Transitory uptake of serotonin in the developing sensory pathways of the common marmoset

Abstract

Serotonin (5-HT) affects brain development during sensitive developmental periods. In rodents, transient sites of high affinity capture of 5-HT were demonstrated in the primary sensory neurons and in the sensory thalamocortical afferents. This uptake is required to adjust 5-HT receptor stimulation during the formation of sensory maps. To determine whether similar mechanisms exist in primates, we analyzed staged embryos and postnatal pups in the common marmoset (total gestation time, 142 days). Immunocytochemical analyses were performed using antisera to 5-HT, to the serotonin transporter (SERT), and to the vesicular monoamine transporter (VMAT2). 5-HT, SERT, and VMAT2 labeled the raphe neurons and their terminal network from embryonic day (E)70 to adulthood. In addition, from E70-130 VMAT2 and SERT were observed in all the sensory cranial nerves, the olfactory nerve, the gustatory, the trigeminal, the auditory fibers, in the retinal ganglion cells, and the optic tract up to the lateral geniculate nucleus and the superior colliculus. All the spinal sensory ganglia and their peripheral sensory branches were labeled. Accumulation of 5-HT was observed in all the sensory neurons expressing SERT and the corresponding axon tracts. Since these neurons were missing tryptophan hydroxylase (TPH), the synthesizing enzyme for 5-HT, they most likely accumulated 5-HT through the action of the amine transporters, as has been shown in rodents. No transient expression of 5-HT markers was detectable in the sensory thalamocortical axons at any of the ages examined. Thus, the existence of 5-HT uptake in nonserotoninergic neurons appears to be a conserved feature in primates, although the topographic extent of this transient expression is more restricted than that previously demonstrated in rodents.