Structural and functional features of the olfactory epithelium in fish

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Abstract

Structural and functional peculiarities of the peripheral part of the olfactory analyzer in fish are considered. The article is devoted to the characteristics of the main types of receptor cells: their morphology, the peculiarities of their location in the olfactory epithelium, and functional specificity. Some data on the threshold values of fish chemosensitivity to chemical agents, which have an important signaling value for them are presented.

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1. Introduction

Currently, one of the most urgent problems in neuroscience is the study of the fundamental mechanisms of adaptive functioning of the olfactory analyzer in animals and humans (Smith and Bhatnagar, 2019; Dan et al., 2021; Zhu et al., 2021). First of all, these questions concern deciphering the mechanisms providing chemoreception processes at the level of the peripheral part of the olfactory system. Attempts to identify correlations between the structure of receptor neurons, their sensitivity, and the implementation of specific forms of animal behavior have not yet yielded inambiguous results. In this regard, one of the important problems is the search for morpho-functional criteria for the sensitivity levels of receptor cells in animals at different stages of their evolutionary development. In particular, this concerns the adaptive behavior of fish, which in the course of evolution have mastered various water horizons and are characterized by the high plasticity of their chemosensory apparatus (Korsching, 2020; Calvo-Ochoa et al., 2021). In this regard, one of the key tasks is to study the types of receptor cells, their molecular receptors, and the mechanisms of transduction of chemical signals from the external environment. The data obtained in fish may be important for understanding the structural and functional organization and evolution of the mechanisms that provide olfactory perception.

2. Functional specialization of olfactory receptor cells

Olfaction plays a leading role in the organisation of feeding, reproductive, social, and other complex behaviors in fish (Kasumyan, 2004; Calvo-Ochoa and Byrd-Jacobs, 2019; Korsching, 2020; Bowers et al., 2023; Oka, 2023). Similar to other vertebrates, phylogenetically different fish have a sensory section of the olfactory analyzer that is essentially a pseudostratified neuroepithelium consisted of three types of cells: receptor, supporting, and basal. The attribution of the cells to a certain type depends on their location in the thickness of the olfactory epithelium (OE), on morphological features, and on the presence of specific antigenic determinants (markers) (Bronshtein, 1977; Graziadei and Graziadei, 1979; Schwob, 2002; Villamayor et al., 2021). The OE of fish was described to contain five types of olfactory sensor neurons (OSNs): ciliated, microvillous, pear-shaped, crypt, and kappe (Ahuja et al., 2014; Yoshihara, 2014; Wakisaka et al., 2017).

Similar to other vertebrates, neurogenesis in the OE of fish is maintained throughout life by the proliferative activity of regional stem cells, which produce various types of cells (Graziadei and Graziadei, 1979; Demirler et al., 2020; Calvo-Ochoa et al., 2021; Kocagöz et al., 2022). Model experiments in fish and other animals show that various forms of sensory deprivation can tangibly increase the natural neurogenesis rate typical of intact animals. It was previously shown that neurogenesis processes in the OE can be activated after intranasal administration of toxic or neurotrophic factors, after axon transection, or as a result of bulbectomy (Graziadei et al., 1978; Carr and Farbman, 1992; Frontera et al., 2016; Cervino et al., 2017). It was found recently in fish that prolonged exposure to a non-toxic mixture of amino acids and peptides leads at first to local neurodegenerative changes in the OE and then to the development of compensatory neurogenesis processes (Klimenkov et al., 2020). Mature OSNs in fish are monospecific and express only one type of receptors (Sato et al., 2007). The axons of OSNs expressing a given olfactory receptor converge on a few defined glomeruli within the olfactory bulb (OB). This way, a topographical map of olfactory signal processing emerges in the brain (Friedrich and Korsching, 1997; Shao et al., 2017; Imamura et al., 2020).

Different fish species have a representation of several tens to over a thousand functionally active genes coding receptive proteins (Saraiva and Korsching, 2007; Alioto and Ngai, 2006; Calvo-Ochoa et al., 2019; Policarpo et al., 2022). The detection of odorous substances is mediated in fish by a superfamily of receptors associated with G protein (Korsching, 2009; Calvo-Ochoa et al., 2019; Policarpo et al., 2022). There are three types of receptors: olfactory receptors (ОRs) (Alioto and Ngai, 2006; Bayramli et al., 2017); trace amine-associated receptors (TAARs) (Michel et al., 2003; Saraiva and Korsching, 2007; Dieris et al., 2021; Dewan, 2021); and vomeronasal receptors (V1R, V2R), which are thought to be able to bind pheromones (Matsunami and Buck, 1997; Pfister and Rodriguez, 2005; Kowatschew and Korsching, 2022; Kowatschew et al., 2022).

