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. 1997 Jan 1;498(Pt 1):249–275. doi: 10.1113/jphysiol.1997.sp021856

Spindle and motoneuronal contributions to the phase advance of the human stretch reflex and the reduction of tremor.

P B Matthews 1
PMCID: PMC1159249  PMID: 9023783

Abstract

1. The human stretch reflex is known to produce a phase advance in the EMG reflexly evoked by sinusoidal stretching, after allowing for the phase lag introduced by simple conduction. Such phase advance counteracts the tendency to tremor introduced by the combined effect of the conduction delay and the slowness of muscle contraction. The present experiments confirm that the EMG advance cannot be attributed solely to the phase advance introduced by the muscle spindles, and show that a major additional contribution is provided by the dynamic properties of individual motoneurones. 2. The surface EMG was recorded from biceps brachii when two different types of sinusoidally varying mechanical stimuli were applied to its tendon at 2-40 Hz. The first was conventional sinusoidal displacement ('stretch'); the spindle discharge would then have been phase advanced. The second was a series of weak taps at 103 Hz, with their amplitude modulated sinusoidally ('modulated vibration'). The overall spindle discharge should then have been in phase with the modulating signal, since the probability of any individual 1 a fibre responding to a tap would increase with its amplitude. The findings with this new stimulus apply to motoneurone excitation by any rhythmic input, whether generated centrally or peripherally. 3. The sinusoidal variation of the EMG elicited by the modulated vibration still showed a delay-adjusted phase advance, but the value was less than that for simple stretching. At 10 Hz the difference was 70-80 deg. This was taken to be the phase advance introduced by the spindles, very slightly underestimated because of the lags produced by tendon compliance in transmitting sinusoidal stretch to the muscle proper. The adjusted phase advance with modulated vibration was taken to represent that introduced by the reflex centres, undistorted by tendon compliance. At 10 Hz the reflex centres produced about the same amount of phase advance as the muscle spindles. 4. At modulation frequencies above 10 Hz the adjusted central phase advance remained approximately constant. However, when the frequency was reduced to below 6 Hz the central phase advance decreased. The depth of EMG modulation (reflex gain) also fell rapidly, starting from a slightly higher frequency. Thus the central phase advance mechanisms behave like a high-pass filter. 5. A simple model of the motoneurone, incorporating synaptic noise and an after-hyperpolarization, was tested with sinusoidal inputs and gave a phase advance over a wide range of frequencies. The effect was tightly linked to two particular facets of the motor discharge; these were the ratio between the stimulus frequency and the mean firing rate (the 'carrier frequency' of the unit), and the coefficient of variation of the interspike interval distribution. The gain rose to a maximum at the carrier frequency, while the phase advance showed a maximum at 0.8 of the carrier. The more regular the discharge, the greater were these effects. The phase advance might increase to above 90 deg, showing that the motoneurone potentially provides a major contribution to the phase advance of the stretch reflex. Related effects have already been observed in other neuronal models and for the discharge of the muscle spindle, without their significance for the motoneurone being appreciated. In essence, a rhythmically firing neurone is particularly affected by a rhythmic stimulus when the two frequencies approximately coincide. 6. Recording from single human motor units confirmed the role of the 'carrier frequency' in determining the phase advance with sinusoidal inputs. In particular, for both stretching and modulated vibration, the phase advance of the response elicited by a fixed sinusoidal stimulus changed appropriately when the firing rate of the unit varied 'spontaneously' over a long recording period. 7. Thus a combination of modelling and experiment has shown that the motoneurones themselves produce a significant phase advance.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashby P., Zilm D. Relationship between EPSP shape and cross-correlation profile explored by computer simulation for studies on human motoneurons. Exp Brain Res. 1982;47(1):33–40. doi: 10.1007/BF00235883. [DOI] [PubMed] [Google Scholar]
  2. Baker S. N., Lemon R. N. Non-linear summation of responses in averages of rectified EMG. J Neurosci Methods. 1995 Jul;59(2):175–181. doi: 10.1016/0165-0270(94)00180-o. [DOI] [PubMed] [Google Scholar]
  3. Baldissera F., Campadelli P., Piccinelli L. The dynamic response of cat alpha-motoneurones investigated by intracellular injection of sinusoidal currents. Exp Brain Res. 1984;54(2):275–282. doi: 10.1007/BF00236227. [DOI] [PubMed] [Google Scholar]
  4. Burke D., Hagbarth K. E., Löfstedt L., Wallin B. G. The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol. 1976 Oct;261(3):673–693. doi: 10.1113/jphysiol.1976.sp011580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Elble R. J., Higgins C., Hughes L. Phase resetting and frequency entrainment of essential tremor. Exp Neurol. 1992 Jun;116(3):355–361. doi: 10.1016/0014-4886(92)90014-h. [DOI] [PubMed] [Google Scholar]
