The process of reinnervation in the dentate gyrus of adult rats: An ultrastructural study of changes in presynaptic terminals as a result of sprouting

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Abstract
The present study was undertaken to define the ultrastructure of synapses of the crossed temporodentate pathway after they had sprouted to reinnervate the dentate gyrus following the destruction of the normal ipsilateral temporodentate pathway. The synapses of the sprouted crossed temporodentate pathway were identified at the EM level by using autoradiographic techniques and by evaluating the degeneration of the pathway following secondary lesions. Both EM autoradiography and EM degeneration revealed that the terminals of the sprouted crossed temporodentate pathway formed asymmetric synapses on spines; individual terminals appeared to make more synaptic contacts per terminal (multiple synapses) than in the case of the normal crossed pathway. In the two lesioned animals exhibiting the best labeling, labeled terminals made an average of 3.0 ± 2.2 and 2.0 ± 1.3 contacts per terminal. In contrast, labeled terminals in normal animals exhibited only one contact per terminal. The terminals of the sprouted pathway were also larger than those of the normal crossed pathway. The synapses of the crossed temporodentate pathway that degenerated after a secondary lesion of the entorhinal cortex exhibited both electron‐lucent and electron‐dense forms of degeneration at 2 days postlesion. In two animals that were quantitatively analyzed, the density of degenerating synaptic terminals was 281 and 218/10,000 μm2 in the terminal field of the sprouted crossed pathway. These values are much higher than in normal animals, where the density of degenerating synaptic terminals was only 2.12/10,000 μm2 at 2 days postlesion. Because degenerating terminals were evident at 2 days postlesion, the sprouted crossed pathway does not appear to exhibit the very rapid degeneration that is characteristic of the normal crossed pathway. We conclude that sprouting in this pathway involves terminal proliferation (an increase in the number of presynaptic elements), and terminal hypertrophy (an increase in the size of presynaptic terminals, together with an increase in the number of synaptic contacts formed by individual terminals).

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