Increase in Polyneuronal Innervation in Frog Muscle After Muscle Injury

Overview

Journal J Physiol

Specialty Physiology

Date 1986 Feb 1

PMID 3486269

Authors

M Pecot-Dechavassine

Affiliations

Soon will be listed here.

Abstract

The proportion of polyneuronal innervation was evaluated electrophysiologically in curare-blocked frog cutaneous pectoris muscles after local injury to the muscle fibres on one side. Focal polyneuronal innervation was revealed by recording end-plate potentials evoked by a gradual increase in the stimulus intensity applied to the motor nerve. An increase in the proportion of focally polyneuronally innervated muscle fibres appeared in the injured muscle 3-5 days after injury. The difference between the values obtained 3-5 days and 7-9 days (31 and 38%, respectively) and the control value (18%) was highly significant. A similar increase in the proportion of pluri-innervated muscle fibres was observed in the contralateral muscle, but after a longer period. The different components of complex end-plate potentials (e.p.p.s) usually had similar latencies and rise times in control and experimental muscles. This may indicate that the axons had similar conduction velocities and that synapses were located close to each other. A repeated muscle fibre section 24 h after the initial injury resulted in an enhanced polyneuronal innervation (52%) 7-9 days after the first section. The experiments were repeated on partially blocked muscles in order to detect small e.p.p.s with an amplitude similar to that of spontaneous miniature end-plate potentials (m.e.p.p.s). The proportion of polyneuronally innervated fibres estimated by this technique in control muscles approximated 40%. Polyneuronal innervation was also found to be significantly increased in cut muscles 7-9 days after muscle injury and a week later in contralateral muscles. Combined silver and cholinesterase staining was used to detect morphologically polyneuronal innervation. The comparison of morphological and electrophysiological data indicated that the increase in polyneuronal innervation after muscle injury is likely due to nerve sprouting and formation of new synapses. The results suggest that the signal for nerve sprouting originates from the damaged muscle cell and that it is transferred transneuronally to the contralateral side.

References

EDDS Jr M . Collateral nerve regeneration. Q Rev Biol. 1953; 28(3):260-76. DOI: 10.1086/399699. View

Trussell L, Grinnell A . The regulation of synaptic strength within motor units of the frog cutaneous pectoris muscle. J Neurosci. 1985; 5(1):243-54. PMC: 6565081. View

Decino P . Transmitter release properties along regenerated nerve processes at the frog neuromuscular junction. J Neurosci. 1981; 1(3):308-17. PMC: 6564120. View

Wernig A, Pecot-Dechavassine M, Stover H . Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare. J Neurocytol. 1980; 9(3):278-303. DOI: 10.1007/BF01181538. View

Dennis M, Miledi R . Characteristics of transmitter release at regenerating frog neuromuscular junctions. J Physiol. 1974; 239(3):571-94. PMC: 1330959. DOI: 10.1113/jphysiol.1974.sp010583. View

Pecot-Dechavassine M, Wernig A, Stover H . A combined silver and cholinesterase method for studying exact relations between the pre- and the postsynaptic elements at the frog neuromuscular junction. Stain Technol. 1979; 54(1):25-8. DOI: 10.3109/10520297909110671. View

Herrera A . Polyneuronal innervation and quantal transmitter release in formamide-treated frog sartorius muscles. J Physiol. 1984; 355:267-80. PMC: 1193490. DOI: 10.1113/jphysiol.1984.sp015418. View

Weakly J, Yao Y . Synaptic efficacy at singly- and dually-innervated neuromuscular junctions in the frog, Rana pipiens. Brain Res. 1983; 273(2):319-23. DOI: 10.1016/0006-8993(83)90856-9. View

Herrera A, Grinnell A . Contralateral denervation causes enhanced transmitter release from frog motor nerve terminals. Nature. 1981; 291(5815):495-7. DOI: 10.1038/291495a0. View

10.

Katz B, Miledi R . THE DEVELOPMENT OF ACETYLCHOLINE SENSITIVITY IN NERVE-FREE SEGMENTS OF SKELETAL MUSCLE. J Physiol. 1964; 170:389-96. PMC: 1368823. DOI: 10.1113/jphysiol.1964.sp007339. View

11.

Rotshenker S . Synapse formation in intact innervated cutaneous-pectoris muscles of the frog following denervation of the opposite muscle. J Physiol. 1979; 292:535-47. PMC: 1280877. DOI: 10.1113/jphysiol.1979.sp012870. View

12.

Rotshenker S, McMahan U . Altered patterns of innervation in frog muscle after denervation. J Neurocytol. 1976; 5(6):719-30. DOI: 10.1007/BF01181583. View

13.

. An anatomical and electrophysiological study of synapse elimination at the developing frog neuromuscular junction. Dev Biol. 1983; 99(2):298-311. DOI: 10.1016/0012-1606(83)90279-8. View

14.

Brown M, Matthews P . An investigation into the possible existence of polyneuronal innervation of individual skeletal muscle fibres in certain hind-limb muscles of the cat. J Physiol. 1960; 151:436-57. PMC: 1363274. DOI: 10.1113/jphysiol.1960.sp006450. View

15.

Anzil A, Bieser A, Wernig A . Light and electron microscopic identification of nerve terminal sprouting and retraction in normal adult frog muscle. J Physiol. 1984; 350:393-9. PMC: 1199275. DOI: 10.1113/jphysiol.1984.sp015207. View

16.

Vyskocil F, Magazanik L . Dual end-plate potentials at the single neuromuscular junction of the adult frog. Pflugers Arch. 1977; 368(3):271-3. DOI: 10.1007/BF00585207. View

17.

Rotshenker S . Transneuronal and peripheral mechanisms for the induction of motor neuron sprouting. J Neurosci. 1982; 2(10):1359-68. PMC: 6564418. View

18.

DAlonzo A, Grinnell A . Profiles of evoked release along the length of frog motor nerve terminals. J Physiol. 1985; 359:235-58. PMC: 1193373. DOI: 10.1113/jphysiol.1985.sp015583. View

19.

Hoffman H . Local re-innervation in partially denervated muscle; a histophysiological study. Aust J Exp Biol Med Sci. 1950; 28(4):383-97. DOI: 10.1038/icb.1950.39. View

20.

Tal M, Rotshenker S . Sprouting and synapse formation produced by Carbocaine. J Neurosci. 1984; 4(2):458-63. PMC: 6564904. View