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. 1995 Nov 1;488(Pt 3):833–840. doi: 10.1113/jphysiol.1995.sp021015

Increased resting discharge of human spindle afferents following voluntary contractions.

L R Wilson 1, S C Gandevia 1, D Burke 1
PMCID: PMC1156749  PMID: 8576873

Abstract

1. The aim of this study was to assess the incidence of lasting alterations in discharge rate of muscle spindle afferents innervating human ankle and toe dorsiflexor muscles following isometric contractions. 2. The subjects performed controlled isometric ankle dorsiflexions maintained for approximately 5 s. During the contraction the discharge of all but one spindle afferent increased above the precontraction level. After complete relaxation, there was prolonged enhancement of the discharge rate of nineteen of fifty-five muscle spindle afferents and none of three Golgi tendon organ afferents. Ten of the nineteen spindle afferents had been silent prior to the contraction. For the population of fifty-five spindle afferents, the mean 'postcontraction' discharge rate was 65% higher than the mean precontraction discharge rate, with the mean rate increasing from 2.3 to 3.9 Hz (P < 0.001). The mean duration of the enhanced postcontraction discharge was 52 s (range, 8-240 s). 3. Stretch applied to the tendon of the receptor-bearing muscle in twelve of fourteen spindle afferents with an enhanced postcontraction discharge rate eliminated or reduced the enhanced discharge rate. 4. The high incidence of an enhanced spindle discharge after voluntary contraction (35% of spindle afferents) suggests that muscle 'history' should be taken into account when interpreting changes in spindle discharge rates. The enhanced discharge rates following contraction probably reflect a long-lasting effect of the contraction-associated increase in fusimotor drive on intrafusal stiffness, rather than the persistence of fusimotor drive following relaxation.

