The Arrangement of the Peripheral Olfactory System of Pleuragramma antarcticum: A Well-Exploited Small Sensor, an Aided Water Flow, and a Prominent Effort in Primary Signal Elaboration

Abstract

The olfactory system is constituted in a consistent way across vertebrates. Nasal structures allow water/air to enter an olfactory cavity, conveying the odorants to a sensory surface. There, the olfactory neurons form, with their axons, a sensory nerve projecting to the telencephalic zone-named the olfactory bulb. This organization comes with many different arrangements, whose meaning is still a matter of debate. A morphological description of the olfactory system of many teleost species is present in the literature; nevertheless, morphological investigations rarely provide a quantitative approach that would help to provide a deeper understanding of the structures where sensory and elaborating events happen. In this study, the peripheral olfactory system of the Antarctic silverfish, which is a keystone species in coastal Antarctica ecosystems, has also been described, employing some quantitative methods. The olfactory chamber of this species is connected to accessory nasal sacs, which probably aid water movements in the chamber; thus, the head of the Antarctic silverfish is specialized to assure that the olfactory organ keeps in contact with a large volume of water-even when the fish is not actively swimming. Each olfactory organ, shaped like an asymmetric rosette, has, in adult fish, a sensory surface area of about 25 mm², while each olfactory bulb contains about 100,000 neurons. The sensory surface area and the number of neurons in the primary olfactory brain region show that this fish invests energy in the detection and elaboration of olfactory signals and allow comparisons among different species. The mouse, for example-which is considered a macrosmatic vertebrate-has a sensory surface area of the same order of magnitude as that of the Antarctic silverfish, but ten times more neurons in the olfactory bulb. Catsharks, on the other hand, have a sensory surface area that is two orders of magnitude higher than that of the Antarctic silverfish, while the number of neurons has the same order of magnitude. The Antarctic silverfish is therefore likely to rely considerably on olfaction.

Keywords: Antarctic silverfish; fish olfaction; isotropic fractionator; olfactory bulb; olfactory nerve; olfactory rosette.

Figure 1

Schematic drawing of the adult P. antarcticum head with olfactory organ and brain. (a) Each nostril has a single, dorsally located opening. The position of the olfactory organ, nerve, bulb, and of the rest of the brain (in orange) is shown as if the head were transparent. (b) The nostril is open at the level of the anterior part of the rosette. The olfactory nerve runs along the orbit before entering the olfactory bulb. (c) The olfactory rosette has two unequal rows of lamellae; the shorter one is located medio-dorsally. B = brain; L = lamella; N = nostril; OB = olfactory bulb; ON = olfactory nerve; OR = olfactory rosette; R = raphe.

Figure 2

Gross morphology and histology of the olfactory organ of P. antarcticum. (a) Partially dissected head with the olfactory rosette visible in place in the olfactory chamber. The three white lines indicate the cutting plane in (c,d), and in Figure 3 (asterisk). (b) A dissected olfactory rosette showing the two unequal rows of lamellae. Anteriorly, the slightly lacerated tissue where the rosette was attached dorsally to the roof of the nasal chamber is visible. (c) Histological section of the olfactory chamber (asterisks) with the olfactory rosette, anterior to the opening of the nostril. The olfactory rosette is fused ventrally to the floor of the chamber and dorsally to its roof. The lamellae are not enveloped in a capsule nor fused with the wall of the olfactory chamber. A branch of the accessory nasal sac is visible in the low-right corner of the picture (double asterisk). (d) Histological section of the olfactory chamber with olfactory rosette, at the level of the opening of the nostril. The olfactory rosette is attached only to the floor of the olfactory chamber. FO = fila olfactoria; L = lamellae; N = nostril; ON = olfactory nerve; OR = olfactory rosette; R = raphe.

