Tail Muscles Become Slow but Fatigable in Chronic Sacral Spinal Rats With Spasticity

Abstract

Paralyzed skeletal muscle sometimes becomes faster and more fatigable after spinal cord injury (SCI) because of reduced activity. However, in some cases, pronounced muscle activity in the form of spasticity (hyperreflexia and hypertonus) occurs after long-term SCI. We hypothesized that this spastic activity may be associated with a reversal back to a slower, less fatigable muscle. In adult rats, a sacral (S2) spinal cord transection was performed, affecting only tail musculature and resulting in chronic tail spasticity beginning 2 wk later and lasting indefinitely. At 8 mo after injury, we examined the contractile properties of the segmental tail muscle in anesthetized spastic rats and in age-matched normal rats. The segmental tail muscle has only a few motor units (<12), which were easily detected with graded nerve stimulation, revealing two clear motor unit twitch durations. The dominant faster unit twitches peaked at 15 ms and ended within 50 ms, whereas the slower unit twitches only peaked at 30-50 ms. With chronic injury, this slow twitch component increased, resulting in a large overall increase (>150%) in the fraction of the peak muscle twitch force remaining at 50 ms. With injury, the peak muscle twitch (evoked with supramaximal stimulation) also increased in its time to peak (+48.9%) and half-rise time (+150.0%), and decreased in its maximum rise (-35.0%) and decay rates (-40.1%). Likewise, after a tetanic stimulation, the tetanus half-fall time increased by 53.8%. Therefore the slow portion of the muscle was enhanced in spastic muscles. Consistent with slowing, posttetanic potentiation was 9.2% lower and the stimulation frequency required to produce half-maximal tetanus decreased 39.0% in chronic spinals. Interestingly, in spastic muscles compared with normal, whole muscle twitch force was 81.1% higher, whereas tetanic force production was 38.1% lower. Hence the twitch-to-tetanus ratio increased 104.0%. Inconsistent with overall slowing, whole spastic muscles were 61.5% more fatigable than normal muscles. Thus contrary to the classical slow-to-fast conversion that is seen after SCI without spasticity, SCI with spasticity is associated with a mixed effect, including a preservation/enhancement of slow properties, but a loss of fatigue resistance.