Central Sprouting and Functional Plasticity of Regenerated Primary Afferents

A combination of neuroanatomical and electrophysiological techniques was used to study the effects of peripheral axotomy and regeneration of primary afferents on their central projections in the spinal cord. Individual regenerated afferent fibers were impaled with HRP-filled electrodes in the dorsal columns of alpha-chloralose-anesthetized cats and activated by current pulses delivered via the intracellular electrode. The resulting cord dorsum potentials (CDPs) were recorded at four rostrocaudal locations and HRP was iontophoretically injected into the fiber. Central distributions of boutons and CDPs were compared with peripheral receptor type to determine the accuracy of peripheral regeneration and the effects of central-peripheral mismatches. Reconstruction of the central projections of 13 individual afferents for which the adequate stimulus and CDPs had been recorded revealed many abnormalities. For example, unlike controls, four group I and II afferents with central projections typical of proprioceptors (concentrated in laminae V, VI, and VII) innervating either cutaneous or noncutaneous targets evoked measurable CDPs. Three other group II or A beta afferents innervating low-threshold mechanoreceptors with central terminations confined to the dorsal horn exhibited extensive collateralization in laminae I and II in addition to large numbers of terminals in laminae III-IV. These fibers activated central networks whose adaptation behavior was identical to those evoked by high-threshold mechanoreceptive afferents in controls. These results suggest that primary afferents and their central connections are capable of significant modifications following axotomy and regeneration. In addition, the anatomical studies indicate some reorganization in the laminar distribution of boutons as well as in bouton size.