Figure 3

Histology of the head of P. antarcticum. The complete scan of this histological section at 100× is available in Supplementary File S1. Transverse cutting plane. Azan Trichrome. (a) Complete section of half head; level indicated by the third line (with asterisk) in Figure 2a. The olfactory rosette is obliquely positioned in the nasal chamber, with the medial row of lamellae (the shorter row) being dorsal to the lateral (and longer) row of lamellae. The olfactory chamber is in continuity with accessory nasal sacs, which are narrow and branched. The ventromedial accessory nasal sac (number 2) runs internally to the palatine bone and reaches the roof of the mouth, being divided from the oral cavity by the oral mucosa. The ventrolateral accessory nasal sac (number 3) runs between the palatine and the preorbital bones. (b) Detail of the photograph in (a). The roof of the main nasal chamber is characterized by a thicker layer of fibrous connective tissue, compared to the rest of the wall of the main and accessory nasal sac. A large blood vessel (asterisk) is visible running along the raphe. (c) Detail of the photograph in (a). The ventromedial accessory nasal sac presents some diverticula of unknown function (asterisks). LRL = lateral row of lamellae; Ma = Maxilla; Me = mesethmoid; MRL = medial row of lamellae; OC = olfactory chamber; OrC = oral cavity; ON = olfactory nerve; Pa = Palatine bone; PrM = premaxilla; PrO = Preorbital bone; ROC = roof of the olfactory chamber; VMANS = ventromedial accessory nasal sac.

Figure 4

Histology of the olfactory rosette of P. antarcticum. (a) Hematoxylin-Eosin of the anterior half of an olfactory rosette. The cutting plane is parallel to the dorsal surface of the rosette, as seen in Figure 2b. (b) Masson’s Trichrome; detail of the sensory epithelium along the lamellae surface. (c) Masson’s Trichrome; apical part of two lamellae. The sensory epithelium covers the lamellae and only the free edge of each lamella shows a different, non-sensory epithelium. The connective tissue of the lamina propria is quite loose, and the blue of the collagen—indicating a more compact tissue—runs in a thin layer just under the basal lamina. (d) Masson’s Trichrome; basal part of two lamellae and one interlamellar curve. The basal layer of the sensory epithelium, in the interlamellar curve, is thicker than along the lamellae and shows at least two layers of round nuclei (asterisk). ant = anterior part of the rosette; ILC = interlamellar curve; L = lamella; mid = middle part of the rosette in an anterior-posterior direction; NSE = non-sensory epithelium; R = raphe; SE = sensory epithelium.

Figure 5

Scatter plot representing data in Table 1. The regression function is y = 0.0524 × 1.3654 (R2 = 0.9756). Aa: Anguilla anguilla, Dm: Dissostichus mawsoni, El: Esox lucius, Ga: Gasterosteus aculeatus, Gg: Gobio gobio, Ll: Lota lota, Nb: Nemachilus barbatulus, Pa: Pleuragramma antarcticum, Pf: Perca fluviatilis, Pp: Phoxinus phoxinus, Sc: Squalius cephalus, Si: Salmo irideus, Tt: Tinca tinca.

Figure 6

Gross morphology and histology of the olfactory rosette and nerve of P. antarcticum. (a) Lateral view of an olfactory rosette with the olfactory nerve. The two lines indicate the cutting plane of histological photographs in (b,c). (b) Hematoxylin-Eosin; the fila olfactoria gather to form the olfactory nerve in the connective tissue under the raphe. The large blood vessel that runs along the raphe, follows the fila olfactoria. (c) Hematoxylin-Eosin; transverse section of the olfactory nerve. BV = blood vessel; L = lamellae; ON = olfactory nerve.

Figure 7

Scatterplots representing part of data in Table 2. Quantitative data from olfactory rosette and bulb of P. antarcticum (present work), and G. melastomus and S. canicula [51]. (a) Scatterplot showing the number of neurons in one olfactory bulb. (b) Scatterplot showing the number of neurons in one olfactory bulb normalized to the mm² of surface area of the olfactory organ.