Do synaptic rearrangements underlie compensatory reflex enhancement in spinal motoneurons after partial cell loss?

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In adult cats, avulsion of a spinal ventral root induces retrograde cell death among the corresponding motoneurons and, also, enhanced monosynaptic reflexes ipsilaterally in the adjacent uninjured spinal cord segments. The present study investigates possible mechanisms behind this reflex potentiation. At 1-12 weeks after unilateral L7 ventral root avulsion, the L7 dorsal root ganglia were bilaterally injected with choleragenoid-HRP to light microscopically quantify the amount of HRP-labeled terminals in the motor nuclei of the lesioned L7 segment and adjacent intact L6+S1 segments. In addition, motoneuron synaptology and individual HRP-labeled boutons were analyzed electron microscopically. In the L7 segment, the loss of motoneurons at 12 weeks after ventral root avulsion was accompanied by a marked loss of HRP-labeled boutons in the corresponding ventral horn. In the L6/S1 segments, the monosynaptic reflex enhancement found ipsilaterally at 12 weeks postoperatively (mean 212%) was not accompanied by an increased HRP-labeling in the ventral horn (mean 109%), indicating that no sprouting or enlargement of the monosynaptic boutons had occurred. Ultrastructurally, the values for apposition length, total active site length, cross-sectional area, and mitochondrial density of the labeled boutons were also similar between the two sides. However, ipsilaterally the L6/S1 motoneurons exhibited an increased membrane covering by presumably excitatory boutons. The present results indicate that after partial cell death in a motoneuron pool the remaining motoneurons may undergo compensatory synaptic rearrangements leading to increased excitability and enhanced reflexes.