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

Abstract

Dimitrova DM, Allman BL, Shall MS, Goldberg SJ. Polyneuronal innervation of single muscle fibers in cat eye muscle: inferior oblique. J Neurophysiol 101: 2815-2821, 2009. First published March 18, 2009 doi:10.1152/jn.90828.2008. 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 Ͼ1 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.

Percutaneous pulmonary valve implantation preceded by routine prestenting with a bare metal stent

“…En grappe endplates are scattered longitudinally along a single muscle fiber, suggesting that many en grappe‐type junctions along a single muscle fiber are innervated by the same motor neuron. Moreover, unlike en grappe‐type junctions in other vertebrate muscles (Wilkinson and Lichtman, 1985; Lichtman et al, 1985), a lack of unoccupied AChR‐rich regions of the muscle membrane suggested that EOM en grappe‐type junctional sites are innervated by a single nerve terminal (Bach‐y‐Rita and Lennerstrand, 1975; but see Dimitrova et al, 2009). Unexpectedly, analysis of thy1:yfp‐lineH mice also demonstrated that some en grappe and en plaque NMJs were contacted by the same motor axon (Figs.…”

A Novel Type of Multiterminal Motor Endplate in Human Extraocular Muscles

“…30 Electrophysiological data elegantly show that the sum of twitch and tetanic tensions in response to individual nerve branch stimulation is greater than that when the whole EOM nerve is simultaneously stimulated, indicating the presence of polyneuronal innervation. 27,28 In addition, by using silver teasing and/or acetylcholinesterase staining method, Dietert 5 and Oda 20 demonstrate multiterminal endplates that are innervated by several different motor axons, indicating the presence of polyneuronal innervation also in human EOMs.…”

“…However, the finding of neighboring en plaque endings with distinct AChR subunit composition on a given myofiber favors the possibility of polyneuronal innervation. The presence of polyneuronal innervation has been recognized electrophysiologically in the EOMs of mammals, including cat, [24][25][26][27][28] monkey, 26,29 and rat. 30 Electrophysiological data elegantly show that the sum of twitch and tetanic tensions in response to individual nerve branch stimulation is greater than that when the whole EOM nerve is simultaneously stimulated, indicating the presence of polyneuronal innervation.…”

Clinically Differentiated Abnormalities of the Architecture and Expression of Myosin Isoforms of the Human Cremaster Muscle in Cryptorchidism and Retractile Testis

“…This peculiar fiber array is possibly linked to multifocal innervation of the CM, with multiple end plates per single fiber [1]. Multi-innervation, as observed in EOMs [22] and laryngeal muscles [30], is likely to be related with the specific function of CM in the cremasteric reflex, allowing a subtle modulation of contractile parameters.…”

“…The most recent classifications individuate 11 MyHC isoforms in mammalian skeletal muscles, encompassing “classic” as well as “atypical” heavy chains, restricted to highly specialized muscular districts, such as extrinsic ocular muscles (EOMs) and jaw and laryngeal muscles [21]. These striated muscles share with the CM a nonsomitic embryological origin and peculiar morphological/functional features: multiple innervation with multiple plate ends [22, 23] and distinctive expression of MyHCs [24].…”