Skip to main content
SpringerLink
Log in

Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We obtained intracellular recordings of 84 Purkinje cells in vitro from guinea pig slices and of 35 cells in vivo from ketamine-anesthetized rats in order to assess detailed properties of synaptic responses in Purkinje cells following granule cell activation. In vitro, electrical stimulation of the granule cell layer underlying recorded Purkinje cells was used in sagittal slices to predominantly activate synapses on ascending granule cell axons. In vivo, stimulation of the upper lip was used to activate Purkinje cells overlying the upper lip patch in the granule cell layer of crus IIa. In the presence of a GABAA antagonist, Purkinje cells at resting membrane potential responded to both electrical stimulation in vitro and peripheral stimulation in vivo, with a depolarization of 1–10 mV amplitude that lasted for 100–300 ms in the absence of climbing fiber input. Similar prolonged depolarizations could also be induced by brief depolarizing current pulses delivered through the recording electrode, demonstrating that either synaptic or direct depolarization may activate inward currents leading to a sustained response. In support of this hypothesis we found that prolonged depolarizations were shortened significantly when stimulation in the granule cell layer or intracellular current pulses were delivered during hyperpolarizing current steps. Stimulation in the granule cell layer or intracellular current pulses delivered during periods of spontaneous somatic spiking resulted in prolonged depolarizations in dendritic recordings, which were accompanied by an increase in somatic spiking frequency. Following upper lip stimulation in vivo, this increase in somatic spiking was interrupted by an inhibition of 10–50 ms duration. In a majority of recordings, this inhibition did not completely abolish prolonged depolarizations, however, and a delayed increase in somatic spike frequency was still observed. These results suggest that prolonged increases in Purkinje cell spike frequency following peripheral stimulation are due to an underlying prolonged dendritic depolarization induced by granule cell input. Further, a single, short burst of input via ascending granule cell axons appears to be sufficient to induce these responses.

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

  • Aalto TK, Raivio KO (1990) Adenine nucleotide depletion from endothelial cells exposed to xanthine oxidase. Am J Physiol 259:C883-C888

    Google Scholar 

  • Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61

    Google Scholar 

  • Ascher P, Nowak L (1988) The role of divalent cations in the N-methyl-d-aspartate responses of mouse central neurones in culture. J Physiol (Lond) 399:247–266

    Google Scholar 

  • Batchelor AM, Garthwaite J (1993) Novel synaptic potentials in cerebellar Purkinje cells: probable mediation by metabotropic glutamate receptors. Neuropharmacology 32:11–20

    Google Scholar 

  • Bishop GA (1993) An analysis of HRP-filled basket cell axons in the cat's cerebellum. I. Morphometry and configuration. Anat Embryol 188:287–297

    Google Scholar 

  • Bisti S, Iosif G, Marchesi GF, Strata P (1971) Pharmacological properties of inhibitions in the cerebellar cortex. Exp Brain Res 14:24–37

    Google Scholar 

  • Bower JM, Kassel J (1990) Variability in tactile projection patterns to cerebellar folia crus-IIa of the Norway rat. J Comp Neurol 302:768–778

    Google Scholar 

  • Bower JM, Woolston DC (1983) Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 49:745–765

    Google Scholar 

  • Braitenberg V, Atwood R (1958) Morphological observations on the cerebellar cortex. J Comp Neurol 109:1–33

    Google Scholar 

  • Campbell NC, Hesslow G (1984) Plateau potentials evoked by climbing-fibre stimulation are restricted to the Purkinje cell dendrites of the cat. Neurosci Lett 45:187–192

    Google Scholar 

  • Campbell NC, Ekerot C-F, Hesslow G, Oscarsson O (1983a) Dendritic plateau potentials evoked in Purkinje cells by parallel fibre volleys in the cat. J Physiol (Lond) 340:209–223

    Google Scholar 

  • Campbell NC, Ekerot C-F, Hesslow G (1983b) Interaction between responses in Purkinje cells evoked by climbing fibre impulses and parallel fibre volleys in the cat. J Physiol (Lond) 340:225–238

    Google Scholar 

  • Crepel F, Audinat E (1991) Excitatory amino acid receptors of cerebellar Purkinje cells: development and plasticity. Prog Biophys Molec Biol 55:31–46

    Google Scholar 

  • Crepel F, Jaillard D (1991) Pairing of pre- and postsynaptic activities in cerebellar Purkinje cells induces long-term changes in synaptic efficacy in vitro. J Physiol (Lond) 432:123–141

