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Volumetric analysis and morphological assessment of the ascending olfactory pathway in an elasmobranch and a teleost using diceCT

Brain Structure and Function volume 225, pages 2347–2375 (2020)Cite this article

Abstract

The size (volume or mass) of the olfactory bulbs in relation to the whole brain has been used as a neuroanatomical proxy for olfactory capability in a range of vertebrates, including fishes. Here, we use diffusible iodine-based contrast-enhanced computed tomography (diceCT) to test the value of this novel bioimaging technique for generating accurate measurements of the relative volume of the main olfactory brain areas (olfactory bulbs, peduncles, and telencephalon) and to describe the morphological organisation of the ascending olfactory pathway in model fish species from two taxa, the brownbanded bamboo shark Chiloscyllium punctatum and the common goldfish Carassius auratus. We also describe the arrangement of primary projections to the olfactory bulb and secondary projections to the telencephalon in both species. Our results identified substantially larger olfactory bulbs and telencephalon in C. punctatum compared to C. auratus (comprising approximately 5.2% vs. 1.8%, and 51.8% vs. 11.8% of the total brain volume, respectively), reflecting differences between taxa, but also possibly in the role of olfaction in the sensory ecology of these species. We identified segregated primary projections to the bulbs, associated with a compartmentalised olfactory bulb in C. punctatum, which supports previous findings in elasmobranch fishes. DiceCT imaging has been crucial for visualising differences in the morphological organisation of the olfactory system of both model species. We consider comparative neuroanatomical studies between representative species of both elasmobranch and teleost fish groups are fundamental to further our understanding of the evolution of the olfactory system in early vertebrates and the neural basis of olfactory abilities.

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Raw data available in Supplementary Material.

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Acknowledgements

The authors acknowledge the facilities, scientific and technical assistance of the Microscopy Australia (MA) facility at the Centre for Microscopy, Characterisation and Analysis (CMCA), a facility funded by UWA, and the State and Commonwealth Governments. The authors would also like to thank Caroline Kerr and Lyn Kirilak for laboratory assistance, and Dr. Jonathan D. Mitchell for providing comments improving the manuscript.

Funding

VCA was supported by the Australian Federal Government and The University of Western Australia (UWA), in the form of an Australian Research Training Program and The UWA Safety-Net Top-Up scholarships. The research was funded by The UWA Faculty of Science, School of Biological Sciences.

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Authors and Affiliations

  1. School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Victoria Camilieri-Asch

  2. Oceans Institute, Indian Ocean Marine Research Centre (IOMRC), The University of Western Australia, Cnr Fairway and Service Road 4, Crawley, WA, 6009, Australia

    Victoria Camilieri-Asch, Julian C. Partridge & Shaun P. Collin

  3. Centre for Microscopy, Characterisation and Analysis (CMCA), The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Jeremy A. Shaw

  4. Department of Biology and Marine Biology and the Center for Marine Science, University of North Carolina Wilmington, 5600 Marvin K Moss Lane, Wilmington, NC, 28409, USA

    Kara E. Yopak

  5. Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope, Stocker Road, Exeter, EX4 4QD, UK

    Lucille Chapuis

  6. Ocean Graduate School, IOMRC, The University of Western Australia, Cnr Fairway and Service Entrance 4, Crawley, WA, 6009, Australia

    Shaun P. Collin

  7. School of Life Sciences, La Trobe University, Plenty Road and Kingsbury Drive, Bundoora, VIC, 3086, Australia

    Shaun P. Collin

  8. Centre for Transformative Biomimetics in Bioengineering, Institute of Health and Biomedical Innovation (IHBI), Queensland University of Technology, Q Block Level 7, 60 Musk Avenue, Kelvin Grove, QLD, 4059, Australia

    Victoria Camilieri-Asch

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  1. Victoria Camilieri-Asch
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  2. Jeremy A. Shaw
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Contributions

SPC, KEY, JAS and VCA conceived this research. LC donated the shark specimens. VCA acquired, analysed and interpreted the data, under the technical guidance of JAS. JCP and LC assisted with the interpretation of the data. VCA drafted the manuscript. All authors collaborated in its revision.

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Correspondence to Victoria Camilieri-Asch.

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Camilieri-Asch, V., Shaw, J.A., Yopak, K.E. et al. Volumetric analysis and morphological assessment of the ascending olfactory pathway in an elasmobranch and a teleost using diceCT. Brain Struct Funct 225, 2347–2375 (2020). https://doi.org/10.1007/s00429-020-02127-1

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Keywords

  • Brain
  • Neuroanatomy
  • Morphometrics
  • Olfaction
  • Elasmobranch
  • Teleost
  • X-ray tomography