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Multimodal Imaging and Analysis of the Neuroanatomical Organization of the Primary Olfactory Inputs in the Brownbanded Bamboo Shark, Chiloscyllium punctatum
journal contributionposted on 2021-01-18, 03:12 authored by V Camilieri-Asch, HT Caddy, A Hubbard, P Rigby, B Doyle, JA Shaw, A Mehnert, JC Partridge, KE Yopak, Shaun CollinShaun Collin
© Copyright © 2020 Camilieri-Asch, Caddy, Hubbard, Rigby, Doyle, Shaw, Mehnert, Partridge, Yopak and Collin. There is currently a limited understanding of the morphological and functional organization of the olfactory system in cartilaginous fishes, particularly when compared to bony fishes and terrestrial vertebrates. In this fish group, there is a clear paucity of information on the characterization, density, and distribution of olfactory receptor neurons (ORNs) within the sensory olfactory epithelium lining the paired olfactory rosettes, and their functional implications with respect to the hydrodynamics of incurrent water flow into the nares. This imaging study examines the brownbanded bamboo shark Chiloscyllium punctatum (Elasmobranchii) and combines immunohistochemical labeling using antisera raised against five G-protein α-subunits (Gαs/olf, Gαq/11/14, Gαi–1/2/3, Gαi–3, Gαo) with light and electron microscopy, to characterize the morphological ORN types present. Three main ORNs (“long”, “microvillous” and “crypt-like”) are confirmed and up to three additional microvilli-bearing types are also described; “Kappe-like” (potential or homologous “Kappe” as in teleosts), “pear-shaped” and “teardrop-shaped” cells. These morphotypes will need to be confirmed molecularly in the future. Using X-ray diffusible iodine-based contrast-enhanced computed tomography (diceCT), high-resolution scans of the olfactory rosettes, olfactory bulbs (OBs), peduncles, and telencephalon reveal a lateral segregation of primary olfactory inputs within the OBs, with distinct medial and lateral clusters of glomeruli, suggesting a potential somatotopic organization. However, most ORN morphotypes are found to be ubiquitously distributed within the medial and lateral regions of the olfactory rosette, with at least three microvilli-bearing ORNs labeled with anti-Gαo found in significantly higher densities in lateral lamellae [in lateral lamellae] and on the anterior portion of lamellae (facing the olfactory cavity). These microvilli-bearing ORN morphotypes (microvillous, “Kappe-like,” “pear-shaped,” and “teardrop-shaped”) are the most abundant across the olfactory rosette of this species, while ciliated ORNs are less common and crypt cells are rare. Spatial simulations of the fluid dynamics of the incurrent water flow into the nares and within the olfactory cavities indicate that the high densities of microvilli-bearing ORNs located within the lateral region of the rosette are important for sampling incoming odorants during swimming and may determine subsequent tracking behavior.
VC-A was supported by the Australian Federal Government and The University of Western Australia (UWA), in the form of an Australian Training Program and the UWA Safety-Net Top-up scholarships. This study was funded by the UWA School of Biological Sciences research funds for Ph.D. students and the Ada Jackson Irwin Street Commemoration Award for Women in Zoology.
JournalFrontiers in Neuroanatomy
Pagination25p. (p. 1-25)
Rights StatementThe Author reserves all moral rights over the deposited text and must be credited if any re-use occurs. Documents deposited in OPAL are the Open Access versions of outputs published elsewhere. Changes resulting from the publishing process may therefore not be reflected in this document. The final published version may be obtained via the publisher’s DOI. Please note that additional copyright and access restrictions may apply to the published version.
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Science & TechnologyLife Sciences & BiomedicineAnatomy & MorphologyNeurosciencesNeurosciences & Neurologyolfactory pathwayelasmobranchdiceCTLMSEMTEMIHC3D simulationsPROTEIN ALPHA-SUBUNITSRECEPTOR NEURONSSENSORY NEURONSCHEMOSENSORY RECEPTORSFUNCTIONAL-MORPHOLOGYELASMOBRANCH FISHCRYPT NEURONSAMINO-ACIDSGENE FAMILYCELL-TYPES