Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles

Abstract

1. The inferior rectus muscle of rat, one of the extraocular muscles, contains two populations of multiply innervated fibers (MIFs): orbital MIFs, located in the orbital layer of the muscle and global MIFs, found in the global layer. The electrical properties and the responses to nerve stimulation of orbital MIFs were studied with single intracellular electrodes and compared with those of twitch fibers of the orbital layer, MIFs of the global layer, and tonic fibers of the frog. 2. About 90% of the orbital MIFs did not produce overshooting action potentials. In these fibers the characteristics and time course of the responses to nerve stimulation varied along the length of the fibers. Within 2 mm of the end-plate band of the muscle, the responses consisted of several small end-plate potentials (EPPs) and a nonovershooting spike. Distal to 2 mm, the responses in most fibers consisted of large and small EPPs with no spiking response. Some fibers produced very small spikes surmounted on large EPPs. 3. Overshooting action potentials were observed in approximately 10% of the orbital MIFs recorded between the end-plate band and 2 mm distal. The presence or absence of action potentials was not related to the magnitude of the resting potential of the fibers. 4. The threshold of nerve stimulated responses in orbital MIFs was the same as that in orbital twitch fibers. A large number of orbital MIFs had latencies equal to those for the orbital twitch fibers recorded at the same distance from the end-plate band, but the average latency was greater in the MIFs. The latency of orbital MIFs was about one-half of that for the MIFs of the global layer. The values for the effective resistance and membrane time constant of orbital MIFs fell between those for orbital twitch fibers on the one hand, and global MIFs and frog tonic fibers on the other. 5. In order to compare electrical properties with innervation patterns, fibers identified electrophysiologically as orbital MIFs were injected with the fluorescent dye Lucifer yellow and then traced in Epon-embedded, serial transverse sections. In addition to numerous superficial endings distributed along the fibers, a single "en plaque" ending was also found in the end-plate band that resembled the end plates of the adjacent orbital twitch fibers. 6. From these results we conclude that the electrical activity of orbital MIFs varies along the length of the fibers.(ABSTRACT TRUNCATED AT 400 WORDS)

Measurement of contractile force of skeletal and extraocular muscles: Effects of blood supply, muscle size and in situ or in vitro preparation

“…Yet, these methods are advantageous because the muscle's origin is preserved, its orientation is largely conserved, and an intact blood supply maintains the viability of the muscle (Bach-yRita and Ito, 1966;Barmack et al, 1971;Hanson and Lennerstrand, 1977;Shall and Goldberg, 1992;Dimitrova et al, 2002;Shall et al, 2003). The relative ease of in vitro preparations for the determination of extraocular muscle force is reflected by their extensive use (Close and Luff, 1974;Luff, 1981;Chiarandini, 1980Chiarandini, , 1987Asmussen and Gaunitz, 1981;Jacoby et al, 1989;Chen and von Bartheld, 2004;McLoon et al, 2006;Anderson et al, 2006). While in vitro methods have the advantage of being technically less demanding and do not require general anesthesia, they may not be optimal for obtaining accurate contractile measurements of extraocular muscle.…”

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

“…Indeed the tension excess during tetanic contractions of IO muscle was still present and even larger (Յ28% at the higher frequencies of stimulation) in comparison with the tension excess during twitch muscle contractions. The larger extent of tension excess during tetanic over twitch stimulation could also reflect the presence of nontwitch multiply innervated muscle fibers (Bondi and Chiarandini 1983;Jacoby et al 1989) and/or nontwitch motor units (Nelson et al 1986). Obviously, nontwitch units would not be activated using single twitch stimulation paradigms.…”

“…The multiply innervated fibers in the orbital layer of EOM exhibited different electrical properties in the end-plate zone of the muscle as opposed to areas distal to that zone (Jacoby et al 1989). In addition, two types of nerve endings were identified, morphologically and histochemically, along the length of these fibers in rat and monkey (Jacoby et al 1989;Pachter 1982Pachter 1984.…”

“…In addition, two types of nerve endings were identified, morphologically and histochemically, along the length of these fibers in rat and monkey (Jacoby et al 1989;Pachter 1982Pachter 1984. Therefore it would seem likely that the multiply innervated fibers receive polyneuronal (or at least dual) innervation.…”

Motoneurons of the Lateral and Medial Rectus Extraocular Muscles in Squirrel Monkey and Cat

“…It is well known that a large proportion of extraocular muscle fibers have multiple end plates [Mühlendyck, 1978], but it has generally been assumed that the end plates on a particular fiber were all from the same neuron [Lennerstrand, 1974]. However, Mühlendyck [1978] reasoned, based on his review of extraocular system anatomical data, that eye muscle fibers with multiple end plates could be innervated by multiple neurons and recent studies appear to confirm this view [Jacoby et al, 1989a;Porter and Baker, 1996]. There also appear to be different myosin isoforms along the length of a single muscle fiber [Jacoby et al, 1989b].…”