Experimental Brain Research

, Volume 106, Issue 3, pp 365–376 | Cite as

Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat

  • C.-F. Ekerot
  • H. Jörntell
  • M. Garwicz
Research Article

Abstract

The functional relation between receptive fields of climbing fibres projecting to the C1, C3 and Y zones and forelimb movements controlled by nucleus interpositus anterior via the rubrospinal tract were studied in cats decerebrated at the pre-collicular level. Microelectrode tracks were made through the caudal half of nucleus interpositus anterior. This part of the nucleus receives its cerebellar cortical projection from the forelimb areas of these three sagittal zones. The C3 zone has been demonstrated to consist of smaller functional units called microzones. Natural stimulation of the forelimb skin evoked positive field potentials in the nucleus. These potentials have previously been shown to be generated by climbing fibre-activated Purkinje cells and were mapped at each nuclear site, to establish the climbing fibre receptive fields of the afferent microzones. The forelimb movement evoked by microstimulation at the same site was then studied. The movements usually involved more than one limb segment. Shoulder retraction and elbow flexion were frequently evoked, whereas elbow extension was rare and shoulder protraction never observed. In total, movements at the shoulder and/or elbow occurred for 96% of the interpositus sites. At the wrist, flexion and extension movements caused by muscles with radial, central or ulnar insertions on the paw were all relatively common. Pure supination and pronation movements were also observed. Movements of the digits consisted mainly of dorsal flexion of central or ulnar digits. A comparison of climbing fibre receptive fields and associated movements for a total of 110 nuclear sites indicated a general specificity of the input-output relationship of this cerebellar control system. Several findings suggested that the movement evoked from a particular site would act to withdraw the area of the skin corresponding to the climbing fibre receptive field of the afferent microzones. For example, sites with receptive fields on the dorsum of the paw were frequently associated with palmar flexion at the wrist, whereas sites with receptive fields on the ventral side of the paw and forearm were associated with dorsiflexion at the wrist. Correspondingly, receptive fields on the lateral side of the forearm and paw were often associated with flexion at the elbow, whereas sites with receptive fields on the radial side of the forearm were associated with elbow extension. The proximal movements that were frequently observed also for distal receptive fields may serve to produce a general shortening of the limb to enhance efficiency of the withdrawal. It has previously been suggested that the cerebellar control of forelimb movements via the rubrospinal tract has a modular organisation. Each module would consist of a cell group in the nucleus interpositus anterior and its afferent microzones in the C1, C3 and Y zones, characterised by a homogenous set of climbing fibre receptive fields. The results of the present study support this organisational principle, and suggest that the efferent action of a module is to withdraw the receptive field from an external stimulus. Possible functional interpretations of the action of this system during explorative and reaching movements are discussed.

