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. 1992 Jan;445:1–24. doi: 10.1113/jphysiol.1992.sp018909

Sensory characteristics of monkey thalamic and motor cortex neurones.

E G Butler 1, M K Horne 1, J A Rawson 1
PMCID: PMC1179967  PMID: 1501128

Abstract

1. Extracellular single-cell recordings were made from the cerebellar thalamus, the ventro-posterior lateralis par caudalis (VPLc) and motor cortex of three conscious monkeys. Recordings were made from the thalamus as well as the cortex in two monkeys. In all, recordings were made from the thalamus in four hemispheres and from the motor cortex in four hemispheres. The animals were trained to permit a detailed examination when relaxed. Unexpected perturbations were applied to the wrist. Seventy-seven wrist-related neurones were recorded in the cerebellar thalamus, forty-two neurones from the VPLc and eighty-four neurones in motor cortex. 2. Cerebellar nuclear stimulation was used to physiologically identify thalamic neurones receiving input from the cerebellum. The location of all neurones was verified histologically. 3. The majority of cerebellar thalamic neurones had deep sensory receptive fields related to a single muscle, a group of synergists or a single joint. There was a distinct topographical organization. These fields were similar to sensory fields in motor cortical neurones, but had higher thresholds. 4. VPLc neurones had discrete deep or cutaneous sensory fields, or a combination of these fields, which suggests convergence. VPLc neurones had fields with lower thresholds than cerebellar thalamic neurones. The somatotopically located forelimb area in the VPLc was posterior to and continuous with the forelimb area in the cerebellar thalamus. 5. VPLc neurones responded with a shorter latency to wrist perturbations than did cerebellar thalamic neurones. VPLc neurones with deep sensory fields changed firing significantly earlier than those with cutaneous fields. The VPLc is likely to be the major source of sensory input to the motor cortex, and based on the results of this study we suggest that the VPLc is the thalamic nucleus best placed to transmit short-latency afferent input from the forelimb. 6. The timing of the neuronal discharge of cerebellar thalamic and VPLc cells, which resulted from perturbations of the wrist, was best linked to the duration of movement rather than its amplitude. The cells began firing as soon as the velocity changed sign and continued firing until the sign of the velocity changed again. In subsequent corrective movements neuronal discharge in the VPLc appeared to also encode movement acceleration.

