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Bistability in cerebellar Purkinje cell dendrites modelled with high-threshold calcium and delayed-rectifier potassium channels

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Abstract

Phase-plane analysis of the ionic currents underlying dendritic plateau potentials was carried out to study the nonlinear dynamics and steady-state transfer properties of the dendritic tree in cerebellar Purkinje cells. The results of an analysis of the P-type calcium and delayed rectifier potassium channel system are presented in this study. These channels constitute a simple system that can support bistability and plateau potentials. By requiring both the steady-state current-voltage curve and nullclines to mimic basic plateau potential properties, we obtained well-defined ranges of specific conductance that can support bistability. Hysteresis was found to be surprisingly prevalent in this simple ion-channel system. Using the steady-state current voltage relationship, we derive concise, algebraic expressions for the voltage and current thresholds of state transitions as functions of specific conductance. The significance of bistability in this ion-channel system is discussed with respect to the generation of plateau potentials in Purkinje cells dendrites and the role of the cerebellum in motor control.

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References

  • Anderson JA, Rosenfeld E (1988) Neurocomputing: foundations of research. MIT Press, Cambridge, Mass.

    Google Scholar 

  • Andersson G, Campbell NC, Ekerot C-F, Hesslow G, Oscarsson O (1984) Integration of mossy fiber and climbing fiber inputs to Purkinje cells. Exp Brain Res (Suppl) 9:145–150

    Google Scholar 

  • Benson MW, Bree GM, Kinahan PE, Hoffmann GW (1987) A teachable neural network based on an unorthodox neuron. Physica D 22:233–246

    Google Scholar 

  • Berthier NE, Singh SR, Barto AG, Houk JC (1993) Distributed representation of limb motor programs in arrays of adjustable pattern generators. J Cogn Neurosci 5:56–78

    Google Scholar 

  • Bush PC, Sejnowski TJ (1991) Simulations of a reconstructed cerebellar Purkinje cell based on simplified channel kinetics. Neural Comput 3:321–332

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Fitzhugh R (1959) Thresholds and plateaus in the Hodgkin-Huxley nerve equations. J Gen Physiol 43:867–896

    Google Scholar 

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

    Google Scholar 

  • Gear CW (1971) Numerical initial value problems in ordinary differential equations. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Gutman AM (1991) Bistability of dendrites. Int J Neural Sys 1:291–304

    Google Scholar 

  • Gutman AM (1994) Gelfand-Tsetlin principle of minimal afferentation and bistability of dendrites. Int J Neural Syst 5:83–86

    Google Scholar 

  • Guttman R, Lewis S, Rinzel J (1980) Control of repetitive firing in squid axon membrane as a model for a neuroneoscillator. J Physiol (Lond) 305:377–395

    Google Scholar 

  • Hille B (1984) Ionic channels of excitable membranes. Sinauer Associates, Sunderland

    Google Scholar 

  • Hockberger PE, Nam SC (1994) High-voltage-activated calcium current in developing neurons is insensitive to nifedipine. Pflugers Arch 426:402–411

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol (Lond) 117:500–544

    Google Scholar 

  • Hoffmann GW (1986) A neural network model based on the analogy with the immune system. J Theor Biol 122:33–67

    Google Scholar 

  • Hopfield JJ, Tank DW (1986) Computing with neural circuits: a model. Science 233:625–633

    Google Scholar 

  • Houk JC, Barto AG (1992) Distributed sensorimotor learning. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior II. Elsevier, Amsterdam, pp 71–100

    Google Scholar 

  • Houk JC, Wise SP (1995) Distributed modular architectures linking basal ganglia, cerebellum and cerebral cortex: their role in planning and controlling action. Cerebral Cortex 5:95–110

    Google Scholar 

  • Houk JC, Singh SP, Fisher C, Barto AG (1990) An adaptive sensorimotor network inspired by the anatomy and physiology of the cerebellum. In: Miller WT, Sutton RS, Werbos PJ (eds) Neural networks for control. MIT Press, Cambridge, Mass, pp 301–348