    Google Scholar 

  • Crepel F, Daniel H, Hemart N, Jaillard D (1991) Effects of ACPD and AP3 on parallel-fibre-mediated EPSPs of Purkinje cells in cerebellar slices in vitro. Exp Brain Res 86:402–406

    Google Scholar 

  • De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. J Neurophysiol 71:375–400

    Google Scholar 

  • Dupont JL, Crepel F, Delhaye-Bouchaud N (1979) Influence of bicuculline and picrotoxin on reversal properties of excitatory synaptic potentials in cerebellar Purkinje cells of the rat. Brain Res 173:577–580

    Google Scholar 

  • Eccles JC, Llinás R, Sasaki K (1966a) Intracellularly recorded responses of the cerebellar Purkinje cell. Exp Brain Res 1:161–183

    Google Scholar 

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

    Google Scholar 

  • Ekerot C-F, Oscarsson O (1981) Prolonged depolarization elicited in Purkinje cell dendrites by climbing fibre impulses in the cat. J Physiol (Lond) 318:207–221

    Google Scholar 

  • Farrant M, Cull-Candy SG (1991) Excitatory amino acid receptor-channels in Purkinje cells in thin cerebellar slices. Proc R Soc Lond [Biol] 244:179–184

    Google Scholar 

  • Fujita M (1982) Simulation of adaptive modification of the vestibulo-ocular reflex with an adaptive filter model of the cerebellum. Biol Cybern 45:207–214

    Google Scholar 

  • Garwicz M, Andersson G (1992) Spread of synaptic activity along parallel fibres in cat cerebellar anterior lobe. Exp Brain Res 88:615–622

    Google Scholar 

  • Glaum SR, Slater NT, Rossi DJ, Miller RJ (1992) Role of metabotropic glutamate (ACPD) receptors at the parallel fiber-Purkinje cell synapse. J Neurophysiol 68 (4): 1453–1462

    Google Scholar 

  • Gruol DL, Dionne VE, Yool AJ (1989) Multiple voltage-sensitive K+ channels regulate dendritic excitability in cerebellar Purkinje neurons. Neurosci Lett 97:97–102

    Google Scholar 

  • Gruol DL, Jacquin T, Yool AJ (1991) Single-channel K+ currents recorded from the somatic and dendritic regions of cerebellar Purkinje neurons in culture. J Neurosci 11:1002–1015

    Google Scholar 

  • Gundappa-Sulur G, Bower JM (1990) Differences in ultramorphology and dendritic termination sites of synapses associated with the ascending and parallel fiber segments of granule cell axons in the cerebellar cortex of the albino rat. Soc Neurosci Abstr 16 (1): 896

    Google Scholar 

  • Harvey RJ, Napper RMA (1988) Quantitative study of granule and Purkinje cells in the cerebellar cortex of the rat. J Comp Neurol 274:151–157

    Google Scholar 

  • Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990) Analysis of excitatory synaptic action in pyramidal cells using whole-cell recordings from rat hippocampal slices. J Physiol (Lond) 422:203–225

    Google Scholar 

  • Hillman D, Chen S, Aung TT, Cherksey B, Sugimori M, Llinás R (1991) Localization of P-type calcium channels in the central nervous system. Proc Natl Acad Sci USA 88:7076–7080

    Google Scholar 

  • Hussain S, Gardner CR, Bagust J, Walker RJ (1991) Receptor sub-types involved in responses of Purkinje cell to exogenous excitatory amino acids and local electrical stimulation in cerebellar slices in the rat. Neuropharmacology 30 (10): 1029–1037

    Google Scholar 

  • Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85–102

    Google Scholar 

  • Kaneda M, Wakamori M, Akaike N (1989) GABA-induced chloride current in rat isolated Purkinje cells. Am J Physiol 256:C1153-C1159

    Google Scholar 

  • Kanerva P (1988) Sparse distributed memory. MIT Press

  • Kawaguchi Y (1992) Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments, and excitatory postsynaptic currents. J Neurophysiol 67:1669–1682

    Google Scholar 

  • King JS, Chen YF, Bishop GA (1993) An analysis of HRP-filled basket cell axons in the cat's cerebellum. II. Axonal distribution. Anat Embryol 188:299–305

    Google Scholar 

  • Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci USA 87:2662–2665

    Google Scholar 

  • Larson-Prior LJ, McCrimmon DR, Slater NT (1990) Slow excitatory amino acid receptor-mediated synaptic transmission in turtle cerebellar Purkinje cells. J Neurophysiol 63:637–650

