Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats.

Evidence from previous light-microscopic studies suggested that lumbosacral dorsal rhizotomy in cats elicits sprouting of converging undamaged systems into partially deafferented Clarke's nucleus and lamina II. We therefore applied quantitative electron-microscopic methods to determine whether this sprouting is associated with replacement of synaptic terminals (reactive reinnervation). We used stereological and morphometric methods to estimate terminal number per cross section in right and left lamina II and Clarke's nucleus in adult cats after acute and chronic unilateral (right-sided) lumbosacral deafferentation. Planimetric measurements of area indicated no significant shrinkage of either region as a result of the deafferentation; an increase in area occupied by glial cytoplasm (gliosis) equaled the decrease occupied by axonal components. The gliosis appears to persist indefinitely, although the degenerative debris stainable with conventional light-microscopic methods does not persist. Analysis of the synaptic population of lamina II reveals that the large central or "scalloped" terminals comprise a substantial fraction (greater than 40%) of the total area occupied by terminals in control material and that this population is largely lost upon deafferentation, leaving a large population of small terminals with spherical vesicles. Nevertheless, estimates of total terminal number indicate no difference between control and deafferented lamina II, suggesting a rapid and virtually complete replacement of lost dorsal root terminals by small terminals containing spherical vesicles. Terminal number in Clarke's nucleus also remains constant despite the loss of the dorsal root input. We conclude that there is also a virtually complete and rapid replacement of lost terminals in Clarke's nucleus by terminals containing spherical vesicles. These data provide an example of a case in which axonal sprouting demonstrated with light-microscopic methods is associated with electron-microscopic evidence of reactive reinnervation.