Summary
The effects of unilateral lesions of the deep cerebellar nuclei on the corticocortical (CC) projection from the somatosensory to the motor cortex were studied in adult cats, utilizing electrophysiological and electron microscopical methods. Axon terminals in the motor cortex belonging to CC afferents were labeled by degeneration induced by lesions of the somatosensory cortex; neurons in the motor cortex were labeled by the Golgi/EM method. In each cat, data from the motor cortex (MCx) contralateral (experimental) and ipsilateral (control) to the cerebellar lesion were compared. Cerebellar lesions produced marked motor deficits, which receded gradually and disappeared after 30 to 40 days. Subsequent lesions of the somatosensory cortex (area 2) contralateral to the cerebellar lesions resulted in the reappearance of the cerebellar symptoms. The number of CC synapses per unit area in experimental MCx was significantly higher than in control MCx. The increase in the number of CC synapses was apparent throughout layers II–V of the MCx, but was most prominent in layers II/III. The increase in the number of CC synapses in experimental MCx was due mainly to an increase of axon terminals synapsing with dendritic spines belonging to pyramidal neurons. In comparison, the numbers and spatial distribution of CC synapses with aspinous, nonpyramidal neurons from both experimental and control MCx were similar. Field potentials in the experimental MCx, evoked by stimulation of area 2, were altered following cerebellar lesions. In experimental MCx, the polarity of the early component of the field potentials reversed at cortical depths corresponding to layers II–III, whereas this reversal was not observed in control MCx. These findings suggest that lesions of the cerebellar nuclei induced sprouting of axon terminals in the MCx to establish a new function. The results provide the first anatomical evidence for the generation of new synapses in the adult CNS which is not induced by elimination of existing synapses.
Similar content being viewed by others
References
Asanuma H, Arissian K (1982) Motor deficits following interruption of sensory inputs to the motor cortex of the monkey. In: Buser PA, Cobb WA, Okuma T (ed) Kyoto symposia. EEG Suppl. 36:415–421
Asanuma H, Arnold A, Zarzecki P (1976) Further study on the excitation of pyramidal tract cells by intracortical microstimulation. Exp Brain Res 26:443–461
Asanuma H, Bornschlegl M (1988) Plasticity and function of associational input to the motor cortex. In: Flohr H (ed) Post-lesion neural plasticity. Springer, Berlin, pp 519–525
Asanuma H, Kosar E, Tsukahara N, Robinson H (1985) Modification of the projection from the sensory cortex to the motor cortex following the elimination of thalamic projections to the motor cortex in cats. Brain Res 345:79–86
Botterell EH, Fulton JF (1938) Functional localization in the cerebellum of primates. II. Lesions of the midline structures and deep nuclei. J Comp Neurol 69:47–62
Cajal SR (1911) Anatomicophysiological considerations on the cerebrum. In: DeFelipe J, Jones EG (ed) Cajal on the cerebral cortex: an annotated translation of the complete writings. Oxford University Press, New York, pp 465–490
Calford MB, Tweedale R (1988) Immediate and chronic changes in response of somatosensory cortex in adult flying-fox after digit amputation. Nature 332:446–448
Donoghue JP, Sanes JN (1988) Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats. J Neurosci 8:3221–3232
Fairen A, Peters A, Saldanha J (1977) A new procedure for examining Golgi-impregnated neurons by light and electron microscopy. J Neurocytol 6:311–337
Feldman ML (1984) Morphology of the neocortical pyramidal neuron. In: Peters A, Jones EG (ed) Cerebral cortex, Vol 1. Cellular components of the cerebral cortex. Plenum Press, New York, pp 123–200
Flohr H (1988) Post-lesion neural plasticity. Springer, Berlin
Fujito Y, Tsukahara N, Oda Y, Yoshida M (1982) Formation of functional synapses in the adult cat red nucleus from the cerebrum following cross-innervation of forelimb flexor and extensor nerves. II. Analysis of newly appeared synaptic potentials. Exp Brain Res 45:13–18
Hassler R, Muhs-Clement K (1964) Arkitektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze. J Hirnforsch 6:377–420
Hebb DO (1949) The organization of behavior: a neurophysiological theory. John Wiley and Sons, New York, pp 227–231
Hersch SM, White EL (1982) A quantitative study of the thalamocortical and other synapses in layer IV of pyramidal cells projecting from mouse SmI cortex to the caudate-putamen nucleus. J Comp Neurol 211:217–255
