Transient uptake of serotonin by newborn olfactory projection neurons

Abstract

A life-long turnover of sensory and interneuronal populations has been documented in the olfactory pathways of both vertebrates and invertebrates, creating a situation where the axons of new afferent and interneuronal populations must insert into a highly specialized glomerular neuropil. A dense serotonergic innervation of the primary olfactory processing areas where these neurons synapse also is a consistent feature across species. Prior studies in lobsters have shown that serotonin promotes the branching of olfactory projection neurons. This paper presents evidence that serotonin also regulates the proliferation and survival of projection neurons in lobsters, and that the serotonergic effects are associated with a transient uptake of serotonin into newborn neurons.T he olfactory pathways of vertebrates and invertebrates show a remarkable degree of life-long structural plasticity. The basis of this plasticity is the turnover of olfactory receptor neurons (1, 2) as well as of interneuronal populations (3-5). The new afferents and interneurons insert their axons into existing synaptic regions, which are organized into a highly ordered array of glomeruli. These glomeruli are thought to be arranged odotopically, with each glomerulus having a specific role in the coding of odor quality (6-8). Throughout life, as the processes of new sensory neurons and interneurons are added to the glomeruli, their structural integrity is stable: there is no evidence for the formation of new glomeruli or the loss of existing glomeruli (9-11). The intercalation of the processes of new neurons into the glomeruli, in which pre-and postsynaptic populations of neurons need to be matched, presents major challenges for the nervous system in preserving odotopic order.A feature that is common to olfactory systems across phylogenetic lines is a dense serotonergic innervation of the regions where the olfactory receptor neurons synapse onto second-order cells. In vertebrates, the olfactory bulb is one of the major forebrain targets of serotonergic neurons ascending from the brainstem (12). In molluscs, serotonergic interneurons innervate the protocerebral olfactory neuropil where serotonin is thought to be involved in the storage of odor memory (13,14). Among the arthropods, giant serotonergic neurons innervate the antennal lobes of insects (15) and the olfactory lobes (OLs) of crustaceans (16). The present study examines the role this serotonergic innervation may play in the assembly and maintenance of olfactory areas in the lobster, Homarus americanus, by testing whether serotonin depletion influences the proliferation and survival of projection neurons and by documenting a transient uptake of serotonin by the newborn cells.The crustacean olfactory pathway consists of primary sensory neurons that synapse with local and projection interneurons within the glomeruli of the OLs. These two categories of interneurons are functionally analogous to the local (periglomerular and granule) and projection (mitral and tufted) neurons of the vertebrate olf...

Adult neurogenesis and cell cycle regulation in the crustacean olfactory pathway: from glial precursors to differentiated neurons

“…Towards this end, we have examined serotonin and nitric oxide as possible endogenous modulators of neurogenesis. Various in vitro and in vivo studies have shown that increases in serotonin levels result in an upregulation of neurogenesis in both the MPZ and LPZ of juvenile clawed lobsters (Benton and Beltz 2001a;Beltz et al 2001) and that decreases inhibit the branching of newborn projection neurons (Sullivan et al 2000). Furthermore, brain serotonin levels are under circadian control (Wildt et al 2004).…”

“…These studies may ultimately reveal mechanisms by which other exogenous factors are translated into changes in neurogenesis. In this regard, it is important to note that we believe that serotonin may influence olfactory neuronal precursors both via release from fine fibers of the serotonergic dorsal giant neuron (DGN; Beltz et al 2001) and via a blood-born pathway. Recent in vitro studies in the clawed lobster demonstrate that neurogenesis in the LPZ is most sensitive to serotonin at very low (10 −10 M) concentrations (Fig.…”

Regulation of serotonin levels by multiple light-entrainable endogenous rhythms

“…In the brain of the American lobster, reduced serotonin levels result in a decrease in neurogenesis among the deutocerebral local and projection neurons (clusters 9 and 10; Fig.·1) Beltz et al, 2001), while elevated serotonin levels result in an increased rate of neurogenesis (J. L. Benton, E. M. Goergen and B. S. Beltz, unpublished results). It is also known that a bundle of fine serotonergic fibers from the DGN terminate blindly in the region where new projection neurons are born in cluster 10 .…”

“…In both vertebrate and invertebrate species, serotonin is a potent regulator of neurogenesis Daszuta, 1999, 2000;Benton and Beltz, 2001;Beltz et al, 2001;Jacobs, 2002;Radley and Jacobs, 2002;Malberg and Duman, 2003). In the brain of the American lobster, reduced serotonin levels result in a decrease in neurogenesis among the deutocerebral local and projection neurons (clusters 9 and 10; Fig.·1) Beltz et al, 2001), while elevated serotonin levels result in an increased rate of neurogenesis (J. L. Benton, E. M. Goergen and B. S. Beltz, unpublished results).…”

“…Serotonin has also been implicated as a regulator of life-long neurogenesis in the lobster brain Beltz et al, 2001), and the generation of new neurons in this system is under circadian control, with a peak rate at dusk. This finding may be correlated with the habits of lobsters, which are most active around dusk (Weiss, 1970;Cooper and Uzmann, 1980;Chabot et al, 2001).…”