C. elegans food choice exhibits effort discounting-like behavior
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eLife Assessment
This important work develops C. elegans as a model organism for studying effort-based discounting by asking the worms to choose between easy and hard to digest bacteria. The authors provide convincing evidence that the nematodes are effort-discounting. However, evidence regarding the role of dopamine is incomplete and this weakens the authors connection of the behavior in C. elegans with mammals.
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Abstract
Cost-benefit decisions are ubiquitous in both human and animal behavior. Economists have developed formal models of cost-benefit decision-making by focusing on discounting behavior, the devaluation of a reward based on the costs associated with it. The phylogenetic limits of discounting behavior remain unknown. Here, we provide evidence that the nematode C. elegans exhibits behavior closely resembling effort discounting. Given a choice between food options that are easy or difficult to consume, worms devalue the latter in a manner predicted by economic models. We identified a plausible mechanism for this behavior based on differential rates of leaving food patches and demonstrated that this mechanism is disrupted by deficits in dopamine signaling, as in rodents. Together, these results establish C. elegans as a potential invertebrate model for discounting behavior and set new phylogenetic bounds on this type of cost-benefit decision-making.
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eLife Assessment
This important work develops C. elegans as a model organism for studying effort-based discounting by asking the worms to choose between easy and hard to digest bacteria. The authors provide convincing evidence that the nematodes are effort-discounting. However, evidence regarding the role of dopamine is incomplete and this weakens the authors connection of the behavior in C. elegans with mammals.
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Reviewer #1 (Public Review):
Summary:
Here, Millet et al. consider whether the nematode C. elegans 'discounts' the value of reward due to effort in a manner similar to that shown in other species, including rodents and humans. They designed a T-maze effort choice paradigm inspired by previous literature, but manipulated how effortful the food is to consume. C. elegans worms were sensitive to this novel manipulation, exhibiting effort-discounting-like behaviour that could be shaped by varying the density of food at each alternative in order to calculate an indifference point. This discounting-like behaviour was related to worms' rates of patch leaving, which differed between the low and high effort patches in isolation. The authors also found a potential relationship to dopamine signalling, and also that this discounting behaviour was …
Reviewer #1 (Public Review):
Summary:
Here, Millet et al. consider whether the nematode C. elegans 'discounts' the value of reward due to effort in a manner similar to that shown in other species, including rodents and humans. They designed a T-maze effort choice paradigm inspired by previous literature, but manipulated how effortful the food is to consume. C. elegans worms were sensitive to this novel manipulation, exhibiting effort-discounting-like behaviour that could be shaped by varying the density of food at each alternative in order to calculate an indifference point. This discounting-like behaviour was related to worms' rates of patch leaving, which differed between the low and high effort patches in isolation. The authors also found a potential relationship to dopamine signalling, and also that this discounting behaviour was not specific to lab-based strains of C. elegans.
Strengths:
The question is well-motivated, and the approach taken here is novel. The authors are careful in their approach to altering and testing the properties of the effortful, elongated bacteria. Similarly, they go to some effort to understand what exactly is driving behavioural choices in this context, both through the application of simple standard models of effort discounting and a kinetic analysis of patch leaving. The comparisons to various dopamine mutants further extend the translational potential of their findings. I also appreciate the comparison to natural isolate strains, as the question of whether this behaviour may be driven by some sort of strain-specific adaptation to the environment is not regularly addressed in mammalian counterparts. The manuscript is well-written, and the figures are clear and comprehensible.
Weaknesses:
Discounting is typically defined as the alteration of a subjective value by effort (or time, risk, etc.), which is then used to guide future decision-making. By adapting the standard t-maze task for C. elegans as a patch-leaving paradigm, the authors observe behaviour strongly consistent with discounting models, but that is likely driven by a different process, in particular by an online estimate of the type of food in the current patch, which then influences patch-leaving dynamics (Figure 3). This is fundamentally different from decision-making strategies relating to effort that have been described in the rodent and human literatures. Similarly, the calculation of indifference points at the group instead of at the individual level also suggests a different underlying process and limits the translational potential of their findings. The authors do not discuss the implications of these differences or why they chose not to attempt a more analogous trial-based experiment.
In the case of both the dopamine and natural isolate experiments, the data are very noisy despite large (relative to other C. elegans experiments) sample sizes. In the dopamine experiment, disruption of dop-1, dop-2, and cat-2 had no statistically significant effect. There do not appear to be any corrections for multiple comparisons, and the single significant comparison, for dop-3, had a small effect size. More detailed behavioural analyses on both these and the wild isolate strains, for example by applying their kinetic analysis, would likely give greater insight as to what is driving these inconsistent effects.
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Reviewer #2 (Public Review):
Summary:
Millet et al. show that C. elegans systematically prefers easy-to-eat bacteria but will switch its choice when harder-to-eat bacteria are offered at higher densities, producing indifference points that fit standard economic discounting models. Detailed kinetic analysis reveals that this bias arises from unchanged patch-entry rates but significantly elevated exit rates on effortful food, and dop-3 mutants lose the preference altogether, implicating dopamine in effort sensitivity. These findings extend effort-discounting behavior to a simple nematode, pushing the phylogenetic boundary of economic cost-benefit decision-making.
