Skip to main content
SpringerLink
Log in

Maturation of evoked climbing fiber input to rat cerebellar Purkinje cells (I.)

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

An analysis of evoked responses of Purkinje cells in developing rat cerebellum to climbing fiber input was conducted to determine which identifying properties of this afferent system are established early in development and which specific features mature with age. Rat pups at various ages were anesthetized with 0.5% halothane and unit recordings made with glass micropipettes. By the third postnatal day, electrical stimulation of the sensorimotor cortex and limbs at low stimulation rates (<1/sec) could elicit distinct burst responses appearing at long latencies (180 msec), indicating that pathways of both ascending and descending climbing fiber systems are intact early in cerebellar cortical development. A distinctive feature maturing over the first 1–1.5 weeks was the characteristic of the all-or-none burst response since before about day 11 the interspike interval, amount of inactivation, and number of spikes in evoked burst responses all varied from stimulation to stimulation. Mean latencies decreased from 180 msec at day 3 to 50 msec by day 10, but did not achieve the adult value of 20 msec until the fourth week. Typically, climbing fiber responses could only follow at stimulation rates of less than 0.2/sec at day 3, but by day 12 could follow up to 10/sec, which is the same as in the adult. The data indicate that the climbing fiber system establishes connectivity from diverse sources and exhibits identifying characteristics similar to the adult early in cerebellar development. Most aspects of the maturation of transmission can be explained if there were a decrease in the time scale of function of the synapses involved, mainly those in the inferior olive.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Addison, W.H.F.: The development of the Purkinje cells and of the cortical layers in the cerebellum of the albino rat. J. comp. Neurol. 21, 459–488 (1911)

    Google Scholar 

  • Allen, G.I., Azzena, G.B., Ohno, T.: Cerebellar Purkinje cell responses to inputs from sensorimotor cortex. Exp. Brain Res. 20, 239–254 (1974)

    Google Scholar 

  • Allen, G.I., Tsukahara, N.: Cerebrocerebellar communication systems. Physiol. Rev. 54, 957–1006 (1974)

    Google Scholar 

  • Altman, J.: Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J. comp. Neurol. 145, 353–398 (1972a)

    Google Scholar 

  • Altman, J.: Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells of the molecular layer. J. comp. Neurol. 145, 399–464 (1972b)

    Google Scholar 

  • Altman, J.: Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer. J. comp. Neurol. 145, 465–514 (1972c)

    Google Scholar 

  • Altman, J., Anderson, W.J.: Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged X-irradiation started at birth. J. comp. Neurol. 146, 355–405 (1972)

    Google Scholar 

  • Armstrong, D.M.: Functional significance of connections of the inferior olive. Physiol. Rev. 59, 358–417 (1974)

    Google Scholar 

  • Armstrong, D.M., Eccles, J.C., Harvey, R.J., Matthews, P.B.C.: Responses in the dorsal accessory olive of the cat to stimulation of hindlimb afferents. J. Physiol. (Lond.) 194, 125–145 (1968)

    Google Scholar 

  • Armstrong-James, M.: The functional status and columnar organization of single cells responding to cutaneous stimulation in neonatal rat somatosensory cortex. SI. J. Physiol. (Lond.) 246, 501–538 (1975)

    Google Scholar 

  • Axelsson, J., Thesleff, S.: A study of supersensitivity in denervated mammalian skeletal muscle. J. Physiol. (Lond.) 147, 178–193 (1959)

    Google Scholar 

  • Bloedel, J.R., Roberts, W.J.: Action of climbing fibers in the cerebellar cortex of the cat. J. Neurophysiol. 34, 17–31 (1971)

    Google Scholar 

  • Crepel, F.: Maturation of climbing fiber responses in the rat. Brain Res. 35, 272–276 (1971)

    Google Scholar 

  • Crepel, F.: Excitatory and inhibitory processes acting upon cerebellar Purkinje cells during maturation in the rat; influence of hypothyroidism. Exp. Brain Res. 20, 403–420 (1974)

    Google Scholar 

  • Crill, W.E.: Unitary multiple-spiked responses in cat inferior olive nucleus. J. Neurophysiol. 33, 199–209 (1970)

    Google Scholar 

  • Del Cerro, M.R., Snider, R.S.: Axo-somatic and axo-dendritic synapses in the cerebellum of the newborn rat. Brain Res. 43, 581–586 (1972)

