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.
Similar content being viewed by others
References
Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61
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 327–354
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 81:447–461
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) 385:107–134
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 165–173
Asanuma H, Hunsperger O (1975) Functional significance of projection from the cerebellar nuclei to the motor cortex in the cat. Brain Res 98:73–92
Cheney PD, Fetz EE, Mewes K (1991) Neural mechanisms underlying corticospinal and rubrospinal control of limb movements. Prog Brain Res 87:213–252
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 36:201–217
Ekerot C-F, Larson B (1979b) The dorsal spino-olivocerebellar system in the cat. II. Somatotopical organization. Exp Brain Res 36:219–232
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 48:185–198
Ekerot C-F, Kano M (1985) Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res 36:201–217
Ekerot C-F, Kano M (1989) Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci Res 6:264–268
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] 5:1059
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) 441:257–274
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) 441:275–284
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 32:171.3
Flament D, Hore J (1986) Movement and electromyographic disorders associated with cerebella dysmetria. J Neurophysiol 55:1221–1233
Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J Neurophysiol 62:198–211
Garwicz M (1992) Cerebellar control of forelimb movements: modular organization revealed by nociceptive and tactile climbing fibre input. PhD thesis, Lund University
Garwicz M, Ekerot C-F (1994) Topographical organization of cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol (Lond) 474/2:245–260
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 4:289–295
Gellman R, Gibson AR, Houk JC (1985) Inferior olivary neurones in the awake cat: detection of contact and passive body displacement. J Neurophysiol 54/1:40–60
Gibson AR, Houk JC, Kohlerman NJ (1985a) Magnocellular red nucleus activity during different types of limb movement in the macaque monkey. J Physiol (Lond) 358:527–549
Gibson AR, Houk JC, Kohlerman NJ (1985b) Relation between red nucleus discharge and movement parameters in trained macaque monkeys. J Physiol (Lond) 358:550–570
Gibson AR, Robinson FR, Houk JC (1987) Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum. J Comp Neurol 260:362–377
Gilbert PFC, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309–328
Giuffrida R, Li Volsi G, Pantr MR, Perciavalle V, Sepienza S, Urbano A (1980) Single muscle organization of interposito-rubral projections. Exp Brain Res 39:261–267
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) 271:515–536
Harvey RJ, Porter R, Rawson JA (1979) Discharges of intracerebellar nuclear cells in monkeys. J Physiol (Lond) 297:559–580
Höre J, Wild B, Diener HC (1991) Cerebellar dysmetria at the elbow, wrist and fingers. J Neurophysiol 65:563–571
Ito M (1984) The cerebellum and neural control. Raven Press, New York
Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85–102
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) 324:113–134
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 11–19
MacKay WA (1988) Unit activity in the cerebellar nuclei related to arm reaching movements. Brain Res 442:240–254
Marple-Horvat DE, Stein JF (1987) Cerebellar neuronal activity related to arm movements in trained rhesus monkeys. J Physiol (Lond) 394:351–366
Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437–470
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) 469:213–243
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 172–200
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 279–289
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 47:365–380
Robinson FR, Houk JC, Gibson AR (1987) Limb specific relations of the cat magnocellular red nucleus. J Comp Neurol 257:553–577
Rosén I, Asanuma H (1972) Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations. Exp Brain Res 14:257–273
Schouenborg J, Kalliomäki J (1990) Functional organization of the nociceptive withdrawal reflexes. I. Activation of hindlimb muscles in the rat. Exp Brain Res 83:67–78
Shinoda Y, Arnold A, Asanuma H (1976) Spinal branching of corticospinal axons in the cat. Exp Brain Res 26:215–234
Shinoda Y, Ghez C, Arnold A (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30:203–218
Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and adaptive coordination of movement. Annu Rev Neurosci 15:403–442
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 66:318–338
Van Kan PLE, Houk JC, Gibson AR (1993) Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69:57–73
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 134–161
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 207–234
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ekerot, CF., Jörntell, H. & Garwicz, M. Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Exp Brain Res 106, 365–376 (1995). https://doi.org/10.1007/BF00231060
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00231060