Asymmetric Overlap in Neuronal Sensation Constraints Rational Choice in C. elegans

Rational choice theory in economics assumes optimality indecision-making. One of the basic axioms of economic rationality is "Independence of Irrelevant Alternatives" (IIA), according to which a preference ratio between two options should be unaffected by introducing additional alternatives to the choice set. Violations of IIA have been demonstrated in both humans and in various animals, and could therefore stem from common neuronal constraints. We used the nematode Caenorhabditis elegans, an animal with only 302 neurons and a fully mapped connectome, to examine when and why economic rationality and violations of rationality occur. We developed tests for IIA violations by characterizing the choices that C. elegans make in olfactory chemotaxis assays. In each assay, we exposed the worm to different odors that activate only specific neurons, thus involving in the choice process only defined neuronal networks, and tested whether particular neuronal architectures are prone to producing irrational choices. We found that C. elegans are capable of maintaining robust binary olfactory preferences irrespectively of the presence of a third attractive odor. However, in very specific olfactory contexts, which we term asymmetric overlaps, the preference ratio between the two odors was altered due to the addition of a third inferior odor, in a manner that violates IIA, and in certain cases can be considered "irrational" based on the economic definition of rationality. Our results suggest that different network configurations vary in their propensity to give rise to inconsistent decision making. Thus, non-optimal choices, assumed to be an outcome of high-order cognitive and mental processes, could result from much more basic attributes of neuronal activity and constrained computational mechanisms.