Abstract
Whether an intact innervation is essential for postnatal muscle differentiation was examined in the rat by recording physiological contraction parameters. Muscles in one leg were denervated neonatally (within 24 h of birth) and, between 3-28 days after the operation, their contractions were compared with those of the contralateral control muscles. Experiments were performed on the extensor digitorum longus (edl, a fast muscle) and the soleus (a slow muscle) muscles and contractions were recorded in vitro, at 35 degrees C and with direct stimulation. When compared with the control muscles, 3-4-day-old neonatally denervated fast and slow muscles had longer twitch contractions, higher twitch/tetanus ratios and certain other specific differences in their contraction parameters. These denervation-induced changes in neonatal muscles were essentially similar to those produced 3-7 days after denervation in the differentiated (4-week-old) fast muscle. Despite differences in their absolute values, the contraction parameters of neonatally denervated and control edl muscles changed similarly during development, indicating that postnatal differentiation of fast muscle fibres is independent of a neuronal influence. In the case of the neonatally denervated soleus muscle, the developmental changes in contraction parameters, i.e. shortening of the twitch duration, increase of rate of rise and rate of relaxation in the tetanus and increase of the maximum shortening velocity, were more pronounced than in the control slow muscle; also, there were similarities with the pattern of fast muscle differentiation. Thus, muscle fibre differentiation in soleus becomes altered towards that of a fast muscle after neonatal denervation.
MeSH Terms
Age Factors
Animals
Animals, Newborn
Cell Differentiation
Isometric Contraction
Male
Motor Neurons/physiology
Muscle Contraction
Muscle Denervation
Muscles/cytology,innervation,physiology
Rats
Rats, Inbred Strains
Sciatic Nerve
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Elmubarak M H
Department of Physiology, Medical School, University of Bristol, U.K.
Ranatunga K W
References (30)
30 references, click to expand
-
Dynamic properties of mammalian skeletal muscles.
Physiol Rev. 1972 Jan;52(1):129-97
PMID: 4256989
-
Differentiation of fast and slow muscles in the cat hind limb.
J Physiol. 1960 Feb;150:399-416
PMID: 13805873
-
Matching of muscle properties and motoneurone firing patterns during early stages of development.
J Exp Biol. 1985 Mar;115:113-23
PMID: 4031759
-
Development, innervation, and activity-pattern induced changes in skeletal muscle.
Annu Rev Physiol. 1981;43:531-52
PMID: 7011198
-
Factors determining the subunit composition of tropomyosin in mammalian skeletal muscle.
Biochem J. 1985 Mar 1;226(2):461-8
PMID: 3994668
-
Temperature-dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle.
J Physiol. 1982 Aug;329:465-83
PMID: 7143257
-
THE RATE OF TENSION DEVELOPMENT IN ISOMETRIC TETANIC CONTRACTIONS OF MAMMALIAN FAST AND SLOW SKELETAL MUSCLE.
J Physiol. 1965 Feb;176:337-54
PMID: 14288512
-
Myogenic and neurogenic contributions to the development of fast and slow twitch muscles in rat.
Dev Biol. 1978 Feb;62(2):473-85
PMID: 146629
-
Development of a mammalian fast muscle: dynamic and biochemical properties correlated.
J Physiol. 1973 Oct;234(1):29-42
PMID: 4271901
-
The force-velocity relation of rat fast- and slow-twitch muscles examined at different temperatures.
J Physiol. 1984 Jun;351:517-29
PMID: 6747875
-
Myosin isoenzyme transitions in muscle development, maturation, and disease.
Int Rev Cytol. 1985;97:97-131
PMID: 2934345
-
Impaired skeletal muscle maturation following neonatal neurectomy.
Dev Biol. 1968 Jun;17(6):713-23
PMID: 5690648
-
Effect of denervation at birth on the development of skeletal muscle cell types in the rat.
Exp Neurol. 1983 Oct;82(1):131-42
PMID: 6628604
-
Effect of denervation on the differentiation of twitch muscles in the kitten hind limb.
Nat New Biol. 1973 Feb 28;241(113):285-6
PMID: 4511919
-
ATPase activity of myosin correlated with speed of muscle shortening.
J Gen Physiol. 1967 Jul;50(6):Suppl:197-218
PMID: 4227924
-
FURTHER OBSERVATIONS ON THE DIFFERENTIATION OF SKELETAL MUSCLES IN THE KITTEN HIND LIMB.
J Physiol. 1965 Feb;176:355-70
PMID: 14288513
-
Trophic effects on the contractile and histochemical properties of rat soleus muscle.
J Neurosci. 1985 Aug;5(8):2189-96
PMID: 3160837
-
Potentiation of the isometric twitch and mechanism of tension recruitment in mammalian skeletal muscle.
Exp Neurol. 1979 Feb;63(2):266-76
PMID: 437004
-
Temperature-dependent transitions in isometric contractions of rat muscle.
J Physiol. 1983 Jun;339:87-95
PMID: 6887040
-
Myosin isoenzymes as molecular markers for muscle physiology.
J Exp Biol. 1985 Mar;115:43-53
PMID: 3897445
-
Changes produced by chronic denervation in the temperature-dependent isometric contractile characteristics of rat fast and slow twitch skeletal muscles.
J Physiol. 1977 Dec;273(1):255-62
PMID: 599424
-
Spinal transection and the postnatal differentiation of slow myosin isoenzymes.
Muscle Nerve. 1980 Nov-Dec;3(6):483-6
PMID: 7005669
-
Temperature dependence of contraction characteristics in developing rat muscles.
Muscle Nerve. 1987 Nov-Dec;10(9):775-82
PMID: 3683450
-
Different pattern of recovery of fast and slow muscles following nerve injury in the rat.
J Physiol. 1984 Apr;349:397-410
PMID: 6737299
-
The effects of denervation on contractile properties or rat skeletal muscle.
J Physiol. 1981;319:81-92
PMID: 7320930
-
Force-velocity properties of fast-twitch and slow-twitch muscles of the kitten.
J Physiol. 1985 Oct;367:377-85
PMID: 4057104
-
Effects of the spinal cord section and of subsequent denervation on the mechanical properties of fast and slow muscles.
Experientia. 1978 Jan 15;34(1):55-7
PMID: 271614
-
DYNAMIC PROPERTIES OF FAST AND SLOW SKELETAL MUSCLES OF THE RAT DURING DEVELOPMENT.
J Physiol. 1964 Sep;173:74-95
PMID: 14205033
-
The size of motor units during post-natal development of rat lumbrical muscle.
J Physiol. 1979 Dec;297(0):463-78
PMID: 536920
-
Role of activity in the differentiation of slow and fast muscles.
Nature. 1973 Jul 20;244(5412):178-9
PMID: 4583504