The most abundant group of receptor cells is composed of ciliated and microvillous OSNs. These are bipolar neurons whose bodies are located in the thickness of the OE. The cells are spindle-shaped with a transverse diameter of 5–8 µm. The perinuclear zone is a place of localization of granular endoplasmic reticulum channels, the Golgi apparatus, mitochondria, multivesicular bodies, free ribosomal rosettes, and other organelles. The body of the lower part of the cell narrows sharply to form an axon, which, together with other axons of similar cells, forms part of the unmyelinated olfactory nerve connecting receptor cells to the OB of the forebrain. A dendrite extends from the upper pole of the cell body; the diameter of the dendrite is 1–3 μm. The cytoplasm of the dendrite contains usually fragments of smooth endoplasmic reticulum, mitochondria, and microtubules. The apical part of the receptor cells (olfactory knob) can have processes of two types (cilia or microvilli), which have no microtubular apparatus. Based on this characteristic , they are divided into ciliated and microvillous receptor cells (Yamamoto, 1982; Zeiske et al., 1992; Belanger et al., 2003; Lazzari et al., 2007; Hansen and Zielinski, 2005; Pintos et al., 2020; Rincón-Camacho et al., 2022; Bettini et al., 2023). Ciliated OSNs use a Golf/adenylyl cyclase signaling cascade to activate CNG channels; microvillous OSNs use a Gq/phospholipase C pathway together with TRPC2 (Speca et al., 1999; Hansen et al., 2003; Sato et al., 2005). Electroolfactogram recordings were used to show that ciliated OSNs (cORNs) respond to bile salts and microvillous cells (mORNs) are sensitive to amino acids (Thommesen, 1983). Similar responses of microvillous neurons to amino acids were also recorded in (Speca et al., 1999; Lipschitz and Michel, 2002). Based on a study of olfaction in rainbow trout, Sato and Suzuki (2001) argued that cORNs are “generalists”, i.e., they respond to a wide range of odors including pheromones, while mORNs are “specialists”, specific to amino acids. Hansen et al. (2003) conducted a study in channel catfish to show that microvillous neurons can respond to nucleotides and that amino acid odorants activate both ciliated and microvillous neurons, but via different signaling pathways.

Owing to the development of immunocytochemistry methods, intravital visualization of the functional activity of cells, and transcriptome analysis, recently researchers began to identify new morphological types of receptor neurons in fish. In addition to the ciliated and microvillous neurons mentioned above, they discovered another type of sensitive elements, i.e., crypt cells (Hansen and Zeiske, 1998; Hansen and Finger, 2000; Ferrando et al., 2010; Ahuja et al., 2014; Lazzari et al., 2022). This type of cells is the least abundant group of receptor neurons. For example, their proportion in trout and mackerel is only 2% of the total number of neurons while that of microvillous and ciliated neurons is 8 and 90%, respectively (Schmachtenberg, 2006). In some fish species, these cells are identified not only in adult specimens but also on the second or third day of their development (Camacho et al., 2010). A distinctive feature of crypt cells is that their bodies are located in the uppermost layer of the OE and are spherical or pear-shaped. They are usually completely surrounded by the bodies of one or two supporting cells, with which they form local gap contacts to ensure the sustainability of the cells to mechanical stress (Schmachtenberg, 2006). Crypt cells are though to have no conspicuous dendrites and their receptive area has both cilia and microvilli (Hansen and Finger, 2000). Crypt cells are characterized by an unusual way of expression, i.e., “one cell type—one receptor”, where the same receptor is expressed by the entire population of crypt neurons (Ahuja et al., 2013). In order to determine the functional specialization of these cells, attempts are made to identify specific markers that do not occur in other types of olfactory neurons. They were shown to express the G proteins Gαo and Gαq, adenylate cyclase III, and the glial marker protein S-100 and TrkA. Nevertheless, it was noted that these proteins may not be present in all crypt cells (Hansen et al., 2003; 2004; Catania et al., 2003; Vielma et al., 2008). Subsequently, TrkA proved to be a reliable molecular marker of crypt cells in zebrafish (Bettini et al., 2016). To determine the spectrum of odorous substances perceived by crypt cells, studies are carried out to identify their odorant-binding receptors. Crypt cells were shown to express a single V1R receptor, i.e., V1R4, coupled to Gαi; although their ligands are unknown, it was suggested that these receptors respond to pheromones (Ahuja et al., 2013). Cytochemical studies in crucian carp have shown that the localization of pheromone-sensitive crypt cells varies substantially throughout the year; in summer, i.e., during the transition to spawning, their bodies move to more superficial layers of the epithelium (Hamdani and Døving, 2007). The authors believe that these observations demonstrate a direct relationship between hormones circulating in the blood and the perception of sex pheromones. To determine the spectrum of olfactory sensitivity of crypt cells, it makes sense to look at studies identifying neural projections of these cells in the central structures of the brain. Thus, it was found in crucian carp that the axons of second-order neurons (forming synapses with crypt cells) are connected to the olfactory cortex via the medial tract, which transmits sensory information relevant to reproduction (Hamdani and Døving, 2007). Based on these facts, the authors of the latter work assume that crypt cells ensure selective perception of pheromonal sex signals involved in the chemical communication in fish during spawning. Recently, the patch clamp method and intravital Са2+ ion imaging were used in a study on mackerel and juvenile trout to show that different subpopulations of crypt cells respond to amino acids, bile acids, or pheromonal signals (Schmachtenberg, 2006; Vielma et al., 2008; Bazáes and Schmachtenberg, 2012). In adult trout specimens, the majority of crypt cells responded only to reproductive pheromones, suggesting that their response profile is largely dependent on the sexual maturity and sex of a given fish (Bazáes and Schmachtenberg, 2012). Moreover, experiments in zebrafish with retrograde labeling of cell crypts by injecting a fluorescent dye into the OB showed that these cells send their axons to only one OB glomerulus. This finding indicates the existence of a specialized “labeled line” that combines odor signals from all crypt cells present in the epithelium in one OB glomerulus (Ahuja et al., 2013).

