Odorant organization in the olfactory bulb of the sea lamprey

Abstract

Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labelling established that lateral and dorsal bulbar territories receive the axons of sensory neurons broadly distributed in the main olfactory epithelium and that the medial region receives sensory neuron input only from neurons projecting from the accessory olfactory organ. The response duration for local field potential recordings was similar in the lateral and dorsal regions, and both were longer than medial responses. All three regions responded to amino acid odorants. The dorsal and medial regions, but not the lateral region, responded to steroids. These findings show evidence for olfactory streams in the sea lamprey olfactory bulb: the lateral region responds to amino acids from sensory input in the main olfactory epithelium, the dorsal region responds to steroids (taurocholic acid and pheromones) and to amino acids from sensory input in the main olfactory epithelium, and the medial bulbar region responds to amino acids and steroids stimulating the accessory olfactory organ. These findings indicate that olfactory subsystems are present at the base of vertebrate evolution and that regionality in the lamprey olfactory bulb has some aspects previously seen in other vertebrate species.

GABAergic modulation of olfactomotor transmission in lampreys

“…Similarly, the main and accessory (i.e., vomeronasal) systems of terrestrial vertebrates are segregated until at least the third-order neurons and their respective activation elicits different behaviors [ 152 – 155 ]. Physiological evidence in lampreys also supports this hypothesis, as OB local field recordings showed that the medOB and MOB have overlapping but different response profiles to feeding cues and pheromones [ 33 , 34 ]. Moreover, we show that the pathways from the OB to the motor control centers differ for the two olfactory subsystems.…”

“…The main olfactory bulb (MOB), which occupies the whole OB except its medial part (i.e., the medOB), receives inputs from the main olfactory epithelium. The medOB, on the other hand, receives inputs from OSNs located in the accessory olfactory organ [ 32 – 34 ]. The OB of vertebrates constitutes the primary olfactory center of the CNS and, as such, filters and actively shapes sensory inputs to secondary olfactory structures [ 35 , 36 ].…”

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): I. Neuroanatomy and physiology

“…This would then result in a continuous stimulation of the receptors by the pheromones. The chemical sensitivity of the lamprey SCC system is thus different from the olfactory system, which is highly sensitive to basic amino acids (arginine and histidine) and pheromones (Green et al, ; Li, ) and at least partially different from that of the gustatory system that responds to substances that are not stimulatory for the SCC system (sucrose, quinine) in L . planeri (Baatrup & Døving, ).…”

Conservation of Glomerular Organization in the Main Olfactory Bulb of Anuran Larvae

“…In fishes, ORNs expressing different odorant receptors are intermingled in a single olfactory surface (Hamdani and Døving, 2007 ). ORNs expressing receptors belonging to the same gene family often project to segregated glomerular clusters or regions in the olfactory bulb, putatively constituting functionally distinct odorant processing streams (Baier and Korsching, 1994 ; Hamdani et al, 2001 ; Frontini et al, 2003 ; Hansen et al, 2003 , 2004 ; Sato, 2005 ; Braubach et al, 2012 ; Green et al, 2017 ). In anurans, a detailed analysis of the glomerular array is only available from the African Clawed frog Xenopus laevis (Gaudin and Gascuel, 2005 ; Manzini et al, 2007 ).…”