Strengths:
(1) Extends the well-characterized concept of effort discounting into _C. elegans_, setting a new phylogenetic boundary and opening invertebrate genetics to …
Reviewer #2 (Public Review):
Summary:
Millet et al. show that C. elegans systematically prefers easy-to-eat bacteria but will switch its choice when harder-to-eat bacteria are offered at higher densities, producing indifference points that fit standard economic discounting models. Detailed kinetic analysis reveals that this bias arises from unchanged patch-entry rates but significantly elevated exit rates on effortful food, and dop-3 mutants lose the preference altogether, implicating dopamine in effort sensitivity. These findings extend effort-discounting behavior to a simple nematode, pushing the phylogenetic boundary of economic cost-benefit decision-making.
Strengths:
(1) Extends the well-characterized concept of effort discounting into _C. elegans_, setting a new phylogenetic boundary and opening invertebrate genetics to economic-behavior studies.
(2) Elegant use of cephalexin-elongated bacteria to manipulate "effort" without altering nutritional or olfactory cues, yielding clear preference reversals and reproducible indifference points.
(3) Application of standard discounting models to predict novel indifference points is both rigorous and quantitatively satisfying, reinforcing the interpretation of worm behavior in economic terms.
(4) The three-state patch-model cleanly separates entry and exit dynamics, showing that increased leaving rates-rather than altered re-entry-drive choice biases.
(5) Investigates the role of dopamine in this behavior to try to establish shared mechanisms with vertebrates.
(6) Demonstration of discounting in wild strain (solid evidence).
Weaknesses:
(1) The kinetic model omits rich trajectory details-such as turning angles or hazard functions-that could distinguish a bona fide roaming transition from other exit behaviors.
(2) Only _dop-3_ shows an effect, and the statistical validity of this result is questionable. It is not clear if the authors corrected for multiple comparisons, and the effect size is quite small and noisy, given the large number of worms tested. Other mutants do not show effects. Given these two concerns, the role of dopamine in c. elegans effort discounting was unconvincing.
(3) With only five wild isolates tested (and variable data quality), it's hard to conclude that effort discounting isn't a lab-strain artifact or how broadly it varies in natural populations.
(4) Detailed analysis of behavior beyond preference indices would strengthen the dopamine link and the claim of effort discounting in wild strains.
(5) A few mechanistic statements (e.g., tying satiety exclusively to nutrient signals) would benefit from explicit citations or brief clarifications for non-worm specialists.
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Reviewer #3 (Public Review):
Summary:
The authors establish a behavioral task to explore effort discounting in C. elegans. By using bacterial food that takes longer to consume, the authors show that, for equivalent effort, as measured by pumping rate, they obtain less food, as measured by fat deposition.
The authors formalize the task by applying a formal neuroeconomic decision-making model that includes value, effort, and discounting. They use this to estimate the discounting that C. elegans applies based on ingestion effort by using a population-level 2-choice T-maze.
They then analyze the behavioral dynamics of individual animals transitioning between on-food and off-food states. Harder to ingest bacteria led to increased food patch leaving.
Finally, they examined a set of mutants defective in different aspects of dopamine signaling, …
Reviewer #3 (Public Review):
Summary:
The authors establish a behavioral task to explore effort discounting in C. elegans. By using bacterial food that takes longer to consume, the authors show that, for equivalent effort, as measured by pumping rate, they obtain less food, as measured by fat deposition.
The authors formalize the task by applying a formal neuroeconomic decision-making model that includes value, effort, and discounting. They use this to estimate the discounting that C. elegans applies based on ingestion effort by using a population-level 2-choice T-maze.
They then analyze the behavioral dynamics of individual animals transitioning between on-food and off-food states. Harder to ingest bacteria led to increased food patch leaving.
Finally, they examined a set of mutants defective in different aspects of dopamine signaling, as dopamine plays a key role in discounting in vertebrates and regulates certain aspects of C. elegans foraging.
Strengths:
The behavioral experiments and neuroeconomic analysis framework are compelling and interesting, and make a significant contribution to the field. While these foraging behaviors have been extensively studied, few include clearly articulated theoretical models to be tested.
Demonstrating that C. elegans effort discounting fits model predictions and has stable indifference points is important for establishing these tasks as a model for decision making.
Weaknesses:
The dopamine experiments are harder to interpret. The authors point out the perplexing lack of an effect of dat-1 and cat-2. dop-3 leads to general indifference. I am not sure this is the expected result if the argument is a parallel functional role to discounting in vertebrates. dop-3 causes a range of locomotor phenotypes and may affect feeding (reduced fat storage), and thus, there may be a general defect in the ability to perform the task rather than anything specific to discounting.
That said, some of the other DA mutants also have locomotor defects and do not differ from N2. But there is no clear result here - my concern is that global mutants in such a critical pathway exhibit such pleiotropy that it's difficult to conclude there is a clear and specific role for DA in effort discounting. This would require more targeted or cell-specific approaches.
Meanwhile, there are other pathways known to affect responses to food and patch leaving decisions: serotonin, pigment-dispersing factor, tyramine, etc. The paper would have benefited from a clarification about why these were not considered as promising candidates to test (in addition to or instead of dopamine).
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