Summary
The aim of the study was to investigate the contribution of the primary sensory cortex in the compensation of cerebellar deficits during self-paced movements. For this purpose, monkeys were trained on motor tasks which required goal-reaching and independent finger movements. The intermediate and lateral deep cerebellar nuclei and the sensory cortex were lesioned in isolation and in sequence and the course of motor recovery was studied on the test performances. The deep nuclei were lesioned by kainic acid injections, the sensory cortex was removed by ablation. Cerebellar lesions in isolation produced obvious deficits at proximal and distal joints, affecting both slow and fast motor adjustments. Only lesions of the anterior portions of the intermediate and lateral deep nuclear complexes produced deficiencies in voluntary movements. Lesions of the posterior portions produced postural disturbances. The process of recovery following cerebellar lesions was slow and, depending on the nature of the task, was found to be differentially disruptive for motor performances requiring fast and slow motor adjustments. The deficits at distal joints appeared to be more enduring than those at proximal joints. Sensory cortical lesions in isolation produced much less severe and more transient motor deficits. They consisted of hand clumsiness and their recovery was fast and reached higher levels of performance than following cerebellar lesions. When the sensory cortex was removed secondarily to a cerebellar lesion and after recovery from the cerebellar deficits, the initially recovered motor performance became much worse again (decompensation). Removal of the sensory cortex prior to a cerebellar lesion exaggerated the cerebellar deficits and severely limited their recovery. Slow and fast motor performances were completely abolished for three weeks following sequential lesions. Signs of recovery subsequently appeared and stabilized at low levels of performance by five to seven weeks. The effects of combined, sequential cerebellar and sensory cortical lesions were much worse than expected if the effects from the two lesions were merely additive. This indicates that there is some functional interrelationship between the sensory cortex and the cerebellum, which promotes compensation. The somatosensory cortex appears to play a crucial role in the process of recovery from cerebellar motor deficits and it is likely that sensation is an important component in the process of recovery. It is suggested that the sensory cortex exerts its compensatory actions via a structure or structures which receives convergent cerebellar and sensory cortical inputs.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alstermark B, Gorska T, Johannison T, Lundberg A (1986) Effects of dorsal column transection in the upper cervical segments on visually guided forelimb movements. Neurosci Res 3: 462–466
Aring CD, Fulton JF (1936) Relation of the cerebrum to the cerebellum. II. Cerebellar tremor in the monkey and its absence after removal of the principal excitable areas of the cerebral cortex (areas 4 and 6). III. Accentuation of cerebellar tremor following lesions of the premotor area (area 6, upper part). Arch Neurol Psychiat 35: 439–466
Asanuma H, Larsen KD, Yumiya H (1980) Peripheral input pathways to the monkey motor cortex. Exp Brain Res 38: 349–355
Asanuma H, Arissian K (1982) Motor deficits following interruption of sensory inputs to the motor cortex of the monkey. In: Buser PA, Cobb WA, Okuna T (eds) Kyoto Symposia (EEG Suppl. No.36), Elsevier, Amsterdam, pp 415–421
Asanuma H, Arissian K (1984) Experiments on the functional role of peripheral input to the motor cortex during voluntary movements in the monkey. J Neurophysiol 52: 212–227
Asanuma H, Kosar E, Tsukahara N, Robinson H (1985) Modification of the projection from the sensory cortex to the motor cortex following elimination of thalamic projections to the motor cortex in cats. Brain Res 345: 79–86
