Selective reinnervation of intercostal muscles transplanted from different segmental levels to a common site

We transplanted external intercostal muscles from one of several thoracic (T) levels to the neck of adult rats. The cervical sympathetic trunk, which innervates the superior cervical ganglion, was cut, and its proximal end was apposed to the muscle. Preganglionic axons in the trunk reinnervated muscle fibers in the transplants. We determined the segmental origin of synaptic inputs to transplanted muscles by recording intracellularly from muscle fibers while stimulating individual ventral roots which supply axons to the trunk. In one series of experiments, T2 or T8 muscles were transplanted from the thorax to the neck of the same rat. While T2 and T8 muscles were reinnervated to a similar extent, they differed in the segmental origin of the innervation they received: T2 muscles received more inputs from rostral segments (T1 and T2) than did T8 muscles, and T8 muscles received more inputs from caudal segments (T4 to T6) than did T2 muscles. This difference between reinnervation of T2 and T8 muscles was detected both 2 to 4 weeks and 10 to 14 weeks after surgery. In a separate series, using rats of an inbred strain, T3, T4, or T5 muscles were transplanted from one rat to a separate host. Again, the average segmental origin of inputs to transplants from different levels differed systematically: it was most rostral to T3 muscles, intermediate to T4 muscles, and most caudal to T5 muscles. Finally, T3 and T5 muscles were soaked in a myotoxin, Marcaine, before reimplantation. This treatment kills muscle fibers but not myoblastic satellite cells; therefore, muscle fibers were replaced by regeneration. Marcaine-treated T3 and T5 muscles were successfully reinnervated but did not differ significantly in the segmental origin of their inputs. Our results show that adult mammalian muscles can be selectively reinnervated, and they raise the possibility that the selectivity is based on some positional quality that matches axons and muscles from corresponding segments. However, while differences among muscles survive denervation and transplantation, their expression or accessibility may change during regeneration.