Skip to main content
Log in

Voltage-imaging and simulation of effects of voltage- and agonist-activated conductances on soma-dendritic voltage coupling in cerebellar Purkinje cells

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

We investigated the spread of membrane voltage changes from the soma into the dendrites of cerebellar Purkinje cells by using voltage-imaging techniques in combination with intracellular recordings and by performing computer simulations using a detailed compartmental model of a cerebellar Purkinje cell. Fluorescence signals from single Purkinje cells in cerebellar cultures stained with the styryl dye di-4-ANEPPS were detected with a 10 × 10 photodiode array and a charge coupled device (CCD). Fluorescence intensity decreased and increased with membrane depolarization and hyperpolarization, respectively. The relation between fractional fluorescence change (ΔF/F) and membrane potential could be described by a linear function with a slope of up to − 3%/100 mV. Hyperpolarizing and depolarizing voltage jumps applied to Purkinje cells voltage-clamped with an intrasomatic recording electrode induced dendritic dye signals, demonstrating that these voltage transients invaded the dendrites. Dye signals induced by depolarizing somatic voltage jumps were weaker in the dendrites, when compared with those induced by hyperpolarizing voltage jumps. Dendritic responses to hyperpolarizing voltage steps applied at the soma were attenuated when membrane conductance was increased by muscimol, an agonist for GABAAreceptors.

Corresponding experimental protocols were applied to a previously developed detailed compartmental model of a Purkinje cell. In the model, as in the electrophysiological recordings, voltage attenuation from soma to dendrites increased under conditions where membrane conductance is increased by depolarization or by activation of GABAA receptors, respectively.

We discuss how these results affect voltage clamp studies of synaptic currents and synaptic integration in Purkinje cells.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bernander Ö, Douglas R, Martin KAC, and Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. cad. Sci. 88:11569–11573.

    Google Scholar 

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

    PubMed  Google Scholar 

  • De Schutter E and Bower J (1994b) An active membrane model of the cerebellar Purkinje cell: II. Simulation of synaptic responses. J. Neurophysiol. 71:401–419.

    PubMed  Google Scholar 

  • Ehrenberg B, Farkas DL, Fluhler EN, Lojewska Z, and Loew LM (1987) Membrane potential induced by external electric field pulses can be followed with a potentiometric dye. Biophys. J. 51:833–837.

    PubMed  Google Scholar 

  • Fromherz P and Lambacher A (1991) Spectra of voltage-sensitive fluorescence of styryl-dye in neuron membrane. Biochim. Biophys. Acta 1068:149–156.

    PubMed  Google Scholar 

  • Gähwiler BH and Knöpfel T (1990) Cultures of brain slices. In Preparations of Vertebrate Central Nervous System in Vitro, ed. by H. Jahnsen, John Wiley & Sons Ltd. GB-Chichester, pp. 77–100.

    Google Scholar 

  • Gähwiler BH and Llano I (1989) Sodium and potassium conductances in somatic membranes of rat Purkinje cells from organotypic cerebellar cultures. J. Physiol. 417:105–122.

    PubMed  Google Scholar 

  • Grinvald A, Salzberg BM, Lev-Ram V, and Hildesheim R (1987) Optical recording of synaptic potentials from processes of single neurons using intracellular potentiometric dyes. Biophys. J. 51:643–651.

    PubMed  Google Scholar 

  • Grinvald A, Frostig RD, Lieke E, and Hildesheim R (1988) Optical imaging of neuronal activity. Physiol. Rev. 68:1285–1366.

    PubMed  Google Scholar 

  • Gross D, Loew LM, and Webb WW (1987) Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys. J. 50:339–348.

    Google Scholar 

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

    Google Scholar 

  • Hackett JT, Hou S-M, and Cochran SL (1979) Glutamate and synaptic depolarization of Purkinje cells evoked by parallel fibers and by climbing fibers. Brain. Res. 170:377–380.

    PubMed  Google Scholar 

  • Jack JJ, Noble D, and Tsien RW (1975) Electric Current Flow in Excitable Cells. Clarendon Press. Oxford.

