scholarly journals Excitatory Motor Neurons are Local Central Pattern Generators in an Anatomically Compressed Motor Circuit for Reverse Locomotion

2017 ◽  
Author(s):  
Shangbang Gao ◽  
Sihui Asuka Guan ◽  
Anthony D. Fouad ◽  
Jun Meng ◽  
Taizo Kawano ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Calcium Imaging ◽  
Central Pattern Generators ◽  
Oscillatory Activity ◽  
Intrinsic Activity ◽  
C Elegans ◽  
Class A ◽  
Cell Ablation ◽  
Pattern Generators

AbstractCentral pattern generators are cell‐ or network-driven oscillators that underlie motor rhythmicity. The existence and identity of C. elegans CPGs remain unknown. Through cell ablation, electrophysiology, and calcium imaging, we identified oscillators for reverse locomotion. We show that the cholinergic and excitatory class A motor neurons exhibit intrinsic and oscillatory activity, and such an activity can drive reverse locomotion without premotor interneurons. Regulation of their oscillatory activity, either through effecting an endogenous constituent of oscillation, the P/Q/N high voltage-activated calcium channel UNC-2, or, via dual regulation – inhibition and activation ‐ by the descending premotor interneurons AVA, determines the propensity, velocity, and sustention of reverse locomotion. Thus, the reversal motor executors themselves serve as oscillators; regulation of their intrinsic activity controls the reversal motor state. These findings exemplify anatomic and functional compression: motor executors integrate the role of rhythm generation in a locomotor network that is constrained by small cell numbers.

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

2018 ◽  
Vol 373 (1758) ◽  
pp. 20170370 ◽  
Author(s):  
Quan Wen ◽  
Shangbang Gao ◽  
Mei Zhen
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
Oscillatory Activity ◽  
C Elegans ◽  
Ventral Cord ◽  
Small Neuron ◽  
Motor Rhythm ◽  
Pattern Generators

The intrinsic oscillatory activity of central pattern generators underlies motor rhythm. We review and discuss recent findings that address the origin of Caenorhabditis elegans 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 C. elegans sensorimotor system. C. elegans 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. C. elegans 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 C. elegans at cellular resolution’.

scholarly journals Excitatory motor neurons are local oscillators for backward locomotion

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Shangbang Gao ◽  
Sihui Asuka Guan ◽  
Anthony D Fouad ◽  
Jun Meng ◽  
Taizo Kawano ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Oscillatory Activity ◽  
Intrinsic Activity ◽  
Chemical Synapse ◽  
C Elegans ◽  
Cell Ablation ◽  
State Dependent ◽  
Evolutionarily Conserved ◽  
Dependent Inhibition ◽  
Descending Interneurons

Cell- or network-driven oscillators underlie motor rhythmicity. The identity of C. elegans oscillators remains unknown. Through cell ablation, electrophysiology, and calcium imaging, we show: (1) forward and backward locomotion is driven by different oscillators; (2) the cholinergic and excitatory A-class motor neurons exhibit intrinsic and oscillatory activity that is sufficient to drive backward locomotion in the absence of premotor interneurons; (3) the UNC-2 P/Q/N high-voltage-activated calcium current underlies A motor neuron’s oscillation; (4) descending premotor interneurons AVA, via an evolutionarily conserved, mixed gap junction and chemical synapse configuration, exert state-dependent inhibition and potentiation of A motor neuron’s intrinsic activity to regulate backward locomotion. Thus, motor neurons themselves derive rhythms, which are dually regulated by the descending interneurons to control the reversal motor state. These and previous findings exemplify compression: essential circuit properties are conserved but executed by fewer numbers and layers of neurons in a small locomotor network.

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

2018 ◽  
Vol 2 (3) ◽  
pp. 323-343 ◽  
Author(s):  
Erick O. Olivares ◽  
Eduardo J. Izquierdo ◽  
Randall D. Beer
Keyword(s):  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Computational Models ◽  
Neural Circuit ◽  
Central Pattern Generators ◽  
C Elegans ◽  
Segmentation Analysis ◽  
Pattern Generators ◽  
Neural Unit

C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circuit that supports intrinsic network oscillations. With a fully reconstructed connectome, the question of whether it is possible to have a CPG in the ventral nerve cord (VNC) of C. elegans can be answered through computational models. We modeled a repeating neural unit based on segmentation analysis of the connectome. We then used an evolutionary algorithm to determine the unknown physiological parameters of each neuron so as to match the features of the neural traces of the worm during forward and backward locomotion. We performed 1,000 evolutionary runs and consistently found configurations of the neural circuit that produced oscillations matching the main characteristic observed in experimental recordings. In addition to providing an existence proof for the possibility of a CPG in the VNC, we suggest a series of testable hypotheses about its operation. More generally, we show the feasibility and fruitfulness of a methodology to study behavior based on a connectome, in the absence of complete neurophysiological details.

scholarly journals Functionally asymmetric motor neurons coordinate locomotion of Caenorhabditis elegans