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Selected References

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  1. Andersson S. A., Landgren S., Wolsk D. The thalamic relay and cortical projection of group I muscle afferents from the forelimb of the cat. J Physiol. 1966 Apr;183(3):576–591. doi: 10.1113/jphysiol.1966.sp007885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bedingham W., Tatton W. G. Kinematic representation of imposed forearm movements by pericruciate neurons (areas 4 and 3a) in the awake cat. J Neurophysiol. 1985 Apr;53(4):886–909. doi: 10.1152/jn.1985.53.4.886. [DOI] [PubMed] [Google Scholar]
  3. Berkley K. J. Spatial relationships between the terminations of somatic sensory motor pathways in the rostral brainstem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon. J Comp Neurol. 1983 Oct 20;220(2):229–251. doi: 10.1002/cne.902200210. [DOI] [PubMed] [Google Scholar]
  4. Brinkman J., Bush B. M., Porter R. Deficient influence of peripheral stimuli on precentral neurones in monkeys with dorsal column lesions. J Physiol. 1978 Mar;276:27–48. doi: 10.1113/jphysiol.1978.sp012218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burton J. E., Onoda N. Interpositus neuron discharge in relation to a voluntary movement. Brain Res. 1977 Jan 31;121(1):167–172. doi: 10.1016/0006-8993(77)90447-4. [DOI] [PubMed] [Google Scholar]
  6. Butler E. G., Horne M. K., Churchward P. R. A frequency analysis of neuronal activity in monkey thalamus, motor cortex and electromyograms in wrist oscillations. J Physiol. 1992 Jan;445:49–68. doi: 10.1113/jphysiol.1992.sp018911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butler E. G., Horne M. K., Hawkins N. J. The activity of monkey thalamic and motor cortical neurones in a skilled, ballistic movement. J Physiol. 1992 Jan;445:25–48. doi: 10.1113/jphysiol.1992.sp018910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Chung J. M., Lee K. H., Surmeier D. J., Sorkin L. S., Kim J., Willis W. D. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol. 1986 Aug;56(2):370–390. doi: 10.1152/jn.1986.56.2.370. [DOI] [PubMed] [Google Scholar]
  10. Clark F. J., Burgess P. R. Slowly adapting receptors in cat knee joint: can they signal joint angle? J Neurophysiol. 1975 Nov;38(6):1448–1463. doi: 10.1152/jn.1975.38.6.1448. [DOI] [PubMed] [Google Scholar]
  11. Cody F. W., Moore R. B., Richardson H. C. Patterns of activity evoked in cerebellar interpositus nuclear neurones by natural somatosensory stimuli in awake cats. J Physiol. 1981 Aug;317:1–20. doi: 10.1113/jphysiol.1981.sp013810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ellaway P. H. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978 Aug;45(2):302–304. doi: 10.1016/0013-4694(78)90017-2. [DOI] [PubMed] [Google Scholar]
  13. Evarts E. V. Activity of thalamic and cortical neurons in relation to learned movement in the monkey. Int J Neurol. 1971;8(2):321–326. [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. Flament D., Hore J. Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey. J Neurophysiol. 1988 Oct;60(4):1268–1284. doi: 10.1152/jn.1988.60.4.1268. [DOI] [PubMed] [Google Scholar]
  18. Friedman D. P., Jones E. G. Thalamic input to areas 3a and 2 in monkeys. J Neurophysiol. 1981 Jan;45(1):59–85. doi: 10.1152/jn.1981.45.1.59. [DOI] [PubMed] [Google Scholar]
  19. Ghosh S., Brinkman C., Porter R. A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J Comp Neurol. 1987 May 15;259(3):424–444. doi: 10.1002/cne.902590309. [DOI] [PubMed] [Google Scholar]
  20. Harvey R. J., Porter R., Rawson J. A. Discharges of intracerebellar nuclear cells in monkeys. J Physiol. 1979 Dec;297(0):559–580. doi: 10.1113/jphysiol.1979.sp013057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Horne M. K., Porter R. The discharges during movement of cells in the ventrolateral thalamus of the conscious monkey. J Physiol. 1980 Jul;304:349–372. doi: 10.1113/jphysiol.1980.sp013328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Horne M. K., Tracey D. J. The afferents and projections of the ventroposterolateral thalamus in the monkey. Exp Brain Res. 1979 Jun 1;36(1):129–141. doi: 10.1007/BF00238473. [DOI] [PubMed] [Google Scholar]
