Incomplete rematching of nerve and muscle properties in motor units after extensive nerve injuries in cat hindlimb muscle

Abstract

Motor units were characterized in partially denervated or completely denervated and reinnervated cat medial gastrocnemius (MG) muscles where the number of innervating motor axons was severely reduced to determine (1) to what extent the nerve and muscle properties are rematched in enlarged motor units, (2) whether the normal size relationships between axon size, unit tetanic force and contractile speed are re‐established, and (3) whether the type of nerve injury and/or repair affects the re‐establishment of nerve and muscle properties. Single MG units were sampled in (1) partially denervated muscles and in reinnervated muscles after either (2) crushing or (3) transecting the nerve and suturing its proximal end to either the distal nerve stump (N‐N), or (4) directly to the muscle fascia (N‐M). The majority (75‐88 %) of motor units in all muscles were classified as S (slow), FR (fast fatigue resistant), FI (fast fatigue intermediate) and FF (fast fatigable). However, there was an increased number of FI and unclassifiable motor units compared to normal. These results suggest that motor unit properties are not entirely regulated by the reinnervating motoneurone. Despite more overlap in the range of unit force between different motor unit types the tetanic force of each type increased in all muscles when reinnervated by few (< 50 %) motor axons. This increase in unit force was due to an expansion in motor unit innervation ratio. The normal relationships between axon size, unit tetanic force, and contractile speed were re‐established in all muscles except when reinnervated by < 50 % of their normal complement of motor units after N‐M suture. This lack of correlation was due to the reduced fast glycolytic (FG) fibre size and the proportionately greater increase in force of the S units. After reinnervation the ranges in fibre cross‐sectional area within single FF units were very similar to those found within the entire FG fibre population. These results show that when few axons make functional connections in partially denervated or reinnervated muscles the normal relationships between axon size and motor unit contractile properties are re‐established provided the nerves regenerate within the distal nerve sheath. This rematching of motoneurone size and motor unit contractile properties occurs primarily because the size of the motor axon governs the number of muscle fibres it supplies.

Regional distribution of slow‐twitch muscle fibers after reinnervation in adult rat hindlimb muscles

“…Furthermore, during development a correct matching also takes place between the functional properties of the slow‐ and fast‐twitch motoneurons and those of their muscle fibers 20. For this latter aspect, (re‐)matching mechanisms are still present in adults, although to varying degrees in different fibers and situations 7, 21, 29, 33, 40. However, with regard to the guidance mechanisms for regenerating motor axons, inter ‐muscular path‐selections apparently become dysfunctional soon after birth (rats),1, 17 whereas intra‐ muscular path‐selections remain (partly) available also in adults (Figs.…”

Superior muscle reinnervation after autologous nerve graft or poly-L-lactide-?-caprolactone (PLC) tube implantation in comparison to silicone tube repair

“…By means of terminal collateral sprouting regenerated axons reinnervate a higher number of muscle fibers than originally (Brown et al, 1981; Gordon et al, 1991). Due to this increase of motor unit size almost the same strength and CMAP amplitude can be achieved with less motoneurons than in the normal state (Rafuse and Gordon, 1998).…”

Polysialylated Neural Cell Adhesion Molecule Is Necessary for Selective Targeting of Regenerating Motor Neurons

“…However, there are several examples in which selective axon regeneration likely occurs. For example, physiologically distinct classes of fast and slow motor neurons have a propensity to reinnervate their appropriate class of muscle fibers preferentially (Soileau et al, 1987;Everett, 1990, 1991;Nemeth et al, 1993;Unguez et al, 1993;Rafuse and Gordon, 1998;Wang et al, 2002). Similarly, transected motor neurons reinnervate the diaphragm in the same topographically correct manner as occurs during development (Laskowski and Sanes, 1988), suggesting that many of the same guidance cues expressed during embryogenesis are reexpressed after peripheral nerve injury.…”