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Effects of unilateral climbing fibre deafferentation on cytochrome oxidase activity in the developing rat cerebellum

  • Published:
Journal of Neurocytology

Summary

In a previous study, we found a relationship between climbing fibre synaptogenesis and cytochrome oxidase activity in Purkinje cells during normal development of the rat cerebellum. To determine whether removal of a major depolarizing afferent would alter the level of cytochrome oxidase activity in a post-synaptic neuron, climbing fibre input to Purkinje cells in the right hemicerebellum was interrupted by unilateral pedunculotomy in postnatal day 1 rat pups. After survival to postnatal day 5 (P5) or postnatal day 10 (P10), the cytochrome oxidase reactivity of mitochondria, packing density of mitochondria and perikaryal area of Purkinje cell somata were quantitifed at the electron microscopic level and compared with the same parameters in both sham-operated animals and normal controls. We found that the areal and numerical densities of darkly reactive mitochondria were lower in deafferented cells than those in the sham-operated animals. Cells of sham-operated animals, however, had higher densities of darkly reactive mitochondria than those in normal animals of the same age group, indicating that cell shrinkage or retarded growth had an effect on the levels of cytochrome oxidase activity in the operated animals. In addition, both operated groups had higher numerical densities of mitochondria than cells of normal animals, reflecting the decreased cell size of the sham and deafferented groups. From these data, we concluded that neonatal destruction of climbing fibres leads to lower levels of cytochrome oxidase activity in Purkinje cell somata that survived to both P5 and P10. The data from the P5 animals was more striking than that from P10, perhaps reflecting the increased number of synaptic interactions of Purkinje cells at P10. We also concluded that destruction of excitatory input did not lead to changes in the total area or number of mitochondria in a post-synaptic neuron, indicating that there was a conversion from darkly to lightly reactive mitochondria in the partially deafferented neurons; however, this may also reflect the smaller cell size of the deafferented group. Thus, our results further substantiate the close relationship between the levels of cytochrome oxidase activity in Purkinje cell somata and the type of input that they receive or fail to receive.

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References

  • Altman, J., Das, G. D. &Sudarshan, K. (1970) The influence of nutrition on neural and behavioral development. I. Critical review of some data on the growth of the body and the brain following dietary deprivation during gestation and lactation.Developmental Psychobiology 3, 281–301.

    Google Scholar 

  • Angaut, P., Alvarado-Mallart, R. M. &Sotelo, C. (1982) Ultrastructural evidence for compensatory sprouting of climbing and mossy afferents to the cerebellar hemisphere after ipsilateral pedunculotomy in the newborn rat.Journal of Comparative Neurology 205, 101–11.

    Google Scholar 

  • Angaut, P., Alvarado-Mallart, R. M. &Sotelo, C. (1985) Compensatory climbing fiber innervation after unilateral pedunculotomy in the newborn rat, origin and topographic organization.Journal of Comparative Neurology 236, 161–78.

    Google Scholar 

  • Bachelard, H. S. (1975) Energy used by neurotransmitters. InBrain Work (edited byIngvar, D. H. &Lassen, N. A.) pp. 79–81. New York: Academic Press.

    Google Scholar 

  • Baetans, D., Garcia-Segura, L. M. &Perrelet, A. (1982) Effects of climbing fiber destruction on large dendritic spines of Purkinje cells.Experimental Brain Research 48, 256–62.

    Google Scholar 

  • Baetans, D., Tribollet, E. &Garcia-Segura, L. M. (1983) colchicine injection in the inferior olivary nucleus increases the number of Purkinje cell dendritic spines.Neuroscience Letters 38, 239–44.

    Google Scholar 

  • Bardin, J. M., Batini, C., Billard, J. M., Buisseretdelmas, C., Conrath-Verrier, J. &Corvaja, N. (1983) Cerebellar output regulation by the climbing and mossy fibers with and without the inferior olive.Journal of Comparative Neurology 213, 464–77.

    Google Scholar 

  • Barnes, D. &Altman, J. (1973) Effects of different schedules of early undernutrition on the preweaning growth of the rat cerebellum.Experimental Neurology 38, 406–19.

