Deafferentation-induced expansion of saphenous terminal field labelling in the adult rat dorsal horn following pronase injection of the sciatic nerve

Abstract

We have examined the effect of the degeneration of sciatic nerve afferents on the distribution of saphenous terminals in the adult rat dorsal horn. Deafferentation was produced by injection into the sciatic nerve of pronase, a combination of proteolytic enzymes, which causes death of ganglion cells and degeneration of their terminal fields. The saphenous terminal fields were labelled by exposing the cut nerve to a combination of horseradish peroxidase (HRP) and wheat germ agglutinin-horseradish peroxidase (WGA-HRP). Terminals were mainly found in the superficial dorsal horn, indicating that small-diameter afferents were heavily labelled. In one group of control animals, the normal sciatic and normal saphenous terminal fields were shown to be bilaterally symmetrical. In the experimental group, the initial injection of one sciatic nerve with pronase was followed 4 months later by bilateral HRP/WGA-HRP labelling of both saphenous nerves. In each animal, the terminal field of the saphenous nerve on the lesioned side was expanded in the medial, lateral, and caudal directions. Medially and laterally, the expanded terminal field overlapped more of the sciatic territory than normal; caudally, saphenous terminals were found in the rostral portion of the L5 segment, in an area normally filled by sciatic terminals and devoid of saphenous terminals. The expansion resulted in a total saphenous area 26% larger than the control side. Electron microscopy demonstrated that the label in both the normal and expanded territories was primarily contained in axons and terminals, with minor transneuronal labelling. Labelled terminals in the expanded areas were both simple terminals with round, clear vesicles, and glomerular terminals with multiple synaptic contacts; these terminal types resemble those previously described for primary afferents in the superficial dorsal horn. Although the preexistence of "silent" synaptic terminals in the expanded areas cannot be disproven, the data support the hypothesis that primary afferents in the adult have the potential to sprout and establish synapses when the conditions of the deafferentation are favorable.