Advertisement

Journal of Computational Neuroscience

, Volume 2, Issue 4, pp 299–312 | Cite as

A minimal, compartmental model for a dendritic origin of bistability of motoneuron firing patterns

  • Victoria Booth
  • John Rinzel
Article

Abstract

Various nonlinear regenerative responses, including plateau potentials and bistable repetitive firing modes, have been observed in motoneurons under certain conditions. Our simulation results support the hypothesis that these responses are due to plateau-generating currents in the dendrites, consistent with a major role for a noninactivating calcium L-type current as suggested by experiments. Bistability as observed in the soma of low- and higher-frequency spiking or, under TTX, of near resting and depolarized plateau potentials, occurs because the dendrites can be in a near resting or depolarized stable steady state. We formulate and study a two-compartment minimal model of a motoneuron that segregates currents for fast spiking into a soma-like compartment and currents responsible for plateau potentials into a dendrite-like compartment. Current flows between compartments through a coupling conductance, mimicking electrotonic spread. We use bifurcation techniques to illuminate how the coupling strength affects somatic behavior. We look closely at the case of weak coupling strength to gain insight into the development of bistable patterns. Robust somatic bistability depends on the electrical separation since it occurs only for weak to moderate coupling conductance. We also illustrate that hysteresis of the two spiking states is a natural consequence of the plateau behavior in the dendrite compartment.

Keywords

motoneurons dendrites bistability plateau potentials compartmental modeling 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amitai Y, Friedman A, Connors BW, Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex.Cerebral Cortex 3:26–38.Google Scholar
  2. Brownstone RM, Gossard J-P, Hultborn H (1994) Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat.Exp. Brain Res. 102:34–44.Google Scholar
  3. Conway BA, Hultborn H, Kiehn O, Mintz I (1988) Plateau potentials in α-motoneurones induced by intravenous injection of L-DOPA and clonidine in the spinal cat.J. Physiol. 405:369–384.Google Scholar
  4. Edelstein-Keshet L (1988) Mathematical Models in Biology. Random House, New York. pp. 311–360.Google Scholar
  5. Eken T, Kiehn O (1989) Bistable firing properties of soleus motor units in unrestrained rats.Acta Physiol. Scand. 136:383–394.Google Scholar
  6. Fujita Y (1989) Dendritic spikes in normal spinal motoneurons of cats.Neuroscience Res. 6:299–308.Google Scholar
  7. Gutman AM (1971) Further remarks on the effectiveness of the dendrite synapses.Biofizika 16:131–138.Google Scholar
  8. Gutman AM (1991) Bistability of dendrites.Intl. J. Neural Sys. 1:291–304.Google Scholar
  9. Hounsgaard J, Hultborn H, Jesperson B, Kiehn O (1988a) Bistability of α-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan.J. Physiol. 405:345–367.Google Scholar
  10. Hounsgaard J, Kiehn O (1989) Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential.J. Physiol. 414:265–282.Google Scholar
  11. Hounsgaard J, Kiehn O (1993) Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneuronesin vitro, J. Physiol. 468:245–259.Google Scholar
  12. Hounsgaard J, Kiehn O, Mintz I (1988b) Response properties of motoneurones in a slice preparation of the turtle spinal cord.J. Physiol. 398:575–589.Google Scholar
  13. Hounsgaard J, Mintz 1 (1988) Calcium conductance and firing properties of spinal motoneurones in the turtle.J. Physiol. 398:591–603.Google Scholar
  14. Huguenard JR, Hamill OP, Prince DA (1989) Sodium channels in dendrites of rat cortical pyramidal neurons.Proc. Nat. Acad. Sci. USA 86:2473–2477.Google Scholar
  15. Kiehn O (1991) Plateau potentials and active integration in the “final common pathway” for motor behavior.TINS 14:68–73.Google Scholar
  16. Kiehn O, Eken T (1992) Discontinuous changes in discharge pattern of human motor units. (Abstract)J. Physiol. 452:277P.Google Scholar
  17. Llinas R, Sugimori M (1980) Electrophysiological properties ofin vitro Purkinje cell dendrites in mammalian cerebellar slices.J. Physiol. 305:197–213.Google Scholar
  18. Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber.Biophys. J. 35:193–213.Google Scholar
  19. Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons.J. Comput. Neuro. 1:39–60.Google Scholar
  20. Powers RK (1993) A variable-threshold motoneuron model that incorporates time- and voltage-dependent potassium and calcium conductances.J. Neurophysiol. 70:246–262.Google Scholar
  21. Rall W (1962) Theory of physiological properties of dendrites.Ann. N.Y. Acad. Sci. 96:1071–1092.Google Scholar
  22. Reuveni I, Friedman A, Amitai Y, Gutnick MJ (1993) Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: Evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites.J. Neurosci. 13:4609–4621.Google Scholar
  23. Rhodes PA, Gray CM (1994) Simulations of intrinsically bursting neocortical pyramidal neurons.Neural Computation 6:1086–1110.Google Scholar
  24. Rinzel J, Baer SM (1988) Threshold for repetitive activity for a slow stimulus ramp: A memory effect and its dependence on fluctuations.Biophys. J. 54:551–555.Google Scholar
  25. Rinzel J, Ermentrout GB (1989) Analysis of neural excitability and oscillations. In: Koch C, Segev I, eds. Methods in Neuronal Modeling: From Synapses to Networks. MIT Press, Cambridge, MA. pp. 135–169.Google Scholar
  26. Schwindt PC, Crill WE (1984) Membrane properites of cat spinal motoneurons. In: Davidoff R, ed. Handbook of the Spinal Cord. Marcel Dekker, New York, NY. pp. 199–242.Google Scholar
  27. Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.Nature 367:69–72.Google Scholar
  28. Traub R, Wong R, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances.J. Neurophysiol. 66:635–649.Google Scholar
  29. Walton K, Fulton BP (1986) Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studiedin vitro. Neuroscience 19:669–683.Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • Victoria Booth
    • 1
  • John Rinzel
    • 1
  1. 1.Mathematical Research BranchNIDDK, National Institutes of HealthBethesda

Personalised recommendations