    Google Scholar 

  • Knöpfel T, Kasper HJ, Kohler B, Zglinski Z, Zeller L, and Gähwiler BH (1988) Optical recording of neuronal activity in organotypic slice cultures. Soc. Neurosci. Abstr. 14:247. (Abstract)

    Google Scholar 

  • Knöpfel T, Audinat E, and Gähwiler BH (1990a) Climbing fiber responses in olivo-cerebellar slice cultures. I. Microelectrode recordings from Purkinje cells. Eur. J. Neurosci. 2:726–732.

    PubMed  Google Scholar 

  • Knöpfel T, Staub C, and Gähwiler BH (1990b) Spatial spread of voltage transients in cerebellar Purkinje cells. Soc. Neurosci. Abstr. 16:636. (Abstract)

    Google Scholar 

  • Knöpfel T, Vranesic I, Staub C, and Gähwiler BH (1991) Climbing fibre responses in olivo-cerebellar slice cultures. II. Dynamics of cytosolic calcium in Purkinje cells. Eur. J. Neurosci. 3:343–348.

    PubMed  Google Scholar 

  • Koch C, Poggio T, and Torre V (1982) Retinal ganglion cells: a functional interpretation of dendritic morphology. Phil. Trans. R. Soc. London 298:227–264.

    Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

  • Llinas RR and Nicolson C (1976) Reversal properties of climbing fiber potential in cat Purkinje cells: an example of a distributed synapse. J. Neurophysiol. 39:311–323.

    PubMed  Google Scholar 

  • Llinas RR and Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (London) 305:171–195.

    Google Scholar 

  • Llinas RR and Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (London) 305:197–213.

    Google Scholar 

  • Llinás RR, Sugimori M, and Cherksey B (1989) Voltage-dependent calcium conductances in mammalian neurons: The P channel. Ann. N.Y. Acad. Sci. 560:103–111.

    PubMed  Google Scholar 

  • Major G (1993) Solutions for transients in arbitrarily branching cables: III Voltage clamp problems. Biophys. J. 65:469–491.

    PubMed  Google Scholar 

  • Rall W (1959) Branching dendritic trees and motoneuron membrane resistivity. Exp. Neurology 1:491–527.

    Google Scholar 

  • Rall W and Rinzel J (1973) Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys. J. 13:648–688.

    PubMed  Google Scholar 

  • Rall W and I Segev (1985) Space-clamp problems when voltage clamping branched neurons with intracelluiar microelectrodes. In Voltage and Patch Clamping with Microelectrodes, ed. by TG Smith, H Lecar, SJ Redman and PW Gage, Am Physiol. Socs., Bethesda, Maryland, pp. 191–215.

    Google Scholar 

  • Rall W (1989) Cable theory for dendritic neurons. In Methods in Neuronal Modeling, ed. by Koch, C and I Segev, MIT Press. Cambridge, London, pp. 9–62.

    Google Scholar 

  • Rapp M, Segev I, and Yarom Y (1994) Physiology, morphology and detailed passive models of cerebellar Purkinje cells. J. Physiol. (London) 474:87–99.

    Google Scholar 

  • Rapp M, Yarom Y, and Segev I (1992) The impact of parallel fiber background activity on the cable properties of cerebellar Purkinje cells. Neural Comput. 4:518–533.

    Google Scholar 

  • Shelton DP (1985) Membrane resistivity estimated for the Purkinje neuron by means of a passive computer model. Neuroscience 14:111–131.

    PubMed  Google Scholar 

  • Spruston N, Jaffe DB, Williams SH, and Johnston D (1993) Voltage- and space-clamp erros associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70:781–802.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Sugimori M, and Llinás RR (1992) Dual patch clamping of mammalian Purkinje cells in cerebellar slices. Abstr. Soc. Neurosci. 18:1358–1358.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Staub, C., De Schutter, E. & Knöpfel, T. Voltage-imaging and simulation of effects of voltage- and agonist-activated conductances on soma-dendritic voltage coupling in cerebellar Purkinje cells. J Comput Neurosci 1, 301–311 (1994). https://doi.org/10.1007/BF00961878

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00961878

Keywords

Navigation