The nematode worm C. elegans chooses between bacterial foods as if maximizing economic utility
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Evaluation Summary:
This paper establishes a behavioural paradigm to study concepts developed in the field of economic decision making using the tractable model organisms C. elegans. It is therefore interesting to scientists studying the neuronal mechanisms of decision making and animal cognition.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
In value-based decision making, options are selected according to subjective values assigned by the individual to available goods and actions. Despite the importance of this faculty of the mind, the neural mechanisms of value assignments, and how choices are directed by them, remain obscure. To investigate this problem, we used a classic measure of utility maximization, the Generalized Axiom of Revealed Preference, to quantify internal consistency of food preferences in Caenorhabditis elegans , a nematode worm with a nervous system of only 302 neurons. Using a novel combination of microfluidics and electrophysiology, we found that C. elegans food choices fulfill the necessary and sufficient conditions for utility maximization, indicating that nematodes behave as if they maintain, and attempt to maximize, an underlying representation of subjective value. Food choices are well-fit by a utility function widely used to model human consumers. Moreover, as in many other animals, subjective values in C. elegans are learned, a process we find requires intact dopamine signaling. Differential responses of identified chemosensory neurons to foods with distinct growth potentials are amplified by prior consumption of these foods, suggesting that these neurons may be part of a value-assignment system. The demonstration of utility maximization in an organism with a very small nervous system sets a new lower bound on the computational requirements for utility maximization and offers the prospect of an essentially complete explanation of value-based decision making at single neuron resolution in this organism.
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Evaluation Summary:
This paper establishes a behavioural paradigm to study concepts developed in the field of economic decision making using the tractable model organisms C. elegans. It is therefore interesting to scientists studying the neuronal mechanisms of decision making and animal cognition.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In this work, Katzen et al. establish a behavioural paradigm to test whether C. elegans worms are consistent in their food choice behaviour to maximize utility, i.e., do they make consistent and optimal decision to maximize nutritious food intake? The experimental design is guided by revealed preference theory and the Generalized Axiom of Revealed Preference (GARP). In this framework, subjects should be consistent in their choices given various options of goods to choose from to satisfy (or maximize) their internal needs, that correspond to a utility function, while facing a limited budget. The ability to study decision making in a small nematode worm in this framework would quite be exciting as this would enable researchers to investigate with relative ease the neuronal circuit mechanisms that compute task …
Reviewer #1 (Public Review):
In this work, Katzen et al. establish a behavioural paradigm to test whether C. elegans worms are consistent in their food choice behaviour to maximize utility, i.e., do they make consistent and optimal decision to maximize nutritious food intake? The experimental design is guided by revealed preference theory and the Generalized Axiom of Revealed Preference (GARP). In this framework, subjects should be consistent in their choices given various options of goods to choose from to satisfy (or maximize) their internal needs, that correspond to a utility function, while facing a limited budget. The ability to study decision making in a small nematode worm in this framework would quite be exciting as this would enable researchers to investigate with relative ease the neuronal circuit mechanisms that compute task parameters such as subjective value, utility, choice etc. However, I am confused whether the behavioural task employed here can be directly compared with the GARP experiments outlined in the introduction of this paper (Fig 1). I think simple, however still unknown, mechanisms of chemoreception can explain the behavioural results and I wonder whether the GARP framework rather over-complicates the story or not. Perhaps, the authors could dilute this concern by better discussing the pros and cons of their experimental setup. Otherwise, the experiments are carefully performed, and the analyses seem rigorous. Beyond this one major criticisms, I have only minor concerns and suggestion to improve the manuscript.