  23. Jones E. G., Friedman D. P. Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. J Neurophysiol. 1982 Aug;48(2):521–544. doi: 10.1152/jn.1982.48.2.521. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Lemon R. N., van der Burg J. Short-latency peripheral inputs to thalamic neurones projecting to the motor cortex in the monkey. Exp Brain Res. 1979 Aug 1;36(3):445–462. doi: 10.1007/BF00238515. [DOI] [PubMed] [Google Scholar]
  26. Loe P. R., Whitsel B. L., Dreyer D. A., Metz C. B. Body representation in ventrobasal thalamus of macaque: a single-unit analysis. J Neurophysiol. 1977 Nov;40(6):1339–1355. doi: 10.1152/jn.1977.40.6.1339. [DOI] [PubMed] [Google Scholar]
  27. MacKay W. A., Murphy J. T. Responses of interpositus neurons to passive muscle stretch. J Neurophysiol. 1974 Nov;37(6):1410–1423. doi: 10.1152/jn.1974.37.6.1410. [DOI] [PubMed] [Google Scholar]
  28. Macpherson J. M., Rasmusson D. D., Murphy J. T. Activities of neurons in "motor" thalamus during control of limb movement in the primate. J Neurophysiol. 1980 Jul;44(1):11–28. doi: 10.1152/jn.1980.44.1.11. [DOI] [PubMed] [Google Scholar]
  29. Maendly R., Rüegg D. G., Wiesendanger M., Wiesendanger R., Lagowska J., Hess B. Thalamic relay for group I muscle afferents of forelimb nerves in the monkey. J Neurophysiol. 1981 Nov;46(5):901–917. doi: 10.1152/jn.1981.46.5.901. [DOI] [PubMed] [Google Scholar]
  30. Orioli P. J., Strick P. L. Cerebellar connections with the motor cortex and the arcuate premotor area: an analysis employing retrograde transneuronal transport of WGA-HRP. J Comp Neurol. 1989 Oct 22;288(4):612–626. doi: 10.1002/cne.902880408. [DOI] [PubMed] [Google Scholar]
  31. POGGIO G. F., MOUNTCASTLE V. B. THE FUNCTIONAL PROPERTIES OF VENTROBASAL THALAMIC NEURONSSTUDIED IN UNANESTHETIZED MONKEYS. J Neurophysiol. 1963 Sep;26:775–806. doi: 10.1152/jn.1963.26.5.775. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Schell G. R., Strick P. L. The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci. 1984 Feb;4(2):539–560. doi: 10.1523/JNEUROSCI.04-02-00539.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shinoda Y., Futami T., Kano M. Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. II. Input-output organization of single thalamocortical neurons in the ventrolateral thalamus. Neurosci Res. 1985 Feb;2(3):157–180. doi: 10.1016/0168-0102(85)90010-0. [DOI] [PubMed] [Google Scholar]
  35. Soso M. J., Fetz E. E. Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. J Neurophysiol. 1980 Apr;43(4):1090–1110. doi: 10.1152/jn.1980.43.4.1090. [DOI] [PubMed] [Google Scholar]
  36. Strick P. L. Activity of ventrolateral thalamic neurons during arm movement. J Neurophysiol. 1976 Sep;39(5):1032–1044. doi: 10.1152/jn.1976.39.5.1032. [DOI] [PubMed] [Google Scholar]
  37. Strick P. L. Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J Neurophysiol. 1976 Sep;39(5):1020–1031. doi: 10.1152/jn.1976.39.5.1020. [DOI] [PubMed] [Google Scholar]
  38. Strick P. L. The influence of motor preparation on the response of cerebellar neurons to limb displacements. J Neurosci. 1983 Oct;3(10):2007–2020. doi: 10.1523/JNEUROSCI.03-10-02007.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thach W. T. Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol. 1978 May;41(3):654–676. doi: 10.1152/jn.1978.41.3.654. [DOI] [PubMed] [Google Scholar]
  40. Tracey D. J., Asanuma C., Jones E. G., Porter R. Thalamic relay to motor cortex: afferent pathways from brain stem, cerebellum, and spinal cord in monkeys. J Neurophysiol. 1980 Sep;44(3):532–554. doi: 10.1152/jn.1980.44.3.532. [DOI] [PubMed] [Google Scholar]
  41. Uno M., Yoshida M., Hirota I. The mode of cerebello-thalamic relay transmission investigated with intracellular recording from cells of the ventrolateral nucleus of cat's thalamus. Exp Brain Res. 1970;10(2):121–139. doi: 10.1007/BF00234726. [DOI] [PubMed] [Google Scholar]
  42. Vilis T., Hore J. Central neural mechanisms contributing to cerebellar tremor produced by limb perturbations. J Neurophysiol. 1980 Feb;43(2):279–291. doi: 10.1152/jn.1980.43.2.279. [DOI] [PubMed] [Google Scholar]
  43. Waldron J. N., Ghosh S., Zarzecki P. Multiple inputs to a population of thalamocortical neurons projecting to cat somatosensory cortex. Exp Brain Res. 1989;74(1):105–115. doi: 10.1007/BF00248284. [DOI] [PubMed] [Google Scholar]

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