Conservation of Glomerular Organization in the Main Olfactory Bulb of Anuran Larvae

Abstract

The glomerular array in the olfactory bulb of many vertebrates is segregated into molecularly and anatomically distinct clusters linked to different olfactory functions. In anurans, glomerular clustering is so far only described in Xenopus laevis. We traced olfactory projections to the bulb in tadpoles belonging to six distantly related anuran species in four families (Pipidae, Hylidae, Bufonidae, Dendrobatidae) and found that glomerular clustering is remarkably conserved. The general bauplan consists of four unequally sized glomerular clusters with minor inter-species variation. During metamorphosis, the olfactory system undergoes extensive remodeling. Tracings in metamorphotic and juvenile Dendrobates tinctorius and Xenopus tropicalis suggest a higher degree of variation in the glomerular organization after metamorphosis is complete. Our study highlights, that the anatomical organization of glomeruli in the main olfactory bulb (MOB) is highly conserved, despite an extensive ecomorphological diversification among anuran tadpoles, which suggests underlying developmental constraints.

Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

“…Since Xenopus remains fully aquatic after metamorphosis is completed, it is conceivable, that there is less or no reduction of functionality in the water-smelling system during metamorphotic climax than in species that change their lifestyle. This idea is further supported by a recent study showing that the glomerular clusters in the water bulb of Dendrobates tinctorius, a terrestrial frog species, seem gradually reduced until postmetamorphosis, when compared to the vMOB in Xenopus (Weiss et al, 2020a).…”

“…Receptor neurons in the VNO project their axons towards their target structures, the glomeruli, in the accessory olfactory bulb (Reiss and Eisthen, 2008; Jungblut et al, 2012). ORNs residing in the PC of larval Xenopus project their axons to glomeruli arranged in the ventral portion of the main olfactory bulb (vMOB) (Reiss and Burd, 1997a; Weiss et al, 2020a). During metamorphosis, these axonal projections from the PC to the vMOB are replaced by ORN axons originating in the newly formed MC, the adult ‘water nose’ (Key and Giorgi, 1986; Hofmann and Meyer, 1991; Franceschini et al, 1992; Reiss and Burd, 1997a).…”

Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

“…Since Xenopus remains fully aquatic after metamorphosis is completed, it is likely, that there is less or no reduction of functionality in the water-smelling system during metamorphic climax, compared with species that change their lifestyle. This idea is further supported by a recent study showing that the glomerular clusters in the water bulb of Dendrobates tinctorius, a terrestrial frog species, seem gradually reduced until postmetamorphosis, when compared to the vMOB in Xenopus (Weiss et al 2020a ).…”

“…Receptor neurons in the VNO project their axons towards their target structures, the glomeruli, in the accessory olfactory bulb (Reiss and Eisthen 2008 ; Jungblut et al 2012 ). ORNs residing in the PC of larval Xenopus project their axons to glomeruli arranged in the ventral portion of the main olfactory bulb (vMOB) (Reiss and Burd 1997b ; Weiss et al 2020a ). During metamorphosis, these axonal projections from the PC to the vMOB are replaced by ORN axons originating in the newly formed MC, the adult “water nose” (Key and Giorgi 1986 ; Hofmann and Meyer 1991 ; Franceschini et al 1992 ; Reiss and Burd 1997b ).…”

“…Medially located glomeruli are putatively connected to ciliated ORNs and mainly respond to alcohols, aldehydes, and amines instead (Gliem et al 2013 ). While there is evidence that the anatomy of the glomeruli in the vMOB remains stable during metamorphosis (Gaudin and Gascuel 2005 ; Weiss et al 2020a ), it is still unknown whether the innervation shift from the larval PC to the adult MC affects its function and/or its behavioral output.…”