In the course of studying the olfactory apparatus of zebrafish, other “crypt-like” cells were also identified within the OE, which sent their axons to a glomerulus that was different from other cell types (Braubach et al., 2012; Ahuja et al., 2014), which is contrary to the principle of convergence of axons in one glomerulus (Mombaerts, 2006). It turned out that these unusual cells, which were called kappe neurons for their characteristic shape, express Gα s/olf proteins and produce no specific markers typical of ciliated, microvillous, or crypt cells. Immunochemical staining of kappe cells revealed no tubulin in them, leading some authors to believe that they contain no cilia (Ahuja et al., 2014). The same study revealed positive staining for actin filaments concentrated mainly in the apical part of the cell. Since actin is an important component of microvilli, the authors are inclined to believe that kappe cells contain only microvillous processes. In our opinion, actin as a marker of crypt cells should be used with caution because it was later discovered in teleost fishes of the suborder Cottoidei in the dendrites and terminals of young OSNs for a short period of time during their migration and incorporation into the surface of the OE (Klimenkov et al., 2018). Particularly, in the apical side of receptory cells was shown the forming of a dense layer of actin microfilaments with the central pore. It is assumed that the functional receptors of odorants generate across this pore the first intracellular signal from environmental water-soluble odorants. At the final stage of morphogenesis, the actin perimembrane layer disappears and is preserved only at the sites of tight junctions with neighbouring supporting cells (Fig. 1). Accordingly, these data points that actin polymerisation may be temporally, what correspond to specific stage of OSN development.

 

Fig.1. Young (a, b) and mature (c) stages of olfactory receptor cells morphological differentiation (by laser scanning confocal microscopy) of Cottocomephorus inermis Jakowlew, 1890 (Cottoidei). (А) – The ellipsoidal nucleus with mitochondria and thick layer of perimembrane F-actin inside the young cell. At the dendritic terminal the perimembrane F-actin layer has a pore which opens to cytoplasm. The apical fragment with the pore is highlighted and enlarged (the membrane patch upper the pore painted with red color); (b) – the hole of the pore is significantly expanded due to actin microfilaments dissociation; (c) – mature cell containing the F-actin only in the tight junctions area (pointed with brace). Notation: 1 – pore in the actin layer; 2 – F-actin; 3 – mitochondria; 4 – nucleus; 5 – plasmalemma; 6 – the membrane patch upper the pore in actin layer.

 

Recently, another small population of OSNs, pear-shaped neurons, was described in the surface layers of the OE in zebrafish (Wakisaka et al., 2017). These neurons were shown to express the A2c receptor, which is present in lower aquatic organisms and mediates the recognition of adenosine (Kowatschew and Korsching, 2021). The gene encoding this receptor was not found in terrestrial vertebrates. Another cell type, olfactory rods, was recently reported to be found in the OE of zebrafish larvae (Cheung et al., 2021). The bodies of these cells are located in the upper parts of the epithelium, and their apical region has an abundance of actin and a 5–10-μm rod-shaped protrusion capable of moving. These cells have no axons; however, it is assumed that they can perform mechanosensory, chemosensory, or multimodal functions.

