Sex pheromone systems in goldfish: comparisons to vomeronasal systems in tetrapods

Most amphibians, reptiles and mammals possess a well defined dual olfactory system comprised of separate neural pathways that regulate different olfactory functions. One pathway originates in the nasal cavity and gives rise to what is commonly referred to as the main olfactory system. The other pathway originates in the vomeronasal organ (VNO) and gives rise to the accessory olfactory system. Functionally, the main olfactory system is thought to subserve, olfactory-mediated tasks such as feeding and grooming, while the accessory olfactory system is believed to be primarily involved in mediating behavioral and physiological responses to sex pheromones. Traditionally, it has been difficult to address whether teleosts possess any components of the vomeronasal system, since they generally do not meet the criteria used to identify vomeronasal systems in other vertebrates. Previous conclusions that the nasal epithelia of fish is olfactory and not vomeronasal in nature are based on observations that teleosts lack a separate VNO-like chemosensory structure and an anatomically distinct accessory olfactory bulb. However, because sex pheromones have been identified in the goldfish, it is now possible to compare the neural substrates that regulate pheromone-induced responses in teleosts to those that mediate similar responses in other vertebrates. The olfactory system in goldfish is particularly well suited for such comparisons, because it comprises anatomical and functional subdivisions that resemble those associated with the main and accessory olfactory systems in tetrapods. The olfactory pathways that mediate endocrine and behavioral responses to sex pheromones in goldfish are described and then compared to the main and accessory olfactory systems of tetrapods. In making these comparisons, a number of similarities become apparent. First, the olfactory pathways that regulate responses to sex pheromones in goldfish are different from those that serve a more general olfactory function. Second, these functional differences appear to be subserved by separate and anatomically distinct olfactory tract projections to the brain. Third, the lateral olfactory tracts and their central projections in goldfish appear to serve a function analogous to that of the main olfactory system, while the medial olfactory tracts and their central projections comprise a pathway remarkably similar to the vomeronasal-accessory olfactory system. These findings suggest that teleosts may possess functional correlates of tetrapod vomeronasal systems, but in a form that has yet to be recognized. If so, medial olfactory tract projections in goldfish may be evolutionarily conserved and expressed in tetrapods as the vomeronasal system, or the medial olfactory tract projections may be new pathways that have evolved to serve the same function.