    Google Scholar 

  • Batini, C., Benedetti, F., Buisseret-Dellmas, C., Montarolo, P. G. &Strata, P. (1984) Metabolic activity of intracerebellar nuclei in the rat: effects of inferior olivary inactivation.Experimental Brain Research 54, 259–65.

    Google Scholar 

  • Batini, C. &Billard, J. M. (1985) Release of cerebellar inhibition by climbing fiber deafferentation.Experimental Brain Research.57, 370–80.

    Google Scholar 

  • Benedetti, F., Montarolo, P. G. &Rabacchi, S. (1984) Inferior olive lesion induces long-lasting functional modification in the Purkinje cells.Experimental Brain Research 55, 368–71.

    Google Scholar 

  • Billard, J. M. &Daniel, H. (1988) Persistent reduction of Purkinje cell inhibition on neurons of the cerebellar nuclei after climbing fiber deafferentation.Neuroscience Letters 88, 21–6.

    Google Scholar 

  • Bourrat, F. &Sotelo, C. (1988) Migratory pathways and neuritic differentiation of inferior olivary neurons in the rat embryo. Axonal tracing study using thein vitro slab technique.Developmental Brain Research 39, 19–37.

    Google Scholar 

  • Bower, A. J. &Payne, J. N. (1987) An ipsilateral olivocerebellar pathway in the normal neonatal rat demonstrated by retrograde transport of True blue.Neuroscience Letters 78, 138–44.

    Google Scholar 

  • Bower, A. J. &Waddington, G. (1981) A simple operative technique for chronically severing the cerebellar peduncles in neonatal rats.Journal of Neuroscience Methods 4, 181–8.

    Google Scholar 

  • Carroll, E. W. &Wong-Riley, M. T. T. (1984) Quantitative light and electron microscopic analysis of cytochrome oxidase rich zones in the striate cortex of the squirrel monkey.Journal of Comparative Neurology 222, 1–17.

    Google Scholar 

  • Chan-Palay, V. &Palay, S. L. (1970) Interrelationships of basket cell axons and climbing fibers in the cerebellar cortex of the rat.Zeitschrift für Anatatomie und EntwicklungsGeschichte 132, 191–227.

    Google Scholar 

  • Colin, F., Manil, J. &Desclin, J. C. (1980) The olivocerebellar system. I. Delayed and slow inhibitory effects, an overlooked salient feature of cerebellar climbing fibers.Brain Research 187, 3–27.

    Google Scholar 

  • Crepel, F. (1971) Maturation of climbing fiber responses in the rat.Brain Research 35, 272–6.

    Google Scholar 

  • Crepel, F., Delhaye-Bouchaud, N. &Dupont, J. L. (1981) Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats.Developmental Brain Research 1, 59–71.

    Google Scholar 

  • Creutzfeldt, O. D. (1975) Neurophysiological correlates of different functional states of the brain. InBrain Work (edited byIngvar, D. H. &Lassen, N. A.) pp. 21–47. New York: Academic Press.

    Google Scholar 

  • Desclin, J. C., &Colin, F. (1980) The olivocerebellar system II. Some ultrastructural correlates of inferior olivary destruction in rats.Brain Research 187, 29–46.

    Google Scholar 

  • Hevner, R. F. &Wong-Riley, M. (1989) Brain cytochrome oxidase: Purification, antibody production and immunohistochemical/histochemical correlations in the CNS.Journal of Neuroscience 9, 3884–98.

    Google Scholar 

  • Kageyama, G. H. &Wong-Riley, M. T. T. (1982) Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways.Neuroscience 7, 2337–61.

    Google Scholar 

  • Kawaguchi, S., Yamamoto, T., Mizuno, N. &Iwahora, N. (1975) The role of climbing fibers in the development of Purkinje cell dendrites.Neuroscience Letters 1, 301–4.

    Google Scholar 

  • Kornguth, S. E. &Scott, G. (1972) The role of climbing fibers in the formation of Purkinje cell dendrites.Journal of Comparative Neurology 146, 61–82.

    Google Scholar 

  • Larramendi, L. M. H. &Victor, T. (1967) Synapses on the Purkinje cell spines in the mouse: an electromicroscopic study.Brain Research 5, 15–30.

