muscular activities. The quantitative effects of worm aging and EF strength, direction, and exposure duration on egg-laying is studied phenotypically using egg-count, body length, head movement, and transient neuronal activity readouts. Electric egg-laying rate increases significantly when worms face the anode and the response is EF-dependent, i.e. stronger (6V/cm) and longer EF (40s) exposure result in a shorter egg laying response duration. Worm aging significantly deteriorates the electric egg-laying behaviour with 88% decrease in the egg-count from Day-1 to Day-4 post young-adult stage. Fluorescent imaging of intracellular calcium dynamics in the main parts of the egg-laying neural circuit demonstrate the involvement and sensitivity of the serotonergic hermaphrodite specific neurons (HSNs), vulva muscles, and ventral cord neurons to the EF. HSN mutation also results in a reduced rate of electric egg-laying allowing the use of this technique for cellular screening and mapping of the neural basis of electrosensation in C. elegans. This novel assay can be parallelized and performed in a high-throughput manner for drug and gene screening applications.

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 Optogenetic analysis of GABAB receptor signaling in Caenorhabditis elegans motor neurons

2011 ◽  
Vol 106 (2) ◽  
pp. 817-827 ◽  
Author(s):  
Christian Schultheis ◽  
Martin Brauner ◽  
Jana F. Liewald ◽  
Alexander Gottschalk
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Gabab Receptor ◽  
Feedback Inhibition ◽  
Cholinergic Neurons ◽  
Gaba Release ◽  
The Body ◽  
Linear Feedback ◽  
Locomotion Behavior ◽  
Contraction And Relaxation

In the nervous system, a perfect balance of excitation and inhibition is required, for example, to enable coordinated locomotion. In Caenorhabditis elegans, cholinergic and GABAergic motor neurons (MNs) effect waves of contralateral muscle contraction and relaxation. Cholinergic MNs innervate muscle as well as GABAergic MNs, projecting to the opposite side of the body, at dyadic synapses. Only a few connections exist from GABAergic to cholinergic MNs, emphasizing that GABA signaling is mainly directed toward muscle. Yet, a GABAB receptor comprising GBB-1 and GBB-2 subunits, expressed in cholinergic MNs, was shown to affect locomotion, likely by feedback inhibition of cholinergic MNs in response to spillover GABA. In the present study, we examined whether the GBB-1/2 receptor could also affect short-term plasticity in cholinergic MNs with the use of channelrhodopsin-2-mediated photostimulation of GABAergic and cholinergic neurons. The GBB-1/2 receptor contributes to acute body relaxation, evoked by photoactivation of GABAergic MNs, and to effects of GABA on locomotion behavior. Loss of the plasma membrane GABA transporter SNF-11, as well as acute photoevoked GABA release, affected cholinergic MN function in opposite directions. Prolonged stimulation of GABA MNs had subtle effects on cholinergic MNs, depending on stimulus duration and gbb-2. Thus GBB-1/2 receptors serve mainly for linear feedback inhibition of cholinergic MNs but also evoke minor plastic changes.

Identified neurons in C. elegans coexpress vesicular transporters for acetylcholine and monoamines

2001 ◽  
Vol 280 (6) ◽  
pp. C1616-C1622 ◽  
Author(s):  
Janet S. Duerr ◽  
Jennifer Gaskin ◽  
James B. Rand
Keyword(s):  
Motor Neurons ◽  
Choline Acetyltransferase ◽  
Egg Laying ◽  
Vesicular Acetylcholine Transporter ◽  
Vesicular Monoamine Transporter ◽  
Monoamine Transporter ◽  
C Elegans ◽  
Vesicular Transporters ◽  
The Individual

We have identified four neurons (VC4, VC5, HSNL, HSNR) in Caenorhabditis elegans adult hermaphrodites that express both the vesicular acetylcholine transporter and the vesicular monoamine transporter. All four of these cells are motor neurons that innervate the egg-laying muscles of the vulva. In addition, they all express choline acetyltransferase, the synthetic enzyme for acetylcholine. The distributions of the vesicular acetylcholine transporter and the vesicular monoamine transporter are not identical within the individual cells. In mutants deficient for either of these transporters, there is no apparent compensatory change in the expression of the remaining transporter. This is the first report of neurons that express two different vesicular neurotransmitter transporters in vivo.

scholarly journals Author response: Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

2016 ◽  
Author(s):  
Kevin M Collins ◽  
Addys Bode ◽  
Robert W Fernandez ◽  
Jessica E Tanis ◽  
Jacob C Brewer ◽  
...  
Keyword(s):  
Feedback Inhibition ◽  
Egg Laying ◽  
Author Response ◽  
C Elegans
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