Regeneration of Axons and Synaptic Complex Formation Rostral to the Site of Hemisection in the Spinal Cord of the Monkey

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Abstract
Historically, injury of the mammalian spinal cord resulted in abortive regeneration. Recent findings have shown regeneration of the spinal cord occurs by limited regrowth of severed nerve fibers and massive regrowth of axonal sprouts of normal axons. The foregoing study investigates the regenerative capacity of the spinal cord in 14 Rhesus monkeys (Macaca mulatto) following left hemisection at vertebral segment T2. In addition to three normals, animals were utilized 7, 14, 21 days and 1, 2, 3, and 4 months posthemisection. Tissue was prepared for Golgi impregnation, Protargol-cresyl violet-eosin staining, and electron microscopy. The motor horn rostral to the site of lesion was investigated. Dendrites of motor horn cells adjacent to and facing the lesion developed varicosities which formed at the terminal end of the dendrite by day 7 and progressed to include the entire dendrite by day 14–30 posthemisection. Motor horn cell dendrites (0–5 mm from lesion) were varicose and many possessed only two short, varicose, dendrites by 1 month posthemisection. Varicosities generally formed only on tertiary and secondary dendrites, 5–9 mm rostral to the lesion; however, dendrites facing degenerating tracts often were completely varicose. Neurite fascicles (predominantly axons), often free of neuroglial cell processes, were observed in the enlarged extracellular spaces. Axons, mainly from the neurite fascicles, made several types of synaptic recombinations with reactive neurons. The most frequent type of synaptic complex had a cup-shaped bouton with a central large extracellular space between pre- and postsynaptic membrane. The peripheral portion of the bouton made synaptic complexes with small, equal, pre- and postsynaptic membrane specializations and a 250-300 Å synaptic cleft. The postsynaptic neuron usually possessed a thickened membrane or a subsurface cistern with thickened membranes associated with the enlarged subsynaptic space. In addition, somatic and dendritic synapses were observed with cisterns or extensive Nissl bodies adjacent to the postsynaptic membrane. Synaptic complexes with normal organelles and synaptic clefts were also observed in different states of maturation. The central nervous system of the monkey undergoes regenerative changes involving both dendritic modification and synapse formation. The regenerating nerve fibers synapse on neurons proximal to the site of lesion and do not enter the cicatrix. The specificity of the regenerating nerve fibers for neurons and neuronal membrane is discussed.