This study examines the projection of dorsal root fibers to the upper dorsal horn of the monkey lumbar spinal cord utilizing degeneration and autoradiographic methods. The animals survived dorsal rhizotomy for periods varying from 18 hours to 28 days. Electron microscopy reveals the earliest degeneration to be neurofilamentous alteration of large synaptic profiles in lamina III and the inner zone of the substantia gelatinosa (IIi). This degeneration begins 18 hours after rhizotomy, reaches a peak at three days postoperatively and disappears by the end of the first week. Degenerating myelinated axons in the spinal gray matter, dorsal column white matter and Lissauer's tract first appear three days postoperatively. The second tye of degeneration of synapses occurs in lamina I and outer gelatinosa (IIo) and consists of electron lucent alteration of moderate size synapses, especially those having large granular vesicles (LGVs) and some neurofilamentous and dense degeneration. This synaptic degeneration in lamina I begins two days following rhizotomy and reaches a peak between five to seven days, declines markedly by ten days and is absent at four weeks survival. The third type of degeneration occurs in the substantia gelatinosa (laminae IIo and IIi) initially as an enlargement of synaptic vesicles at two days and then progresses to large numbers of electron dense small synapses, the peak of degeneration occurring at seven days and persisting as long as four weeks postoperatively. Some of the dense synapses can be seen to arise from small, nonmyelinated axons. These axons are first seen to be degenerating in the gelatinosal and marginal layers at four days survival and the first definite degeneration of nonmyelinated axons in Lissauer's tract is at seven days postoperatively. It is concluded that the largest axons projecting to this region of the dorsal horn degenerate most rapidly and that these axons are distributed to laminae III and IIi. Axons of intermediate diameter degenerate next and are distributed principally to laminae I and IIo. Fine diameter axons, probably nonmyelinated, degenerate more slowly and terminate principally in the substantia gelatinosa (IIi and IIo). There is some overlap in these projection domains, in that the principal projection to lamina III extends into the lower part of the gelatinosa and the projection to the marginal layer overlaps the outer gelatinosa. The axon terminals in gelatinosa of C fibers are sometimes postsynaptic in axoaxonal synapses as are several of the axon terminals of larger A fibers in lamina III. Most of the synapses of primary afferent origin in lamina I are not involved in axoaxonal synapses. It is likely that the terminations of many primary afferent fibers in laminae II and III are subject to presynaptic inhibition and those in lamina I are not. Some of the primary afferents in all three laminae synapse upon presynaptic dendrites and thus may influence transmitter release from these profiles. The LGV profiles are distributed in a manner similar to the distribution of substance P and it is suggested that the degenerating LGV profiles may contain substance P. Most of the LGV profiles and many of the round vesicle profiles do not appear to be derived from dorsal root, but most of the central synaptic profiles are of primary afferent origin. In no case was there evidence that flat vesicle synapses were derived from primary afferents. Following dorsal root ganglia injections with H3 leucine, light microscopic autoradiography at short postoperative survival times demonstrated heavy grain distribution over marginal and gelatinosal layers with somewhat less numbers of grains over lamina III. There were also many grains over the dorsal column white matter and Lissauer's tract. Electron microscopic autoradiography revealed that the majority of labeled structures seen with fast axonal transport in the upper dorsal horn are not synapses but are myelinated and nonmyelinated axons. Labeled synapses were the same types as those undergoing degeneration following rhizotomy: round vesicle profiles, central synaptic profiles and LGV profiles. Each of the labeled types was distributed throughout the upper laminae, with the exception of LGV profiles which are uncommon in layers deep to the outer zone of the gelatinosa. It is concluded that fast axon transport autoradiography is not a selective label for synapses in the cord and light microscopic autoradiography does not provide direct estimates of synaptic densities in the dorsal horn. Copyright © 1979 The Wistar Institute Press
