The somatotopic organization of the olfactory bulb in elasmobranchs

Abstract

The olfactory bulbs (OBs) are bilaterally paired structures in the vertebrate forebrain that receive and process odor information from the olfactory receptor neurons (ORNs) in the periphery. Virtually all vertebrate OBs are arranged chemotopically, with different regions of the OB processing different types of odorants. However, there is some evidence that elasmobranch fishes (sharks, rays, and skates) may possess a gross somatotopic organization instead. To test this hypothesis, we used histological staining and retrograde tracing techniques to examine the morphology and organization of ORN projections from the olfactory epithelium (OE) to the OB in three elasmobranch species with varying OB morphologies. In all three species, glomeruli in the OB received projections from ORNs located on only the three to five lamellae situated immediately anterior within the OE. These results support that the gross arrangement of the elasmobranch OB is somatotopic, an organization unique among fishes and most other vertebrates. In addition, certain elasmobranch species possess a unique OB morphology in which each OB is physically subdivided into two or more "hemi-olfactory bulbs." Somatotopy could provide a preadaptation which facilitated the evolution of olfactory hemibulbs in these species.

Clarification of the Terminology of the Olfactory Lamellae in Chondrichthyes

“…The organization of the olfactory bulb in this class is likely to be somatotopic instead of chemotopic, which is the typical organization observed in other vertebrates; the meaning of this different arrangement of the olfactory projection from the olfactory epithelium to the first brain districts has been linked to the great size of the olfactory organs in Chondrichthyan species and to a better, simpler organization in sub‐bulbs (Meredith et al, ).…”

“…Morphological differences of the nostrils have been described in more active or sedentary species, in order to optimize the water flow in the olfactory chamber (Bell, ), thus this kind of correlation cannot be ruled out for the morphology of the olfactory rosette. Finally, the number of folds could have a neuroanatomical meaning in the light of the somatotopic organization of the olfactory bulb described exclusively in Chondrichthyes, where sensory neurons from each few folds project to a subregion of the bulb (Meredith and Kajiura, ; Meredith et al, ).…”

Is the olfactory system of cartilaginous fishes a vomeronasal system?

“…The odor coding in Chondrichthyes, different from that of all other vertebrates, is further supported by the recent discovery of the somatotopic organization of the OB in elasmobranchs, a unique organization among other vertebrates, in which the OB shows chemotopic organization (Meredith et al, 2013). …”

Anatomy of the olfactory bulb in Greenland shark Somniosus microcephalus (Bloch & Schneider, 1801)

“…Two main types of OB are described for elasmobranchs: one with two independent sub‐bulbs (Atlantic sharpnose shark Rhizoprionodon terranovae and lemon shark Negaprion brevirostris ; Dryer & Graziadei, ; Meredith, Kajiura, & Hansen, ), and another elongated and characterized by several, aligned sub‐bulbs (bonnethead shark Sphyrna tiburo and Atlantic stingray Dasyatis Sabina ; Dryer & Graziadei, ; Meredith et al., ). Information on the shape of the OB in elasmobranch species is sporadically reported in the literature.…”

“…Information on the shape of the OB in elasmobranch species is sporadically reported in the literature. A complete review of the available information is beyond the scope of this paper, however, analysis of photographs and diagrams included in recent papers allowed us to roughly recognize three types of OB, instead of two: the blue shark Prionace glauca (Lisney & Collin, ), the bull shark Carcharhinus leucas (Lisney, ), the blacktip reef shark Carcharhinus melanopterus (Lisney, ), and the tiger shark Galeocerdo cuvier (Yopak, Lisney, & Collin, ) show an OB completely divided into two sub‐bulbs connected by a thin strip of tissue; the scalloped hammerhead Sphyrna lewini (Yopak et al., ), the argus skate Dipturus polyommata (Yopak et al., ), the sting ray Pastinachus atrus (Yopak et al., ), and the thornback guitarfish Platyrhinoidis triseriat a (Hofmann & Northcutt, ) have an elongated OB and the possible division into several sub‐bulbs could be hypothesized (because of the similarity with the species described by Dryer & Graziadei, and Meredith et al., ) but it is not obvious from the macroscopic photographs. The bigeye houndshark Iago omanensis (Fishelson & Baranes, ), the crocodile shark Pseudocarcharias kamoharai (Lisney & Collin, ), the lesser‐spotted catshark (Ferrando et al., ), and the epaulette shark Hemyscyllum ocellatum (Yopak et al., ) have an incomplete division of the OB into two tissue masses.…”