Why have neurogenesis in adult olfactory systems? The Presidential Symposium at the 2006 AChemS Conference.

The topic of the Presidential Symposium at the 28th Annual Meeting of the Association for Chemoreception Sciences, on 29 April 2006, was ‘‘Why Have Neurogenesis in Adult Olfactory Systems?’’ This introductory paper plus the following 3 papers arose from the science presented in that symposium. Cell proliferation has long been known to occur in adult animals. It occurs in many tissues, including the epidermis and intestinal lining wherein it functions in the turnover and repair of tissue normally exposed to harsh environments. For many years, cell proliferation was thought to be absent from the nervous system of adult animals. This was the prevailing dogma until the 1960s, when radiolabeled molecules became more available for biological studies. This included tritiated thymidine, which could be used to label cells in the S-phase of the cell cycle. This provided a convenient and reliable marker of cells replicating their DNA and, at least in many cases, thus in the process of mitosis. This methodology allowed for claims of neurogenesis in brains of adult rodents in the 1960s by Altman and colleagues (e.g., Altman and Das 1966; Altman 1969). The claims were received with a mixture of skepticism, enthusiasm, and indifference, and they were not fully appreciated until later studies using the same and new techniques replicated and extended their findings. Now, with nonradiolabeled markers of DNA replication such as bromodeoxyuridine and antibodies for molecules specifically expressed in different phases of the cell cycle, identifying cell division in tissues is relatively simple and commonplace and has led to demonstrations of neurogenesis in the brains of adult animals representing an impressive phylogenetic range. Although adult neurogenesis is phylogenetically widespread in the brains of adult vertebrates, including representatives of the major classes of vertebrates—elasmobranchs, teleosts, amphibians, reptiles, birds, and mammals—it is limited to very few brain regions. The 2 vertebrate brain regions most recognized as sites of adult neurogenesis are the subventricular zone/olfactory bulb and the dentate gyrus of the hippocampus. Other areas in the adult mammalian brain, including the cortex, have been reported to undergo neurogenesis, but this topic is being debated. Adult neurogenesis occurs in other animal groups in addition to the vertebrates, most notably in some insects and crustaceans. In these groups as in the vertebrates, adult neurogenesis occurs only in limited parts of the nervous system and often associated with olfaction. In insects, it occurs in the mushroom bodies, which are large neuropils containing intrinsic interneurons called Kenyon cells. Kenyon cells are higher order multimodal integrators that receive their most prominent inputfromtheantennal lobes,whicharetheinsect’s primary olfactory neuropils. In crustaceans, adult neurogenesis principally occurs in 2 parts of the brain: the olfactory lobes and the optic lobes. Neurogenesis occurs not only in the brain but also in the peripheral olfactory systems of many animals, including vertebrates, crustaceans, and snails. A focus of research on adult neurogenesis is elucidating the cellular and molecular mechanisms of cell birth and migration (e.g., Merkle and Alvarez-Buylla 2006; Sawamoto et al. 2006). Receiving much less attention has been the ‘‘function’’ of olfactory neurogenesis in adults. Adult neurogenesis is certainly not limited to the olfactory system, but if adult neurogenesis occurs in a species, it is likely to occur in the olfactory pathway. Why is this so? What is different about olfaction that makes adult neurogenesis so prevalent? This led me to organize the 2006 AChemS Presidential Symposium on the topic, Why have adult olfactory neurogenesis? There are many reasons why adult animals might have olfactory neurogenesis. Many animals have indeterminate growth such that they increase in size throughout their life. Olfactory neurogenesis allows their olfactory system to keep pace with the increase in body surface. This effect, however, is not necessarily olfactory specific, as other parts of the body, including other sensory systems, may also expand with body size. A second reason for adult olfactory neurogenesis is that some animals respond to damage to or loss of the olfactory organ with regeneration and repair. Crustaceans are an excellent model of this. The olfactory organ is particularly susceptible to damage because its sensory function requires that it be intimately exposed to the external environment. Damage to and death of olfactory sensory neurons in such conditions are to be expected. So the continuous Chem. Senses doi:10.1093/chemse/bjm011