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Selected References

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  1. Brown M. C., Goodwin G. M., Matthews P. B. After-effects of fusimotor stimulation on the response of muscle spindle primary afferent endings. J Physiol. 1969 Dec;205(3):677–694. doi: 10.1113/jphysiol.1969.sp008990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burke D., Aniss A. M., Gandevia S. C. In-parallel and in-series behavior of human muscle spindle endings. J Neurophysiol. 1987 Aug;58(2):417–426. doi: 10.1152/jn.1987.58.2.417. [DOI] [PubMed] [Google Scholar]
  3. Crone C., Nielsen J. Methodological implications of the post activation depression of the soleus H-reflex in man. Exp Brain Res. 1989;78(1):28–32. doi: 10.1007/BF00230683. [DOI] [PubMed] [Google Scholar]
  4. Duchateau J., Hainaut K. Behaviour of short and long latency reflexes in fatigued human muscles. J Physiol. 1993 Nov;471:787–799. doi: 10.1113/jphysiol.1993.sp019928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Edin B. B., Vallbo A. B. Stretch sensitization of human muscle spindles. J Physiol. 1988 Jun;400:101–111. doi: 10.1113/jphysiol.1988.sp017113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Enoka R. M., Hutton R. S., Eldred E. Changes in excitability of tendon tap and Hoffmann reflexes following voluntary contractions. Electroencephalogr Clin Neurophysiol. 1980 Jun;48(6):664–672. doi: 10.1016/0013-4694(80)90423-x. [DOI] [PubMed] [Google Scholar]
  7. GRANIT R., HOMMA S., MATTHEWS P. B. Prolonged changes in the discharge of mammalian muscle spindles following tendon taps or muscle twitches. Acta Physiol Scand. 1959 Jun 24;46:185–193. doi: 10.1111/j.1748-1716.1959.tb01747.x. [DOI] [PubMed] [Google Scholar]
  8. Gregory J. E., Mark R. F., Morgan D. L., Patak A., Polus B., Proske U. Effects of muscle history on the stretch reflex in cat and man. J Physiol. 1990 May;424:93–107. doi: 10.1113/jphysiol.1990.sp018057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gregory J. E., Morgan D. L., Proske U. Changes in size of the stretch reflex of cat and man attributed to aftereffects in muscle spindles. J Neurophysiol. 1987 Sep;58(3):628–640. doi: 10.1152/jn.1987.58.3.628. [DOI] [PubMed] [Google Scholar]
  10. Hagbarth K. E., Hägglund J. V., Nordin M., Wallin E. U. Thixotropic behaviour of human finger flexor muscles with accompanying changes in spindle and reflex responses to stretch. J Physiol. 1985 Nov;368:323–342. doi: 10.1113/jphysiol.1985.sp015860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hill D. K. Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol. 1968 Dec;199(3):637–684. doi: 10.1113/jphysiol.1968.sp008672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jahnke M. T., Proske U., Struppler A. Measurements of muscle stiffness, the electromyogram and activity in single muscle spindles of human flexor muscles following conditioning by passive stretch or contraction. Brain Res. 1989 Jul 24;493(1):103–112. doi: 10.1016/0006-8993(89)91004-4. [DOI] [PubMed] [Google Scholar]
  13. KUFFLER S. W., HUNT C. C., QUILLIAM J. P. Function of medullated small-nerve fibers in mammalian ventral roots; efferent muscle spindle innervation. J Neurophysiol. 1951 Jan;14(1):29–54. doi: 10.1152/jn.1951.14.1.29. [DOI] [PubMed] [Google Scholar]
  14. Macefield G., Hagbarth K. E., Gorman R., Gandevia S. C., Burke D. Decline in spindle support to alpha-motoneurones during sustained voluntary contractions. J Physiol. 1991;440:497–512. doi: 10.1113/jphysiol.1991.sp018721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McKeon B., Burke D. Identification of muscle spindle afferents during in vivo recordings in man. Electroencephalogr Clin Neurophysiol. 1980 May;48(5):606–608. doi: 10.1016/0013-4694(80)90297-7. [DOI] [PubMed] [Google Scholar]
  16. Morgan D. L., Prochazka A., Proske U. The after-effects of stretch and fusimotor stimulation on the responses of primary endings of cat muscle spindles. J Physiol. 1984 Nov;356:465–477. doi: 10.1113/jphysiol.1984.sp015477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nielsen J., Nagaoka M., Kagamihara Y., Kakuda N., Tanaka R. Discharge of muscle afferents during voluntary co-contraction of antagonistic ankle muscles in man. Neurosci Lett. 1994 Apr 11;170(2):277–280. doi: 10.1016/0304-3940(94)90337-9. [DOI] [PubMed] [Google Scholar]
  18. Proske U. Stretch-evoked potentiation of responses of muscle spindles in the cat. Brain Res. 1975 May 2;88(2):378–383. doi: 10.1016/0006-8993(75)90403-5. [DOI] [PubMed] [Google Scholar]
  19. Ribot-Ciscar E., Tardy-Gervet M. F., Vedel J. P., Roll J. P. Post-contraction changes in human muscle spindle resting discharge and stretch sensitivity. Exp Brain Res. 1991;86(3):673–678. doi: 10.1007/BF00230541. [DOI] [PubMed] [Google Scholar]
  20. Smith J. L., Hutton R. S., Eldred E. Postcontraction changes in sensitivity of muscle afferents to static and dynamic stretch. Brain Res. 1974 Sep 27;78(2):193–202. doi: 10.1016/0006-8993(74)90546-0. [DOI] [PubMed] [Google Scholar]
  21. Srinivasan M. A., Whitehouse J. M., LaMotte R. H. Tactile detection of slip: surface microgeometry and peripheral neural codes. J Neurophysiol. 1990 Jun;63(6):1323–1332. doi: 10.1152/jn.1990.63.6.1323. [DOI] [PubMed] [Google Scholar]
  22. Vallbo A. B. Discharge patterns in human muscle spindle afferents during isometric voluntary contractions. Acta Physiol Scand. 1970 Dec;80(4):552–566. doi: 10.1111/j.1748-1716.1970.tb04823.x. [DOI] [PubMed] [Google Scholar]

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