Key words

Climbing fibres Rubrospinal tract Motor control Motor learning Cat 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61Google Scholar
  2. Alstermark B, Lundberg A (1992) The C3–C4 propriospinal system: target-reaching and food-taking. In: Jami L, Pierrot-Deseilligny E, Zytnicki D (eds) Muscle afferents and spinal control of movements. Pergamon Press, Oxford pp 327–354Google Scholar
  3. Alstermark B, Kummel H, Pinter MJ, Tantisira B (1990) Integration in descending motor pathways controlling the forelimb in the cat. 17. Axonal projection and termination of C3–C4 propriospinal neurones in the C6-Th1 segments. Exp Brain Res 81:447–461Google Scholar
  4. Andersson G, Armstrong DM (1987) Complex spikes in Purkinje cells in the lateral vermis (b-zone) of the cat cerebellum during locomotion. J Physiol (Lond) 385:107–134Google Scholar
  5. Andersson G, Ekerot C-F, Oscarsson O, Schouenborg J (1987) Convergence of afferent paths to olivo-cerebellar complexes. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. Plenum, New York, pp 165–173Google Scholar
  6. Asanuma H, Hunsperger O (1975) Functional significance of projection from the cerebellar nuclei to the motor cortex in the cat. Brain Res 98:73–92Google Scholar
  7. Cheney PD, Fetz EE, Mewes K (1991) Neural mechanisms underlying corticospinal and rubrospinal control of limb movements. Prog Brain Res 87:213–252Google Scholar
  8. Ekerot C-F, Larson B (1979a) The dorsal spino-olivocerebellar system in the cat. I. Functional organization of and termination in the anterior lobe. Exp Brain Res 36:201–217Google Scholar
  9. Ekerot C-F, Larson B (1979b) The dorsal spino-olivocerebellar system in the cat. II. Somatotopical organization. Exp Brain Res 36:219–232Google Scholar
  10. Ekerot C-F, Larson B (1982) Branching of olivary axons to innervate pairs of sagittal zones in the cerebellar anterior lobe of the cat. Exp Brain Res 48:185–198Google Scholar
  11. Ekerot C-F, Kano M (1985) Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res 36:201–217Google Scholar
  12. Ekerot C-F, Kano M (1989) Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci Res 6:264–268Google Scholar
  13. Ekerot C-F, Garwicz M (1992) Relation between climbing fibre receptive fields of afferent microzones to nucleus interpositus anterior and forelimb movements evoked by microstimulation in the cat. Eur J Neurosci [Suppl] 5:1059Google Scholar
  14. Ekerot C-F, Garwicz M, Schouenborg J (1991a) Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J Physiol (Lond) 441:257–274Google Scholar
  15. Ekerot C-F, Garwicz M, Schouenborg J (1991b) The postsynaptic dorsal column pathway mediates cutaneous nociceptive information to cerebellar climbing fibres in the cat. J Physiol (Lond) 441:275–284Google Scholar
  16. Ekerot C-F, Garwicz M, Jörntell H (1993) Modular organization of cerebellar control of movements via the rubrospinal tract in the cat. Proc Int Union Physiol Sci Glasgow 32:171.3Google Scholar
  17. Flament D, Hore J (1986) Movement and electromyographic disorders associated with cerebella dysmetria. J Neurophysiol 55:1221–1233Google Scholar
  18. Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J Neurophysiol 62:198–211Google Scholar
  19. Garwicz M (1992) Cerebellar control of forelimb movements: modular organization revealed by nociceptive and tactile climbing fibre input. PhD thesis, Lund UniversityGoogle Scholar
  20. Garwicz M, Ekerot C-F (1994) Topographical organization of cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol (Lond) 474/2:245–260Google Scholar
  21. Garwicz M, Ekerot C-F, Schouenborg J (1992) Distribution of cutaneous nociceptive and tactile climbing fibre input to sagittal zones in cat cerebellar anterior lobe. Eur J Neurosci 4:289–295Google Scholar
  22. Gellman R, Gibson AR, Houk JC (1985) Inferior olivary neurones in the awake cat: detection of contact and passive body displacement. J Neurophysiol 54/1:40–60Google Scholar
  23. Gibson AR, Houk JC, Kohlerman NJ (1985a) Magnocellular red nucleus activity during different types of limb movement in the macaque monkey. J Physiol (Lond) 358:527–549Google Scholar
  24. Gibson AR, Houk JC, Kohlerman NJ (1985b) Relation between red nucleus discharge and movement parameters in trained macaque monkeys. J Physiol (Lond) 358:550–570Google Scholar
  25. Gibson AR, Robinson FR, Houk JC (1987) Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum. J Comp Neurol 260:362–377Google Scholar