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Reviewer #2 (Public Review):
In this work, Katzen et al. aim to model the feeding behavior of C. elegans in terms of well-established economic theories of value assignment and rational decision-making. This rigorous, quantitative analysis takes advantage of a powerful experimental system in which food quality and "cost" can be precisely controlled while carefully monitoring consumption. By immobilizing worms in a chamber in which they are simultaneously exposed to two streams of food of varying quality and abundance/cost, the authors measure changes in the geometry of head swings, pump rates, and therefore relative food consumption. Interestingly, they present evidence that worms are able to make these decisions as though they are maximizing economic utility, based on the idea that the "price" of the food is a function of its density. …
Reviewer #2 (Public Review):
In this work, Katzen et al. aim to model the feeding behavior of C. elegans in terms of well-established economic theories of value assignment and rational decision-making. This rigorous, quantitative analysis takes advantage of a powerful experimental system in which food quality and "cost" can be precisely controlled while carefully monitoring consumption. By immobilizing worms in a chamber in which they are simultaneously exposed to two streams of food of varying quality and abundance/cost, the authors measure changes in the geometry of head swings, pump rates, and therefore relative food consumption. Interestingly, they present evidence that worms are able to make these decisions as though they are maximizing economic utility, based on the idea that the "price" of the food is a function of its density. Interestingly, these choices seem to be most robust after worms have learned something about the relative nutritional value of the two food sources, and the authors provide evidence that this process requires the AWC chemosensory neurons as well as dopamine signaling. The authors also identify the behavioral mechanism that optimizes rational choice: animals modulate the angle of their head swings but not their rate of pumping to bring about utility maximization. By examining AWC's physiological responses to stimulation by food, the authors attempt to determine whether AWC's responses might encode a quantity that the worm's nervous system uses in calculating economic utility, but the results of these analyses provide no obvious simple answer. One significant concern about the work is a technical one: the authors infer bacterial density from spectrophotometry (OD600), which can be problematic when trying to make accurate assessments of this quantity. It's possible that errors in concentration estimation could undermine the conclusions drawn from these analyses.
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Reviewer #3 (Public Review):
This work is examining aspects of C. elegans foraging behavior under a new light, the one of behavioral economics. Authors focus on utility maximization and the Generalized Axiom of Revealed Preference (GARP), which are topics well studied in economics, and they attempt to confirm that nematodes' foraging decisions follow the equations that describe human consumption when they are presented with certain goods choices. This approach is completely novel and quite thought-provoking, and the topic can be very interesting to a broad range of researchers. Authors employ behavioral assays, microfluidics technology, electrophysiogy, and live imaging techniques to interrogate the system and collect data. Experiments are well designed, and in general, their partial conclusions are supported by the data. The findings …
Reviewer #3 (Public Review):
This work is examining aspects of C. elegans foraging behavior under a new light, the one of behavioral economics. Authors focus on utility maximization and the Generalized Axiom of Revealed Preference (GARP), which are topics well studied in economics, and they attempt to confirm that nematodes' foraging decisions follow the equations that describe human consumption when they are presented with certain goods choices. This approach is completely novel and quite thought-provoking, and the topic can be very interesting to a broad range of researchers. Authors employ behavioral assays, microfluidics technology, electrophysiogy, and live imaging techniques to interrogate the system and collect data. Experiments are well designed, and in general, their partial conclusions are supported by the data. The findings about the neuronal circuits involved in the choice assays is a significant contribution on its own. The main challenge with this work, though, is the framework that is proposed as an interpretation context for nematodes' behavior. The suggestion that C. elegans make decisions as if they were rational agents (a key assumption regarding human consumers in economics) is inherently problematic and could be considered a hasty attempt to marry economics with invertebrate neuroethology, since it does not address the key assumptions missing. Similarly, the claim that worms behave in a way to achieve utility maximization, is supposedly supported in the manuscript merely because nematodes' behavior is phenomenologically described by some behavioral economics equations. However, the question of what is it that nematodes are interested in maximizing (what constitutes utility for them?) remains loudly unanswered, as the authors admit. The above, in combination with other, less important unsupported claims (e.g., about nematodes' satisfaction and how it is achieved) raise doubts regarding the proposed approach.
Strengths:
The manuscript is written in a way that can be read by a broad range of researchers, and allows people who are not expert in economics to follow the authors' thought smoothly. Experiments are well designed, and all the techniques and assays are carefully selected and justified to serve the experimental needs. The T-maze assay and the pharyngeal electrophysiology assays in particular will most probably be used by many more researchers in the future. The attempt to provide an experimental system for behavioral economics is a creative idea, and the authors' meticulous work to this end is much appreciated. It is possible that this effort will inspire others to look for research ideas beyond traditional boundaries. The findings about the neuronal circuits that steer foraging decisions are very interesting and constitute an impactful contribution.
Weaknesses:
The suggestion that C. elegans make decisions as if they were rational agents, a key assumption regarding human consumers in economics, needs much more to be supported than just behavior conforming with selected behavioral economics equations. In addition, the claim that worms obey utility maximization principles sounds unconvincing since there is no answer of what they are trying to maximize. Moreover, there are other unsupported claims: i) about nematodes' satisfaction, when no definition or measurement of satisfaction is provided, ii) conclusions about the behavioral outcome of AWC neuron activation when it has been previously shown that there is not a deterministic correlation between strength of neuronal activation and behavioral outcome, and iii) stating that C. elegans food choices maximize their fitness, when there is not such experimental evidence.
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