Abstract
Computer simulations of a dendrite possessing voltage-sensitive potassium conductances were used to determine the effects of these conductances on synaptic transmission and on the propagation of synaptic signals within the dendritic tree. Potassium conductances had two principal effects on voltage transients generated by current injections or synaptic conductances. Locally (near the source of the transient), voltage-gated potassium channels produced a potassium shunt current that reduced the amplitude of voltage transients generated by depolarizing currents. This shunt current increased as the amplitude of the depolarizing transient increased and so acted to prevent large synaptic transients from reaching levels that would saturate due to a reduction in driving force. In the presence of rapidly activating potassium currents, excitatory synapses produced larger synaptic currents that were more linearly related to synaptic conductance, but these produced smaller voltage transients. The maximum amplitudes of the voltage transients were limited by the voltage sensitivity of the K+ conductance and the rate at which it could activate. Sufficiently rapid synaptic currents could outrun the K+ conductance and thus achieve high local peak amplitudes. These effects of K+ conductances were unrelated to whether they were located on dendrites or not, being related only to their proximity to the source of synaptic current. The second class of effects of K+ conductances depended on their alteration of the electrotonic structure of the postsynaptic cell and so were observed only when they were located on postsynaptic dendrites. Voltage-gated K+ conductances produced voltage-dependent electrotonic expansion of depolarized dendrites, which had the effect of isolating synaptic inputs on depolarized dendrites from events on the rest of the neuron. Thus, synapses on the same dendrite interacted destructively to a degree much greater than that expected from the classical driving force nonlinearity. Synapses located proximally to a depolarized dendritic region were less effected than those located distally, and the range of the nonlinear interaction between synapses was dependent on the kinetics of activation and deactivation of the conductance. When present in conjunction with rapidly activating dendritic sodium conductance, the potassium conductance sharpened the requirement for spatial and temporal coincidence to produce synaptic boosting by inward currents, and suppressed out-of-synchrony synaptic inputs.
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References
Adams DJ and Nonner W (1989) Voltage-dependent potassium channels: gating, ion permeation and block. In, NS Cook, ed. Potassium Channel: Structure, Classification, Function and Therapeutic Potential. Ellis Horwood, Chichester. pp. 42–69.
Agmon-Snir H and Segev I (1993) Signal delay and input synchronization in passive dendritic structures.J. Neurophysiol. 70:2066–2085.
Amitai Y, Friedman A, Connors BW, and Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex.Cerebral Cortex 3:26–38.
Bernander O, Douglas, RJ, Martin KA, and Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells.Proc. Natl. Acad. Sci. USA 88:11569–11573.
Byrne JH (1980) Quantitative aspects of ionic conductance mechanisms contributing to firing pattern of motor cells mediating inking behavior in Aplysia California.J. Neurophysiol. 43:651–668.
Cauller LJ and Connors BW (1994) Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex.J. Neurosci. 14:751–762.
Connor JA and Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata.J. Physiol. (Lond.) 213:21–30.
Covarrubias M, Wei A, and Saldoff L (1991) Shaker, Shal, Shab. and Shaw express independent K+ current systems.Neuron 7:763–773.
Destexhe A, Babloyantz A, and Sejnowski TJ (1993) Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons.Biophys. J. 65:1538–1552.
Foehring RC and Surmeier DJ (1993) Voltage-gated potassium currents in acutely dissociated rat cortical neurons.J. Neurophysiol. 70:51–63.
Hestrin S (1993) Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons.Neuron 11:1083–1091.
Hodgkin AL and Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve.J. Physiol. (Lond.) 117:500–544.
Hoshi T and Aldrich RW (1989) Gating kinetics of four classes of voltage-dependent K channels in pheochromocytoma cells.J. Gen. Physiol. 91:107–131.
Huguenard FR and McCormick DA (1992) Simulation of the currents involved in rhythmic oscilations in thalamic relay neurons.J. Neurophysiol. 68:1373–1383.
Jan LY and Jan YN (1990) How might the diversity of potassium channels be generated?TINS 13:415–419.
Kim HG and Connors BW (1993) Apical dendrites of the neoscortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology.J. Neurosci. 13:5301–5311.
Larkman AU, Major G, Stratford KJ, and Jack JJ (1992) Dendritic morphology of pyramidal neurones of the visual cortex of the rat. IV: Electric geometry,J. Comp. Neurol 323:137–152.
Major G, Evans JD, and Jack JJB (1994) Solutions for transients in arbitrarily branching cables: I. Voltage recording with a somatic shunt.Biophys. J. 65:423–449.
McCormick DA (1991) Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons.J. Neurophysiol. 66:1176–1189.
Narahashi T and Herman MD (1992) Overview of toxins and drugs as tools to study excitable membrane ion channels: I. Voltage-activated channels. In: B Rudy and LE Inverson, eds. Methods in Enzymology: Ion Channels, 207. Academic Press, San Diego, pp. 123–131.
Nicoll A, Larkman A, and Blakemore C (1993) Modulation of EPSP shape and efficacy by intrinsic membrane conductances in rat neocortical pyramidal neurons in vitro.J. Physiol. (Lond.) 468:693–710.
Nisenbaum ES, Xu ZC, and Wilson CJ (1994) Contribution of a slowly inactivating potassium current to the transition of firing o neostriatal spiny projection neurons.J. Neuropysiol. 71:1174–1189.
Rall W, Burke RE, Smith TG, Nelson PG, and Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons.J. Neurophysiol. 30:1169–1193.
Reuveni I, Firedman A, Amitai Y, and Gutnick MJ (1994) Step wise repolarization from Ca2+ plateaus in neocortical pyramidal cells: evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites.J. Neurosci. 13:4609–4621.
Rogawski MA (1985) The A-current: how ubiquitous a feature of excitable cell is it?TINS 8:214–219.
Salkoff L, Baker K, Butler A, Corvarrubias M, Pak MD, and Wei A (1992) An essential “set” of K+ channels conserved in flies, mice and humans.TINS 15:161–166.
Sheng M, Tsaur M-L, Jan YN, and Jan LY (1994) Contrasting sub-celluler localization of the Kvl.2 K+ channel subunit in different neurons of rat brain.J. Neurosci. 14:2408–2417.
Softky W (1994) Sub-millisecond coincidence detection in active dendritic trees.Neuroscience 58:13–41.
Spain WJ, Schwindt PC, and Crill WE (1991) Two transient potassium currents in layer V pyramidal neurones from cat sensorimotor cortex.J. Physiol. 434:591–607.
Storm JF (1988) Temporal integration by a slowly inactivating K+ current in hippocampal neurons.Nature Lond. 336:379–383.
Stuart GJ and Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.Nature 367:69–72.
Surmeier DJ, Wilson CJ, and Eberwine J (1994) Patch-clamp techniques for studying potassium currents in mammalian brain neurons. In: T Narahashi, ed. Methods in Neurosciences, Vol. 19. Academic Press, San Diego, pp. 39–67.
Wilson CJ (1992) Dendritic morphology, inward rectification and the functional properties of neostriatal neurons. In: T McKenna, J Davis, and SF Zornetzer, eds. Single Neuron Computation. Academic Press, San Diego, pp. 141–171.
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Wilson, C.J. Dynamic modification of dendritic cable properties and synaptic transmission by voltage-gated potassium channels. J Comput Neurosci 2, 91–115 (1995). https://doi.org/10.1007/BF00961882
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DOI: https://doi.org/10.1007/BF00961882