Terminal proliferation and synaptogenesis following partial deafferentation: The reinnervation of the inner molecular layer of the dentate gyrus following removal of its commissural afferents

Abstract

The inner one-third of the dendritic region of the dentate gyrus granule cells in adult rats receives projections primarily from the commissural fibers of the contralateral hippocampus and the associational fibers of the ipsilateral hippocampus. At two to four days following the complete removal of the contralateral hippocampus, approximately 25% of the terminals in the inner molecular layer are observed degenerating. This provides an excellent model system to investigate possible terminal proliferation induced by deafferentation since (1) the experimental lesion is easily reproducible, (2) no retrograde reactions occur in the granule cells as a direct result of the lesion, (3) no shrinkage is detected in this region following commissural deafferentation, (4) the same dendritic region can be relocated precisely in each animal, and (5) the synaptic counts are highly consistent between animals. Results from this study and from previous investigations demonstrate that the commissural projection is contained within a 0–80 μ zone directly above the granule cell layer. Complete photomontages of this zone were taken, but only the 40–80 μ zone was quantified for neuronal and glial changes in three normal, five 2- to 4-day, and five 50- to 75-day postlesion animals. The average synaptic count dropped to 64% of control values by 2 to 4 days, but returned to 97% by 50- to 75 days postlesion. The number of terminals showing multiple synaptic contacts increased slightly in the long-term animals. Measurements of average terminal area showed no change between the short- and long-term survival groups. These results indicate that this dendritic region is reinnervated following partial deafferentation and that the reinnervation is due primarily to the formation of new terminals rather than the expansion of pre-existing terminals.