    Google Scholar 

  • Delhaye-Bouchaud, N., Crepel, F., Mariani, J.: Neurophysiologie. Mise en évidence d'une multiinnervation temporaire des cellules de Purkinje du cervelet par les fibres grimpantes au cours du développement chez le Rat. C.R. Acad. Sci. (Paris) 281, 909–911 (1975)

    Google Scholar 

  • Eccles, J.C., Faber, D.S., Murphy, J.T., Sabah, N.G., Táboříková, H.: Afferent volleys in limb nerves influencing impulse discharges in cerebellar cortex. II. In Purkinje cells. Exp. Brain Res. 13, 36–53 (1971)

    Google Scholar 

  • Eccles, J.C., Ito, M., Szentágothai, J.: The Cerebellum as a Neuronal Machine. p. 335. New York: Springer 1967

    Google Scholar 

  • Eccles, J.C., Llinás, R., Sasaki, K.: The excitatory action of climbing fibers on the Purkinje cells of the cerebellum. J. Physiol. (Lond.) 182, 268–296 (1966)

    Google Scholar 

  • Fox, M., Williams, T.D.: Responses evoked in the cerebellar cortex by stimulation of the caudate nucleus in the cat. J. Physiol. (Lond.) 198, 435–450 (1968)

    Google Scholar 

  • Greene, E.C.: Anatomy of the rat. Trans. Am. Phil. Soc., Vol. 27. New York: Hafner 1968

    Google Scholar 

  • Hall, R.D., Lindholm, E.P.: Organization of motor and somatosensory neocortex in the albino rat. Brain Res. 66, 23–38 (1974)

    Google Scholar 

  • Hubel, D.M., Wiesel, T.N.: Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26, 994–1002 (1963)

    Google Scholar 

  • Huttenlocher, P.R.: Development of cortical neuronal activity in the neonatal cat. Exp. Neurol. 17, 247–262 (1967)

    Google Scholar 

  • Huttenlocher, P.R.: Myelinization and the development of function in immature pyramidal tract. Exp. Neurol. 29, 405–415 (1970)

    Google Scholar 

  • Kitai, S.T., Oshima, T., Provini, L., Tsukahara, N.: Cerebrocerebellar connections mediated by fast and slow conducting pyramidal tract fibres of the cat. Brain Res. 15, 267–271 (1969)

    Google Scholar 

  • Larsell, O.: The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J. comp. Neurol. 97, 281–356 (1952)

    Google Scholar 

  • Llinás R., Baker, R., Sotelo, C.: Electrotonic coupling between neurons in cat inferior olive. J. Neurophysiol. 37, 560–571 (1974)

    Google Scholar 

  • Llinás, R., Hillman, D.E., Precht, W.: Neuronal circuit reorganization in mammalian agranular cerebellar cortex. J. Neurobiol. 4, 69–94 (1973)

    Google Scholar 

  • Murphy, J.T., Sabah, N.H.: Inhibitory effect of climbing fibre activation upon cerebellar Purkinje cells. Brain Res. 19, 486–490 (1970)

    Google Scholar 

  • Oscarsson, O.: Functional organization of spinocerebellar paths. In: Handbook of Sensory Physiology, Vol. II, pp. 339–380 (ed. A. Iggo). New York: Springer 1973

    Google Scholar 

  • Palay, S., Chan-Palay, V.: Cerebellar Cortex: Cytology and Organization. p. 348. New York: Springer 1974

    Google Scholar 

  • Purpura, D.P., Shofer, R.J., Housepain, E.M., Noback, C.R.: Comparative ontogenesis of structure-function relations in cerebral and cerebellar cortex. Progr. Brain Res. 4, 187–221 (1964)

    Google Scholar 

  • Purpura, D.P., Shofer, R.J., Scarff, T.: Properties of synaptic activities and spike potentials of neurons in immature neocortex. J. Neurophysiol. 28, 925–942 (1965)

    Google Scholar 

  • Puro, D.G., Woodward, D.J.: Ontogenesis of the climbing fiber afferent system of the rat cerebellar cortex. Soc. Neurosci. 5, 758 (1975)

    Google Scholar 

  • Puro, D.G., Woodward, D.J.: Maturation of mossy fiber input to rat cerebellar Purkinje cells. Exp. Brain Res. 28 (1977)