Beppu H, Suda M, Tanaka R (1984) Analysis of cerebellar motor disorders by visually guided elbow tracking movement. Brain 107: 787–809
Botterell EH, Fulton JF (1938a) Functional localization in the cerebellum of primates. II. Lesions of the midline structures and deep nuclei. J Comp Neurol 69: 47–62
Botterell EH, Fulton JF (1938b) Functional localization in the cerebellum of primates. III. Lesions of hemispheres (neocerebellum). J Comp Neurol 69: 63–87
Brinkman C, Bush BM, Porter R (1978) Deficient influences of peripheral stimuli on precentral neurons in monkeys with dorsal column lesions. J Physiol 276: 27–48
Brooks VB, Thach WT (1981) Cerebellar control of posture and movement. In: Brooks VB (ed) Handbook of physiology, Sect 1, Vol 2, Part 2. American Physiological Society, Bethesda, pp 877–946
Carpenter MB, Correll JW (1961) Spinal pathways mediating cerebellar dyskinesia in rhesus monkey. J Neurophysiol 24: 535–551
Carrea RME, Mettler FA (1947) Physiological consequences following extensive removals of the cerebellar cortex and deep cerebellar nuclei and effect of secondary cerebral ablations in the primate. J Comp Neurol 87: 169–288
Denny-Brown D (1966) The cerebral control of movement. Charles C Thomas, Springfield, Ill
Dow RS, Moruzzi G (1958) The physiology and pathology of the cerebellum. University of Minnesota Press, Minnesota
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
Freund H-J, Hummelsheim H (1985) Lesions of premotor cortex in man. Brain 108: 697–733
Frigyesi TL, Rinvik E, Yahr MD (1972) Corticothalamic projections and sensorimotor activities. Raven Press, New York
Gilman S, Carr D, Hollenberg J (1976) Kinematic effects of deafferentation and cerebellar ablation. Brain 99: 311–330
Goldberger ME, Growdon JH (1973) Pattern of recovery following cerebellar deep nuclear lesions in monkey. Exp Neurol 39: 307–322
Gorska T, Sybirska E (1980) Effects of pyramidal lesions on forelimb movements in the cat. Acta Neurobiol Exp 40: 843–859
Growdon JH, Chamber WW, Liu CN (1967) An experimental study of cerebellar dyskinesia in the rhesus monkey. Brain 90: 603–632
Heath CJ, Hore J, Philipps CG (1976) Inputs from low threshold muscle afferents from hand and forearm to areas 3a and 3b of baboon's cerebral cortex. J Physiol 257: 199–227
Holmes G (1922) Clinical symptoms of cerebellar disease and their interpretation. The Croonian Lectures II. Lancet 1: 1231–1237
Holmes G (1939) The cerebellum of man. Brain 62: 157–168
Horvath FE, Atkin A, Kozlovskaya IB, Fuller DRG, Brooks VB (1970) Effects of cooling the dentate nucleus on alternating bar-pressing performance in monkey. Int J Neurol 7: 252–270
Hyvärinen J (1982) The parietal cortex of monkey and man. Studies of brain functions, Vol 8. Springer, Berlin Heidelberg New York
Ito M, Jastreboff PF, Miyashita Y (1980) Retrograde influence of surgical and chemical flocculectomy upon dorsal cap neurons of the inferior olive. Neurosci Lett 20: 45–48
Ito M (1985) The cerebellum and neural control. Raven Press, New York
Jones EG, Coulter JD, Hendry SHC (1978) Intracortical connectivity of architectonic fields in the somatic sensory motor and parietal cortex of monkeys. J Comp Neurol 181: 291–349
Kawaguchi S, Miyata H, Kato N (1986) Regeneration of the cerebellofugal projection after transsection of the superior cerebellar peduncle in kittens: morphological and electrophysiological studies. J Comp Neurol 245: 258–273
Keller AD, Roy RS, Chase WP (1937) Extirpation of the neocerebellar cortex without eliciting so-called cerebellar signs. Am J Physiol 11: 720–733
Kluver H, Barrera E (1953) A method for the combined staining of cells and fibers in the nervous system. J Neuropathol Exp Neurol 12: 400–403
Kornhuber HH (1971) Motor functions of cerebellum and basal ganglia: the cerebellocortical saccadic (ballistic) clock, the cerebellonuclear hold regulator, and the basal ganglia ramp (voluntary speed smooth movement) generator. Kybernetik 8: 157–162
