Abstract
The vomeronasal system (VNS) is an accessory olfactory system that in tetrapod vertebrates is composed of specific receptor neurons in the nasal organ and a set of centers in the forebrain that receive and relay the information consecutively towards the hypothalamus. Thus, only in tetrapods the VNS comprises a discrete vomeronasal (Jacobson's) organ, which contains receptor cells that are morphologically distinct from those of the olfactory epithelium and use different transduction mechanisms. The axons of the vomeronasal receptors in tetrapods project to the accessory olfactory bulb (AOB) in the rostral telencephalon. Secondary vomeronasal connections exist through the medial amygdala to the hypothalamus. Currently, the lungfishes are considered the closest living relatives of tetrapods. Here we show that the African lungfish, Protopterus dolloi, has epithelial crypts at the base of the lamellae of the olfactory epithelium that express markers of the vomeronasal receptors in tetrapods. The projections of these crypts allow us to identify an AOB on the lateral margin of the main olfactory bulb. The projections of this AOB reach a region that is topologically, hodologically, and immunohistochemically identical to the medial amygdala and could represent its homolog. Neurons of this putative medial amygdala were demonstrated to project to the lateral hypothalamus, as they do in tetrapods. All these features that lungfishes share with tetrapods indicate that lungfishes have the complete set of brain centers and connections involved in processing vomeronasal information and that these features were already present in the last common ancestor of lungfishes and tetrapods.
Highlights
The vomeronasal system (VNS), or accessory olfactory system, is a discrete sensory system that consists of a peripheral vomeronasal organ, an accessory olfactory bulb (AOB), and the AOB’s projections to distinct zones in the caudal telencephalon and from there to the hypothalamus (Halpern and Martínez-Marcos, 2003)
As a strict morphological entity formed by the chain of structures from the nasal organ to the hypothalamus, the VNS has not been recognized in fishes (Grus and Zhang, 2006), but VNS-specific genes were recently identified in bony fishes, elasmobranches, and lampreys indicating that genetic components of the VNS-specific signal transduction pathway arose early in vertebrate evolution (Grus and Zhang, 2009)
The multiple immunohistochemical detections conducted either in single or in combined procedures will be described for the main centers of the VNS, i.e. the olfactory organ, the olfactory bulbs and the region of the caudal telencephalon where the putative vomeronasal amygdala is located
Summary
The vomeronasal system (VNS), or accessory olfactory system, is a discrete sensory system that consists of a peripheral vomeronasal organ, an accessory olfactory bulb (AOB), and the AOB’s projections to distinct zones in the caudal telencephalon and from there to the hypothalamus (Halpern and Martínez-Marcos, 2003). The presence of a separate, accessory chamber or diverticulum of the nasal cavity containing a sensory epithelium that is histologically distinguishable from the olfactory epithelium present in the main chamber of the nasal cavity; and an AOB in the anterior telencephalon in larval and permanently aquatic amphibians challenged the idea that the VNS is an adaptation for air breathing (Eisthen, 2000) This prompted us to investigate lungfishes for the possible presence of specializations in the olfactory organ and distinct pathways within the central nervous system comparable to the VNS in tetrapods (Halpern and Martínez-Marcos, 2003)
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