Fine structural alteration in target-deprived axonal terminals in the rat thalamus

Lesioning of thalamic target neurons in the adult rat provokes a resorption of terminal axonal branches of afferent neurons from the dorsal column nuclei. There is, however, no massive neuronal loss in the dorsal column nuclei. In the adult, therefore, the thalamic post synaptic target cells influence primarily the extent of the terminal component of the afferent neurons. The subcellular changes underlying the regression of these adult terminals are unknown. To address this issue, we have looked at the electron microscopic level for the ultrastructural correlates of this retraction of the terminal compartment of target-deprived neurons in the adult rat thalamus. By analysing the fine structure of target-deprived axons and their immunoreactivity for a specific synaptic protein, synaptophysin, we have observed that all the organelles and the protein formed in the cell body, including dense-core vesicles, continue to be transported to the terminal compartment and accumulate at this level. At the terminal level, engorgement of organelles induces the formation of varicosities. An enormous increase in local degradative activity occurs in parallel to this accumulation. In contrast, organelles involved in membrane turnover and degradation (including synaptic and coated vesicles, multivesicular bodies, lysosomes) in the nerve terminals are clearly modified. There is a progressive loss of synaptic vesicles, whereas clathrin-coated vesicles and multivesicular bodies are numerous. We propose that the resorption of terminal axonal branches after thalamic target deprivation in the adult is associated with a bias of the system of membrane recycling at the axonal terminals towards degradation. In the absence of apparent changes in the pathways originating from the cell body in these conditions, it is unlikely that presynaptic neurons in the adult thalamus are dependent upon post synaptic target neurons for the delivery of organelles and proteins to the terminals.