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The Journal of Neuroscience, August 20, 2003, 23(20):7525-7542

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Apamin-Sensitive Small Conductance Calcium-Activated Potassium Channels, through their Selective Coupling to Voltage-Gated Calcium Channels, Are Critical Determinants of the Precision, Pace, and Pattern of Action Potential Generation in Rat Subthalamic Nucleus Neurons In Vitro

Nicholas E. Hallworth,¹ Charles J. Wilson,² and Mark D. Bevan³

¹University of Tennessee, Anatomy and Neurobiology, Memphis, Tennessee 38163, ²Division of Life Science, University of Texas, San Antonio, Texas 78294, and ³Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611-3008

Distinct activity patterns in subthalamic nucleus (STN) neurons are observed during normal voluntary movement and abnormal movement in Parkinson's disease (PD). To determine how such patterns of activity are regulated by small conductance (SK) calcium-activated potassium channels (K_Ca) and voltage-gated calcium (Ca_v) channels, STN neurons were recorded in the perforated patch configuration in slices, [which were prepared from postnatal day 16 (P16)-P30 rats and held at 37°C] and then treated with the SK K_Ca channel antagonist apamin or the SK K_Ca agonist 1-ethyl-2-benzimidazolinone or the Ca_v channel antagonists -conotoxin GVIA (Ca_v2.2-selective) or nifedipine (Ca_v1.2-1.3-selective). In other experiments, fura-2 was introduced as an indicator of intracellular calcium dynamics.

A component of the current underlying single-spike afterhyperpolarization was sensitive to apamin, phase-locked to calcium entry via Ca_v2.2 channels, and necessary for precise, autonomous, single-spike oscillation. SK K_Ca/Ca_v2.2 channel coupling did not underlie spike-frequency adaptation but limited activity in response to current injection by encoding the accumulation of intracellular calcium, maintained the characteristic sigmoidal frequency-intensity relationship and generated a post-train afterhyperpolarization. In addition, SK K_Ca channels terminated rebound burst activity more effectively in neurons with short-duration bursts (<100 msec) than neurons with long-duration bursts (>100 msec), presumably through their activation by Ca_v3 channels. Ca_v1.2-1.3 channels were not strongly coupled to SK K_Ca channels and therefore supported secondary range and long-duration rebound burst firing. In summary, SK K_Ca channels play a fundamental role in autonomous, driven, and rebound activity and oppose the transition from autonomous, rhythmic, single-spike activity to burst firing in STN neurons.

Key words: basal ganglia; oscillation; afterhyperpolarization; rebound burst; apamin; EBIO

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Received Jan. 16, 2003; revised Jun. 24, 2003; accepted Jun. 30, 2003.

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