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

eLife ◽  
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.

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

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.

scholarly journals Descending octopaminergic neurons modulate sensory-evoked activity of thoracic motor neurons in stick insects

2019 ◽  
Vol 122 (6) ◽  
pp. 2388-2413 ◽  
Author(s):  
Thomas Stolz ◽  
Max Diesner ◽  
Susanne Neupert ◽  
Martin E. Hess ◽  
Estefania Delgado-Betancourt ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Stick Insect ◽  
Neuron Activity ◽  
Sense Organs ◽  
Descending Neurons ◽  
Walking Activity ◽  
Stick Insects ◽  
Evoked Activity ◽  
Sensory Evoked ◽  
Stimulation Of

Neuromodulatory neurons located in the brain can influence activity in locomotor networks residing in the spinal cord or ventral nerve cords of invertebrates. How inputs to and outputs of neuromodulatory descending neurons affect walking activity is largely unknown. With the use of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and immunohistochemistry, we show that a population of dorsal unpaired median (DUM) neurons descending from the gnathal ganglion to thoracic ganglia of the stick insect Carausius morosus contains the neuromodulatory amine octopamine. These neurons receive excitatory input coupled to the legs’ stance phases during treadmill walking. Inputs did not result from connections with thoracic central pattern-generating networks, but, instead, most are derived from leg load sensors. In excitatory and inhibitory retractor coxae motor neurons, spike activity in the descending DUM (desDUM) neurons increased depolarizing reflexlike responses to stimulation of leg load sensors. In these motor neurons, descending octopaminergic neurons apparently functioned as components of a positive feedback network mainly driven by load-detecting sense organs. Reflexlike responses in excitatory extensor tibiae motor neurons evoked by stimulations of a femur-tibia movement sensor either are increased or decreased or were not affected by the activity of the descending neurons, indicating different functions of desDUM neurons. The increase in motor neuron activity is often accompanied by a reflex reversal, which is characteristic for actively moving animals. Our findings indicate that some descending octopaminergic neurons can facilitate motor activity during walking and support a sensory-motor state necessary for active leg movements. NEW & NOTEWORTHY We investigated the role of descending octopaminergic neurons in the gnathal ganglion of stick insects. The neurons become active during walking, mainly triggered by input from load sensors in the legs rather than pattern-generating networks. This report provides novel evidence that octopamine released by descending neurons on stimulation of leg sense organs contributes to the modulation of leg sensory-evoked activity in a leg motor control system.

scholarly journals The UBR-1 Ubiquitin Ligase Regulates Glutamate Metabolism to Generate Coordinated Motor Pattern in C. elegans

2018 ◽  
Author(s):  
Jyothsna Chitturi ◽  
Wesley Hung ◽  
Anas M. Abdel Rahman ◽  
Min Wu ◽  
Maria A. Lim ◽  
...  
Keyword(s):  
Protein Degradation ◽  
Motor Neurons ◽  
Ubiquitin Ligase ◽  
Motor Pattern ◽  
Motor Deficit ◽  
Neuron Activity ◽  
Glutamate Metabolism ◽  
E3 Ligases ◽  
C Elegans ◽  
Glutamate Level

AbstractUBR1 is an E3 ubiquitin ligase best known for its ability to target protein degradation by the N-end rule. The physiological functions of UBR family proteins, however, remain not fully understood. We found that the functional loss of C. elegans UBR-1 leads to a specific motor deficit: when adult animals generate reversal movements, A-class motor neurons exhibit synchronized activation, preventing body bending. This motor deficit is rescued by removing GOT-1, a transaminase that converts aspartate to glutamate. Both UBR-1 and GOT-1 are expressed and critically required in premotor interneurons of the reversal motor circuit to regulate the motor pattern. ubr-1 and got-1 mutants exhibit elevated and decreased glutamate level, respectively. These results raise an intriguing possibility that UBR proteins regulate glutamate metabolism, which is critical for neuronal development and signaling.Author SummaryUbiquitin-mediated protein degradation is central to diverse biological processes. The selection of substrates for degradation is carried out by the E3 ubiquitin ligases, which target specific groups of proteins for ubiquitination. The human genome encodes hundreds of E3 ligases; many exhibit sequence conservation across animal species, including one such ligase called UBR1. Patients carrying mutations in UBR1 exhibit severe systemic defects, but the biology behinds UBR1’s physiological function remains elusive. Here we found that the C. elegans UBR-1 regulates glutamate level. When UBR-1 is defective, C. elegans exhibits increased glutamate; this leads to synchronization of motor neuron activity, hence defective locomotion when animals reach adulthood. UBR1-mediated glutamate metabolism may contribute to the physiological defects of UBR1 mutations.

