The development of the synaptic organization of the serotonergic system differs in brain areas with different functions

The serotonergic innervation of the developing superior colliculus and ventrolateral nucleus of the thalamus of the rat were studied with light and electron microscope immunocytochemistry. We compared the pattern of innervation and synaptic organization of the serotonin (5-HT) system in the superficial and deep layers of the superior colliculus. We also compared the developmental pattern of synaptic incidence of 5-HT varicosities in the superior colliculus with that in the ventrolateral nucleus. Serotonin fibers were present in the superior colliculus at birth, concentrated mainly in the deep layers, whereas the superficial layers were only sparsely innervated. By the end of the first postnatal week the overall density of 5-HT fibers increased, but was still higher in the deep than in the superficial layers. The distribution pattern, density, and morphology of serotonergic axons acquired mature features by the end of the third postnatal week. In the adult, these axons were thin, varicose, forming a complex network which was denser in the lower part of the superficial layers and the upper part of the deep layers. Electron microscopical analysis revealed that the vast majority of 5-HT varicosities established symmetrical synapses with dendritic shafts in all layers of the superior colliculus throughout development. In the superficial layers, known to be involved in visual functions, the proportion of varicosities forming synapses increased gradually from birth to reach a peak at the end of the first postnatal week, then declined markedly in the subsequent 2 weeks before rising again at later stages. In contrast, in the deep layers and in the ventrolateral nucleus of the thalamus, areas involved in motor functions, the proportion of 5-HT varicosities engaged in synaptic contacts showed a continuous increase from birth until adulthood. Considering these results together with data from our previous studies, we speculate that the regional heterogeneity in the synaptic organization of the serotonergic system may reflect a differential role of 5-HT in the development of brain areas with different functions. (C) 1998 Academic Press.