Convergence of Olfactory Inputs within the Central Nervous System of a Cartilaginous and a Bony Fish: An Anatomical Indicator of Olfactory Sensitivity

Abstract

The volume of the olfactory bulbs (OBs) relative to the brain has been used previously as a proxy for olfactory capabilities in many vertebrate taxa, including fishes. Although this gross approach has predictive power, a more accurate assessment of the number of afferent olfactory inputs and the convergence of this information at the level of the telencephalon is critical to our understanding of the role of olfaction in the behaviour of fishes. In this study, we used transmission electron microscopy to assess the number of first-order axons within the olfactory nerve (ON) and the number of second-order axons in the olfactory peduncle (OP) in established model species within cartilaginous (brownbanded bamboo shark, <i>Chiloscyllium punctatum</i> [CP]) and bony (common goldfish, <i>Carassius auratus</i> [CA]) fishes. The total number of axons varied from a mean of 18.12 ± 7.50 million in the ON to a mean of 0.38 ± 0.21 million in the OP of CP, versus 0.48 ± 0.16 million in the ON and 0.09 ± 0.02 million in the OP of CA. This resulted in a convergence ratio of approximately 50:1 and 5:1, respectively, for these two species. Based on astroglial ensheathing, axon type (unmyelinated [UM] and myelinated [M]) and axon size, we found no differentiated tracts in the OP of CP, whereas a lateral and a medial tract (both of which could be subdivided into two bundles or areas) were identified for CA, as previously described. Linear regression analyses revealed significant differences not only in axon density between species and locations (nerves and peduncles), but also in axon type and axon diameter (<i>p</i> < 0.05). However, UM axon diameter was larger in the OPs than in the nerve in both species (<i>p</i> = 0.005), with no significant differences in UM axon diameter in the ON (<i>p</i> = 0.06) between species. This study provides an in-depth analysis of the neuroanatomical organisation of the ascending olfactory pathway in two fish taxa and a quantitative anatomical comparison of the summation of olfactory information. Our results support the assertion that relative OB volume is a good indicator of the level of olfactory input and thereby a proxy for olfactory capabilities.

Morphometric analysis of the elasmobranch olfactory rosette

“…Studies have investigated potential reasons for interspecific variation. Researchers have not been able to correlate organ size and complexity to odor sensitivity in teleosts nor elasmobranchs, indicating that rosette size may not be a good proxy for odor detection abilities (Camilieri‐Asch, Yopak, et al, 2020; Hansen & Zielinski, 2005; Meredith & Kajiura, 2010). While a potential relationship between size of teleosts and the number of olfactory lamellae, this has not been found in elasmobranchs and rosette size was shown to be positively correlated with body size (Ferrando et al, 2017; Pashchenko & Kasumyan, 2017; Schluessel et al, 2010; Theiss et al, 2009).…”

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

“…There are five main ORN morphotypes currently described in teleosts: ciliated, microvillous, crypt (Fishelson et al, 2010 ; Kermen et al, 2013 ; Muller, 1984 ), kappe (Ahuja et al, 2014 ), and pear (Calvo‐Ochoa & Byrd‐Jacobs, 2019 ). Although empirical identification of individual subtypes was outside of the scope of this study, as they cannot be confirmed without immunohistochemistry (e.g., Camilieri‐Asch, Yopak, et al, 2020 ), the presence of OKs with apparent morphological differences between fry and adult specimens suggests there may be ontogenetic changes in ORN subtype number and density. However, it is important to approach this with caution, as morphological differences from SEM can be due to fixation artifacts or tissue preparation, rather than true anatomical variation.…”

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

“…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. They conclude that the dimensions can be considered a valid proxy for olfactory ability in elasmobranchs.…”