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The Journal of Neuroscience, July 23, 2003, 23(16):6460-6469
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Contribution of TWIK-Related Acid-Sensitive K+ Channel 1 (TASK1) and TASK3 Channels to the Control of Activity Modes in Thalamocortical Neurons
Sven G. Meuth, * Thomas Budde, * Tatyana Kanyshkova, Tilman Broicher, Thomas Munsch, andHans-Christian Pape Institute of Physiology, Otto-von-Guericke-Universität, D-39120 Magdeburg, Germany
The thalamocortical network is characterized by rhythmic burst activity during natural sleep and tonic single-spike activity during wakefulness. The change between these two activity modes is partially governed by transmitters acting on leak K+ currents in the thalamus, although the nature of the constituting ion channels is not yet known. In the present study, the contribution of members of the two-pore domain K+ channel family to the leak current was investigated using whole-cell patch-clamp techniques and molecular biological techniques. RT-PCR and in situ hybridization revealed the expression of TWIK-related acid-sensitive K+ channel 1 (TASK 1) and TASK3 channels in the rat dLGN. Voltage-clamp recordings of thalamocortical relay neurons in slice preparations demonstrated the existence of a current component sensitive to the TASK channel blocker bupivacaine, which reversed at the presumed K+ equilibrium potential, showed outward rectification, and contributed
40% to the standing outward current at depolarized values of the membrane potential (-28 mV). The pharmacological profile was indicative of TASK channels, in that the current was sensitive to changes in extracellular pH, reduced by muscarine and increased by halothane, and these effects were occluded by a near-maximal action of bupivacaine. Pharmacological manipulation of this current under current-clamp conditions resulted in a shift between burst and tonic firing modes. It is concluded that TASK1 and TASK3 channels contribute to the muscarine- and halothane-sensitive conductance in thalamocortical relay neurons, thereby contributing to the change in the activity mode of thalamocortical networks observed during the sleep-wake cycle and on application of inhalational anesthetics.
Key words: whole-cell patch clamp; RT-PCR; in situ hybridization; thalamic activity mode; anesthetics; muscarinic receptor; sleep-wake cycle
Received Apr. 11, 2003; revised May. 20, 2003; accepted May. 30, 2003.
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