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. 1984 Apr;349:249–272. doi: 10.1113/jphysiol.1984.sp015155

Corticomotoneuronal cells contribute to long-latency stretch reflexes in the rhesus monkey.

P D Cheney, E E Fetz
PMCID: PMC1199336  PMID: 6737294

Abstract

To test the hypothesis that a transcortical reflex contributes to the stretch-evoked long-latency electromyographic (e.m.g.) response we documented the responses of identified corticomotoneuronal (c.m.) cells and their target muscles to perturbations of active wrist movements. Macaque monkeys performed ramp-and-hold wrist movements against elastic loads, alternating between flexion and extension zones; brief (25 ms) torque pulses were intermittently applied during the hold period. C.m. cells were identified by a clear post-spike facilitation in spike-triggered averages of forelimb muscle e.m.g. activity. Activity of c.m. cells and twelve wrist and digit flexor and extensor muscles was recorded during: (a) active ramp-and-hold wrist movements, (b) passive ramp-and-hold wrist movements, and (c) torque perturbations applied during the hold phase of active flexion and extension which either lengthened or shortened the c.m. cell's target muscles. Muscle-lengthening perturbations evoked a reproducible pattern of average e.m.g. activity in the stretched muscles, consisting of two peaks: the first response (M1) had an onset latency of 11.2 +/- 2.1 ms (mean +/- S.D.), and the second (M2) began at 27.9 +/- 5.1 ms. Torque perturbations which shortened the active muscles also evoked a characteristic e.m.g. response consisting of an initial cessation of activity at 13.5 +/- 3.4 ms followed by a peak beginning at 33.9 +/- 3.0 ms. The responses of twenty-one c.m. cells which facilitated wrist muscles were documented with torque pulse perturbations applied during active muscle contraction. Twenty of twenty-one c.m. cells responded at short latency (23.4 +/- 8.8 ms) to torque perturbations which stretched their target muscles. For each c.m. cell-target muscle pair, transcortical loop time was calculated as the sum of the onset latency of the c.m. cell's response to lengthening perturbations (afferent time) and the onset latency of post-spike facilitation (efferent time). The mean transcortical loop time was 30.4 +/- 10.2 ms, comparable to the mean onset latency of the M2 peak (27.9 +/- 5.1). The duration of a c.m. cell's response to torque perturbations provides a further measure of the extent of its potential contribution to the M2 muscle response. In all cases but two, the c.m. cell response, delayed by the latency of the post-spike facilitation, overlapped the M2 e.m.g. peak.

