Serotonin promotes exploitation in complex environments by accelerating decision-making

Iwanir, Shachar; Brown, Adam S.; Nagy, Stanislav; Najjar, Dana; Kazakov, Alexander; Lee, Kyung Suk; Zaslaver, Alon; Levine, Erel; Biron, David

doi:10.1186/s12915-016-0232-y

Cited by 52 publications

(63 citation statements)

References 74 publications

(132 reference statements)

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“…While early experiments suggested that ADF may have a role in the detection of dauer pheromone [44], a role for the ADF neurons in sex pheromone attraction has not been previously described. In hermaphrodites, ADF is best known for its roles in detection of foodrelated compounds, release of serotonin, inhibition of entry into the dauer stage, and modulation of food-dependent behaviors [44,[67][68][69][70]. Our results indicate that, in males, ADF also detects ascr#3 (and perhaps other ascarosides), and that the transmission of this signal is independent of serotonin release.…”

Section: Discussionmentioning

confidence: 64%

“…Here, we favor the idea that ascaroside detection by the male ADF differentially engages shared navigational circuits. Indeed, ADF activation is associated with locomotor slowing in hermaphrodites [68,70] (though ADF-derived serotonin is also implicated in promoting roaming [75]), and exposure to ascr#3-containing plates increases male reversal rate [17].…”

Section: Discussionmentioning

confidence: 99%

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A chemosensory switch couples genetic sex to behavioral valence

Luo

et al. 2017

Preprint

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As a fundamental dimension of internal state, biological sex modulates neural circuits to generate naturally occurring behavioral variation. Understanding how and why circuits are tuned by sex can provide important insights into neural and behavioral plasticity. Here, we find that sexually dimorphic behavioral responses to C. elegans ascaroside sex pheromones are implemented by the functional modulation of shared chemosensory circuitry. In particular, the sexual state of a single sensory neuron pair, ADF, determines the nature of an animal's behavioral response regardless of the sex of the rest of the body. Genetic feminization of ADF causes males to be repelled by, rather than attracted to, ascarosides, while masculinization of ADF is sufficient to make ascarosides attractive to hermaphrodites. Genetic sex modulates ADF function by tuning chemosensation: ADF is able to detect the ascaroside ascr#3 only in males, a consequence of cell-autonomous action of the master sexual regulator tra-1. Genetic sex regulates behavior in part through the conserved DMRT gene mab-3, whose male-specific expression in ADF promotes ascaroside attraction. The sexual modulation of ADF has a key role in reproductive fitness, as feminization or ablation of ADF renders males unable to use ascarosides to locate mates. These results demonstrate that DMRT genes can functionally modulate shared neural circuits; moreover, they reveal an adaptive mechanism in which chromosomal sex controls a cell-autonomous switch that tunes sensory function, determines behavioral valence, and promotes reproductive fitness.

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Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 99%

A chemosensory switch couples genetic sex to behavioral valence

Luo

et al. 2017

Preprint

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“…Recent findings, however, demonstrate a synergistic role for HSN and NSM in promoting a locomotion behavioral state known as dwelling, where worms inside a bacteria lawn move slowly and turn frequently to explore locally. This behavior relies on serotonin production in both the NSM and HSN neurons, but not in ADF 26,50 .…”

Section: Discussionmentioning

confidence: 97%

Serotonin-dependent kinetics of bursts of feeding underlie a graded response to food availability

Iwanir

et al. 2016

Preprint

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Animals integrate physiological and environmental signals to modulate their food uptake. Failure to regulate feeding may have devastating results, including obesity and diabetes, underscoring the importance of understanding its underlying mechanisms. The nematode C. elegans, whose food uptake consists of pumping bacteria from the environment into the gut, provides excellent opportunities for discovering principles of conserved regulatory mechanisms. Here we show that worms implement a graded feeding response to the concentration of environmental bacteria by modulating a commitment to bursts of fast pumping. Using longterm, high-resolution, longitudinal recordings of feeding dynamics under defined conditions, we find that the frequency and duration of pumping bursts increase and the duration of long pauses diminishes in environments richer in bacteria. The bioamine serotonin, a known feeding regulator in metazoa, is required for food-dependent induction of bursts as well as for maintaining their high rate of pumping through two distinct mechanisms. Following this phenotype quantitatively we identify the essential serotonergic neurons and the differential roles of distinct families of serotonin receptors. We propose that regulation of bursts is a conserved mechanism of behavior and motor control.

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“…Alternative strategies for coping with heterogeneous environment have been proposed, for example, in bacteria and worms (32)(33)(34)(35). It is expected that the significance of resetting is diminished if changes to the environment are slow or smooth.…”

Section: Discussionmentioning

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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Serotonin promotes exploitation in complex environments by accelerating decision-making

Cited by 52 publications

References 74 publications

A chemosensory switch couples genetic sex to behavioral valence

A chemosensory switch couples genetic sex to behavioral valence

Serotonin-dependent kinetics of bursts of feeding underlie a graded response to food availability

Stochastic feeding dynamics arise from the need for information and energy

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