Ichikawa M, Arissian K, Asanuma H (1985) Distribution of corticocortical and thalamocortical synapses on identified motor cortical neurons in the cat: Golgi, electron microscopic and degeneration study. Brain Res 345:87–101
Ichikawa M, Arissian K, Asanuma J (1987) Reorganization of the projection from the sensory cortex to the motor cortex following elimination of the thalamic projection to the motor cortex in cats: Golgi, electron microscope and degeneration study. Brain Res 437:131–141
Iriki A, Pavlides C, Keller A, Asanuma H (1989) Long term potentiation in the motor cortex. Science 245:1385–1387
Jasper HH, Ajmone-Marsan C (1954) A stereotaxic atlas of the diencephalon of the cat. National Research Council of Canada, Ottawa
Jones EG, Powell TPS (1968) The ipsilateral cortical connections of the somatic sensory cortex in the cat. Brain Res 9:71–94
Jones EG, Powell TPS (1970) An electron microscopic study of terminal degeneration in the neocortex of the cat. Philos Trans R Soc Lond B 257:29–43
Kluver H, Barrera E (1953) A method for the combined staining of cells and fibers in the nervous system. Exp Neurol 12:400–403
Kosar E, Waters RS, Tsukahara N, Asanuma H (1985) Anatomical and physiological properties of the projection from the sensory cortex to the motor cortex in normal cats: the difference between corticocortical and thalamocortical projections. Brain Res 345:68–78
Lund RD, Lund JS (1971) Modification of synaptic patterns in the superior colliculus of the rat during development and following deafferentation. Vision Res Suppl 3:281–298
Mackel R (1987) The role of the monkey sensory cortex in the recovery from cerebellar injury. Exp Brain Res 66:638–652
McKinley PA, Kruger L (1988) Nonoverlapping thalamocortical connections to normal and deprived primary somatosensory cortex for similar forelimb receptive fields in chronic spinal cats. Somatosen Res 5:311–323
Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1984) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224:591–605
Peters A, Palay SL, Webster HF (1976) The fine structure of the nervous system: the neurons and supporting cells. WB Saunders Co, Philadelphia
Porter L, Sakamoto K (1988) Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat. J Comp Neurol 271:387–396
Raisman G (1969) Neuronal plasticity in the septal nuclei of the adult rat. Brain Res 14:25–48
Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138–1168
Sakamoto T, Arissian K, Asanuma H (1989) Functional role of the sensory cortex in learning motor skills in cats. Brain Res 503:258–264
Sakamoto T, Porter LL, Asanuma H (1987) Long lasting potentiation of synaptic potentials in the motor cortex produced by stimulation of the sensory cortex in the cat: a basis of motor learning. Brain Res 413:360–364
Schwarcz R, Hokfelt T, Fuxe K, Jonsson G, Goldstein M, Terenius L (1979) Ibotenic acid-induced neuronal degeneration: a morphological and neurochemical study. Exp Brain Res 37:199–216
Sloper JJ, Powell TPS (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos Trans R Soc Lond B 285:199–225
Thach WT (1987) Ataxia, cerebellar. In: Adelman G (ed) Encyclopedia of neuroscience. Birkhäuser, Boston, pp 83–86
Travis AM, Woolsey CN (1956) Motor performance of monkeys after bilateral partial and total cerebral decortications. Am J Phys Med 35:273–289
Tsukahara N (1988) Cellular basis of classical conditioning mediated by the red nucleus in the cat. In: Edelman GM, Gall WE, Cowan WM (eds) Synaptic function. J Wiley and Sons, New York, pp 447–469
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 nerves. I. Appearance of new synaptic potentials. Exp Brain Res 45:1–12
Vaughan DW, Peters A (1985) Proliferation of thalamic afferents in cerebral cortex altered by callosal deafferentation. J Neurocytol 14:705–716
Wall JT, Cusick CG (1986) The representation of periperal nerve inputs in the S-1 hindpaw cortex of rats raised with incompletely innervated hinpaws. J Neurosci 6:1129–1147
White EL, Keller A (1987) Intrinsic circuitry involving the local axonal collaterals of corticothalamic projection cells in mouse SmI cortex. J Comp Neurol 26:213–26
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Keller, A., Arissian, K. & Asanuma, H. Formation of new synapses in the cat motor cortex following lesions of the deep cerebellar nuclei. Exp Brain Res 80, 23–33 (1990). https://doi.org/10.1007/BF00228843
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228843