  • Rakic, P., Sidman, R.L.: Organization of cerebellar cortex secondary to deficit of granule cells in Weaver mutant. J. comp. Neurol. 152, 133–162 (1973)

    Google Scholar 

  • Retzius, G.: Kleinere Mitteilungen von dem Gebiete der Nervenhistologie. I. Über die Golgischen Zellen und die Kletterfarne Ramón y Cayal's in der Kleinhirnrinde. Biol. Untersuch. N.F. 4, 57 (1892). Referred to by Scheibel and Scheibel (1954)

    Google Scholar 

  • Rubel, E.W.: A comparison of somatotopic organization in sensory neocortex of newborn kittens and adult cats. J. comp. Neurol. 143, 447–480 (1971)

    Google Scholar 

  • Scheibel, M.E., Scheibel, A.B.: Observations on the intracortical relations of the climbing fibers of the cerebellum. J. comp. Neurol. 101, 733–763 (1954)

    Google Scholar 

  • Shofer, R.J., Sax, D.S., Strom, M.G.: Analysis of auditory and cerebrocortically evoked activity in the immature and adult cat cerebellum. In: Neurobiology of Cerebellar Evolution and Development (ed. R. Llinás), pp. 703–717. Chicago: A.M.A. Press 1969

    Google Scholar 

  • Thach, W.T.: Somatosensory receptive fields of single units in cat cerebellar cortex. J. Neurophysiol. 30, 675–696 (1967)

    Google Scholar 

  • Thomas, R.C., Wilson, V.J.: Precise localization of Renshaw cells with a new marking technique. Nature (Lond.) 206, 211–213 (1965)

    Google Scholar 

  • Tsukahara, N., Kosaka, K.: The mode of cerebral excitation of red nucleus neurons. Exp. Brain Res. 5, 102–117 (1968)

    Google Scholar 

  • Walberg, F.: Descending connections to the inferior olive. J. comp. Neurol. 104, 77–173 (1956)

    Google Scholar 

  • Woodward, D.J.: PISH — poststimulus time and interspike interval histogram. Digital Equipment Co. Users Society-Program Library, Decus no. 12–65. Mass.: Maynard 1972

    Google Scholar 

  • Woodward, D.J., Hoffer, B.J., Altman, J.: Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal X-irradiation. J. Neurobiol. 5, 283–304 (1974)

    Google Scholar 

  • Woodward, D.J., Hoffer, B.J., Lapham, L.W.: Postnatal development of electrical and enzyme histochemical activity in Purkinje cells of rat. Exp. Neurol. 23, 120–139 (1969a)

    Google Scholar 

  • Woodward, D.J., Hoffer, B.J., Lapham, L.W.: Correlative survey of electrophysiological, neuropharmacological and histochemical aspects of cerebellar maturation in rat. In: Neurobiology of Cerebellar Evolution and Development (ed. R. Llinás), pp. 725–741. Chicago: A.M.A. Press 1969b

    Google Scholar 

  • Woodward, D.J., Hoffer, B.J., Siggins, G.R., Bloom, F.E.: The ontogenetic development of synaptic junctions, synaptic activation, and responsiveness to neurotransmitter substances in rat cerebellar Purkinje cells. Brain Res. 34, 73–97 (1971)

    Google Scholar 

Download references

Author information

Author notes

  1. D. G. Puro

    Present address: Laboratory of Biochemical Genetics, N.H.L.I., N.I.H., 20014, Bethesda, Maryland, USA

  2. D. J. Woodward

    Present address: Department of Cell Biology, The University of Texas, Health Science Center at Dallas, 5323 Harry Hines Boulevard, 75235, Dallas, Texas, USA

Authors and Affiliations

  1. Department of Physiology, University of Rochester, School of Medicine and Dentistry, 14642, Rochester, New York, USA

    D. G. Puro & D. J. Woodward

Authors
  1. D. G. Puro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. J. Woodward
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by N.I.H. Grant 5-R01-6M00133 and N.S.F. Grant GB 43301

Rights and permissions

Reprints and permissions

About this article

Cite this article

Puro, D.G., Woodward, D.J. Maturation of evoked climbing fiber input to rat cerebellar Purkinje cells (I.). Exp Brain Res 28, 85–100 (1977). https://doi.org/10.1007/BF00237088

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00237088

Key words

Search

Navigation