Does a third intermediate model for the vomeronasal processing of information exist? Insights from the macropodid neuroanatomy

Mateo V Torres,Pablo Sanchez-Quinteiro,José Luis Rois,Andrea Ferreiro,Irene Ortiz-Leal,Paula R Villamayor

doi:10.1007/s00429-021-02425-2

Mateo V Torres, Pablo Sanchez-Quinteiro + Show 4 more

Open Access

https://doi.org/10.1007/s00429-021-02425-2

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Abstract

The study of the α-subunit of Gi2 and Go proteins in the accessory olfactory bulb (AOB) was crucial for the identification of the two main families of vomeronasal receptors, V1R and V2R. Both families are expressed in the rodent and lagomorph AOBs, according to a segregated model characterized by topographical anteroposterior zonation. Many mammal species have suffered from the deterioration of the Gαo pathway and are categorized as belonging to the uniform model. This scenario has been complicated by characterization of the AOB in the tammar wallaby, Notamacropus eugenii, which appears to follow a third model of vomeronasal organization featuring exclusive Gαo protein expression, referred to as the intermediate model, which has not yet been replicated in any other species. Our morphofunctional study of the vomeronasal system (VNS) in Bennett’s wallaby, Notamacropus rufogriseus, provides further information regarding this third model of vomeronasal transduction. A comprehensive histological, lectin, and immunohistochemical study of the Bennett’s wallaby VNS was performed. Anti-Gαo and anti-Gαi2 antibodies were particularly useful because they labeled the transduction cascade of V2R and V1R receptors, respectively. Both G proteins showed canonical immunohistochemical labeling in the vomeronasal organ and the AOB, consistent with the anterior–posterior zonation of the segregated model. The lectin Ulex europaeus agglutinin selectively labeled the anterior AOB, providing additional evidence for the segregation of vomeronasal information in the wallaby. Overall, the VNS of the Bennett’s wallaby shows a degree of differentiation and histochemical and neurochemical diversity comparable to species with greater VNS development. The existence of the third intermediate type in vomeronasal information processing reported in Notamacropus eugenii is not supported by our lectin-histochemical and immunohistochemical findings in Notamacropus rufogriseus.

Highlights

The sense organs transmit physical or chemical signals
These attempts have been hampered by the broad morphofunctional (Salazar et al 2007; Stoyanov et al 2021), molecular (Isogai et al 2011; Katreddi and Forni 2021), and genomic (Grus et al 2005; Villamayor et al 2021) diversity of this system among mammals, which makes the establishment of a valid general pattern challenging, even among species belonging to the same order, such as Rodentia (Torres et al 2020)
The medial side of the vomeronasal organ (VNO) lays over the lateral lamina of the vomer bone, and the ventral portion of the VNO rests on the continuous ridge formed by the palatine processes of the incisive and maxillary bones

Summary

Introduction

The sense organs transmit physical (sight, hearing, and touch) or chemical (smell and taste) signals. To intervene in chemical communications, a solid morphofunctional foundation of the VNS is necessary to allow for the understanding of the mechanism of action mediated by various pheromones in different species. These attempts have been hampered by the broad morphofunctional (Salazar et al 2007; Stoyanov et al 2021), molecular (Isogai et al 2011; Katreddi and Forni 2021), and genomic (Grus et al 2005; Villamayor et al 2021) diversity of this system among mammals, which makes the establishment of a valid general pattern challenging, even among species belonging to the same order, such as Rodentia (Torres et al 2020)

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