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

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. Innate odor preferences in C. elegans are controlled by the activation of a pair of olfactory sensory neurons. Here, the authors show that asymmetric activation of the AWCON and AWCOFF neurons can lead to irrational olfactory preferences that are explained by a model of normalization of sensory gain control.