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. 1992 Apr;449:85–108. doi: 10.1113/jphysiol.1992.sp019076

The effect of the stimulation pattern on the fatigue of single motor units in adult cats.

L Bevan 1, Y Laouris 1, R M Reinking 1, D G Stuart 1
PMCID: PMC1176069  PMID: 1522528

Abstract

1. The main purpose of this study was to examine the effects of two subtly different stimulus patterns on the force developed by fast-twitch, fatiguable motor units in a cat hindlimb muscle during control (pre-fatigue) and fatiguing contractions. 2. The peak force and the force-time integral responses of nineteen high fatigue (FF) and three intermediate fatigue (FI) motor units of the tibialis posterior muscle in five deeply anaesthetized adult cats were measured at selected times during the course of a 360-s fatigue test. 3. The fatigue test involved a pseudo-random alternation of two patterns of stimulation. One pattern (regular) was composed of a train of stimuli with constant interpulse intervals, set at 1.8 x the twitch contraction time of each unit (interval range, 27-51 ms), and delivered for 500 (or 400) ms. For the total (FF + FI) motor-unit sample, the mean (+/- S.D.) stimulation frequency was 26 +/- 4 Hz (range, 19-37 Hz). The other stimulus pattern (optimized) consisted of three initial stimuli with short (10 ms) interpulse intervals, followed by a constant interpulse-interval train that was adjusted (interval range, 29-62 ms; frequency, 23 +/- 5 Hz; frequency range, 16-36 Hz) such that the total train had the same number of pulses, and the same average frequency and duration as the regular train. 4. The stimulus trains were delivered at 1 s-1 for 360 s, using three-train sequences of each pattern, randomly alternating with one another. The response of the third train in each sequence was selected for the force measurements. The force profile obtained from the fatigue test was subsequently decomposed into two profiles: one attributable to regular and one to optimized stimulation. 5. During the initial responses to the fatigue test, the optimized stimulus pattern produced significantly more force than the regular stimulus pattern. For FF units, the mean increase in peak force (141%) was significantly greater than the increase in the force-time integral (59%). 6. All motor units exhibited an initial potentiation of peak force with the regular stimulation pattern, whereas peak force declined monotonically with the optimized pattern. In contrast, the force-time integral potentiated in the first 30 s for both regular and optimized stimulus patterns. 7. Each motor unit maintained an increased force response to optimized stimulation during the fatigue test, with the greatest relative increase occurring about 120 s into the test, well after the potentiation effect had subsided.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Adrian E. D., Bronk D. W. The discharge of impulses in motor nerve fibres: Part II. The frequency of discharge in reflex and voluntary contractions. J Physiol. 1929 Mar 20;67(2):i3–151. [PMC free article] [PubMed] [Google Scholar]
  2. Andreassen S., Rosenfalck A. Regulation of the firing pattern of single motor units. J Neurol Neurosurg Psychiatry. 1980 Oct;43(10):897–906. doi: 10.1136/jnnp.43.10.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BROWN M. C., MATTHEWS P. B. 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 Jun;151:436–457. doi: 10.1113/jphysiol.1960.sp006450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bawa P., Calancie B. Repetitive doublets in human flexor carpi radialis muscle. J Physiol. 1983 Jun;339:123–132. doi: 10.1113/jphysiol.1983.sp014707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bigland-Ritchie B., Johansson R., Lippold O. C., Woods J. J. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol. 1983 Jul;50(1):313–324. doi: 10.1152/jn.1983.50.1.313. [DOI] [PubMed] [Google Scholar]
  6. Binder-Macleod S. A., Barker C. B., 3rd Use of a catchlike property of human skeletal muscle to reduce fatigue. Muscle Nerve. 1991 Sep;14(9):850–857. doi: 10.1002/mus.880140909. [DOI] [PubMed] [Google Scholar]
