Irrational behavior in C. elegans arises from asymmetric modulatory effects within single sensory neurons

Shachar Iwanir,Eduard Bokman,Christian O Pritz,Eyal Itskovits,Rotem Ruach,Alon Zaslaver

doi:10.1038/s41467-019-11163-3

Shachar Iwanir, Eduard Bokman + Show 4 more

Open Access

https://doi.org/10.1038/s41467-019-11163-3

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Journal: Nature Communications	Publication Date: Jul 19, 2019
Citations: 17	License type: open-access

Affiliation: Hebrew University of Jerusalem

Abstract

C. elegans worms exhibit a natural chemotaxis towards food cues. This provides a potential platform to study the interactions between stimulus valence and innate behavioral preferences. Here we perform a comprehensive set of choice assays to measure worms’ relative preference towards various attractants. Surprisingly, we find that when facing a combination of choices, worms’ preferences do not always follow value-based hierarchy. In fact, the innate chemotaxis behavior in worms robustly violates key rationality paradigms of transitivity, independence of irrelevant alternatives and regularity. These violations arise due to asymmetric modulatory effects between the presented options. Functional analysis of the entire chemosensory system at a single-neuron resolution, coupled with analyses of mutants, defective in individual neurons, reveals that these asymmetric effects originate in specific sensory neurons.

Highlights

DDW DA DA DA 5–5 –3 2–2Stimulus = DA-3 1 DDW TT TT 5–5 –3 Stimulus c Stimulus = IA-1 *–1 DDW TT TT TT 5–5 –3 2–2Stimulus = TT2-2 1 0.8 0.6 0.4 0.2 0 –0.2 –0.4 –0.6 –0.8 –1DDW IA IA IA –4 –3 –1 d Stimulus = DA-3–1 DDW IA IA IA –4 –3 –1
When option B was a null option, we denoted it as the Basal Chemotaxis Index, basal preference to the stimulus (BCI)(A)
Analysis of the relative preferences between pairs of stimuli revealed that worms typically (> 85%) preferred the option with the higher BCI, suggesting that worms’ innate behavior generally conforms to a hierarchical preference structure

Summary

Introduction

DDW IA IA IA –4 –3 –1 d Stimulus = DA-3. Following the finding of modulatory effects that TT exerts on IA (but not on DA, Fig. 4b–c), we were able to design experimental conditions that will exploit this asymmetry to demonstrate violations of IIA and regularity (Fig. 7). In this case, trans-modulatory effects, rather than cross-modulatory effects, lead to violations of these paradigms, where option C (TT) modulates the preference to option A (DA) differently than it modulates the preference to option B (IA) (Fig. 8b)

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Conclusion