Serotonin-dependent kinetics of feeding bursts underlie a graded response to food availability in C. elegans

Lee, Kyung Suk; Iwanir, Shachar; Kopito, Ronen B.; Scholz, Monika; Calarco, John A.; Biron, David; Levine, Erel

doi:10.1038/ncomms14221

Cited by 66 publications

(87 citation statements)

References 63 publications

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“…Indeed, the pumping rate approaches 1 at µ = T as p becomes smaller. We note that in previous experiments no such maximum was observed, suggesting that C. elegans may follow a lessstringent rule (3,4).…”

Section: The Required Confidence Level Affects Performance When Resoumentioning

confidence: 87%

“…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%

“…This conceptualization of feeding behavior suggests optimal feeding strategies in response to conflicting inputs and to fluctuating environments. ambient density we collected feeding times series from multiple worms by automatically tracking the motion of their grinder (3,4). Exemplary trajectories show bursts of consecutive pumps and pauses ( Fig.…”

Section: Elegansmentioning

confidence: 99%

“…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.…”

mentioning

confidence: 99%

“…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 (6) methods.…”

mentioning

confidence: 99%

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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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Section: The Required Confidence Level Affects Performance When Resoumentioning

confidence: 87%

Section: Elegansmentioning

confidence: 99%

Section: Elegansmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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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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Spatiotemporal Tracking of Near‐Infrared Fluorescent Single‐Walled Carbon Nanotubes in C. Elegans Nematodes Confined in a Microfluidics Platform

Sharaga,

Hendler‐Neumark,

Kamber

et al. 2023

Adv Materials Technologies

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Caenorhabditis elegans (C. elegans) nematodes are a powerful model organism for diverse biological and biomedical studies, benefiting from their genetic similarities to humans, small size, and transparency. However, fluorescence imaging of C. elegans can be challenging due to the strong autofluorescence in the visible range, which obscures the signal of common fluorescent proteins or dyes. Single‐walled carbon nanotubes (SWCNTs) fluoresce in the near‐infrared (NIR) range, where there is no autofluorescence background. Herein, a platform is developed for in vivo NIR imaging of C. elegans gastrointestinal tract using biocompatible SWCNTs functionalized by single‐stranded DNA or phospholipid‐polyethylene glycol (PEG). The SWCNTs serve as fluorescent tracking probes within the worm gut, following internalization along with food intake. A microfluidic confinement device is employed to ensure an anesthetics‐free feeding environment, allowing spatiotemporal control over the SWCNTs intake imaging. Furthermore, improvements in spectral colocalization, real‐time detection of intracorporeal SWCNT dynamics, and digestive trajectory tracking are demonstrated. Owing to the unique optical properties of SWCNTs and the confinement of the worms in the microfluidics system, the proposed platform facilitates advanced in vivo imaging of C. elegans in both the visible and NIR regions, opening numerous avenues for advancing research of C. elegans and other microscopic model organisms.

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Fermented barley β‐glucan regulates fat deposition in Caenorhabditis elegans

et al. 2020

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BACKGROUNDBarley contains a relatively high concentration of the mixed‐linkage (1 → 3) (1 → 4) β‐glucan, which has been reported to be a functional food with prebiotic potential. In the current study we compared the properties of two neutral barley β‐glucans, obtained from raw barley: raw barley β‐glucan (RBG) and Lactobacillus plantarum dy‐1‐fermented barley (FBG).RESULTSMolecular characteristics revealed that the molecular weight of barley β‐glucan decreased from 1.13 × 105 D to 6.35 × 104 D after fermentation. Fermentation also improved the water / oil holding capacity, solubility, and swelling capacity of barley β‐glucan. Both RBG and FBG significantly improved the locomotive behavior of nematodes, thereby increasing their energy consumption and reducing fat deposition – the effect was more significant with FBG. These effects could potentially depend on nhr‐49, TGF‐daf‐7 mediated pathways and so on, in which nhr‐49 factor is particularly required.CONCLUSIONThese results suggested that fermentation may enhance in vitro physiological activities of barley β‐glucan, thereby altering the effects on the lipid metabolism in vivo. © 2020 Society of Chemical Industry

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Serotonin-dependent kinetics of feeding bursts underlie a graded response to food availability in C. elegans

Cited by 66 publications

References 63 publications

Stochastic feeding dynamics arise from the need for information and energy

Stochastic feeding dynamics arise from the need for information and energy

Spatiotemporal Tracking of Near‐Infrared Fluorescent Single‐Walled Carbon Nanotubes in C. Elegans Nematodes Confined in a Microfluidics Platform

Fermented barley β‐glucan regulates fat deposition in Caenorhabditis elegans

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