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

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.

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

2021 ◽  
Author(s):  
Yangning Lu ◽  
Tosif Ahamed ◽  
Ben Mulcahy ◽  
Daniel Witvliet ◽  
Sihui Asuka Guan ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Motor Patterns ◽  
Motor Circuit ◽  
C Elegans ◽  
Motor Circuits ◽  
Inhibitory Motor Neurons ◽  
Functional Gait ◽  
Circuit Configuration

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.

Octopamine induces steady-state reflex reversal in crayfish thoracic ganglia

1996 ◽  
Vol 76 (1) ◽  
pp. 93-108 ◽  
Author(s):  
P. Skorupski
Keyword(s):  
Spontaneous Activity ◽  
Motor Neurons ◽  
Motor Output ◽  
Reflex Response ◽  
Neuron Activity ◽  
Chordotonal Organ ◽  
Nerve Activity ◽  
Group 2 ◽  
Stimulation Of ◽  
Group 1

1. This paper investigates the effect of octopamine on spontaneous and reflex motor output of crayfish leg motor neurons. Octopamine modulated spontaneous activity, both rhythmic and tonic, and dramatically modulated the pattern of reflex motor output elicited by stimulating identified proprioceptors of the basal limb. 2. Spontaneous reciprocal motor patterns, involving alternating bursts of promotor and remotor motor neuron activity, were reversibly abolished by octopamine. The threshold concentration for this effect was approximately 1 microM. 3. At concentrations greater than approximately 10 microM octopamine inhibited spontaneous promotor nerve activity in both bursting and nonbursting preparations. In some experiments promotor inhibition was correlated with the induction of tonic remotor nerve activity. The EC50 for complete inhibition of promotor nerve activity by octopamine was 20-30 microM. 4. Reflexes mediated by two basal limb proprioceptors, the thoracocoxal muscle receptor organ (TCMRO; which signals leg promotion) and the thoracocoxal chordotonal organ (TCCO; which signals leg remotion) were analyzed in a number of promotor and remotor motor neurons. In both cases assistance reflexes (excitation of promotors by the TCCO and remotors by the TCMRO) were restricted to subgroups of the motor pool. Among remotor motor neurons, the first two units recruited during bursts of spontaneous activity were members of the assistance reflex group (group 1). A third unit, sometimes recruited during more intense spontaneous bursts, was excited by TCCO stimulation and was therefore a member of the resistance reflex group (group 2). Other resistance group remotors were also excited by the TCCO, but this input normally remained subthreshold. 5. Stimulation of the TCCO afferent nerve elicited excitatory postsynaptic potentials (EPSPs) in group 2 (resistance group) remotor motor neurons at a latency compatible with a monosynaptic connection. The same stimulation excited group 1 (assistance group) promotor motor neurons, but at a greater and more variable latency. Thus the remotor resistance reflex from the TCCO is probably monosynaptic, but the promotor assistance reflex, also elicited by TCCO stimulation, is likely to be di- or polysynaptic. Assistance group (group 1) remotor motor neurons are inhibited by mechanical stimulation of the TCCO, or electrical stimulation of its nerve. 6. Octopamine had selective effects on individual remotor units. First, assistance group remotor motor neurons were affected in two ways. One unit was inhibited, so that reflex spiking in response to TCMRO stimulation was abolished. A second unit was not inhibited, but its reflex response mode changed, so that instead of responding to TCMRO input with an assistance reflex, it responded to TCCO input with a resistance reflex. Second, among motor neurons that normally respond to TCCO input with resistance reflexes, these responses were enhanced by octopamine. 7. Promotor motor neurons were inhibited by octopamine and reflex responses were also affected selectively. Responses to TCCO input (assistance reflexes) were abolished; whereas, responses to TCMRO input (resistance reflexes) were relatively less affected. 8. Intracellular recordings revealed that the majority of remotor motor neurons depolarized in the presence of octopamine. In preparations where these could be classified on the basis of TCMRO/ TCCO inputs, all were identified as group 2 (resistance group). A minority of remotor motor neurons were hyperpolarized by octopamine. All of these were identified as group 1 (assistance group), with strong TCMRO input. 9. The majority of promotor motor neurons were depolarized by octopamine. This depolarization was nevertheless inhibitory since it reversed slightly positive to rest and was associated with a substantial fall in inp

