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

Camilieri-Asch, Victoria; Shaw, Jeremy; Yopak, Kara E.; Chapuis, Lucille; Partridge, Julian C.; Collin, Shaun P.

doi:10.1007/s00429-020-02127-1

Cited by 15 publications

(11 citation statements)

References 125 publications

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“…The dimensions of the olfactory bulbs were often used to determine the olfactory capacity of a species and would indicate the significance of the olfactory sense in E. lucifer (Camilieri‐Asch, Shaw, et al, 2020 ; Camilieri‐Asch, Yopak, et al, 2020 ; Schluessel et al, 2008 , 2009 ; Theisen et al, 1986 ; Zeiske et al, 1987 ). The sheer size of the nasal capsules does not necessarily allow conclusions on the efficiency of the olfactory system (Gardiner et al, 2012 ; Meredith et al, 2012 ; Meredith & Kajiura, 2010 ), however, Camilieri‐Asch, Yopak, et al ( 2020 ) claim that the dimensions of the olfactory bulbs are correlated with the number of olfactory stimuli through the epithelium.…”

Section: Discussionmentioning

confidence: 99%

“…This study describes the cranial morphology of an etmopterid shark species in detail using (dice)micro‐CT data for the first time. Camilieri‐Asch, Caddy, et al ( 2020 ) and Camilieri‐Asch, Shaw, et al ( 2020 ) have also performed diceCT scans, but of galeomorph sharks, among others, and published the results in two very recent studies. Kamminga et al ( 2017 ) performed CT scans of a wide variety of species but included in their database only hard tissues.…”

Section: Discussionmentioning

confidence: 99%

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Head anatomy of a lantern shark wet‐collection specimen (Chondrichthyes: Etmopteridae)

2023

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In this study, we apply a two‐step (untreated and soft tissue stained) diffusible iodine‐based contrast‐enhanced micro‐computed tomography array to a wet‐collection Lantern Shark specimen of Etmopterus lucifer . The focus of our scanning approach is the head anatomy. The unstained CT data allow the imaging of mineralized (skeletal) tissue, while results for soft tissue were achieved after staining for 120 h in a 1% ethanolic iodine solution. Three‐dimensional visualization after the segmentation of hard as well as soft tissue reveals new details of tissue organization and allows us to draw conclusions on the significance of organs in their function. Outstanding are the ampullae of Lorenzini for electroreception, which appear as the dominant sense along with the olfactory system. Corresponding brain areas of these sensory organs are significantly enlarged as well and likely reflect adaptations to the lantern sharks' deep‐sea habitat. While electroreception supports the capture of living prey, the enlarged olfactory system can guide the scavenging of these opportunistic feeders. Compared to other approaches based on the manual dissection of similar species, CT scanning is superior in some but not all aspects. For example, fenestrae of the cranial nerves within the chondrocranium cannot be identified reflecting the limitations of the method, however, CT scanning is less invasive, and the staining is mostly reversible and can be rinsed out.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Head anatomy of a lantern shark wet‐collection specimen (Chondrichthyes: Etmopteridae)

2023

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“…Based on previous research suggesting no bilateral differences between the left and right olfactory structures in fishes (e.g., Camilieri‐Asch, Shaw, et al, 2020 ), the left rosette was arbitrarily dissected from each specimen to assess its morphology. Following postfixation, the olfactory rosette was separated from the olfactory nerve (nI) and immersed in a 0.1 mol L −1 phosphate buffer solution (PBS) for 24 h. Rosettes were then submerged in 1:1 ratio of osmium tetroxide in a 0.1 mol L −1 PBS for 1 h. Samples were then washed with deionized (DI) water to remove excess fixative and dehydrated through a classic graded ethanol series (20 min for each series).…”

Section: Methodsmentioning

confidence: 99%

Ontogenetic shifts in olfactory rosette morphology of the sockeye salmon, Oncorhynchus nerka

Rheinsmith

Quinn

Dittman

et al. 2022

Journal of Morphology

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Sockeye salmon, Oncorhynchus nerka, are anadromous, semelparous fish that breed in freshwater—typically in streams, and juveniles in most populations feed in lakes for 1 or 2 years, then migrate to sea to feed for 2 or 3 additional years, before returning to their natal sites to spawn and die. This species undergoes important changes in behavior, habitat, and morphology through these multiple life history stages. However, the sensory systems that mediate these migratory patterns are not fully understood, and few studies have explored changes in sensory function and specialization throughout ontogeny. This study investigates changes in the olfactory rosette of sockeye salmon across four different life stages (fry, parr, smolt, and adult). Development of the olfactory rosette was assessed by comparing total rosette size (RS), lamellae number, and lamellae complexity from scanning electron microscopy images across life stages, as a proxy for olfactory capacity. Olfactory RS increased linearly with lamellae number and body size (p < .001). The complexity of the rosette, including the distribution of sensory and nonsensory epithelia and the appearance of secondary lamellar folding, varied between fry and adult life stages. These differences in epithelial structure may indicate variation in odor‐processing capacity between juveniles imprinting on their natal stream and adults using those odor memories in the final stages of homing to natal breeding sites. These findings improve our understanding of the development of the olfactory system throughout life in this species, highlighting that ontogenetic shifts in behavior and habitat may coincide with shifts in nervous system development.

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“…For CP4-6, the contrast levels observed in the head and within the brain allowed us to differentiate nervous tissue from other tissues (epithelial, connective, and muscular). This approach enabled us to segment, i.e., label, the olfactory rosettes, primary projections and olfactory bulbs, following the methods described in Camilieri-Asch et al (2020a, 2020b, using the software Avizo (v9.2.0, Thermo Fisher Scientific, United States). Specifically, this was achieved by cropping down to the region of interest, applying a non-local-means (NLM) filter to attenuate noise, and then interactive labeling using the suite of tools in the segmentation editor.…”

Section: Diffusible Iodine-based Contrast-enhanced Computed Tomographmentioning

confidence: 99%

Multimodal Imaging and Analysis of the Neuroanatomical Organization of the Primary Olfactory Inputs in the Brownbanded Bamboo Shark, Chiloscyllium punctatum

et al. 2020

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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.

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

Cited by 15 publications

References 125 publications

Head anatomy of a lantern shark wet‐collection specimen (Chondrichthyes: Etmopteridae)

Head anatomy of a lantern shark wet‐collection specimen (Chondrichthyes: Etmopteridae)

Ontogenetic shifts in olfactory rosette morphology of the sockeye salmon, Oncorhynchus nerka

Multimodal Imaging and Analysis of the Neuroanatomical Organization of the Primary Olfactory Inputs in the Brownbanded Bamboo Shark, Chiloscyllium punctatum

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