TASK channels are acid-sensitive and anesthetic-activated members of the family of two-pore-domain potassium channels. We have made the surprising discovery that the genetic ablation of TASK-3 channels eliminates a specific type of theta oscillation in the cortical electroencephalogram (EEG) resembling type II theta (4 -9 Hz), which is thought to be important in processing sensory stimuli before initiating motor activity. In contrast, ablation of TASK-1 channels has no effect on theta oscillations. Despite the absence of type II theta oscillations in the TASK-3 knockout (KO) mice, the related type I theta, which has certain neuronal pathways in common and is involved in exploratory behavior, is unaffected. In addition to the absence of type II theta oscillations, the TASK-3 KO animals show marked alterations in both anesthetic sensitivity and natural sleep behavior. Their sensitivity to halothane, a potent activator of TASK channels, is greatly reduced, whereas their sensitivity to cyclopropane, which does not activate TASK-3 channels, is unchanged. The TASK-3 KO animals exhibit a slower progression from their waking to sleeping states and, during their sleeping period, their sleep episodes as well as their REM theta oscillations are more fragmented. These results imply a previously unexpected role for TASK-3 channels in the cellular mechanisms underlying these behaviors and suggest that endogenous modulators of these channels may regulate theta oscillations.I f a sufficient number of neurons participate in network oscillations, then the local field potentials summate, and measurable voltage oscillations can be recorded in the electroencephalogram (EEG). These oscillations are observed over a wide range of frequencies and reflect the synchronous neuronal activity that occurs during a variety of different behaviors. For example, as animals explore their environments, as they learn and lay down memories, as they process sensory input, and as they sleep, characteristic oscillations occur in the ''theta'' range of frequencies (4-12 Hz) (1). These theta oscillations are often divided into two types (1-5): Type I, which occurs at slightly higher frequencies (6-12 Hz), and type II (also known as arousal theta), which occurs at the lower end of the range (4-9 Hz). Type I theta is associated with exploratory behavior, walking, running, and rearing, whereas type II theta is associated with immobility during the processing of sensory stimuli relevant to initiating, or intending to initiate, motor activity.The neuronal networks that generate these theta oscillations involve ascending pathways from the brainstem that project to the hypothalamus and then to the medial septum/diagonal band of Broca and the hippocampus (6-9). Where the true pacemaker is located is unclear, but the basic requirements for a neuron to oscillate are a depolarizing drive (such as a sodium current) together with a restoring drive, such as a repolarizing potassium current. Most computational models (10-12) include several different ionic currents, som...
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