Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat

Abstract

Many dendritic spines in the dentate gyrus normally have polyribosomes under the spine base. The present study asks whether there are changes in these spine-associated polyribosomes when the spines are denervated and reinnervated following lesions. Rats were prepared for electron microscopy 2, 4, 6, 8, 10, 12, and 14 days, and approximately 7 months following unilateral destruction of the entorhinal cortex. Dendritic polyribosomes were evaluated in the denervated neuropil of the dentate gyrus ipsilateral to the lesion and in the neuropil of the contralateral (control) dentate gyrus. Qualitative observations revealed that polyribosomes in denervated dendrites were selectively localized under the base of dendritic spines as is also the case in normal dendrites. However, the incidence of polyribosomes under the base of spines appeared qualitatively much higher than normal, and there appeared to be a substantial increase in the number of spine necks and heads with polyribosomes. Quantitative analyses were undertaken to evaluate (1) the incidence of polyribosomes under spine bases, (2) the number of polyribosome-containing spine necks and heads per area of neuropil, and (3) the total number of polyribosomes within dendritic segments within the denervated zone. The incidence of polyribosomes under spine bases was evaluated in each animal from a series of 21 to 22 photographs of identified spines (a spine visible in its entirety from its point of origin on the parent dendrite to the region of synaptic contact). All identified spines within each photographic field of approximately 60 pm" were scored for the presence of polyribosomes. Over the post-lesion interval, the incidence of polyribosomes associated with identified spines increased about 3-fold from the control incidence of 11.6% (determined from a similar series of photographs from the control side of each animal). Peak incidence was observed at 8 days post-lesion. The number of polyribosomecontaining spine bases per 1000 pm" of neuropil increased with the same time course, indicating that the changes in incidence were not a result of a selective disappearance of spines without polyribosomes. The number of polyribosome-containing spine necks and heads per 1000 pm" of neuropil was defined in the same series of photographs and also increased about 3-fold, with approximately the same time course as the increases in polyribosome-containing spine bases. Despite the dramatic increases in the number of polyribosomes in and around spines, there was only a very modest increase in the total number of dendritic polyribosomes per area of neuropil and essentially no increase in the number of polyribosomes per area of dendrite. The combined results suggest a redistribution of dendritic polyribosomes into the region of the dendrite which is specialized for the receipt of an afferent synapse (the spine and its postsynaptic membrane specialization). This redistribution occurs during a period of terminal proliferation, suggesting that these two processes are related. I propose that these events reflect some process within the denervated dendrites related to the preparation of the dendrite for reinnervation or to the initiation of the sprouting response.