2018 ◽  
Author(s):  
Oleg Tolstenkov ◽  
Petrus Van der Auwera ◽  
Jana F. Liewald ◽  
Wagner Steuer Costa ◽  
Olga Bazhanova ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Gap Junctions ◽  
Motor Neurons ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Body Wave ◽  
Central Pattern Generators ◽  
Physiological Data ◽  
C Elegans ◽  
Pattern Generators

SummaryInvertebrate nervous systems are valuable models for fundamental principles of the control of behavior. Ventral nerve cord (VNC) motor neurons in Caenorhabditis elegans represent one of the best studied locomotor circuits, with known connectivity and functional information about most of the involved neuron classes. However, for one of those, the AS motor neurons (AS MNs), no physiological data is available. Combining specific expression and selective illumination, we precisely targeted AS MNs by optogenetics and addressed their role in the locomotion circuit. After photostimulation, AS MNs induce currents in post-synaptic body wall muscles (BWMs), exhibiting an initial asymmetry of excitatory output. This may facilitate complex regulatory motifs for adjusting direction during navigation. By behavioral and photo-inhibition experiments, we show that AS MNs contribute to propagation of the antero-posterior body wave during locomotion. By Ca2+-imaging in AS MNs and in their synaptic partners, we also reveal that AS MNs play a role in mediating forward and backward locomotion by integrating activity of premotor interneurons (PINs), as well as in coordination of the dorso-ventral body wave. AS MNs do not exhibit pacemaker properties, but potentially gate VNC central pattern generators (CPGs), as indicated by ceasing of locomotion when AS MNs are hyperpolarized. AS MNs provide positive feedback to the PIN AVA via gap junctions, a feature found also in other locomotion circuits. In sum, AS MNs have essential roles in coordinating locomotion, combining several functions, and emphasizing the compressed nature of the C. elegans nervous system in comparison to higher animals.HighlightsA class of motor neurons with unidentified function – AS cholinergic motor neurons - was characterized in C. elegans.AS neurons show asymmetry in both input and output and are specialized in coordination of dorso-ventral undulation bends.AS neurons mediate antero-posterior propagation of the undulatory body wave during locomotion.AS neurons integrate signals for forward and reverse locomotion from premotor interneurons and may gate ventral nerve cord central pattern generators (CPGs) via gap junctions.

scholarly journals The Functional Connectivity between the Locust Leg Pattern Generating Networks and the Subesophageal Ganglion Higher Motor Center

2017 ◽  
Author(s):  
Daniel Knebel ◽  
Jan Rillich ◽  
Leonard Nadler ◽  
Hans-Joachim Pflueger ◽  
Amir Ayali
Keyword(s):  
Motor Neurons ◽  
Central Pattern Generators ◽  
Subesophageal Ganglion ◽  
Motor Center ◽  
Coupling Pattern ◽  
Descending Interneurons ◽  
Pattern Generators ◽  
Leg Movements

AbstractInteractions among different neuronal circuits are essential for adaptable coordinated behavior. Specifically, higher motor centers and central pattern generators (CPGs) induce rhythmic leg movements that act in concert in the control of locomotion. Here we explored the relations between the subesophageal ganglion (SEG) and thoracic leg CPGs in the desert locust. Backfill staining revealed about 300 SEG descending interneurons (DINs) and some overlap with the arborization of DINs and leg motor neurons. In accordance, in in-vitro preparations, electrical stimulation applied to the SEG excited these neurons, and in some cases also induced CPGs activity. Additionally, we found that the SEG regulates the coupling pattern among the CPGs: when the CPGs were activated pharmacologically, inputs from the SEG were able to synchronize contralateral CPGs. This motor output was correlated to the firing of SEG descending and local interneurons. Altogether, these findings point to a role of the SEG in both activating leg CPGs and in coordinating their oscillations, and suggest parallels between the SEG and the brainstem of vertebrates.

Sensory regulation of quadrupedal locomotion: a top-down or bottom-up control system?

2012 ◽  
Vol 108 (3) ◽  
pp. 709-711 ◽  
Author(s):  
Yann Thibaudier ◽  
Marie-France Hurteau
Keyword(s):  
Control System ◽  
Central Pattern Generators ◽  
Top Down ◽  
Bottom Up ◽  
Sensory Inputs ◽  
Sensory Regulation ◽  
Before And After ◽  
Pattern Generators

Propriospinal pathways are thought to be critical for quadrupedal coordination by coupling cervical and lumbar central pattern generators (CPGs). However, the mechanisms involved in relaying information between girdles remain largely unexplored. Using an in vitro spinal cord preparation in neonatal rats, Juvin and colleagues ( Juvin et al. 2012 ) have recently shown sensory inputs from the hindlimbs have greater influence on forelimb CPGs than forelimb sensory inputs on hindlimb CPGs, in other words, a bottom-up control system. However, results from decerebrate cats suggest a top-down control system. It may be that both bottom-up and top-down control systems exist and that the dominance of one over the other is task or context dependent. As such, the role of sensory inputs in controlling quadrupedal coordination before and after injury requires further investigation.

