Abstract

The presence of a terminal nerve complex (TN) in lampreys, including an olfacto-retinalis component, has previously been the subject of much debate. Although extra-bulbar olfactory projections (EBOP) with similar characteristics to the TN found in gnathostomes have been described in lampreys, the absence of a ganglion and the lack of both gonadotropin-releasing hormone (GnRH)- and FMRFamide peptide immunoreactivity (ir) suggest that lampreys may not possess a TN, where TN is an innovation of gnathostomes. Here, we describe EBOP in Mordacia praecox that may serve a comparable function to that of the TN of gnathostomes. Trans-synaptic labeling of ciliated receptors was observed in the main olfactory epithelium (MOE) after an intraocular application of the beta subunit of Cholera toxin (CTb) in adult specimens of M. praecox. Labeled cells were arranged as a pseudo-stratified epithelium and distributed in patches of irregular density across the MOE. Labeled receptors were found to project collateral fibers to cells located in the epithelium of the accessory olfactory system, where terminals were mostly confined to an area surrounding the cell bodies. These MOE fibers then joined the olfactory nerve, entered the olfactory bulb (OB) medially and decussated into two fascicles; one dorsally oriented that terminated in heavily stained varicosities in the dorsomedial neuropil in the posterior OB, and the other ventrally oriented that reached the septal nucleus before descending ventrally, rostral to the optic chiasm in the preoptic area (PA). We also found fibers in the striatum, the PA, the dorsal and ventral hypothalamus (Hyp), the nucleus of the posterior commissure (NPO), and the posterior tuberculum. However, due to our experimental approach, we cannot rule out that other afferent fibers innervate these areas. As previously described in other species of lampreys, we could not find a retinopetal ganglion of the TN or any GnRH-ir EBOP receptors in M. praecox. We infer that the trans-synaptic transport of CTb in the EBOP occurs from synapses located along the PA-Hyp-NPO axis, which is the first region of integration of retinal axons. This region contains FMRFamide-ir retinopetal cells and most of the GnRH-ir cells described in the brain of other lampreys. If this was the case in M. praecox, then the EBOP could exert TN-like control of the reproductive function through the direct modulation of their activity. Similarly, EBOP terminals surrounding somata in the accessory olfactory epithelium and along their projections suggest that EBOP receptors participate in pheromone perception and mating in lampreys.