3. Olfactory sensitivity of fish

The olfactory sensitivity of vertebrates, including fish, depends on their age and physiological state as well as ecology (Keller-Costa et al., 2014; Wakisaka et al., 2017; Doyle and Meeks, 2018; Li et al., 2023; Wagner et al., 2023).

To determine the various parameters of olfactory sensitivity in fish to biologically relevant signals, researchers apply both behavioral (Kasumyan and Marusov, 2018; Wagner et al., 2023) and electrophysiological approaches (Valdés et al., 2015; Sato and Sorensen, 2018). Fish demonstrate high sensitivity to chemical agents that shape complex forms of their feeding and reproductive behavior. For instance, electrophysiological recordings from individual goldfish OSNs revealed that cells are specialized to detect odors associated with specific biological functions such as feeding, reproduction, and aggregation (Sato and Sorensen, 2018). It was also noted that information about sex pheromones is transmitted by individual, narrowly tuned OSNs whereas amino acids and other nutritional signals (polyamines, nucleotides) appear to be detected by a large number of OSNs (Sato and Sorensen, 2018). The sensitivity threshold to some L amino acids (alanine, arginine, glutamine acid, and methionine) associated with common feeding stimulants (Hara, 2006; Rolen et al., 2003) is 10-8М (Sato and Sorensen, 2018; Rolen et al., 2003). The sensitivity threshold to polyamine (feeding stimulants) is 10-8М (Rolen et al., 2003). The minimum concentration of the male sex pheromone androstenedione is 10-11М (Sorensen et al., 2005). The sensitivity threshold to the sex pheromone prostsglandin 2α is 10-10М (Sorensen et al., 1988). An even lower threshold of 10-11М was found for putative aggregation cues (Li et al., 1995) (bile acid mixture) (Sato and Sorensen, 2018).

In recent years, a combination was used of site-directed mutagenesis and molecular modeling of the interaction of ORs with potential odorants (de March et al., 2018; Cong et al., 2019). This approach provides an opportunity to identify the type of ligands and the time profile of their interaction with the G protein-coupled receptors.

4. Conclusion

Тhe analysis of works devoted to the study of adaptive properties of the olfactory system of fish demonstrates the multivariate features structural development of their olfactory epithelium. This is especially true of the representation of certain types of resceptor cells specific to molecular receptors, the class of perceived odorants and the mechanism of their transduction. This is important not only from the point of view of studying the mechanisms of odorant-dependent behavior of hydrobionts, which is of great independent importance. The evolutionary similarity of the molecular and celluar mechanisms of olfactory reseption in fish and mammals (Saraiva et al., 2015; Calvo-Ochoa et al., 2019) shows that fish can also be used as a model for studying the fundamental meshanisms of functioning of the olfactory analyzer in humans in normal and with the development of neurodegenerative diseases, the course of which is accompanied by anosmia.

Acknowledgements

This work was supported by the Russian Science Foundation under grant no 23-24-00513, https://rscf.ru/project/23-24-00513/

Conflict of interest

The authors declare that they have no competing interests.

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About the authors

I. V. Klimenkov

Limnological Institute of the Siberian Branch of the Russian Academy of Sciences

Author for correspondence.
Email: iklimen@mail.ru
Russian Federation, Ulan-Batorskaya Str., 3, Irkutsk, 664033

S. K. Pyatov

Limnological Institute of the Siberian Branch of the Russian Academy of Sciences

Email: iklimen@mail.ru
Russian Federation, Ulan-Batorskaya Str., 3, Irkutsk, 664033

N. P. Sudakov

Limnological Institute of the Siberian Branch of the Russian Academy of Sciences

Email: iklimen@mail.ru
Russian Federation, Ulan-Batorskaya Str., 3, Irkutsk, 664033

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2. Fig.1. Young (a, b) and mature (c) stages of olfactory receptor cells morphological differentiation (by laser scanning confocal microscopy) of Cottocomephorus inermis Jakowlew, 1890 (Cottoidei). (А) – The ellipsoidal nucleus with mitochondria and thick layer of perimembrane F-actin inside the young cell. At the dendritic terminal the perimembrane F-actin layer has a pore which opens to cytoplasm. The apical fragment with the pore is highlighted and enlarged (the membrane patch upper the pore painted with red color); (b) – the hole of the pore is significantly expanded due to actin microfilaments dissociation; (c) – mature cell containing the F-actin only in the tight junctions area (pointed with brace). Notation: 1 – pore in the actin layer; 2 – F-actin; 3 – mitochondria; 4 – nucleus; 5 – plasmalemma; 6 – the membrane patch upper the pore in actin layer.

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