  26. Gilbert PFC, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309–328Google Scholar
  27. Giuffrida R, Li Volsi G, Pantr MR, Perciavalle V, Sepienza S, Urbano A (1980) Single muscle organization of interposito-rubral projections. Exp Brain Res 39:261–267Google Scholar
  28. Harvey RJ, Porter R, Rawson JA (1977) The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey's cerebellum. J Physiol (Lond) 271:515–536Google Scholar
  29. Harvey RJ, Porter R, Rawson JA (1979) Discharges of intracerebellar nuclear cells in monkeys. J Physiol (Lond) 297:559–580Google Scholar
  30. Höre J, Wild B, Diener HC (1991) Cerebellar dysmetria at the elbow, wrist and fingers. J Neurophysiol 65:563–571Google Scholar
  31. Ito M (1984) The cerebellum and neural control. Raven Press, New YorkGoogle Scholar
  32. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85–102CrossRefGoogle Scholar
  33. Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol (Lond) 324:113–134Google Scholar
  34. Kitazawa S, Goto T, Urushihara Y (1993) Quantitative evaluation of reaching movements in cats with and without cerebellar lesions using normalized integral of jerk. In: Mano N, Hamada I, DeLong MR (eds) Role of the cerebellum and basal ganglia in voluntary movement. Elsevier, pp 11–19Google Scholar
  35. MacKay WA (1988) Unit activity in the cerebellar nuclei related to arm reaching movements. Brain Res 442:240–254Google Scholar
  36. Marple-Horvat DE, Stein JF (1987) Cerebellar neuronal activity related to arm movements in trained rhesus monkeys. J Physiol (Lond) 394:351–366Google Scholar
  37. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437–470Google Scholar
  38. Miller LE, Van Kan PLE, Sinkjaer T, Andersen T, Harris GD, Houk JC (1993) Correlation of primate red nucleus discharge with muscle activity during free-form arm movements. J Physiol (Lond) 469:213–243Google Scholar
  39. Miller S, Oscarsson O (1970) Termination and functional organization of spino-olivocerebellar paths. In: Fields WS, Willis WD (eds) The cerebellum in health and disease. Green, St. Louis, pp 172–200Google Scholar
  40. Oscarsson O (1980) Functional organization of olivary projection to cerebellar anterior lobe. In: Courville J, de Montigny C, Lamarre Y (eds) The inferior olivary nucleus: anatomy and physiology. Raven Press, New York, pp 279–289Google Scholar
  41. Rispal-Padel L, Cicirata F, Pons C (1982) Cerebellar nuclear topography of simple and synergistic movements in the alert baboon (Papio papio). Exp Brain Res 47:365–380Google Scholar
  42. Robinson FR, Houk JC, Gibson AR (1987) Limb specific relations of the cat magnocellular red nucleus. J Comp Neurol 257:553–577Google Scholar
  43. Rosén I, Asanuma H (1972) Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations. Exp Brain Res 14:257–273Google Scholar
  44. Schouenborg J, Kalliomäki J (1990) Functional organization of the nociceptive withdrawal reflexes. I. Activation of hindlimb muscles in the rat. Exp Brain Res 83:67–78Google Scholar
  45. Shinoda Y, Arnold A, Asanuma H (1976) Spinal branching of corticospinal axons in the cat. Exp Brain Res 26:215–234Google Scholar
  46. Shinoda Y, Ghez C, Arnold A (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30:203–218Google Scholar
  47. Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and adaptive coordination of movement. Annu Rev Neurosci 15:403–442Google Scholar
  48. Trott JR, Armstrong DM (1987) The cerebellar corticonuclear projection from lobule Vb/c of the cat anterior lobe: a combined electrophysiological and autoradiographic study. I. Projections from the intermediate region. Exp Brain Res 66:318–338Google Scholar
  49. Van Kan PLE, Houk JC, Gibson AR (1993) Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69:57–73Google Scholar
  50. Voogd J (1982) The olivocerebellar projection in the cat. In: Palay SL, Chan-Palay V (eds) The cerebellum, new vistas. Exp Brain Res [Suppl 6] Springer-Verlag, Berlin Heidelberg New York, pp 134–161Google Scholar
  51. Voogd J, Bigaré F (1980) Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: a review. In: Courville J, de Montigny C, Lamarre Y (eds) The inferior olivary nucleus: anatomy and physiology. Raven Press, New York, pp 207–234Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • C.-F. Ekerot
    • 1
  • H. Jörntell
    • 1
  • M. Garwicz
    • 1
  1. 1.Department of Physiology and BiophysicsUniversity of LundLundSweden

Personalised recommendations