Trophic interactions between rat nerves and blood vessels in denervated peripheral arteries and in anterior eye chamber transplants.

ABSTRACT

This investigation was undertaken to examine trophic interrelationships between nerves and arteries in male Wistar rats. Two approaches were used. (1) Surgical denervation of two peripheral muscular arteries in the thigh (the superficial epigastric and saphenous) was carried out on young animals (5-20 days old). (2) Arteries from young adults, either with a high density of innervation in situ (the tail artery), or virtually uninnervated (the femoral artery), were transplanted into intact or sympathectomized anterior eye chambers of adult rat hosts. In the denervation experiments, the maximum length of time before reinnervation occurred was 15 days postoperatively. The only evidence of morphological change in the vessel wall was in the external elastic lamina that became irregular and laminated. Reinnervation followed the typical developmental sequence, and was accelerated in the younger animals and by a double lesion. Translocating the proximal part of the nerve carrying the vasomotor innervation indicated that sprouting was directional toward the muscular arteries, bypassing an artery with very sparse innervation. The transplant experiments into the anterior eye chamber showed that only an artery densely innervated in situ (the tail artery) could induce reinnervation by iridean nerve sprouting. The tail artery, in the chamber lacking adrenergic innervation of the iris, became reinnervated by terminals with small agranular vesicles. These vesicles were part of Schwann cell complexes, at a similar relative density, occupying the same position in the vessel wall, as the ingrowing nerves in the fully innervated iris. The latter also had a proportion of terminals with the small clear vesicles. A small population of large granular vesicles could also be found in both types of terminals. Therefore, tissue normally having only sympathetic innervation cannot be assumed to be completely noninnervated when transplanted into a sympathectomized anterior eye chamber. The denervation and transplant experiments described here demonstrated the presence of trophic interactions between nerves and arteries, but also revealed a heterogeneity of response between vessels with very high and extremely low levels of innervation in situ.