Morphological and physiological species-dependent characteristics of the rodent Grueneberg ganglion

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.

Olfactory Sensitivity in Mammalian Species

“…Although vomeronasal ducts and pits have been observed in humans (Moran et al 1991, Stensaas et al 1991, Boehm and Gasser 1993, Trotier and Doving 1996, evidence of functional vomeronasal receptor neurons connected to the brain has not been found in adult humans (Johnson 1998, Smith et al 2014. In some species, there are two additional spatially segregated clusters of sensory cells, the septal organ (SO) (Storan and Key 2006) and the Grueneberg ganglion (GG), which are particularly well developed in mice (Brechbuhl et al 2014). Each of the four physically segregated apparatuses can convey sensory information about multiple modalities and serve multiple functions.…”

Identification of pyridine analogs as new predator-derived kairomones

“…Noses from OMP-GFP mice (P1-7) of both sexes were dissected in ice-cold artificial cerebrospinal fluid (ACSF), containing 118 mM NaCl, 25 mM NaHCO 3 , 10 mM D-glucose, 2 mM KCl, 2 mM MgCl 2 , 1.2 mM NaH 2 PO 4 , and 2 mM CaCl 2 (pH 7.4) saturated with oxycarbon gas [95% O 2 : 5% CO 2 ; (vol/vol)] under a fluorescence-equipped dissecting microscope (M165 FC; Leica). For calcium imaging experiments, acute tissue slice preparations of the GG were performed (Brechbühl et al, 2008 , 2014 ). Briefly, the tip of the nose was included in a block of low melting 4–5% agar.…”

“…The particularity of the GG olfactory subsystem resides in its specifically tuned chemical detection abilities. Indeed, this rostral olfactory subsystem found in rodents (Grüneberg, 1973 ; Tachibana et al, 1990 ; Fuss et al, 2005 ; Koos and Fraser, 2005 ; Fleischer et al, 2006a ; Roppolo et al, 2006 ; Storan and Key, 2006 ; Fleischer and Breer, 2010 ; Brechbühl et al, 2014 ) is dedicated to the detection of volatile danger molecules from both intra and interspecies origins such as alarm pheromones (Brechbühl et al, 2008 ; Debiec and Sullivan, 2014 ) and kairomones (Brechbühl et al, 2013b ) which share heterocyclic sulfur- or nitrogen-containing structures (Mamasuew et al, 2011 ; Brechbühl et al, 2013a , b ; Hanke et al, 2013 ). These chemical cues initiate, in the recipient animal, stress reactions (Brechbühl et al, 2013b ; Matsuo et al, 2015 ; Perez-Gomez et al, 2015 ).…”

Revisiting the Vomeronasal System From an Integrated Perspective

“…Morphologically, the GgG forms a neat neuronal cluster. It has been described in detail in certain rodents –mouse, rat, hamster and gerbil– displaying subtle differences between them (Brechbühl et al, ). In other groups of mammals its presence is very unclear and, as in the case of the SO, our attempts to identify the ganglion in domestic mammals were unsuccessful, data partially published (Barrios et al, ).…”