  6. Evans C. M., Fellows S. J., Rack P. M., Ross H. F., Walters D. K. Response of the normal human ankle joint to imposed sinusoidal movements. J Physiol. 1983 Nov;344:483–502. doi: 10.1113/jphysiol.1983.sp014953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fitzpatrick R. C., Gorman R. B., Burke D., Gandevia S. C. Postural proprioceptive reflexes in standing human subjects: bandwidth of response and transmission characteristics. J Physiol. 1992 Dec;458:69–83. doi: 10.1113/jphysiol.1992.sp019406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goodwin G. M., Hulliger M., Matthews P. B. The effects of fusimotor stimulation during small amplitude stretching on the frequency-response of the primary ending of the mammalian muscle spindle. J Physiol. 1975 Dec;253(1):175–206. doi: 10.1113/jphysiol.1975.sp011186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hulliger M., Matthews P. B., Noth J. Static and dynamic fusimotor action on the response of Ia fibres to low frequency sinusoidal stretching of widely ranging amplitude. J Physiol. 1977 Jun;267(3):811–838. doi: 10.1113/jphysiol.1977.sp011839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hultborn H., Illert M., Nielsen J., Paul A., Ballegaard M., Wiese H. On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res. 1996 Mar;108(3):450–462. doi: 10.1007/BF00227268. [DOI] [PubMed] [Google Scholar]
  11. Jacks A., Prochazka A., Trend P. S. Instability in human forearm movements studied with feed-back-controlled electrical stimulation of muscles. J Physiol. 1988 Aug;402:443–461. doi: 10.1113/jphysiol.1988.sp017214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kirkwood P. A. On the use and interpretation of cross-correlations measurements in the mammalian central nervous system. J Neurosci Methods. 1979 Aug;1(2):107–132. doi: 10.1016/0165-0270(79)90009-8. [DOI] [PubMed] [Google Scholar]
  13. Knight B. W. Dynamics of encoding in a population of neurons. J Gen Physiol. 1972 Jun;59(6):734–766. doi: 10.1085/jgp.59.6.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lakie M., Walsh E. G., Arblaster L. A., Villagra F., Roberts R. C. Limb temperature and human tremors. J Neurol Neurosurg Psychiatry. 1994 Jan;57(1):35–42. doi: 10.1136/jnnp.57.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Matthews P. B. Interaction between short- and long-latency components of the human stretch reflex during sinusoidal stretching. J Physiol. 1993 Mar;462:503–527. doi: 10.1113/jphysiol.1993.sp019566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matthews P. B., Muir R. B. Comparison of electromyogram spectra with force spectra during human elbow tremor. J Physiol. 1980 May;302:427–441. doi: 10.1113/jphysiol.1980.sp013254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matthews P. B., Stein R. B. The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol. 1969 Feb;200(3):723–743. doi: 10.1113/jphysiol.1969.sp008719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Matthews P. B. The simple frequency response of human stretch reflexes in which either short- or long-latency components predominate. J Physiol. 1994 Dec 15;481(Pt 3):777–798. doi: 10.1113/jphysiol.1994.sp020481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Murthy V. N., Fetz E. E. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5670–5674. doi: 10.1073/pnas.89.12.5670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Partridge L. D. Signal-handling characteristics of load-moving skeletal muscle. Am J Physiol. 1966 May;210(5):1178–1191. doi: 10.1152/ajplegacy.1966.210.5.1178. [DOI] [PubMed] [Google Scholar]
  21. Poppele R. E., Bowman R. J. Quantitative description of linear behavior of mammalian muscle spindles. J Neurophysiol. 1970 Jan;33(1):59–72. doi: 10.1152/jn.1970.33.1.59. [DOI] [PubMed] [Google Scholar]
  22. Poppele R. E., Terzuolo C. A. Myotatic reflex: its input-output relation. Science. 1968 Feb 16;159(3816):743–745. doi: 10.1126/science.159.3816.743. [DOI] [PubMed] [Google Scholar]
  23. Prochazka A., Trend P. S. Instability in human forearm movements studied with feed-back-controlled muscle vibration. J Physiol. 1988 Aug;402:421–442. doi: 10.1113/jphysiol.1988.sp017213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rack P. M., Ross H. F., Thilmann A. F., Walters D. K. Reflex responses at the human ankle: the importance of tendon compliance. J Physiol. 1983 Nov;344:503–524. doi: 10.1113/jphysiol.1983.sp014954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rosenthal N. P., McKean T. A., Roberts W. J., Terzuolo C. A. Frequency analysis of stretch reflex and its main subsystems in triceps surae muscles of the cat. J Neurophysiol. 1970 Nov;33(6):713–749. doi: 10.1152/jn.1970.33.6.713. [DOI] [PubMed] [Google Scholar]
  26. Stein R. B., French A. S., Holden A. V. The frequency response, coherence, and information capacity of two neuronal models. Biophys J. 1972 Mar;12(3):295–322. doi: 10.1016/S0006-3495(72)86087-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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