Polyneuronal Innervation of Single Muscle Fibers in Cat Eye Muscle: Inferior Oblique

Single muscle fibers with multiple axonal endplates (multiply innervated fibers) are normally present in adult extraocular muscles (EOMs), while most other mammalian skeletal muscles contain fibers with a single myoneural junction. Recent findings by others led us to investigate for the presence of polyneuronal innervation (innervation of a single muscle fiber by >1 motoneuron) in the inferior oblique (IO) muscle of pentobarbital anesthetized cats. The IO muscle nerve branches, as they coursed through the orbit, were further divided for independent or simultaneous electrical stimulation with bipolar electrodes. Four of five established tests for polyneuronal innervation gave positive results. The sum of the twitch (1) and tetanic (2) tensions in response to individual nerve branch stimulation was greater than that for simultaneous (whole) nerve stimulation. The summed electromyographic (EMG) responses (3) gave a similar positive result. The result for crossed tetanic potentiation (4) was negative for polyneuronal innervation while the crossed fatigue (5) test was positive. These results are consistent with recent studies. That the EOMs exhibit polyneuronal innervation further explains the eye-movement system's functional integrity during some neuromuscular disorders as well as its ability to operate with precision after the loss of numerous motoneurons.

Properties of motor units after self-reinnervation of the cat superior oblique muscle

1. The mechanical properties of motor units of the cat superior oblique muscle and axonal conduction velocities of trochlear motoneurons have been studied at several postoperative times after intracranial axotomy of the trochlear nerve. 2. Whole muscle twitch forces were generally within the normal range by approximately 4 mo postoperative, indicating that reinnervation is complete at this time. 3. Among animals studied 3.5-4.5 months after trochlear axotomy, average motor-unit tetanic forces were increased by a factor of approximately 2.5 compared with units studied in normal superior oblique muscle. Average motor-unit tetanic forces in animals studied 14.5-23 mo after axotomy were also increased relative to normal, but the difference was not significant. Among all reinnervated motor units, there was a tendency for increased twitch time-to-peak relative to control. Reinnervated motor-unit fatigue properties were similar to normal. 4. Average trochlear motoneuron conduction velocities for animals at all postoperative intervals remained significantly lower than the average conduction velocities from three of four normal animals. 5. Counts of Nissl-stained cell bodies in axotomized and control, contralateral trochlear nuclei showed that some cell loss had occurred, averaging approximately 17% 3.5-4.5 mo postoperative and 24% 14.5-23 mo postoperative. Associated with this loss was an increase (10%) of axotomized motoneuron soma cross-sectional area. 6. Muscle fiber cross-sectional areas (CSA) were measured in reinnervated superior oblique muscles and compared with CSAs from contralateral, control muscles. Average CSA was significantly decreased in all reinnervated muscles, with the relative decreases ranging from approximately 10 to 28%. 7. The results are discussed in terms of factors that determine motor-unit force; muscle fiber CSA, specific force, and innervation ratio. We conclude that the increases of average motor-unit force in short-term reinnervated superior oblique muscles are most likely related to polyneuronal innervation of muscle fibers and that the return of these forces to normal levels in long-term muscles is related to synapse elimination. Our results are compared with those of other self-reinnervation studies, and the potential role played by the time muscle remains denervated in determining the persistence of polyneuronal innervation after reinnervation is considered.