    Google Scholar 

  • Lee M, Bower JM (1991) Temporal and spatial organization of climbing fiber tactile responses in rat cerebellar cortex. Soc Neurosci Abstr 17(2): 1383

    Google Scholar 

  • Llano I, Marty A, Armstrong CM, Konnerth A (1991) Synapticand agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol (Lond) 434:183–213

    Google Scholar 

  • Llinás R (1982) Radial Connectivity in the cerebellar cortex: a novel view regarding the functional organization of the molecular layer. Exp Brain Res [Suppl] 6:189–194

    Google Scholar 

  • Llinás R, Sugimori M (1992) The electrophysiology of the cerebellar Purkinje cell revisited. In: Llinás R, Sotelo C (eds) The cerebellum revisited. Springer Berlin Heidelberg New York, pp167–181

    Google Scholar 

  • Llinás R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171–195

    Google Scholar 

  • Llinás R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197–213

    Google Scholar 

  • Llinás R, Sugimori M, Lin J-W, Cherksey B (1989) Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci USA 86:1689–1693

    Google Scholar 

  • Llinás R, Sugimori M, Hillman DE, Cherksey B (1992) Distribution and functional significance of the P-type, voltage-dependent Ca2+ channels in the mammalian central nervous system. Trends Neurosci 15:351–355

    Google Scholar 

  • Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437–470

    Google Scholar 

  • Martinez FE, Crill WE, Kennedy TT (1971) Electrogenesis of cerebellar Purkinje cell responses in cats. J Neurophysiol 34:348–356

    Google Scholar 

  • Morissette J, Lee M, Bower JM (1991) Temporal relationships between cerebral cortical and cerebellar responses to tactile stimulation in the rat. Soc Neurosci Abstr 17 (2): 1383

    Google Scholar 

  • Napper RMA, Harvey RJ (1988) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168–177

    Google Scholar 

  • Palay SL, Chan-Palay V (1982) The cerebellum: new vistas. Exp Brain Res [Suppl] 6

  • Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991) Excitatory transmission in the basolateral amygdala. J Neurophysiol 66:986–998

    Google Scholar 

  • Regan LJ (1991) Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis. J Neurosci 11:2259–2269

    Google Scholar 

  • Sakurai M (1987) Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J Physiol (Lond) 394:463–480

    Google Scholar 

  • Sato Y, Miura A, Fushiki H, Kawasaki T (1993) Barbiturate depresses simple spike activity of cerebellar Purkinje cells after climbing fiber input. J Neurophysiol 69:1082–1090

    Google Scholar 

  • Shambes GM, Gibson JM, Welker W (1978) Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15:94–140

    Google Scholar 

  • Staub C, Vranesic I, Knöpfel T (1992) Responses to metabotropic glutamate receptor activation in cerebellar Purkinje cells: induction of an inward current. Eur J Neurosci 4:832–839

    Google Scholar 

  • Thompson JH, Bower JM (1991) Prolonged simple spike responses to activation of the granule cell layer in the rat cerebellum. Soc Neurosci Abstr 17 (2): 1383

    Google Scholar 

  • Thompson RF (1986) The neurobiology of learning and memory. Science 233:941–947

    Google Scholar 

  • Usowicz MM, Sugimori M, Cherksey B, Llinás R (1992) P-type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron 9:1185–1199

    Google Scholar 

  • Welker W (1987) Spatial organization of somatosensory projections to granule cell cerebellar cortex: functional and connectional implications of fractured somatotopy (summary of Wisconsin studies). In: New concepts in cerebellar neurobiology. Liss, New York, pp 239–280

    Google Scholar 

  • Winn P, Stone TW, Latimer M, Hastings MH, Clark AJM (1991) A comparison of excitotoxic lesions of the basal forebrain by kainate, quinolinate, ibotenate, N-methyl-d-aspartate or quisqualate, and the effects of toxicity of 2-amino-5-phosphonovaleric acid and kynurenic acid in the rat. Br J Pharmacol 102:904–908

    Google Scholar 

  • Yool AJ, Krieger RM, Gruol DL (1992) Multiple ionic mechanisms are activated by the potent agonist quisqualate in cultured cerebellar Purkinje neurons. Brain Res 573:83–94

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Biology 216-76, California Institute of Technology, 91125, Pasadena, CA, USA

    Dieter Jaeger & James M. Bower

Authors
  1. Dieter Jaeger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James M. Bower
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jaeger, D., Bower, J.M. Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation. Exp Brain Res 100, 200–214 (1994). https://doi.org/10.1007/BF00227191

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227191

Key words

Search

Navigation