Kusuma T, Mabuchi M (1970) Stereotaxic atlas of the brain of Macaca fuscata. University of Tokyo Press, Tokyo
Lashley KS (1933) Integrative functions of the cerebral cortex. Physiol Rev 13: 1–42
Lawrence DG, Kuypers HGJM (1968) The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91: 1–14
Liu CN, Chambers WW (1971) A study of cerebellar dyskinesia in the bilaterally deafferented forelimbs of the monkey (Macacca mulatta and Macacca speciosa). Acta Neurobiol Exp 31: 263–289
Marshall WH, Woolsey CN, Bard P (1937) Cortical representation of tactile sensibility as indicated by cortical potentials. Science 85: 388–390
Massion J, Sasaki K (1979) Cerebro-cerebellar interactions. Elsevier/North Holland Biomedical Press, Amsterdam
Muakassa KF, Strick PL (1979) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized “premotor” areas. Brain Res 177: 176–182
Murakami F, Katsumaru H, Saito K, Tsukahara N (1982) A quantitative study of synaptic reorganization in red nucleus neurons after lesion of the nucleus interpositus of the cat: an electronmicroscopic study involving intracellular injection of horseradish peroxidase. Brain Res 242: 41–53
Passingham RE, Perry VH, Wilkinson F (1983) The long-term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 106: 675–705
Pons TP, Garraghty PE, Lusick CG, Kaas JG (1985) The somatotopic organization of area 2 in macaque monkeys. J Com Neurol 241: 445–466
Ranish NA, Soechting JF (1976) Studies on the control of some simple motor tasks. Effects of thalamic and red nuclei lesions. Brain Res 102: 339–345
Rispal-Padel L, Circirata F, Pons C (1982) Cerebellar nuclear topography of simple and synergistic movements in the alert baboon. Exp Brain Res 47: 365–380
Sasaki K, Kawaguchi S, Oka H, Sakai M, Mizuno N (1976) Electrophysiological studies on the cerebellocerebral projections in monkeys. Exp Brain Res 16: 495–507
Sasaki K, Gemba H (1984) Compensatory motor functions of the somatosensory cortex for dysfunction of the motor cortex following cerebellar hemispherectomy in the monkey. Exp Brain Res 56: 532–538
Shinoda Y, Kano M, Futami T (1985) Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract cells in areas 4 and 6. Neurosci Res 2: 133–156
Szabo J, Cowan WM (1984) A stereotaxic atlas of the brain of the cynomolgus (Macaca fascicularis). J Comp Neurol 222: 265–300
Travis AM, Woolsey CN (1956) Motor performance of monkey after bilateral partial and total cerebral decortications. Am J Phys Med 35: 273–289
Trouche E, Beaubaton D, Amato G, Grangetto A (1979) Impairments and recovery of the spatial and temporal components of a visuomotor pointing movement after unilateral destruction of the dentate nucleus in the baboon. Appl Neurophysiol 42: 248–254
Tsukahara N, Hultborn H, Murakami F, Fujito Y (1975) Electrophysiological study of formation of new synapses and collateral sprouting in red nucleus neurons after partial denervation. J Neurophysiol 38: 1359–1372
Tsukahara N, Fujito Y, Oda Y, Maeda J (1982) Formation of functional synapses in the adult cat red nucleus from the cerebrum following cross-innervation of forelimb flexor and extensor nerve. I. Appearance of new synaptic potentials. Exp Brain Res 45: 1–12
Uno M, Yoshida M, Hirota I (1970) The mode of cerebellothalamic relay transmission investigated with intracellular recording from cells of the ventrolateral nucleus of cat's thalamus. Exp Brain Res 10: 121–139
Vogt BA, Pandya DN (1978) Cortico-cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey. J Comp Neurol 177: 179–189
Voogd J (1967) Comparative aspects of the structure and fiber connections of the mammalian cerebellum. In: Fox CA, Snyder RS (eds) The cerebellum. Progress in brain research. Vol 25. Elsevier, Amsterdam, pp 94–135
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mackel, R. The role of the monkey sensory cortex in the recovery from cerebellar injury. Exp Brain Res 66, 638–652 (1987). https://doi.org/10.1007/BF00270696
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00270696