Bounded rationality in C. elegans is explained by circuit-specific normalization in chemosensory pathways

Dror Cohen,Lilach Elbaum,Dino J Levy,Asaf Madar,Oded Rechavi,Guy Teichman,Meshi Volovich,Yoav Zeevi,Kenway Louie

doi:10.1038/s41467-019-11715-7

Abstract

Rational choice theory assumes optimality in decision-making. Violations of a basic axiom of economic rationality known as “Independence of Irrelevant Alternatives” (IIA) have been demonstrated in both humans and animals and could stem from common neuronal constraints. Here we develop tests for IIA in the nematode Caenorhabditis elegans, an animal with only 302 neurons, using olfactory chemotaxis assays. We find that in most cases C. elegans make rational decisions. However, by probing multiple neuronal architectures using various choice sets, we show that violations of rationality arise when the circuit of olfactory sensory neurons is asymmetric. We further show that genetic manipulations of the asymmetry between the AWC neurons can make the worm irrational. Last, a context-dependent normalization-based model of value coding and gain control explains how particular neuronal constraints on information coding give rise to irrationality. Thus, we demonstrate that bounded rationality could arise due to basic neuronal constraints.

Highlights

Rational choice theory assumes optimality in decision-making
While Independence of Irrelevant Alternatives” (IIA) violations have been observed in a wide variety of organisms5–11, despite numerous repetitions and iterations, we found that in C. elegans the addition of increasing concentrations of odor C did not lead to violations of rationality, as the preference ratio between odors A and B did not change in a statistically significant or physiologically relevant way
In this work, we demonstrate for the first time that even C. elegans, with its extremely minimal nervous system, displays IIA violations in decision-making

Summary

Introduction

Rational choice theory assumes optimality in decision-making. Violations of a basic axiom of economic rationality known as “Independence of Irrelevant Alternatives” (IIA) have been demonstrated in both humans and animals and could stem from common neuronal constraints. Normative models of decision-making, such as rational choice theory in economics and foraging theory in ecology, assume optimality in the behavior of individual choosers. Their core principle is utility maximization, which assumes that choosers act to maximize an internal measure of satisfaction. One central requirement of rationality and stable value functions is independence of irrelevant alternatives, or IIA16 According to this axiom, a preference between two options should be unaffected by the number or quality of any additional options, and the relative choice ratio between options A and B (pA/pB) should remain constant regardless of the choice set. Contextual factors such as choice set size and composition significantly alter animal and human decisions

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