scholarly journals Phase response analyses support a relaxation oscillator model of locomotor rhythm generation in Caenorhabditis elegans

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Hongfei Ji ◽  
Anthony D Fouad ◽  
Shelly Teng ◽  
Alice Liu ◽  
Pilar Alvarez-Illera ◽  
...  

Neural circuits coordinate with muscles and sensory feedback to generate motor behaviors appropriate to an animal’s environment. In C. elegans, the mechanisms by which the motor circuit generates undulations and modulates them based on the environment are largely unclear. We quantitatively analyzed C. elegans locomotion during free movement and during transient optogenetic muscle inhibition. Undulatory movements were highly asymmetrical with respect to the duration of bending and unbending during each cycle. Phase response curves induced by brief optogenetic inhibition of head muscles showed gradual increases and rapid decreases as a function of phase at which the perturbation was applied. A relaxation oscillator model based on proprioceptive thresholds that switch the active muscle moment was developed and is shown to quantitatively agree with data from free movement, phase responses, and previous results for gait adaptation to mechanical loadings. Our results suggest a neuromuscular mechanism underlying C. elegans motor pattern generation within a compact circuit.

2020 ◽  
Author(s):  
Hongfei Ji ◽  
Anthony D. Fouad ◽  
Shelly Teng ◽  
Alice Liu ◽  
Pilar Alvarez-Illera ◽  
...  

AbstractNeural circuits work together with muscles and sensory feedback to generate motor behaviors appropriate to an animal’s environment. In C. elegans, forward locomotion consists of dorsoventral undulations that propagate from anterior to posterior. How the worm’s motor circuit generates these undulations and modulates them based on external loading is largely unclear. To address this question, we performed quantitative behavioral analysis of C. elegans during free movement and during transient optogenetic muscle inhibition. Undulatory movements in the head were found to be highly asymmetric, with bending toward the ventral or dorsal directions occurring slower than straightening toward a straight posture during the locomotory cycle. Phase shifts induced by brief optogenetic inhibition of head muscles showed a sawtooth-shaped dependence on phase of inhibition. We developed a computational model based on proprioceptive postural thresholds that switch the active moment of body wall muscles. We show that our model, a type of relaxation oscillator, is in quantitative agreement with data from free movement, phase responses, and previous results for frequency and amplitude dependence on the viscosity of the external medium. Our results suggest a neuromuscular mechanism that enables C. elegans to coordinate rhythmic motor patterns within a compact circuit.


2001 ◽  
Vol 280 (6) ◽  
pp. G1055-G1060 ◽  
Author(s):  
Pamela J. Hornby

In the last decade, there has been a dramatic increase in academic and pharmaceutical interest in central integration of vago-vagal reflexes controlling the gastrointestinal tract. Associated with this, there have been substantial efforts to determine the receptor-mediated events in the dorsal vagal complex that underlie the physiological responses to distension or variations in the composition of the gut contents. Strong evidence supports the idea that glutamate is a transmitter in afferent vagal fibers conveying information from the gut to the brain, and the implications of this are discussed in this themes article. Furthermore, both ionotropic and metabotropic glutamate receptors mediate pre- and postsynaptic control of glutamate transmission related to several reflexes, including swallowing motor pattern generation, gastric accommodation, and emesis. The emphasis of this themes article is on the potential therapeutic benefits afforded by modulation of these receptors at the site of the dorsal vagal complex.


1996 ◽  
Vol 76 (3) ◽  
pp. 687-717 ◽  
Author(s):  
E. Marder ◽  
R. L. Calabrese

Rhythmic movements are produced by central pattern-generating networks whose output is shaped by sensory and neuromodulatory inputs to allow the animal to adapt its movements to changing needs. This review discusses cellular, circuit, and computational analyses of the mechanisms underlying the generation of rhythmic movements in both invertebrate and vertebrate nervous systems. Attention is paid to exploring the mechanisms by which synaptic and cellular processes interact to play specific roles in shaping motor patterns and, consequently, movement.


1972 ◽  
Vol 38 (2) ◽  
pp. 81-82 ◽  
Author(s):  
B.S Deaver ◽  
J.M Pierce

Author(s):  
Nicholas Dale

AbstractThis brief review recounts how, stimulated by the work of Geoff Burnstock, I developed biosensors that allowed direct real-time measurement of ATP and adenosine during neural function. The initial impetus to create an adenosine biosensor came from trying to understand how ATP and adenosine-modulated motor pattern generation in the frog embryo spinal cord. Early biosensor measurements demonstrated slow accumulation of adenosine during motor activity. Subsequent application of these biosensors characterized real-time release of adenosine in in vitro models of brain ischaemia, and this line of work has recently led to clinical measurements of whole blood purine levels in patients undergoing carotid artery surgery or stroke. In parallel, the wish to understand the role of ATP signalling in the chemosensory regulation of breathing stimulated the development of ATP biosensors. This revealed that release of ATP from the chemosensory areas of the medulla oblongata preceded adaptive changes in breathing, triggered adaptive changes in breathing via activation of P2 receptors, and ultimately led to the discovery of connexin26 as a channel that mediates CO2-gated release of ATP from cells.


2000 ◽  
Vol 20 (17) ◽  
pp. 6619-6630 ◽  
Author(s):  
Deborah J. Baro ◽  
Amir Ayali ◽  
Lauren French ◽  
Nathaniel L. Scholz ◽  
Jana Labenia ◽  
...  

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