Synaptic remodeling of serotonin axon terminals in rat agranular cerebellum

In order to assess the influence of the target zone on the synaptic modeling of central serotonin (5-HT) axons, the 5-HT innervation of the posterior vermal cortex was studied by high resolution radioautography in both normal and X-ray-induced agranular rat cerebella, following topical application of [3H]5-HT. Two major systems of 5-HT afferents were identified in normal cerebellar cortex: (1) typical mossy fibers confined to the granular layer and (2) fine beaded axons diffusely distributed through all layers. The density of this innervation was estimated to be approximately 240,000 varicosities/cu.mm of cortex. The labeled mossy terminals all established synaptic contacts with the dendrites of granule cells. In contrast, only 3% of the varicosities belonging to the 'diffuse system' exhibited active zones in single thin sections, implying that less than 9% were actually engaged in junctional synaptic relationships. In the agranular cerebellar cortex, all 5-HT terminals belonging to the so-called 'diffuse system'. Their density was more than 8 times higher than in normal rat (2 million/cu.mm of cortex), an increase accounted for by the smaller volume of the experimental cerebellum. Thirty-five per cent of these 5-HT varicosities were seen in synaptic contact, indicating that all established at least one junctional complex. Most of these synapses were made on the branchlet spines of Purkinje cell dendrites, but some were also observed on the dendritic shafts of Golgi cells. Thus, in the absence of granule cells, the 5-HT innervation of rat cerebellar cortex evolves from a mostly 'non-junctional' into an entirely 'junctional' input. This finding indicates that the territory of innervation can exert a determinant influence on the synaptic modeling of incoming 5-HT afferents.