scholarly journals Pan-neuronal screening in Caenorhabditis elegans reveals asymmetric dynamics of AWC neurons is critical for thermal avoidance behavior

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Ippei Kotera ◽  
Nhat Anh Tran ◽  
Donald Fu ◽  
Jimmy HJ Kim ◽  
Jarlath Byrne Rodgers ◽  
...  
Keyword(s):  
Avoidance Behavior ◽  
Calcium Imaging ◽  
Functional Screening ◽  
Noxious Heat ◽  
Thermal Nociception ◽  
C Elegans ◽  
Low Efficiency ◽  
Behavioral Transition ◽  
Thermal Stimuli

Understanding neural functions inevitably involves arguments traversing multiple levels of hierarchy in biological systems. However, finding new components or mechanisms of such systems is extremely time-consuming due to the low efficiency of currently available functional screening techniques. To overcome such obstacles, we utilize pan-neuronal calcium imaging to broadly screen the activity of the C. elegans nervous system in response to thermal stimuli. A single pass of the screening procedure can identify much of the previously reported thermosensory circuitry as well as identify several unreported thermosensory neurons. Among the newly discovered neural functions, we investigated in detail the role of the AWCOFF neuron in thermal nociception. Combining functional calcium imaging and behavioral assays, we show that AWCOFF is essential for avoidance behavior following noxious heat stimulation by modifying the forward-to-reversal behavioral transition rate. We also show that the AWCOFF signals adapt to repeated noxious thermal stimuli and quantify the corresponding behavioral adaptation.

Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator of Aplysia

2007 ◽  
Vol 98 (1) ◽  
pp. 29-42 ◽  
Author(s):  
Geidy E. Serrano ◽  
Clarissa Martínez-Rubio ◽  
Mark W. Miller
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
Ingestive Behavior ◽  
Membrane Properties ◽  
Motor Patterns ◽  
Effector System ◽  
Bilateral Pair ◽  
Pattern Generators ◽  
Specific Phase

Multifunctional central pattern generators (CPGs) are circuits of neurons that can generate manifold actions from a single effector system. This study examined a bilateral pair of pharyngeal motor neurons, designated B67, that participate in the multifunctional feeding network of Aplysia californica. Fictive buccal motor programs (BMPs) were elicited with four distinct stimulus paradigms to assess the activity of B67 during ingestive versus egestive patterns. In both classes of programs, B67 fired during the phase of radula protraction and received a potent inhibitory postsynaptic potential (IPSP) during fictive radula retraction. When programs were ingestive, the retraction phase IPSP exhibited a depolarizing sag and was followed by a postinhibitory rebound (PIR) that could generate a postretraction phase of impulse activity. When programs were egestive, the depolarizing sag potential and PIR were both diminished or were not present. Examination of the membrane properties of B67 disclosed a cesium-sensitive depolarizing sag, a corresponding Ih-like current, and PIR in its responses to hyperpolarizing pulses. Direct IPSPs originating from the influential CPG retraction phase interneuron B64 were also found to activate the sag potential and PIR of B67. Dopamine, a modulator that can promote ingestive behavior in this system, enhanced the sag potential, Ih-like current, and PIR of B67. Finally, a pharyngeal muscle contraction followed the radula retraction phase of ingestive, but not egestive motor patterns. It is proposed that regulation of the intrinsic properties of this motor neuron can contribute to generating a program-specific phase of motor activity.

scholarly journals Neuroendocrine Modulation Sustains the C. elegans Forward Motor State

2016 ◽  
Author(s):  
Maria A. Lim ◽  
Jyothsna Chitturi ◽  
Valeriya Laskova ◽  
Jun Meng ◽  
Daniel Findeis ◽  
...  
Keyword(s):  
Electron Microscopy ◽  
Calcium Imaging ◽  
Neural Circuit ◽  
Transcriptome Profiling ◽  
Behavioral State ◽  
Forward Movement ◽  
C Elegans ◽  
Peptidergic Neuron ◽  
Homeobox Transcription Factor

AbstractNeuromodulators shape neural circuit dynamics. Combining electron microscopy, genetics, transcriptome profiling, calcium imaging, and optogenetics, we discovered a peptidergic neuron that modulates C. elegans motor circuit dynamics. The Six/SO-family homeobox transcription factor UNC-39 governs lineage-specific neurogenesis to give rise to a neuron RID. RID bears the anatomic hallmarks of a specialized endocrine neuron: it harbors near-exclusive dense core vesicles that cluster periodically along the axon, and expresses multiple neuropeptides, including the FMRF-amide-related FLP-14. RID activity increases during forward movement. Ablating RID reduces the sustainability of forward movement, a phenotype partially recapitulated by removing FLP-14. Optogenetic depolarization of RID prolongs forward movement, an effect reduced in the absence of FLP-14. Together, these results establish the role of a neuroendocrine cell RID in sustaining a specific behavioral state in C. elegans.

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