Summary
Muscle spindles form de novo in reinnervated muscles of neonatal rats treated with nerve growth factor. Whether the spindles can also form in muscle reinnervated only by afferents was investigated by removing the lumbosacral segment of the spinal cord immediately after crushing the nerve to the medial gastrocnemius muscle at birth, and administering nerve growth factor for 10 days afterwards. As predicted, the medial gastrocnemius muscles were reinnervated by afferents, but not efferents. No motor endplates were visible on any muscle fibers, and extrafusal fibers were atrophied. The reinnervated muscles contained spindle-like encapsulations of one to four fibers at 5, 7, 9 and 30 days after the nerve crush. The number of spindles as well as encapsulated fibers exceeded that of normal medial gastrocnemius muscles. The encapsulated fibers resembled typical intrafusal fibers. They had normal sensory-muscle contacts, but no motor endings. The fibers displayed equatorial clusters of myonuclei and expressed the spindle-specific slow-tonic myosin heavy chain isoform at postnatal day 30. Thus, efferents are not essential for the formation and differentiation of muscle spindles in reinnervated muscles of neonatal rats.
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References
Barker D, Scott JJA, Stacey MJ (1985) Sensory reinnervation of cat peroneus brevis muscle spindles after nerve crush. Brain Res 333:131–138
Boyd IA (1962) The structure and innervation of the nuclear bag muscle fibre system and the nuclear chain muscle fibre system in mammalian muscle spindles. Philos Trans R Soc Lond [Biol] 245:81–136
Bueker ED, Meyers CE (1951) The maturity of peripheral nerves at the time of injury as a factor of nerve regeneration. Anat Rec 109:723–742
Donahue SP, English AW, Roden RL, Schwartz GA (1991) Tenotomy delays both synapse elimination and myogenesis in rat lateral gastrocnemius. Neuroscience 42:275–282
Harris AJ, Fitzsimons RB, McEwan JC (1989) Neural control of the sequence of expression of myosin heavy chain isoforms in foetal mammalian muscles. Development 107:751–769
Kucera J (1980) Myofibrillar ATPase activity of intrafusal fibers in chronically deafferented rat muscle spindles. Histochemistry 67:221–228
Kucera J, Walro JM (1988) The effect of neonatal deafferentiation and deefferentation on myosin heavy chain expression in intrafusal muscle fibers of the rat. Histochemistry 90:151–160
Kucera J, Walro JM (1989) Postnatal expression of myosin heavy chains in muscle spindles of the rat. Anat Embryol 179:369–376
Kucera J, Walro JM (1990a) Treatment with β-bungarotoxin blocks muscle spindle formation in fetal rats. Development 110:483–489
Kucera J, Walro JM (1990b) Origin of intrafusal muscle fibers in the rat. Histochemistry 93:567–580
Kucera J, Walro JM (1991) Aggregation of myonuclei and the spread of slow-tonic myosin immunoreactivity in developing muscle spindles. Histochemistry 96:381–390
Kucera J, Walro JM, Reichler J (1988) Innervation of developing intrafusal muscle fibers in the rat. Am J Anat 183:344–358
Kucera J, Walro JM, Reichler J (1989) The role of nerve and muscle factors in the development of rat muscle spindles. Am J Anat 186:144–160
Kucera J, Walro JM, Reichler J (1991) Neural organization of spindles in three hindlimb muscles of the rat. Am J Anat 190:74–88
Kucera J, Walro JM, Gao Y (1992a) Fusimotor-free spindles in reinnervated muscles of neonatal rats. Neuroscience (in press)
Kucera J, Walro JM, Gao Y (1992b) Influence of muscle substrates on differentiation of intrafusal fiber types in neonatal rats. Neuroscience (in press)
Kucera J, Walro JM, Gorza L (1992c) Expression of type-specific MHC isoforms in rat intrafusal muscle fibers. J Histochem Cytochem 40:293–307
Landon DM (1972) The fine structures of equatorial regions of developing muscle spindles in the rat. J Neurocytol 1:189–210
Milburn A (1973) The early development of muscle spindles in the rat. J Cell Sci 12:175–192
Pierobon-Bormioli S, Sartore S, Vitadello M, Schiaffino S (1980) Slow myosins in vertebrate skeletal muscle. An immnunofluores-cence study. J Cell Biol 85:672–681
Ross JJ, Duxson MJ, Harris AJ (1987) Neural determination of muscle fibre numbers in embryonic rat lumbrical muscles. Development 100:395–409
Schiaffino S, Pierobon-Bormioli S (1976) Morphogenesis of rat muscle spindles after nerve lesion during early postnatal development. J Neurocytol 5:319–336
Sekiya S, Homma S, Miyata Y, Kuno M (1986) Effects of nerve growth factor on differentiation of muscle spindles following nerve lesion in neonatal rats. J Neurosci 6:2019–2025
Shahani U, Vrbová G (1990) Peripheral nerve regeneration in the neonatal rat. J Physiol 417:149P
Smith RS (1966) Properties of intrafusal muscle fibers. In: Granit R (ed) Muscle afferents and motor control. Almquist and Wiksell, Stockholm, pp 69–80
Thornell LE, Pedrosa F (1990) Development of muscle spindle involves special myogenic cell lineages and neurogenic influence. J Neurol Sci 98:46
Zelená J (1957) The morphogenetic influence of innervation on the ontogenic development of muscle spindles. J Embryol Exp Morphol 5:283–292
Zelená J, Hnik P (1960) Absence of spindles in muscles of rats reinnervated during development. Physiol Bohernoslov 9:373–381
Zelená J, Soukup T (1973) Development of muscle spindles deprived of fusimotor innervation. Z Zellforsch Mikrosk Anat 144:435–452
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Kucera, J., Walro, J.M. Superfluousness of motor innervation for the formation of muscle spindles in neonatal rats. Anat Embryol 186, 301–309 (1992). https://doi.org/10.1007/BF00185978
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DOI: https://doi.org/10.1007/BF00185978