 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, August 20, 2003, 23(20):7525-7542
Previous Article | Next Article
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 andMark 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 (KCa) and voltage-gated calcium (Cav) 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 KCa channel antagonist apamin or the SK KCa agonist 1-ethyl-2-benzimidazolinone or the Cav channel antagonists
-conotoxin GVIA (Cav2.2-selective) or nifedipine (Cav1.2-1.3-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 Cav2.2 channels, and necessary for precise, autonomous, single-spike oscillation. SK KCa/Cav2.2 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 KCa 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 Cav3 channels. Cav1.2-1.3 channels were not strongly coupled to SK KCa channels and therefore supported secondary range and long-duration rebound burst firing. In summary, SK KCa 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
Received Jan. 16, 2003; revised Jun. 24, 2003; accepted Jun. 30, 2003.
This article has been cited by other articles:
J. F. Atherton, D. L. Wokosin, S. Ramanathan, and M. D. Bevan
Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus
J. Physiol., December 1, 2008; 586(23): 5679 - 5700.
[Abstract] [Full Text] [PDF]
U. Strauss, F.-W. Zhou, J. Henning, A. Battefeld, A. Wree, R. Kohling, S. J.-P. Haas, R. Benecke, A. Rolfs, and U. Gimsa
Increasing Extracellular Potassium Results in Subthalamic Neuron Activity Resembling That Seen in a 6-Hydroxydopamine Lesion
J Neurophysiol, June 1, 2008; 99(6): 2902 - 2915.
[Abstract] [Full Text] [PDF]
S. Li, J. D. Geiger, and S. Lei
Neurotensin Enhances GABAergic Activity in Rat Hippocampus CA1 Region by Modulating L-Type Calcium Channels
J Neurophysiol, May 1, 2008; 99(5): 2134 - 2143.
[Abstract] [Full Text] [PDF]
J. Baufreton and M. D. Bevan
D2-like dopamine receptor-mediated modulation of activity-dependent plasticity at GABAergic synapses in the subthalamic nucleus
J. Physiol., April 15, 2008; 586(8): 2121 - 2142.
[Abstract] [Full Text] [PDF]
S. Ramanathan, T. Tkatch, J. F. Atherton, C. J. Wilson, and M. D. Bevan
D2-Like Dopamine Receptors Modulate SKCa Channel Function in Subthalamic Nucleus Neurons Through Inhibition of Cav2.2 Channels
J Neurophysiol, February 1, 2008; 99(2): 442 - 459.
[Abstract] [Full Text] [PDF]
M. Teagarden, J. F. Atherton, M. D. Bevan, and C. J. Wilson
Accumulation of cytoplasmic calcium, but not apamin-sensitive afterhyperpolarization current, during high frequency firing in rat subthalamic nucleus cells
J. Physiol., February 1, 2008; 586(3): 817 - 833.
[Abstract] [Full Text] [PDF]
M. Diaz-Rios, D. A. Dombeck, W. W. Webb, and R. M. Harris-Warrick
Serotonin Modulates Dendritic Calcium Influx in Commissural Interneurons in the Mouse Spinal Locomotor Network
J Neurophysiol, October 1, 2007; 98(4): 2157 - 2167.
[Abstract] [Full Text] [PDF]
P. Belujon, E. Bezard, A. Taupignon, B. Bioulac, and A. Benazzouz
Noradrenergic Modulation of Subthalamic Nucleus Activity: Behavioral and Electrophysiological Evidence in Intact and 6-Hydroxydopamine-Lesioned Rats
J. Neurosci., September 5, 2007; 27(36): 9595 - 9606.
[Abstract] [Full Text] [PDF]
D. J. Loane, P. A. Lima, and N. V. Marrion
Co-assembly of N-type Ca2+ and BK channels underlies functional coupling in rat brain
J. Cell Sci., March 15, 2007; 120(6): 985 - 995.
[Abstract] [Full Text] [PDF]
A. Nolting, T. Ferraro, D. D'hoedt, and M. Stocker
An Amino Acid Outside the Pore Region Influences Apamin Sensitivity in Small Conductance Ca2+-activated K+ Channels
J. Biol. Chem., February 9, 2007; 282(6): 3478 - 3486.
[Abstract] [Full Text] [PDF]
Y. Kim and L. O. Trussell
Ion Channels Generating Complex Spikes in Cartwheel Cells of the Dorsal Cochlear Nucleus
J Neurophysiol, February 1, 2007; 97(2): 1705 - 1725.
[Abstract] [Full Text] [PDF]
Y. Yanovsky, S. Velte, and U. Misgeld
Ca2+ release-dependent hyperpolarizations modulate the firing pattern of juvenile GABA neurons in mouse substantia nigra pars reticulata in vitro
J. Physiol., December 15, 2006; 577(3): 879 - 890.
[Abstract] [Full Text] [PDF]
M. D. Humphries, R. D. Stewart, and K. N. Gurney
A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia
J. Neurosci., December 13, 2006; 26(50): 12921 - 12942.
[Abstract] [Full Text] [PDF]
A. Hernandez, O. Ibanez-Sandoval, A. Sierra, R. Valdiosera, D. Tapia, V. Anaya, E. Galarraga, J. Bargas, and J. Aceves
Control of the Subthalamic Innervation of the Rat Globus Pallidus by D2/3 and D4 Dopamine Receptors
J Neurophysiol, December 1, 2006; 96(6): 2877 - 2888.