    Google Scholar 

  • Kiehn O (1991) Plateau potentials and active integration in the ‘final common pathway’ for motor behaviour. Trends Neuro Sci 14:68–73

    Google Scholar 

  • Knight BW (1972) The relationship between the firing rate of a single neuron and the level of activity in a population of neurons. J Gen Physiol 59:767–778

    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 

  • Lasser-Ross N, Ross WN (1992) Imaging voltage and synaptically activated sodium transients in cerebellar Purkinje cells. Proc R Soc Lond Biol 247:35–39

    Google Scholar 

  • Lev-Ram V, Miyakawa H, Lasser-Ross N, Ross WN (1992) Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. J Neurophysiol 68:1167–1177

    Google Scholar 

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

    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 

  • Mascagni MV (1989) Numerical methods for neuronal modeling. In: Koch C, Segev I (eds) Methods in neuronal modeling. MIT Press, Cambridge, Mass, pp 439–484

    Google Scholar 

  • Minsky ML, Papert SA (1969) Perceptrons. MIT Press, Cambridge, Mass.

    Google Scholar 

  • Mintz IM, Adams ME, Bean BP (1992) P-type calcium channels in rat central and peripheral neurons. Neuron 9:85–95

    Google Scholar 

  • Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35:193–213

    Google Scholar 

  • Pellionisz A, Llinás R (1977) A computer model of cerebellar Purkinje cells. Neuroscience 2:37–48

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rinzel J, Ermentrout GB (1989) Analysis of neural excitability and oscillations. In: Koch C, Segev I (eds) Methods in neuronal modeling. MIT Press, Cambridge, Mass., pp 135–169

    Google Scholar 

  • Rose RM, Hindmarsh JL (1985) A model of a thalamic neuron. Proc R Soc Lond [Biol] 225:161–193

    Google Scholar 

  • Ross WN, Werman R (1987) Mapping calcium transients in the dendrites of Purkinje cells from guinea-pig cerebellum in vitro J Physiol (Lond) 389:319–336

    Google Scholar 

  • Rumelhart DE, McClelland JL (1986) Parallel distributed processing: explorations in the microstructure of cognition. Bradford Books/ MIT Press, Cambridge, Mass.

    Google Scholar 

  • Schutter de E, Bower J (1994) An active membrane model of the cerebellar Purkinje cell. J Neurophysiol 71:375–419

    Google Scholar 

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

    Google Scholar 

  • Sinkjaer T, Wu CH, Barto A, Houk JC (1990) Cerebellum control of endpoint position — a simulation model. IJCNN 90 II:705–710

    Google Scholar 

  • Tank DW, Sugimori M, Connor JA, Llinás RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242:773–777

    Google Scholar 

  • Tomovic R, McGhee RB (1966) A finite state approach to the synthesis of bioengineering control systems. IEEE Trans HFE-7:65–69

    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 

  • Wang L, Ross J (1990) Synchronous neural networks of nonlinear threshold elements with hysteresis. Proc Natl Acad Sci USA 87:988–992

    Google Scholar 

  • Yool AJ, Dionne VE, Groul DL (1988) Developmental changes in K selective channel activity during differentiation of the Purkinje neurone in culture. J Neurosci 8:1971–1980

    Google Scholar 

  • Yuen GL, Hockberger PE, Massone LE, Houk JC (1992) Qualitative dynamical model of bistability in Purkinje cell dendrites. Abstr SocNeurosci 18:1206

    Google Scholar 

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Yuen, G.L., Hockberger, P.E. & Houk, J.C. Bistability in cerebellar Purkinje cell dendrites modelled with high-threshold calcium and delayed-rectifier potassium channels. Biol. Cybern. 73, 375–388 (1995). https://doi.org/10.1007/BF00199473

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  • DOI: https://doi.org/10.1007/BF00199473

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