Recognition of familiar food activates feeding via an endocrine serotonin signal in Caenorhabditis elegans

Song, Bomi; Faumont, Serge; Lockery, Shawn R.; Avery, Leon

doi:10.7554/elife.00329

Cited by 78 publications

(98 citation statements)

References 39 publications

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“…Serotonin-deficient tph-1 mutants exhibit reduced pharyngeal pumping relative to wildtype animals (Sze et al, 2000) and restoration of tph-1 to only the ADF neurons, a pair of serotonergic head sensory neurons, confers wildtype pumping under ad libitum fed conditions (Cunningham et al, 2012) and up-regulated pumping in response to familiar food (Song et al, 2013). We found that serotonin deficiency also abrogates fasting-induced hyperactive feeding, which can be partially restored through reconstitution of serotonin biosynthesis in only the ADF neurons (Figure 1B, Table S1).…”

Section: Resultsmentioning

confidence: 99%

Kynurenic Acid Is a Nutritional Cue that Enables Behavioral Plasticity

Lemieux

Cunningham

Lin

et al. 2015

Cell

105

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Summary The kynurenine pathway of tryptophan metabolism is involved in the pathogenesis of several brain diseases but its physiological functions remain unclear. We report that kynurenic acid, a metabolite in this pathway, functions as a regulator of food-dependent behavioral plasticity in C. elegans. The experience of fasting in C. elegans alters a variety of behaviors, including feeding rate, when food is encountered post-fast. Levels of neurally produced kynurenic acid are depleted by fasting leading to activation of NMDA-receptor-expressing interneurons and initiation of a neuropeptide-y like signaling axis that promotes elevated feeding through enhanced serotonin release when animals re-encounter food. Upon re-feeding, kynurenic acid levels are eventually replenished ending the elevated feeding period. Since tryptophan is an essential amino acid, these findings suggest that a physiological role of kynurenic acid is in directly linking metabolism to activity of NMDA and serotonergic circuits, which regulate a broad range of behaviors and physiologies.

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Section: Resultsmentioning

confidence: 99%

Kynurenic Acid Is a Nutritional Cue that Enables Behavioral Plasticity

Lemieux

Cunningham

Lin

et al. 2015

Cell

105

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“…MC ablation in wildtype larvae is sufficient to accelerate their growth in CeMM, indicating that they are involved in how the animal couples mechanical nutrient intake with cellular growth rate. Under standard bacterial diet conditions, the MCs regulate pharyngeal pumping rate through secreting ACh to the pharyngeal muscles 4,34,58 . Our results show that ablation of the MC neurons in the wild type accelerates the developmental rate, suggesting that TMC-1 promotes developmental retardation partly through these neurons.…”

Section: Discussionmentioning

confidence: 99%

TMC-1 attenuates C. elegans development and sexual behaviour in a chemically defined food environment

et al. 2015

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Although diet affects growth and behaviour, the adaptive mechanisms that coordinate these processes in non-optimal food sources are unclear. Here we show that the C. elegans tmc-1 channel, which is homologous to the mammalian tmc deafness genes, attenuates development and inhibits sexual behaviour in non-optimal food, the synthetic CeMM medium. In CeMM medium, signalling from the pharyngeal MC neurons and body wall muscles slows larval development. However, in the non-standard diet, mutation in tmc-1 accelerates development, by impairing the excitability of these cells. The tmc-1 larva can immediately generate ATP when fed CeMM, and their fast development requires insulin signalling. Our findings suggest that the tmc-1 channel indirectly affects metabolism in wild-type animals. In addition to regulating the development, we show that mutating tmc-1 can relax diet-induced inhibition of male sexual behaviour, thus indicating that a single regulator can be genetically modified to promote growth rate and reproductive success in new environments.

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“…This prior can be encoded genetically and epigenetically and therefore can change on evolutionary or generational time scales. Moreover, it is known that food preference and feeding are learned behaviors that can be modulated by life history (19,36). Correspondingly, the parameters a0 and b0 which characterize the prior may be changing on time scales that extend multiple rounds of decision.…”

Section: Discussionmentioning

confidence: 99%

“…We found that the overall pumping activity correlates with the concentration of available food and that pumping does not completely cease when no food was available ( Figs. 1 and 2 A and B) (3,(17)(18)(19). In the absence of food, worms exhibit long pauses (Fig.…”

Section: Elegansmentioning

confidence: 99%

Stochastic feeding dynamics arise from the need for information and energy

Scholz

Dinner

Levine

et al. 2017

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

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Animals regulate their food intake in response to the available level of food. Recent observations of feeding dynamics in small animals showed feeding patterns of bursts and pauses, but their function is unknown. Here, we present a data-driven decisiontheoretical model of feeding in Caenorhabditis elegans. Our central assumption is that food intake serves a dual purpose: to gather information about the external food level and to ingest food when the conditions are good. The model recapitulates experimentally observed feeding patterns. It naturally implements trade-offs between speed versus accuracy and exploration versus exploitation in responding to a dynamic environment. We find that the model predicts three distinct regimes in responding to a dynamical environment, with a transition region where animals respond stochastically to periodic signals. This stochastic response accounts for previously unexplained experimental data.decision theory | feeding behavior | sequential analysis R egulation of food intake is important for maintaining energy balance in animals. Failure can lead, for example, to reduced fitness, metabolic disorders, and cardiovascular diseases (1, 2). To successfully regulate their feeding, animals need to assess the expected availability of food in their environment.Recent advances in automated longitudinal imaging of small animals make the acquisition of large-scale quantitative feeding data possible. Data from worms (3, 4) and flies (5) reveal complex dynamics that are responsive to the availability of food in the animal's environment. These data suggest that food uptake occurs in bouts of high-rate feeding, whose duration and frequency increase with the presence of food. Whether these dynamics serve a function is not known.In this paper we hypothesize that the dynamics of feeding observed in small animals are intimately related to a decisionmaking process. Since feeding behaviors are costly in energy and can expose animals to toxins and pathogens, the decision to feed carries consequences and should be considered carefully by the animal. We posit that food uptake from the environment serves two purposes: to provide the animal with information about the food that is available in the environment and to take up nutrients. To explore the implications of this assertion, we develop, analyze, and experimentally test a quantitative model.We focus on the regulation of feeding by the roundworm Caenorhabditis elegans, a free-living nematode that is found predominantly in fruit composts and feeds on bacteria. The feeding organ of the worm, the pharynx, is a simple neuromuscular pump. Each pump brings a small number of bacteria suspended in water into the pharyngeal lumen. The pharynx then expels the water, grinds the bacteria, and sends them into the intestine. Pumping is therefore a proxy for the behavioral dynamics of feeding. Supported by microfluidics technology, time traces of pumping in individual worms can be obtained over long periods of time using either optical (3, 4) or electrophysiological...

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Recognition of familiar food activates feeding via an endocrine serotonin signal in Caenorhabditis elegans

Cited by 78 publications

References 39 publications

Kynurenic Acid Is a Nutritional Cue that Enables Behavioral Plasticity

Kynurenic Acid Is a Nutritional Cue that Enables Behavioral Plasticity

TMC-1 attenuates C. elegans development and sexual behaviour in a chemically defined food environment

Stochastic feeding dynamics arise from the need for information and energy

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