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

Abstract

During metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges in the middle cavity. Impacts of this metamorphic remodeling on odor processing, behavior, and network structure are still unexplored. Here, we used neuronal tracings, calcium imaging, and behavioral experiments to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity project axons to glomeruli in the ventral main olfactory bulb. These projections are gradually replaced by receptor neuron axons from the newly forming middle cavity epithelium. Despite this reorganization in the ventral bulb, two spatially segregated odor processing streams remain undisrupted and behavioral responses to waterborne odorants are unchanged. Contemporaneously, new receptor neurons in the remodeling principal cavity innervate the emerging dorsal part of the bulb, which displays distinct wiring features. Glomeruli around its midline are innervated from the left and right nasal epithelia. Additionally, postsynaptic projection neurons in the dorsal bulb predominantly connect to multiple glomeruli, while half of projection neurons in the ventral bulb are uni-glomerular. Our results show that the “water system” remains functional despite metamorphic reconstruction. The network differences between the dorsal and ventral olfactory bulb imply a higher degree of odor integration in the dorsal main olfactory bulb. This is possibly connected with the processing of different odorants, airborne vs. waterborne.

Network formation and reorganization of the olfactory system of Xenopus laevis

“…The Xenopus olfactory system is an interesting model to study olfactory evolution and adaptability to different lifestyles (Bear et al, 2016;Silva and Antunes, 2017;Weiss et al, 2021) as they spend early development in a completely aquatic environment, and during metamorphosis they develop a secondarily aquatic lifestyle in which they can detect both water and airborne odorants (Altner, 1962;Hansen et al, 1998;Dittrich et al, 2016). During the course of vertebrate evolution, olfactory systems have shown a tendency towards segregation into various subsystems.…”

“…Another subset of ORNs in the main OE has been found to respond to pharmacological agents that activate cAMP-dependent transduction mechanisms, e.g., forskolin, and are presumed to be ciliated (Figure 1.3). These ciliated ORNs have been proposed to be activated by bile acids and amines (Weiss et al, 2021).…”

“…-locating food sources (Veeranagoudar et al, 2004;Heerema et al, 2020), recognizing con-or heterospecifics, as well as kin (Blaustein and O'hara, 1982;Waldman, 1986), detecting predators or alarm signals (Mirza et al, 2006;Supekar and Gramapurohit, 2018;Raices, 2020), etc. For a comprehensive review of how olfaction plays an important role in behavior in anuran amphibians see (Weiss et al, 2021).…”

“…After metamorphosis is complete, the adult frog possesses a principal cavity that functions as a "air nose" and a middle cavity that functions as a newly formed "water nose", along side the adult vomeronasal organ (Reiss and Burd, 1997;Hansen et al, 1998;Gascuel and Amano, 2013). The major repopulation the OE with new ORNs that occurs during metamorphosis, and subsequent necessity for rewiring glomeruli in the OB, leads to the formation of the fully functional adult olfactory system, that can detect both water and airborne odorants (Weiss et al, 2021).…”

“…During the course of evolution olfactory systems have shown an incredible capacity for adaptation across all types of environmental niches, existing in both fully aquatic and terrestrial species, in vertebrates and invertebrates alike, providing countless adaptive advantages (Ache and Young, 2005;Weiss et al, 2021). Although the input is hugely varied, across different environments and species, olfactory systems across phyla are highly conserved in regards to anatomy, organization and function (Hildebrand and Shepherd, 1997;Gelperin, 1999;Eisthen, 2002;Ache and Young, 2005).…”