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Selected References

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  1. Albe-Fessard D., Liebeskind J. Origine des messages somato-sensitifs activant les cellules du cortex moteur chez le singe. Exp Brain Res. 1966;1(2):127–146. doi: 10.1007/BF00236866. [DOI] [PubMed] [Google Scholar]
  2. Bawa P., Tatton W. G. Motor unit responses in muscles stretched by imposed displacements of the monkey wrist. Exp Brain Res. 1979;37(3):417–437. doi: 10.1007/BF00236815. [DOI] [PubMed] [Google Scholar]
  3. Cheney P. D., Fetz E. E. Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol. 1980 Oct;44(4):773–791. doi: 10.1152/jn.1980.44.4.773. [DOI] [PubMed] [Google Scholar]
  4. Chofflon M., Lachat J. M., Rüegg D. G. A transcortical loop demonstrated by stimulation of low-threshold muscle afferents in the awake monkey. J Physiol. 1982 Feb;323:393–402. doi: 10.1113/jphysiol.1982.sp014079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Conrad B., Meyer-Lohmann J., Matsunami K., Brooks V. B. Precentral unit activity following torque pulse injections into elbow movements. Brain Res. 1975 Aug 29;94(2):219–236. doi: 10.1016/0006-8993(75)90058-x. [DOI] [PubMed] [Google Scholar]
  6. Cooke J. D., Eastman M. J. Long-loop reflexes in the tranquilized monkey. Exp Brain Res. 1977 Apr 21;27(5):491–500. doi: 10.1007/BF00239038. [DOI] [PubMed] [Google Scholar]
  7. Crago P. E., Houk J. C., Hasan Z. Regulatory actions of human stretch reflex. J Neurophysiol. 1976 Sep;39(5):925–935. doi: 10.1152/jn.1976.39.5.925. [DOI] [PubMed] [Google Scholar]
  8. Eklund G., Hagbarth K. E., Hägglund J. V., Wallin E. U. Mechanical oscillations contributing to the segmentation of the reflex electromyogram response to stretching human muscles. J Physiol. 1982 May;326:65–77. doi: 10.1113/jphysiol.1982.sp014177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eklund G., Hagbarth K. E., Hägglund J. V., Wallin E. U. The 'late' reflex responses to muscle stretch: the 'resonance hypothesis' versus the 'long-loop hypothesis'. J Physiol. 1982 May;326:79–90. doi: 10.1113/jphysiol.1982.sp014178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evarts E. V. Motor cortex reflexes associated with learned movement. Science. 1973 Feb 2;179(4072):501–503. doi: 10.1126/science.179.4072.501. [DOI] [PubMed] [Google Scholar]
  11. Evarts E. V., Tanji J. Gating of motor cortex reflexes by prior instruction. Brain Res. 1974 May 17;71(2-3):479–494. doi: 10.1016/0006-8993(74)90992-5. [DOI] [PubMed] [Google Scholar]
  12. Evarts E. V., Tanji J. Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. J Neurophysiol. 1976 Sep;39(5):1069–1080. doi: 10.1152/jn.1976.39.5.1069. [DOI] [PubMed] [Google Scholar]
  13. Fetz E. E., Cheney P. D. Muscle fields of primate corticomotoneuronal cells. J Physiol (Paris) 1978;74(3):239–245. [PubMed] [Google Scholar]
  14. Fetz E. E., Cheney P. D. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol. 1980 Oct;44(4):751–772. doi: 10.1152/jn.1980.44.4.751. [DOI] [PubMed] [Google Scholar]
  15. Fetz E. E., Finocchio D. V., Baker M. A., Soso M. J. Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. J Neurophysiol. 1980 Apr;43(4):1070–1089. doi: 10.1152/jn.1980.43.4.1070. [DOI] [PubMed] [Google Scholar]
  16. Ghez C., Shinoda Y. Spinal mechanisms of the functional stretch reflex. Exp Brain Res. 1978 May 12;32(1):55–68. doi: 10.1007/BF00237390. [DOI] [PubMed] [Google Scholar]
  17. Hagbarth K. E., Hägglund J. V., Wallin E. U., Young R. R. Grouped spindle and electromyographic responses to abrupt wrist extension movements in man. J Physiol. 1981 Mar;312:81–96. doi: 10.1113/jphysiol.1981.sp013617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hagbarth K. E., Young R. R., Hägglund J. V., Wallin E. U. Segmentation of human spindle and EMG responses to sudden muscle stretch. Neurosci Lett. 1980 Sep;19(2):213–217. doi: 10.1016/0304-3940(80)90197-4. [DOI] [PubMed] [Google Scholar]
  19. Hore J., Preston J. B., Cheney P. D. Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon. J Neurophysiol. 1976 May;39(3):484–500. doi: 10.1152/jn.1976.39.3.484. [DOI] [PubMed] [Google Scholar]
  20. Jones G. M., Watt D. G. Observations on the control of stepping and hopping movements in man. J Physiol. 1971 Dec;219(3):709–727. doi: 10.1113/jphysiol.1971.sp009684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kwan H. C., Murphy J. T., Repeck M. W. Control of stiffness by the medium latency electromyographic response to limb perturbation. Can J Physiol Pharmacol. 1979 Mar;57(3):277–285. doi: 10.1139/y79-041. [DOI] [PubMed] [Google Scholar]
  22. Lee R. G., Tatton W. G. Long latency reflexes to imposed displacements of the human wrist: dependence on duration of movement. Exp Brain Res. 1982;45(1-2):207–216. doi: 10.1007/BF00235780. [DOI] [PubMed] [Google Scholar]
