3D atlas describing the ontogenic evolution of the primary olfactory projections in the olfactory bulb of Xenopus laevis

Abstract

The adult Xenopus presents the unique capability to smell odors both in water and air thanks to two different olfactory pathways. Nevertheless, the tadpole can initially perceive only water-borne odorants, as the olfactory receptor neurons (ORN) that will detect air-borne odorants develop later. Such a phenomenon requires major reorganization processes. Here we focused on the precise description of the neuroanatomical modifications occurring in the olfactory bulb (OB) of the tadpole throughout metamorphosis. Using both carbocyanine dyes and lectin staining, we investigated the evolution of ORN projection patterns into the OB from Stages 47 to 66, thus covering the period of time when all the modifications take place. Although our results confirm previous works (Reiss and Burd [1997] Semin Cell Dev Biol 8:171-179), we showed for the first time that the main olfactory bulb (MOB) is subdivided into seven zones at Stage 47 plus the accessory olfactory bulb (AOB). These seven zones receive fibers dedicated to aquatic olfaction ("aquatic fibers") and are conserved until Stage 66. At Stage 48 the first fibers dedicated to the aerial olfaction constitute a new dorsomedial zone that grows steadily, pushing the seven original zones ventrolaterally. Only the part of the OB receiving aquatic fibers is fragmented, reminiscent of the organization described in fish. This raises the question of whether such an organization in zones constitutes a plesiomorphy or is linked to aquatic olfaction. We generated a 3D atlas at several stages which are representative of the reorganization process. This will be a useful tool for future studies of development and function.

Chemosensory reception, behavioral expression, and ecological interactions at multiple trophic levels

“…Whereas Class I receptors are specialized for detecting water-soluble compounds, Class II receptors detect only gaseous volatiles in adults. Ultimately, new central projections connect Class I receptor cells to the ventrolateral olfactory bulb in adults (Reiss and Burd, 1997;Gaudin and Gascuel, 2005).…”

Developmental analysis of the extrabulbar olfactory projections in the ranid frog with some phylogenetic considerations

“…However, among anurans the adult Bufo marinus has an EBOS with a pattern identical to that of X. laevis (Hofmann & Meyer 1989b), but there is no evidence of a water nose in Bufo species. Furthermore, some authors, differ from Hofmann and Meyer (1992), describing the origin of the EBOS from the air nose (Gaudin & Gascuel 2005). Besides anurans, this putative relationship of an EBOS with water-borne odorants does not fit in other amphibian groups as well, in which an EBOS has been reported in species that usually do not smell underwater.…”

Recording Temperature-induced Neuronal Activity through Monitoring Calcium Changes in the Olfactory Bulb of <em>Xenopus laevis</em>

“…The olfactory receptor neurons of premetamorphic X. laevis terminate in tufts, and make synaptic contacts with the dendrites of second-order neurons, the mitral cells. Pre-and postsynaptic fibers intermingle and form skein-like neuropil structures called glomeruli 3 . The abundant synapses of the glomerular layer represent the first processing center of olfactory information.…”

“…The staining by electroporation of two spectrally distinct dyes loaded in the nasal cavities serves to single out the γ-glomerulus 3 through its bilateral innervation by ORNs from both olfactory epithelia. Thus, .…”