  7. Botterman B. R., Cope T. C. Motor-unit stimulation patterns during fatiguing contractions of constant tension. J Neurophysiol. 1988 Oct;60(4):1198–1214. doi: 10.1152/jn.1988.60.4.1198. [DOI] [PubMed] [Google Scholar]
  8. Botterman B. R., Iwamoto G. A., Gonyea W. J. Gradation of isometric tension by different activation rates in motor units of cat flexor carpi radialis muscle. J Neurophysiol. 1986 Aug;56(2):494–506. doi: 10.1152/jn.1986.56.2.494. [DOI] [PubMed] [Google Scholar]
  9. Burke R. E. Group Ia synaptic input to fast and slow twitch motor units of cat triceps surae. J Physiol. 1968 Jun;196(3):605–630. doi: 10.1113/jphysiol.1968.sp008526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burke R. E., Levine D. N., Tsairis P., Zajac F. E., 3rd Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol. 1973 Nov;234(3):723–748. doi: 10.1113/jphysiol.1973.sp010369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Burke R. E., Rudomin P., Zajac F. E., 3rd Catch property in single mammalian motor units. Science. 1970 Apr 3;168(3927):122–124. doi: 10.1126/science.168.3927.122. [DOI] [PubMed] [Google Scholar]
  12. Burke R. E., Rudomin P., Zajac F. E., 3rd The effect of activation history on tension production by individual muscle units. Brain Res. 1976 Jun 18;109(3):515–529. doi: 10.1016/0006-8993(76)90031-7. [DOI] [PubMed] [Google Scholar]
  13. Clamann H. P., Robinson A. J. A comparison of electromyographic and mechanical fatigue properties in motor units of the cat hindlimb. Brain Res. 1985 Feb 18;327(1-2):203–219. doi: 10.1016/0006-8993(85)91514-8. [DOI] [PubMed] [Google Scholar]
  14. Close R. I. Dynamic properties of mammalian skeletal muscles. Physiol Rev. 1972 Jan;52(1):129–197. doi: 10.1152/physrev.1972.52.1.129. [DOI] [PubMed] [Google Scholar]
  15. Cooper R. G., Edwards R. H., Gibson H., Stokes M. J. Human muscle fatigue: frequency dependence of excitation and force generation. J Physiol. 1988 Mar;397:585–599. doi: 10.1113/jphysiol.1988.sp017020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Desmedt J. E., Godaux E. Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J Physiol. 1977 Jan;264(3):673–693. doi: 10.1113/jphysiol.1977.sp011689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dubose L., Schelhorn T. B., Clamann H. P. Changes in contractile speed of cat motor units during activity. Muscle Nerve. 1987 Oct;10(8):744–752. doi: 10.1002/mus.880100811. [DOI] [PubMed] [Google Scholar]
  18. Edwards R. H., Hill D. K., Jones D. A. Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle. J Physiol. 1975 Oct;251(2):287–301. doi: 10.1113/jphysiol.1975.sp011093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Edwards R. H. Human muscle function and fatigue. Ciba Found Symp. 1981;82:1–18. doi: 10.1002/9780470715420.ch1. [DOI] [PubMed] [Google Scholar]
  20. Enoka R. M., Robinson G. A., Kossev A. R. Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol. 1989 Dec;62(6):1344–1359. doi: 10.1152/jn.1989.62.6.1344. [DOI] [PubMed] [Google Scholar]
  21. Gordon D. A., Enoka R. M., Karst G. M., Stuart D. G. Force development and relaxation in single motor units of adult cats during a standard fatigue test. J Physiol. 1990 Feb;421:583–594. doi: 10.1113/jphysiol.1990.sp017963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gordon D. A., Enoka R. M., Stuart D. G. Motor-unit force potentiation in adult cats during a standard fatigue test. J Physiol. 1990 Feb;421:569–582. doi: 10.1113/jphysiol.1990.sp017962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hamm T. M., Reinking R. M., Stuart D. G. Electromyographic responses of mammalian motor units to a fatigue test. Electromyogr Clin Neurophysiol. 1989 Nov-Dec;29(7-8):485–494. [PubMed] [Google Scholar]
  24. Hennig R., Lømo T. Firing patterns of motor units in normal rats. Nature. 1985 Mar 14;314(6007):164–166. doi: 10.1038/314164a0. [DOI] [PubMed] [Google Scholar]
  25. Hoffer J. A., Sugano N., Loeb G. E., Marks W. B., O'Donovan M. J., Pratt C. A. Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. J Neurophysiol. 1987 Feb;57(2):530–553. doi: 10.1152/jn.1987.57.2.530. [DOI] [PubMed] [Google Scholar]