[Abstract] [Full Text] [PDF]
L. Forti, E. Cesana, J. Mapelli, and E. D'Angelo
Ionic mechanisms of autorhythmic firing in rat cerebellar Golgi cells
J. Physiol., August 1, 2006; 574(3): 711 - 729.
[Abstract] [Full Text] [PDF]
P. J. Magill, A. Sharott, J. P. Bolam, and P. Brown
Delayed synchronization of activity in cortex and subthalamic nucleus following cortical stimulation in the rat
J. Physiol., August 1, 2006; 574(3): 929 - 946.
[Abstract] [Full Text] [PDF]
A. Gillies and D. Willshaw
Membrane Channel Interactions Underlying Rat Subthalamic Projection Neuron Rhythmic and Bursting Activity
J Neurophysiol, April 1, 2006; 95(4): 2352 - 2365.
[Abstract] [Full Text] [PDF]
J. I. Kass and I. M. Mintz
Silent plateau potentials, rhythmic bursts, and pacemaker firing: Three patterns of activity that coexist in quadristable subthalamic neurons
PNAS, January 3, 2006; 103(1): 183 - 188.
[Abstract] [Full Text] [PDF]
P. Pedarzani, J. E. McCutcheon, G. Rogge, B. S. Jensen, P. Christophersen, C. Hougaard, D. Strobaek, and M. Stocker
Specific Enhancement of SK Channel Activity Selectively Potentiates the Afterhyperpolarizing Current IAHP and Modulates the Firing Properties of Hippocampal Pyramidal Neurons
J. Biol. Chem., December 16, 2005; 280(50): 41404 - 41411.
[Abstract] [Full Text] [PDF]
B. J. Maher and G. L. Westbrook
SK Channel Regulation of Dendritic Excitability and Dendrodendritic Inhibition in the Olfactory Bulb
J Neurophysiol, December 1, 2005; 94(6): 3743 - 3750.
[Abstract] [Full Text] [PDF]
J. Baufreton, Z.-T. Zhu, M. Garret, B. Bioulac, S. W. Johnson, and A. I. Taupignon
Dopamine receptors set the pattern of activity generated in subthalamic neurons
FASEB J, November 1, 2005; 19(13): 1771 - 1777.
[Abstract] [Full Text] [PDF]
J. Baufreton, J. F. Atherton, D. J. Surmeier, and M. D. Bevan
Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus
J. Neurosci., September 14, 2005; 25(37): 8505 - 8517.
[Abstract] [Full Text] [PDF]
J. F. Atherton and M. D. Bevan
Ionic Mechanisms Underlying Autonomous Action Potential Generation in the Somata and Dendrites of GABAergic Substantia Nigra Pars Reticulata Neurons In Vitro
J. Neurosci., September 7, 2005; 25(36): 8272 - 8281.
[Abstract] [Full Text] [PDF]
F. P. Elsen and J.-M. Ramirez
Postnatal Development Differentially Affects Voltage-Activated Calcium Currents in Respiratory Rhythmic Versus Nonrhythmic Neurons of the Pre-Botzinger Complex
J Neurophysiol, August 1, 2005; 94(2): 1423 - 1431.
[Abstract] [Full Text] [PDF]
S.-W. Ying and P. A. Goldstein
Propofol-Block of SK Channels in Reticular Thalamic Neurons Enhances GABAergic Inhibition in Relay Neurons
J Neurophysiol, April 1, 2005; 93(4): 1935 - 1948.
[Abstract] [Full Text] [PDF]
J. C. F. Lee, J. C. Callaway, and R. C. Foehring
Effects of Temperature on Calcium Transients and Ca2+-Dependent Afterhyperpolarizations in Neocortical Pyramidal Neurons
J Neurophysiol, April 1, 2005; 93(4): 2012 - 2020.
[Abstract] [Full Text] [PDF]
Z. Xiang, L. Wang, and S. T. Kitai
Modulation of Spontaneous Firing in Rat Subthalamic Neurons by 5-HT Receptor Subtypes
J Neurophysiol, March 1, 2005; 93(3): 1145 - 1157.
[Abstract] [Full Text] [PDF]
J. T. Paz, J.-M. Deniau, and S. Charpier
Rhythmic Bursting in the Cortico-Subthalamo-Pallidal Network during Spontaneous Genetically Determined Spike and Wave Discharges
J. Neurosci., February 23, 2005; 25(8): 2092 - 2101.
[Abstract] [Full Text] [PDF]
G. Viana Di Prisco and S. Alford
Quantitative Investigation of Calcium Signals for Locomotor Pattern Generation in the Lamprey Spinal Cord
J Neurophysiol, September 1, 2004; 92(3): 1796 - 1806.
[Abstract] [Full Text] [PDF]
P. J. Magill, A. Sharott, M. D. Bevan, P. Brown, and J. P. Bolam
Synchronous Unit Activity and Local Field Potentials Evoked in the Subthalamic Nucleus by Cortical Stimulation
J Neurophysiol, August 1, 2004; 92(2): 700 - 714.
[Abstract] [Full Text] [PDF]
C. J. Wilson, A. Weyrick, D. Terman, N. E. Hallworth, and M. D. Bevan
A Model of Reverse Spike Frequency Adaptation and Repetitive Firing of Subthalamic Nucleus Neurons
J Neurophysiol, May 1, 2004; 91(5): 1963 - 1980.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|