  23. Lee R. G., Tatton W. G. Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Can J Neurol Sci. 1975 Aug;2(3):285–293. doi: 10.1017/s0317167100020382. [DOI] [PubMed] [Google Scholar]
  24. Lemon R. N., Hanby J. A., Porter R. Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys. Proc R Soc Lond B Biol Sci. 1976 Oct 29;194(1116):341–373. doi: 10.1098/rspb.1976.0083. [DOI] [PubMed] [Google Scholar]
  25. Lenz F. A., Tatton W. G., Tasker R. R. The effect of cortical lesions on the electromyographic response to joint displacement in the squirrel monkey forelimb. J Neurosci. 1983 Apr;3(4):795–805. doi: 10.1523/JNEUROSCI.03-04-00795.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marsden C. D., Merton P. A., Morton H. B. Latency measurements compatible with a cortical pathway for the stretch reflex in man. J Physiol. 1973 Apr;230(1):58P–59P. [PubMed] [Google Scholar]
  27. Marsden C. D., Merton P. A., Morton H. B. Stretch reflex and servo action in a variety of human muscles. J Physiol. 1976 Jul;259(2):531–560. doi: 10.1113/jphysiol.1976.sp011481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Miller A. D., Brooks V. B. Late muscular responses to arm perturbations persist during supraspinal dysfunctions in monkeys. Exp Brain Res. 1981;41(2):146–158. doi: 10.1007/BF00236604. [DOI] [PubMed] [Google Scholar]
  29. Murphy J. T., Wong Y. C., Kwan H. C. Afferent-efferent linkages in motor cortex for single forelimb muscles. J Neurophysiol. 1975 Jul;38(4):990–1014. doi: 10.1152/jn.1975.38.4.990. [DOI] [PubMed] [Google Scholar]
  30. Phillips C. G., Powell T. P., Wiesendanger M. Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J Physiol. 1971 Sep;217(2):419–446. doi: 10.1113/jphysiol.1971.sp009579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Phillips C. G. The Ferrier lecture, 1968. Motor apparatus of the baboon's hand. Proc R Soc Lond B Biol Sci. 1969 May 20;173(1031):141–174. doi: 10.1098/rspb.1969.0044. [DOI] [PubMed] [Google Scholar]
  32. Porter R., Rack P. M. Timing of the responses in the motor cortex of monkeys to an unexpected disturbance of finger position. Brain Res. 1976 Feb 20;103(2):201–213. doi: 10.1016/0006-8993(76)90794-0. [DOI] [PubMed] [Google Scholar]
  33. Sakai T., Preston J. B. Evidence for a transcortical reflex: primate corticospinal tract neuron responses to ramp stretch of muscle. Brain Res. 1978 Dec 29;159(2):463–467. doi: 10.1016/0006-8993(78)90559-0. [DOI] [PubMed] [Google Scholar]
  34. Strick P. L., Preston J. B. Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. J Neurophysiol. 1982 Jul;48(1):150–159. doi: 10.1152/jn.1982.48.1.150. [DOI] [PubMed] [Google Scholar]
  35. Tanji J., Evarts E. V. Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J Neurophysiol. 1976 Sep;39(5):1062–1068. doi: 10.1152/jn.1976.39.5.1062. [DOI] [PubMed] [Google Scholar]
  36. Tanji J., Wise S. P. Submodality distribution in sensorimotor cortex of the unanesthetized monkey. J Neurophysiol. 1981 Mar;45(3):467–481. doi: 10.1152/jn.1981.45.3.467. [DOI] [PubMed] [Google Scholar]
  37. Tatton W. G., Bawa P. Input-output properties of motor unit responses in muscles stretched by imposed displacements of the monkey wrist. Exp Brain Res. 1979;37(3):439–457. doi: 10.1007/BF00236816. [DOI] [PubMed] [Google Scholar]
  38. Tatton W. G., Forner S. D., Gerstein G. L., Chambers W. W., Liu C. N. The effect of postcentral cortical lesions on motor responses to sudden upper limb displacements in monkeys. Brain Res. 1975 Oct 10;96(1):108–113. doi: 10.1016/0006-8993(75)90580-6. [DOI] [PubMed] [Google Scholar]
  39. Tracey D. J., Walmsley B., Brinkman J. 'Long-loop' reflexes can be obtained in spinal monkeys. Neurosci Lett. 1980 May 15;18(1):59–65. doi: 10.1016/0304-3940(80)90213-x. [DOI] [PubMed] [Google Scholar]
  40. Vilis T., Cooke J. D. Modulation of the functional stretch reflex by the segmental reflex pathway. Exp Brain Res. 1976 Jun 18;25(3):247–254. doi: 10.1007/BF00234016. [DOI] [PubMed] [Google Scholar]
  41. Wiesendanger M. Input from muscle and cutaneous nerves of the hand and forearm to neurones of the precentral gyrus of baboons and monkeys. J Physiol. 1973 Jan;228(1):203–219. doi: 10.1113/jphysiol.1973.sp010082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wolpaw J. R. Correlations between task-related activity and responses to perturbation in primate sensorimotor cortex. J Neurophysiol. 1980 Dec;44(6):1122–1138. doi: 10.1152/jn.1980.44.6.1122. [DOI] [PubMed] [Google Scholar]
  43. Wong Y. C., Kwan H. C., Murphy J. T. Activity of precentral neurons during torque-triggered hand movements in awake primates. Can J Physiol Pharmacol. 1979 Feb;57(2):174–184. doi: 10.1139/y79-027. [DOI] [PubMed] [Google Scholar]

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