The Grueneberg ganglion controls odor-driven food choices in mice under threat

Julien Brechbühl,Dean Wood,Aurélie De Vallière,Monique Nenniger Tosato,Marie-Christine Broillet

doi:10.1038/s42003-020-01257-w

Abstract

The ability to efficiently search for food is fundamental for animal survival. Olfactory messages are used to find food while being aware of the impending risk of predation. How these different olfactory clues are combined to optimize decision-making concerning food selection remains elusive. Here, we find that chemical danger cues drive the food selection in mice via the activation of a specific olfactory subsystem, the Grueneberg ganglion (GG). We show that a functional GG is required to decipher the threatening quality of an unfamiliar food. We also find that the increase in corticosterone, which is GG-dependent, enhances safe food preference acquired during social transmission. Moreover, we demonstrate that memory retrieval for food preference can be extinguished by activation of the GG circuitry. Our findings reveal a key function played by the GG in controlling contextual food responses and illustrate how mammalian organisms integrate environmental chemical stress to optimize decision-making.

Highlights

The ability to efficiently search for food is fundamental for animal survival
The conflicting environmental olfactory messages carried by odorants emitted by familiar food and by olfactory danger cues need to be continuously evaluated for risk taking and final food decision-making
We demonstrated that the guanylyl cyclase-D neurons (GC-D) neurons were still present in the main olfactory epithelium (MOE) after GG axotomy (Fig. 1c) thanks to the expression of the enzyme phosphodiesterase 2 A (PDE2A; Fig. 1b and c) which is shared by GG and GC-D circuities[19]

Summary

Introduction

The ability to efficiently search for food is fundamental for animal survival. Olfactory messages are used to find food while being aware of the impending risk of predation. We showed previously that these danger and warning cues are detected in a specialized olfactory subsystem, the Grueneberg ganglion[9,15] (GG) They generate, in the recipient mouse, stereotypical fear-related behaviors, such as freezing and risk assessment as well as stress-related systemic responses[15,18]. Using gene-targeted, surgically treated and sham-operated mice as well as a series of integrative behavioral assays, we functionally determine that the GG olfactory subsystem controls innate and acquired food preferences when mice smell an impending danger. We demonstrate that the acquisition of a food preference itself could be circumstantially reset by the activation of the GG circuitry, providing a decisionmaking advantage for mice

Methods

Results

Conclusion