    Google Scholar 

  • Larsell, O. (1952) The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat.Journal of Comparative Neurology 97, 281–356.

    Google Scholar 

  • Llinas, R., Walton, K., Hillman, D. E. &Sotelo, C. (1975) Inferior Olive: Its role in motor learning.Science 190, 1230–1.

    Google Scholar 

  • McConnell, P. &Berry, M. (1978) The effects of undernutrition on Purkinje cell dendritic growth in the rat.Journal of Comparative Neurology 177, 159–72.

    Google Scholar 

  • Mariani, J. &Changeux, J. P. (1981) Ontogenesis of olivo-cerebellar relationships. 1. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum.Journal of Neuroscience 1, 696–702.

    Google Scholar 

  • Mason, C. A. &Gregory, E. (1984) Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons.Journal of Neuroscience 4, 1715–35.

    Google Scholar 

  • Mawe, G. M. &Gershon, M. D. (1986) Functional heterogeneity in the myenteric plexus: demonstration using cytochrome oxidase as a verified probe of the activity of individual enteric neurons.Journal of Comparative Neurology 249, 381–91.

    Google Scholar 

  • Mjaatvedt, A. E. &Wong-Riley, M. T. T. (1988) The relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum.Journal of Comparative Neurology 277, 155–82.

    Google Scholar 

  • Palay, S. L. &Chan-Palay, V. (1974)Cerebellar Cortex. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • Rossi, F., Cantino, D. &Strata, P. (1987) Morphology of Purkinje cell axon terminals in intracerebellar nuclei following inferior olive lesion.Neuroscience 1, 99–112.

    Google Scholar 

  • Savio, T., &Tempia, F. (1985) On the Purkinje cell activity increase induced by suppression of inferior olive activity.Experimental Brain Research 57, 456–63.

    Google Scholar 

  • Skou, J. C. (1965) enzymatic basis for active transport of sodium and potassium across cell membrane.Physiological Reviews 45, 596–617.

    Google Scholar 

  • Sotelo, C. (1978) Purkinje cell ontogeny: formation and maintenance of spines.Progress in Brain Research 48, 149–70.

    Google Scholar 

  • Sotelo, C. &Arsenio-Nunes, M. L. (1976) Development of Purkinje cells in absence of climbing fibers.Brain Research 111, 389–95.

    Google Scholar 

  • Sotelo, C., Hillman, D. E., Zamora, A. J. &Llinas, R. (1975) Climbing fiber deafferentation: its action on Purkinje cell spines.Brain Research 98, 574–81.

    Google Scholar 

  • Wong-Riley, M. T. T. (1979) changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry.Brain Research 171, 11–28.

    Google Scholar 

  • Wong-Riley, M. T. T. (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity.Trends in Neurosciences 12, 94–101.

    Google Scholar 

  • Wong-Riley, M. T. T., Leake-Jones, P. A., Walsh, S. M. &Merzenich, M. M. (1981) Maintenance of neuronal activity by electrical stimulation of unilaterally deafened cats demonstrable with cytochrome oxidase technique.Annals of Otology, Rhinology and Laryngology 90 (Suppl. 82), 30–2.

    Google Scholar 

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  1. A. E. Mjaatvedt

    Present address: Developmental Genetics Laboratory, Department of Physiology, Johns Hopkins University School of Medicine, 725 N. Wolfe Street, 21205, Baltimore, MD, USA

Authors and Affiliations

  1. Department of Anatomy and Cellular Biology, Medical College of Wisconsin, 8701 Watertown Plank Road, 53226, Milwaukee, Wisconsin, USA

    A. E. Mjaatvedt & M. T. T. Wong-Riley

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  1. A. E. Mjaatvedt
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  2. M. T. T. Wong-Riley
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Mjaatvedt, A.E., Wong-Riley, M.T.T. Effects of unilateral climbing fibre deafferentation on cytochrome oxidase activity in the developing rat cerebellum. J Neurocytol 20, 2–16 (1991). https://doi.org/10.1007/BF01187130

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  • DOI: https://doi.org/10.1007/BF01187130

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