The Journal of Neurophysiology Vol. 81 No. 4 April 1999, pp. 1636-1644
Copyright ©1999 by the American Physiological Society

Ultrastructural Analysis of Ectopic Synaptic Boutons Arising From Peripherally Regenerated Primary Afferent Fibers

 ¹Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261; and  ²Department of Physiology, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599

Koerber, H. Richard, Karoly Mirnics, Anahid M. Kavookjian, and Alan R. Light. Ultrastructural analysis of ectopic synaptic boutons arising from peripherally regenerated primary afferent fibers. The central axons of peripherally regenerated A primary sensory neurons were impaled in the dorsal columns of -chloralose-anesthetized cats 9-12 mo after axotomy. The adequate peripheral stimulus was determined, and the afferent fibers intracellularly stimulated while simultaneously recording the resulting cord dorsum potentials (CDPs). Fibers that successfully had reinnervated the skin responded to light tactile stimulation, and evoked CDPs that suggested dorsally located boutons were stained intracellularly with horseradish peroxidase (HRP). Two HRP-stained regenerated A afferent fibers were recovered that supported large numbers of axon collaterals and swellings in laminae I, II_o, and II_i. Sections containing the ectopic collateral fibers and terminals in the superficial dorsal horn were embedded in plastic. Analyses of serial ultrathin sections revealed that ectopic projections from both regenerated fibers supported numerous synaptic boutons filled with clear round vesicles, a few large dense core vesicles (LDCVs) and several mitochondria (>3). All profiles examined in serial sections (19) formed one to three asymmetric axo-dendritic contacts. Unmyelinated portions of ectopic fibers giving rise to en passant and terminal boutons often contained numerous clear round vesicles. Several boutons (47%) received asymmetric contacts from axon terminals containing pleomorphic vesicles. These results strongly suggest that regenerated A fibers activated by light tactile stimuli support functional connections in the superficial dorsal horn that have distinct ultrastructural features. In addition, the appearance of LDCVs suggests that primary sensory neurons are capable of changing their neurochemical phenotype.