Self-reinnervated cat medial gastrocnemius muscles. II. Analysis of the mechanisms and significance of fiber type grouping in reinnervated muscles

1. The technique of glycogen depletion was used to determine 1) whether regenerating motor axons reestablish the normal regionalization of motor units (MUs) in the cat medial gastrocnemius (MG) muscle, 2) whether the extent of clumping between MU fibers and/or type grouping of muscle fibers progressively in creases with a decrease in reinnervated MU numbers, and 3) whether the pattern of innervation can explain why MUs fail to increase significantly in size when the cut nerve is sutured directly to the muscle, even when few axons make functional connections. 2. Distributions of MU fibers were analyzed in 5 normal and 14 reinnervated cat MG muscles 4.5-16 mo after sectioning of its nerve and suturing of the proximal end to the distal nerve sheaths (N-N suture) or directly to the muscle fascia (N-M suture). Muscle unit distributions were quantified according to location, territory size, density, and extent of clumping between fibers from the same MU. 3. Normal MU fibers were regionalized within five regions along the muscle's longitudinal and transverse axes. Reinnervated MUs were located within similar regions, indicating that regenerating axons follow the major proximal nerve branches to restore normal compartmentalization. 4. Muscle unit fibers were diffusely scattered within discrete MU territories in normal muscles. Territory size tended to increase with MU size, whereas density of muscle unit fibers within the territory decreased. 5. Territories increased with MU size after N-N suture but were smaller and showed little size variation after N-M suture. The extent of muscle unit fiber clumping was inversely related to the number of reinnervated MUs. On average, the extent of clumping was substantially higher in muscles reinnervated after N- M suture. These results indicate that distal nerve sheaths facilitate proximal exon branching, which establishes MU territory size. Once the territory is established, motor axons branch distally to increase MU size, which in turn compensates for reduced MU numbers. 6. Muscles reinnervated by <80% of the MUs exhibited fiber type grouping of type I fibers, and on average the extent of clumping was substantially higher in muscles reinnervated after N-M suture. With less innervation, type grouping increased inversely with the number of reinnervated MUs. However, for a similar number of MUs, type I fiber type grouping was substantially higher in muscle reinnervated after N-M suture. Type grouping therefore reflects muscle unit fiber clumping under conditions where MU size increased (N-N suture) or MU territory size decreased (N-M suture).