Nonredundant function of two highly homologous octopamine receptors in food‐deprivation‐mediated signaling in <i>Caenorhabditis elegans</i>

Yoshida, Midori; Oami, Eitaro; Wang, Min; Ishiura, Shoichi; Suo, Satoshi

doi:10.1002/jnr.23345

Cited by 20 publications

(16 citation statements)

References 30 publications

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“…3C-E). This is despite the observation that exogenous octopamine has been shown to inhibit pharyngeal pumping (27,56) and to be involved in food-dependent responses (60)(61)(62). This suggests that differences in assay may underlie the difference in function found for octopamine.…”

Section: Gaba and Dopamine Promote Pumping During Food Deprivationmentioning

confidence: 94%

Multiple excitatory and inhibitory neural signals converge to fine‐tuneCaenorhabditis elegansfeeding to food availability

et al. 2015

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How an animal matches feeding to food availability is a key question for energy homeostasis. We addressed this in the nematode Caenorhabditis elegans, which couples feeding to the presence of its food (bacteria) by regulating pharyngeal activity (pumping). We scored pumping in the presence of food and over an extended time course of food deprivation in wild-type and mutant worms to determine the neural substrates of adaptive behavior. Removal of food initially suppressed pumping but after 2 h this was accompanied by intermittent periods of high activity. We show pumping is fine-tuned by context-specific neural mechanisms and highlight a key role for inhibitory glutamatergic and excitatory cholinergic/peptidergic drives in the absence of food. Additionally, the synaptic protein UNC-31 [calcium-activated protein for secretion (CAPS)] acts through an inhibitory pathway not explained by previously identified contributions of UNC-31/CAPS to neuropeptide or glutamate transmission. Pumping was unaffected by laser ablation of connectivity between the pharyngeal and central nervous system indicating signals are either humoral or intrinsic to the enteric system. This framework in which control is mediated through finely tuned excitatory and inhibitory drives resonates with mammalian hypothalamic control of feeding and suggests that fundamental regulation of this basic animal behavior may be conserved through evolution from nematode to human.

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Section: Gaba and Dopamine Promote Pumping During Food Deprivationmentioning

confidence: 94%

Multiple excitatory and inhibitory neural signals converge to fine‐tuneCaenorhabditis elegansfeeding to food availability

et al. 2015

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“…The octopamine receptor, SER-3, is found on pharyngeal muscle (Carre-Pierrat et al 2006) and ser-3 mutants have a slightly lower pumping rate compared to N2 in the absence of food. SER-3 occurs on the cholinergic SIA neurons and is required for SIA activation upon food deprivation triggered by octopamine release from RIC neurons (Suo et al 2006;Yoshida et al 2014). However, the role of SIA neurons on feeding behaviour is not known.…”

Section: Octopamine/tyramine and Pharyngeal Pumpingmentioning

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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“…S8A). The ser-6 gene is expressed in a subset of head neurons, including the AWB olfactory neurons and the SIA interneurons (28,29). We found that restoring ser-6 function to ser-6 mutants either in all ser-6-expressing neurons, in AWB only, or in SIA only was sufficient to restore normal CO 2 attraction to starved animals (SI Appendix, Fig.…”

Section: Significancementioning

confidence: 79%

Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans

Rengarajan

Yankura

Guillermin

et al. 2019

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

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Hunger affects the behavioral choices of all animals, and many chemosensory stimuli can be either attractive or repulsive depending on an animal’s hunger state. Although hunger-induced behavioral changes are well documented, the molecular and cellular mechanisms by which hunger modulates neural circuit function to generate changes in chemosensory valence are poorly understood. Here, we use the CO2 response of the free-living nematode Caenorhabditis elegans to elucidate how hunger alters valence. We show that CO2 response valence shifts from aversion to attraction during starvation, a change that is mediated by two pairs of interneurons in the CO2 circuit, AIY and RIG. The transition from aversion to attraction is regulated by biogenic amine signaling. Dopamine promotes CO2 repulsion in well-fed animals, whereas octopamine promotes CO2 attraction in starved animals. Biogenic amines also regulate the temporal dynamics of the shift from aversion to attraction such that animals lacking octopamine show a delayed shift to attraction. Biogenic amine signaling regulates CO2 response valence by modulating the CO2-evoked activity of AIY and RIG. Our results illuminate a new role for biogenic amine signaling in regulating chemosensory valence as a function of hunger state.

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Nonredundant function of two highly homologous octopamine receptors in food‐deprivation‐mediated signaling in Caenorhabditis elegans

Cited by 20 publications

References 30 publications

Multiple excitatory and inhibitory neural signals converge to fine‐tuneCaenorhabditis elegansfeeding to food availability

Multiple excitatory and inhibitory neural signals converge to fine‐tuneCaenorhabditis elegansfeeding to food availability

Caenorhabditis elegans Feeding Behaviors

Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans

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