Neural Circuits: From Structure to Function and Back

Trojanowski, Nicholas F.; Raizen, David M.

doi:10.1016/j.cub.2015.06.048

Cited by 4 publications

(5 citation statements)

References 19 publications

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“…There has emerged a third wave of detailed functional studies on the pharyngeal nervous system aiming to elucidate the neural basis of feeding behavior in worms (commented in ref. 11). C. elegans uses pharyngeal pumping to ingest its food, bacteria (12).…”

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confidence: 99%

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Reciprocal modulation of 5-HT and octopamine regulates pumping via feedforward and feedback circuits in C. elegans

Liu

Qin

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Feeding is vital for animal survival and is tightly regulated by the endocrine and nervous systems. To study the mechanisms of humoral regulation of feeding behavior, we investigated serotonin (5-HT) and octopamine (OA) signaling inCaenorhabditis elegans, which uses pharyngeal pumping to ingest bacteria into the gut. We reveal that a cross-modulation mechanism between 5-HT and OA, which convey feeding and fasting signals, respectively, mainly functions in regulating the pumping and secretion of both neuromodulators via ADF/RIC/SIA feedforward neurocircuit (consisting of ADF, RIC, and SIA neurons) and ADF/RIC/AWB/ADF feedback neurocircuit (consisting of ADF, RIC, AWB, and ADF neurons) under conditions of food supply and food deprivation, respectively. Food supply stimulates food-sensing ADFs to release more 5-HT, which augments pumping via inhibiting OA secretion by RIC interneurons and, thus, alleviates pumping suppression by OA-activated SIA interneurons/motoneurons. In contrast, nutrient deprivation stimulates RICs to secrete OA, which suppresses pumping via activating SIAs and maintains basal pumping and 5-HT production activity through excitation of ADFs relayed by AWB sensory neurons. Notably, the feedforward and feedback circuits employ distinct modalities of neurosignal integration, namely, disinhibition and disexcitation, respectively.

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confidence: 99%

“…5, 9, 13, and 14; commented and reviewed in refs. 3, 10, and 11). Neuromodulatory signals play important roles in pumping regulation.…”

mentioning

confidence: 99%

Reciprocal modulation of 5-HT and octopamine regulates pumping via feedforward and feedback circuits in C. elegans

Liu

Qin

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…This proprioceptive feedback demonstrates an additional layer of complexity in the pharyngeal circuit as it shows that some neurons can have both sensory and motor functions, a phenomenon previously described in a class of motor neurons that regulate C. elegans locomotion 58 . In the future, the combination of genetic manipulations and the monitoring of neuron and muscle activity with genetically encoded calcium or voltage sensors will provide more information about the activity of pharyngeal nervous system, permitting a better understanding of the function of this network 59 .…”

Section: Discussionmentioning

confidence: 99%

Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system

Trojanowski

Raizen

Fang-Yen

2016

Sci Rep

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Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.

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“…This resulted in inhibition of pharyngeal pumping. The third circuit involved light activation of M1 neurons which stimulate pm3 muscles to contract expelling fluid from the mouth, termed spitting by the authors (Trojanowski and Raizen 2015).…”

Section: Circuits Associated With Feedingmentioning

confidence: 99%

“…Probing the neural basis of these food-related decisions has been made tractable by the construction of a 'wiring diagram' or connectome for the C. elegans nervous system (Albertson and Thomson 1976;White et al 1986). Each neuron is identified by a 3 letter nomenclature and this is available in a searchable format www.wormatlas.org and provides a superb resource for neuroscientists interested in the neural basis of feeding behaviour despite the fact that a few functional synapses are not resolved Trojanowski and Raizen 2015). Therefore, using the connectome and the genetic tools available for C. elegans progress has been made towards providing an integrative understanding of how an animal regulates its feeding behaviour, from the suite of food-dependent behaviours that the animal exhibits, through to the cellular and molecular determinants of these behaviours.…”

Section: Introductionmentioning

confidence: 99%

Caenorhabditis elegans Feeding Behaviors

Dallière¹,

Holden‐Dye²,

Dillon³

et al. 2017

Oxford Research Encyclopedia of Neuroscience

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The microscopic free-living nematode worm Caenorhabditis elegans was the first metazoan to have its genome sequenced and for many decades has served as a genetically tractable model for the investigation of neural mechanisms of behavioral plasticity. Many of its behaviors involve the detection of its food, bacteria, which are ingested and transported to the intestine by a muscular pharynx. The structure of the pharynx and the circuitry of the pharyngeal nervous system that regulates pharyngeal activity have been described in some detail. This has provided a platform for understanding how this simple organism finely tunes its feeding behavior in response to the changing availability and quality of its food, and in the context of its own nutritional status. This resonates with fundamental principles of energy homeostasis that occur throughout the animal kingdom.

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Neural Circuits: From Structure to Function and Back

Abstract: The new field of connectomics aims to obtain fine-grained anatomical connectivity data for vertebrate brains. A recent study highlights the types of experiments that will be necessary in order to draw conclusions about function from anatomical connectivity.

Cited by 4 publications

References 19 publications

Reciprocal modulation of 5-HT and octopamine regulates pumping via feedforward and feedback circuits in C. elegans

Reciprocal modulation of 5-HT and octopamine regulates pumping via feedforward and feedback circuits in C. elegans

Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system

Caenorhabditis elegans Feeding Behaviors

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