scholarly journals Rhodopsin-based voltage imaging tools for use in excitable cells of Caenorhabditis elegans

2019 ◽  
Author(s):  
Negin Azimi Hashemi ◽  
Amelie C. F. Bergs ◽  
Rebecca Scheiwe ◽  
Wagner Steuer Costa ◽  
Jana F. Liewald ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Body Wall ◽  
Ca 125 ◽  
Excitable Cells ◽  
Voltage Imaging ◽  
C Elegans ◽  
Non Invasive ◽  
All Optical ◽  
Body Wall Muscles ◽  
Voltage Dynamics

AbstractGenetically encoded voltage indicators (GEVIs) based on microbial rhodopsins utilize the voltage-sensitive fluorescence of the all-trans retinal (ATR) cofactor, while in electrochromic (eFRET) sensors, donor fluorescence drops when the rhodopsin acts as depolarization-sensitive acceptor. We systematically assessed Arch(D95N), Archon, and QuasAr, as well as the eFRET sensors MacQ-mCitrine and QuasAr-mOrange, in C. elegans. ATR-bearing rhodopsins reported on voltage changes in body wall muscles (BWMs) and the pharynx, the feeding organ, where Arch(D95N) showed ca. 125 % ΔF/F increase per 100 mV. The ATR fluorescence is very dim, however, using the retinal analog dimethylaminoretinal (DMAR), it was boosted 250-fold. eFRET sensors provided sensitivities of 45 % to 78 % ΔF/F per 100 mV, induced by BWM action potentials (APs). All sensors reported differences in muscle depolarization induced by a voltage-gated Ca2+-channel mutant. Optogenetically evoked de-or hyperpolarization of motor neurons increased or eliminated AP activity and caused a rise or drop in BWM sensor fluorescence. Last, we could analyze voltage dynamics across the entire pharynx, showing uniform depolarization but compartmentalized repolarization of anterior and posterior parts. Our work establishes all-optical, non-invasive electrophysiology in intact C. elegans.

scholarly journals Hunger neurons drive feeding through a sustained, positive reinforcement signal

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Yiming Chen ◽  
Yen-Chu Lin ◽  
Christopher A Zimmerman ◽  
Rachel A Essner ◽  
Zachary A Knight
Keyword(s):  
Positive Reinforcement ◽  
Neural Mechanisms ◽  
Energy Deficit ◽  
Neuron Activity ◽  
Optogenetic Stimulation ◽  
Neuron Activation ◽  
Positive Valence ◽  
Stimulation Of ◽  
Hunger Drive

The neural mechanisms underlying hunger are poorly understood. AgRP neurons are activated by energy deficit and promote voracious food consumption, suggesting these cells may supply the fundamental hunger drive that motivates feeding. However recent in vivo recording experiments revealed that AgRP neurons are inhibited within seconds by the sensory detection of food, raising the question of how these cells can promote feeding at all. Here we resolve this paradox by showing that brief optogenetic stimulation of AgRP neurons before food availability promotes intense appetitive and consummatory behaviors that persist for tens of minutes in the absence of continued AgRP neuron activation. We show that these sustained behavioral responses are mediated by a long-lasting potentiation of the rewarding properties of food and that AgRP neuron activity is positively reinforcing. These findings reveal that hunger neurons drive feeding by transmitting a positive valence signal that triggers a stable transition between behavioral states.

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