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PMID: 8987739 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: a modeling study.

Jaeger D, De Schutter E, Bower JM

Abstract

We have used a realistic computer model to examine interactions between synaptic and intrinsic voltage-gated currents during somatic spiking in cerebellar Purkinje cells. We have shown previously that this model generates realistic in vivo patterns of somatic spiking in the presence of continuous background excitatory and inhibitory input (). In the present study, we analyzed the flow of synaptic and intrinsic currents across the dendritic membrane and the interaction between the soma and dendrite underlying this spiking behavior. This analysis revealed that: (1) dendritic inward current flow was dominated by a noninactivating P-type calcium current, resulting in a continuous level of depolarization; (2) the mean level of this depolarization was controlled by the mean rate of excitatory and inhibitory synaptic input; (3) the synaptic control involved a voltage-clamping mechanism exerted by changes of synaptic driving force at different membrane potentials; (4) the resulting total current through excitatory and inhibitory synapses was near-zero, with a small outward bias opposing the P-type calcium current; (5) overall, the dendrite acted as a variable current sink with respect to the soma, slowing down intrinsic inward currents in the soma; (6) the somato-dendritic current showed important phasic changes during each spike cycle; and (7) the precise timing of somatic spikes was the result of complex interactions between somatic and dendritic currents that did not directly reflect the timing of synaptic input. These modeling results suggest that Purkinje cells act quite differently from simple summation devices, as has been assumed previously in most models of cerebellar function. Specific physiologically testable predictions are discussed.

MeSH Terms
Action Potentials Animals Electric Conductivity Electric Stimulation Electrophysiology Guinea Pigs Models, Neurological Purkinje Cells/physiology Synapses/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Jaeger D
Division of Biology, California Institute of Technology, Pasadena, California 91125, USA.
De Schutter E
Bower J M
References (41)
41 references, click to expand
  1. Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat?
    Prog Brain Res. 1997;114:463-96 PMID: 9193161
  2. Quantitative studies on the mammalian cerebellum.
    Prog Neurobiol. 1991;36(6):437-63 PMID: 1947173
  3. Sodium and potassium conductances in somatic membranes of rat Purkinje cells from organotypic cerebellar cultures.
    J Physiol. 1989 Oct;417:105-22 PMID: 2559965
  4. Modelling the cerebellar Purkinje cell: experiments in computo.
    Prog Brain Res. 1994;102:427-41 PMID: 7800831
  5. Noise, neural codes and cortical organization.
    Curr Opin Neurobiol. 1994 Aug;4(4):569-79 PMID: 7812147
  6. An active membrane model of the cerebellar Purkinje cell II. Simulation of synaptic responses.
    J Neurophysiol. 1994 Jan;71(1):401-19 PMID: 8158238
  7. Physiology, morphology and detailed passive models of guinea-pig cerebellar Purkinje cells.
    J Physiol. 1994 Jan 1;474(1):101-18 PMID: 8014888
  8. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs.
    J Neurosci. 1993 Jan;13(1):334-50 PMID: 8423479
  9. Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons.
    J Neurosci Methods. 1993 Sep;49(3):157-65 PMID: 7903728
  10. Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex.
    J Neurosci. 1993 Feb;13(2):660-73 PMID: 8381170
  11. Integrator or coincidence detector? The role of the cortical neuron revisited.
    Trends Neurosci. 1996 Apr;19(4):130-7 PMID: 8658595
  12. Reliability of spike timing in neocortical neurons.
    Science. 1995 Jun 9;268(5216):1503-6 PMID: 7770778
  13. Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):4736-40 PMID: 8197127
  14. Simple codes versus efficient codes.
    Curr Opin Neurobiol. 1995 Apr;5(2):239-47 PMID: 7620313
  15. Dendritic spikes and their inhibition in alligator Purkinje cells.
    Science. 1968 Jun 7;160(3832):1132-5 PMID: 5647436
  16. Identification of cell types from action potential waveforms: cerebellar granule cells.
    Brain Res. 1993 Aug 13;619(1-2):313-8 PMID: 8374786
  17. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons.
    Nature. 1995 Jan 12;373(6510):155-8 PMID: 7816097
  18. An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice.
    J Neurophysiol. 1994 Jan;71(1):375-400 PMID: 7512629
  19. Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus.
    J Physiol. 1990 Sep;428:707-22 PMID: 2231430
  20. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices.
    J Physiol. 1980 Aug;305:197-213 PMID: 7441553
  21. Multiple voltage-sensitive K+ channels regulate dendritic excitability in cerebellar Purkinje neurons.
    Neurosci Lett. 1989 Feb 13;97(1-2):97-102 PMID: 2563909
  22. 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. 1983 Mar;49(3):745-66 PMID: 6300353
  23. Adaptive filter model of the cerebellum.
    Biol Cybern. 1982;45(3):195-206 PMID: 7171642
  24. Initiation and spread of sodium action potentials in cerebellar Purkinje cells.
    Neuron. 1994 Sep;13(3):703-12 PMID: 7917300
  25. Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices.
    J Physiol. 1991 Mar;434:183-213 PMID: 1673717
  26. Total numbers of various cell types in rat cerebellar cortex estimated using an unbiased stereological method.
    Brain Res. 1993 Apr 23;609(1-2):262-8 PMID: 8508308
  27. Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis.
    J Neurosci. 1991 Jul;11(7):2259-69 PMID: 1712382
  28. Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation.
    J Neurophysiol. 1992 Oct;68(4):1167-77 PMID: 1432076
  29. A theory of cerebellar cortex.
    J Physiol. 1969 Jun;202(2):437-70 PMID: 5784296
  30. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices.
    J Neurosci. 1994 Aug;14(8):4613-38 PMID: 8046439
  31. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices.
    J Physiol. 1980 Aug;305:171-95 PMID: 7441552
  32. P-type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells.
    Neuron. 1992 Dec;9(6):1185-99 PMID: 1281419
  33. Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat.
    J Comp Neurol. 1988 Aug 8;274(2):168-77 PMID: 3209740
  34. Cerebellar long-term depression might normalize excitation of Purkinje cells: a hypothesis.
    Trends Neurosci. 1995 Jul;18(7):291-5 PMID: 7571005
  35. RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON.
    Biophys J. 1964 Jan;4:41-68 PMID: 14104072
  36. Dynamic clamp: computer-generated conductances in real neurons.
    J Neurophysiol. 1993 Mar;69(3):992-5 PMID: 8463821
  37. Calcium-induced calcium release in cerebellar Purkinje cells.
    Neuron. 1994 Mar;12(3):663-73 PMID: 7512352
  38. Experimental evaluation of input-output models of motoneuron discharge.
    J Neurophysiol. 1996 Jan;75(1):367-79 PMID: 8822564
  39. 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. 1994;100(2):200-14 PMID: 7813659
  40. Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization.
    J Physiol. 1992 Oct;456:453-71 PMID: 1293282
  41. Voltage-imaging and simulation of effects of voltage- and agonist-activated conductances on soma-dendritic voltage coupling in cerebellar Purkinje cells.
    J Comput Neurosci. 1994 Dec;1(4):301-11 PMID: 8792236
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-01-01
Pages
91-106
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793698
Subset
IM
Grants
NINDS NIH HHS · NS-31378 · United States
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