  26. Hoyle G. Forms of modulatable tension in skeletal muscles. Comp Biochem Physiol A Comp Physiol. 1983;76(2):203–210. doi: 10.1016/0300-9629(83)90316-x. [DOI] [PubMed] [Google Scholar]
  27. Hultman E., Sjöholm H. Electromyogram, force and relaxation time during and after continuous electrical stimulation of human skeletal muscle in situ. J Physiol. 1983 Jun;339:33–40. doi: 10.1113/jphysiol.1983.sp014700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jami L., Murthy K. S., Petit J., Zytnicki D. After-effects of repetitive stimulation at low frequency on fast-contracting motor units of cat muscle. J Physiol. 1983 Jul;340:129–143. doi: 10.1113/jphysiol.1983.sp014754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kernell D., Ducati A., Sjöholm H. Properties of motor units in the first deep lumbrical muscle of the cat's foot. Brain Res. 1975 Nov 7;98(1):37–55. doi: 10.1016/0006-8993(75)90508-9. [DOI] [PubMed] [Google Scholar]
  30. Kernell D. Functional properties of spinal motoneurons and gradation of muscle force. Adv Neurol. 1983;39:213–226. [PubMed] [Google Scholar]
  31. Kudina L. P., Churikova L. I. Testing excitability of human motoneurones capable of firing double discharges. Electroencephalogr Clin Neurophysiol. 1990 Apr;75(4):334–341. doi: 10.1016/0013-4694(90)90111-v. [DOI] [PubMed] [Google Scholar]
  32. Lichtman J. W., Wilkinson R. S. Properties of motor units in the transversus abdominis muscle of the garter snake. J Physiol. 1987 Dec;393:355–374. doi: 10.1113/jphysiol.1987.sp016827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Maton B., Gamet D. The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. II. Motor unit firing rate and recruitment. Eur J Appl Physiol Occup Physiol. 1989;58(4):369–374. doi: 10.1007/BF00643511. [DOI] [PubMed] [Google Scholar]
  34. McDonagh J. C., Binder M. D., Reinking R. M., Stuart D. G. A commentary on muscle unit properties in cat hindlimb muscles. J Morphol. 1980 Nov;166(2):217–230. doi: 10.1002/jmor.1051660208. [DOI] [PubMed] [Google Scholar]
  35. McDonagh J. C., Binder M. D., Reinking R. M., Stuart D. G. Tetrapartite classification of motor units of cat tibialis posterior. J Neurophysiol. 1980 Oct;44(4):696–712. doi: 10.1152/jn.1980.44.4.696. [DOI] [PubMed] [Google Scholar]
  36. Nemeth P. M., Norris B. J., Lowry O. H., Gordon D. A., Enoka R. M., Stuart D. G. Activation of muscle fibers in individual motor units revealed by 2-deoxyglucose-6-phosphate. J Neurosci. 1988 Nov;8(11):3959–3966. doi: 10.1523/JNEUROSCI.08-11-03959.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Nordstrom M. A., Miles T. S. Discharge variability and physiological properties of human masseter motor units. Brain Res. 1991 Feb 8;541(1):50–56. doi: 10.1016/0006-8993(91)91072-9. [DOI] [PubMed] [Google Scholar]
  38. ROMANES G. J. The motor cell columns of the lumbo-sacral spinal cord of the cat. J Comp Neurol. 1951 Apr;94(2):313–363. doi: 10.1002/cne.900940209. [DOI] [PubMed] [Google Scholar]
  39. Rankin L. L., Enoka R. M., Volz K. A., Stuart D. G. Coexistence of twitch potentiation and tetanic force decline in rat hindlimb muscle. J Appl Physiol (1985) 1988 Dec;65(6):2687–2695. doi: 10.1152/jappl.1988.65.6.2687. [DOI] [PubMed] [Google Scholar]
  40. Robinson G. A., Enoka R. M., Stuart D. G. Immobilization-induced changes in motor unit force and fatigability in the cat. Muscle Nerve. 1991 Jun;14(6):563–573. doi: 10.1002/mus.880140611. [DOI] [PubMed] [Google Scholar]
  41. Stein R. B., Parmiggiani F. Optimal motor patterns for activating mammalian muscle. Brain Res. 1979 Oct 19;175(2):372–376. doi: 10.1016/0006-8993(79)91019-9. [DOI] [PubMed] [Google Scholar]
  42. Zajac F. E., Young J. L. Discharge properties of hindlimb motoneurons in decerebrate cats during locomotion induced by mesencephalic stimulation. J Neurophysiol. 1980 May;43(5):1221–1235. doi: 10.1152/jn.1980.43.5.1221. [DOI] [PubMed] [Google Scholar]
  43. Zajac F. E., Young J. L. Properties of stimulus trains producing maximum tension-time area per pulse from single motor units in medial gastrocnemiu muscle of the cat. J Neurophysiol. 1980 May;43(5):1206–1220. doi: 10.1152/jn.1980.43.5.1206. [DOI] [PubMed] [Google Scholar]

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