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Target dependence of adult neurons: pattern of terminal arborizations
S Marty1, J M Weinitz, M Peschanski
1INSERM CJF 91-02, Faculté de médecine, Créteil, France.
Abstract:
During development, the survival of neurons in the CNS depends critically on interactions with postsynaptic target cells. The role of target cells on the maintenance of afferent neurons in the adult, however, is a matter of controversy. Morphological alterations of target-deprived neurons, such as axonal retraction or pruning, may occur. We have therefore undertaken an analysis of target-deprived neurons over time after an excitotoxic lesion in order to investigate these potential changes. Dorsal column nuclei (DCN) neurons were deprived of their target neurons in adult rats by the injection of kainic acid into the ventrobasal thalamic complex. Anterogradely transported wheat germ agglutinin conjugated to HRP from the DCN showed a progressive decrease of the density of afferent terminals during the first month after lesion. Density stabilized thereafter through the longest time studied (8 months). In contrast, the extent of the area occupied by DCN projections did not change up to 1 month and then shrank over time. These results indicated a continuous decrease in the number of axonal elements in the lesion, which is the strongest during the first month postlesion. To interpret these data, we then studied axonal morphology. Diffusion-filled lemniscal axons were labeled by WGA-HRP injections aimed at the medial lemniscus. There was no conspicuous alteration of axonal stems in the medial lemniscus. Terminal axonal arborizations and swellings dramatically decreased in number over the first month after the kainate injection, and large axonal varicosities were formed over the same period of time. These morphological data suggest that the decrease in number of axons in an excitotoxic lesion is related, at least during the first month, to a loss of axonal terminal arborizations rather than to a retraction of axonal stems. The pattern of terminal arborizations in the adult CNS may therefore depend critically on interactions of afferents with their target neurons, while the maintenance of the axonal stems does not.
Insights
Target cell interactions are crucial for maintaining adult central nervous system (CNS) afferent neuron terminal arborizations after excitotoxic lesions. Axonal stems remain intact, but terminal structures are lost.
Area of Science:
- Neuroscience
- Cell Biology
- Neuroanatomy
Background:
- Neuronal survival in the developing CNS critically depends on target cell interactions.
- The role of target cells in maintaining adult afferent neurons is debated.
- Excitotoxic lesions can induce morphological changes in target-deprived neurons.
Purpose of the Study:
- To investigate morphological changes in target-deprived neurons over time after an excitotoxic lesion.
- To determine if axonal retraction or pruning occurs in adult CNS afferent neurons.
Main Methods:
- Adult rats received kainic acid injections into the ventrobasal thalamic complex to lesion dorsal column nuclei (DCN) target neurons.
- Anterograde tracing using wheat germ agglutinin conjugated to HRP (WGA-HRP) from the DCN assessed terminal density and projection area.
- Medial lemniscus axons were labeled to study axonal stem and terminal arborization morphology.
Main Results:
- Afferent terminal density in the lesion site progressively decreased during the first month, then stabilized.
- The projection area initially remained constant, then shrank over time.
- Axonal stems showed no significant alteration, while terminal arborizations dramatically decreased, forming varicosities.
Conclusions:
- Axon loss in excitotoxic lesions is primarily due to the loss of terminal arborizations, not axonal stem retraction.
- Adult CNS terminal arborization patterns critically depend on afferent-target neuron interactions.
- Axonal stem maintenance appears independent of target cell contact in the adult CNS.