Abstract

In the mouse, the Grueneberg ganglion (GG) is an olfactory subsystem implicated both in chemo- and thermo-sensing. It is specifically involved in the recognition of volatile danger cues such as alarm pheromones and structurally-related predator scents. No evidence for these GG sensory functions has been reported yet in other rodent species. In this study, we used a combination of histological and physiological techniques to verify the presence of a GG and investigate its function in the rat, hamster, and gerbil comparing with the mouse. By scanning electron microscopy (SEM) and transmitted electron microscopy (TEM), we found isolated or groups of large GG cells of different shapes that in spite of their gross anatomical similarities, display important structural differences between species. We performed a comparative and morphological study focusing on the conserved olfactory features of these cells. We found fine ciliary processes, mostly wrapped in ensheating glial cells, in variable number of clusters deeply invaginated in the neuronal soma. Interestingly, the glial wrapping, the amount of microtubules and their distribution in the ciliary processes were different between rodents. Using immunohistochemistry, we were able to detect the expression of known GG proteins, such as the membrane guanylyl cyclase G and the cyclic nucleotide-gated channel A3. Both the expression and the subcellular localization of these signaling proteins were found to be species-dependent. Calcium imaging experiments on acute tissue slice preparations from rodent GG demonstrated that the chemo- and thermo-evoked neuronal responses were different between species. Thus, GG neurons from mice and rats displayed both chemo- and thermo-sensing, while hamsters and gerbils showed profound differences in their sensitivities. We suggest that the integrative comparison between the structural morphologies, the sensory properties, and the ethological contexts supports species-dependent GG features prompted by the environmental pressure.

Highlights

  • In the nasal cavities of the mouse, close to the opening of the nares, a ganglion structure of unknown function was found in 1973 (Grüneberg, 1973)

  • Detection of danger signals such as chemical warnings emitted by their conspecifics or predator-produced cues takes place in the different olfactory subsystems present in their nasal cavities, which convey multiple sensory informations (Ma, 2010)

  • We here focused on the GG, an olfactory subsystem devoted to the detection of environmental stress (Brechbühl et al, 2008, 2013b), which is located in the rhinarium region (Haidarliu et al, 2012, 2013; Brechbühl et al, 2013a)

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Summary

Introduction

In the nasal cavities of the mouse, close to the opening of the nares, a ganglion structure of unknown function was found in 1973 (Grüneberg, 1973). Histological investigations performed at the time allowed the identification of similar ganglion structures in other mammalian species (Grüneberg, 1973; Tachibana et al, 1990) It was rediscovered in 2005 (Fuss et al, 2005; Koos and Fraser, 2005; Fleischer et al, 2006a; Roppolo et al, 2006; Storan and Key, 2006) during inspection of whole-mount specimens from a particular gene-targeted OMP-GFP (olfactory marker protein-green fluorescent protein) mouse in which all mature olfactory neurons express GFP as a histological reporter under the control of the OMP promoter (Margolis, 1972; Mombaerts et al, 1996; Potter et al, 2001). We found the mouse GG to be involved in the recognition of volatile danger

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