 |
Previous Article | Next Article 
The Journal of Neuroscience, March 1, 2002, 22(5):1618-1628
Physiological Role of Calcium-Activated Potassium Currents in the
Rat Lateral Amygdala
E. S. Louise
Faber and
Pankaj
Sah
Division of Neuroscience, John Curtin School of Medical Research,
Australian National University, Canberra, ACT 2601, Australia
Principal neurons in the lateral nucleus of the amygdala (LA)
exhibit a continuum of firing properties in response to prolonged current injections ranging from those that accommodate fully to those
that fire repetitively. In most cells, trains of action potentials are
followed by a slow afterhyperpolarization (AHP) lasting several
seconds. Reducing calcium influx either by lowering concentrations of
extracellular calcium or by applying nickel abolished the AHP,
confirming it is mediated by calcium influx. Blockade of large
conductance calcium-activated potassium channel (BK) channels with
paxilline, iberiotoxin, or TEA revealed that BK channels are involved
in action potential repolarization but only make a small contribution
to the fast AHP that follows action potentials. The fast AHP was,
however, markedly reduced by low concentrations of 4-aminopyridine and
-dendrotoxin, indicating the involvement of voltage-gated potassium
channels in the fast AHP. The medium AHP was blocked by apamin and
UCL1848, indicating it was mediated by small conductance
calcium-activated potassium channel (SK) channels. Blockade of these
channels had no effect on instantaneous firing. However, enhancement of
the SK-mediated current by 1-ethyl-2-benzimidazolinone or
paxilline increased the early interspike interval, showing that under
physiological conditions activation of SK channels is insufficient to
control firing frequency. The slow AHP, mediated by non-SK BK channels, was apamin-insensitive but was modulated by carbachol and
noradrenaline. Tetanic stimulation of cholinergic afferents to the LA
depressed the slow AHP and led to an increase in firing. These results
show that BK, SK, and non-BK SK-mediated calcium-activated potassium currents are present in principal LA neurons and play distinct physiological roles.
Key words:
AHP; BK channels; SK channels; apamin; paxilline; adaptation
Copyright © 2002 Society for Neuroscience 0270-6474/02/2251618-11$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
R. Krahe, J. Bastian, and M. J. Chacron
Temporal Processing Across Multiple Topographic Maps in the Electrosensory System
J Neurophysiol,
August 1, 2008;
100(2):
852 - 867.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. H. Mehaffey, L. Maler, and R. W. Turner
Intrinsic Frequency Tuning in ELL Pyramidal Cells Varies Across Electrosensory Maps
J Neurophysiol,
May 1, 2008;
99(5):
2641 - 2655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Power and P. Sah
Competition between Calcium-Activated K+ Channels Determines Cholinergic Action on Firing Properties of Basolateral Amygdala Projection Neurons
J. Neurosci.,
March 19, 2008;
28(12):
3209 - 3220.
[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]
|
 |
|

|
 |

|
 |
 
R. Yamamoto, Y. Ueta, and N. Kato
Dopamine Induces a Slow Afterdepolarization in Lateral Amygdala Neurons
J Neurophysiol,
August 1, 2007;
98(2):
984 - 992.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Power and P. Sah
Distribution of IP3-mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons
J. Physiol.,
May 1, 2007;
580(3):
835 - 857.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-H. Zeng, G. R. Benzinger, X.-M. Xia, and C. J. Lingle
BK Channels with {beta}3a Subunits Generate Use-Dependent Slow Afterhyperpolarizing Currents by an Inactivation-Coupled Mechanism
J. Neurosci.,
April 25, 2007;
27(17):
4707 - 4715.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Duvarci and D. Pare
Glucocorticoids Enhance the Excitability of Principal Basolateral Amygdala Neurons
J. Neurosci.,
April 18, 2007;
27(16):
4482 - 4491.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Martina, M.-E. B. Turcotte, S. Halman, and R. Bergeron
The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus
J. Physiol.,
January 1, 2007;
578(1):
143 - 157.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Likhtik, J. G. Pelletier, A. T. Popescu, and D. Pare
Identification of Basolateral Amygdala Projection Cells and Interneurons Using Extracellular Recordings
J Neurophysiol,
December 1, 2006;
96(6):
3257 - 3265.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Luther and S. J. Birren
Nerve Growth Factor Decreases Potassium Currents and Alters Repetitive Firing in Rat Sympathetic Neurons
J Neurophysiol,
August 1, 2006;
96(2):
946 - 958.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Wicher, J. Berlau, C. Walther, and A. Borst
Peptidergic Counter-Regulation of Ca2+- and Na+-Dependent K+ Currents Modulates the Shape of Action Potentials in Neurosecretory Insect Neurons
J Neurophysiol,
January 1, 2006;
95(1):
311 - 322.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Limon, C. Perez, R. Vega, and E. Soto
Ca2+-Activated K+-Current Density Is Correlated With Soma Size in Rat Vestibular-Afferent Neurons in Culture
J Neurophysiol,
December 1, 2005;
94(6):
3751 - 3761.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. de Dios Navarro-Lopez, J. M. Delgado-Garcia, and J. Yajeya
Cooperative Glutamatergic and Cholinergic Mechanisms Generate Short-Term Modifications of Synaptic Effectiveness in Prepositus Hypoglossi Neurons
J. Neurosci.,
October 26, 2005;
25(43):
9902 - 9906.
[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]
|
 |
|

|
 |

|
 |
 
G. C. Tombaugh, W. B. Rowe, and G. M. Rose
The Slow Afterhyperpolarization in Hippocampal CA1 Neurons Covaries with Spatial Learning Ability in Aged Fisher 344 Rats
J. Neurosci.,
March 9, 2005;
25(10):
2609 - 2616.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kroner, J. A. Rosenkranz, A. A. Grace, and G. Barrionuevo
Dopamine Modulates Excitability of Basolateral Amygdala Neurons In Vitro
J Neurophysiol,
March 1, 2005;
93(3):
1598 - 1610.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Fisahn, S. F. Heinemann, and C. J. McBain
The kainate receptor subunit GluR6 mediates metabotropic regulation of the slow and medium AHP currents in mouse hippocampal neurones
J. Physiol.,
January 1, 2005;
562(1):
199 - 203.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. C. Santarelli, J. Chen, S. H. Heinemann, and T. Hoshi
The {beta}1 Subunit Enhances Oxidative Regulation of Large-Conductance Calcium-activated K+ Channels
J. Gen. Physiol.,
September 27, 2004;
124(4):
357 - 370.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Acuna-Goycolea and A. van den Pol
Glucagon-Like Peptide 1 Excites Hypocretin/Orexin Neurons by Direct and Indirect Mechanisms: Implications for Viscera-Mediated Arousal
J. Neurosci.,
September 15, 2004;
24(37):
8141 - 8152.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ghamari-Langroudi and C. W. Bourque
Muscarinic Receptor Modulation of Slow Afterhyperpolarization and Phasic Firing in Rat Supraoptic Nucleus Neurons
J. Neurosci.,
September 1, 2004;
24(35):
7718 - 7726.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Martin, S. Puig, A. Pietrzykowski, P. Zadek, P. Emery, and S. Treistman
Somatic Localization of a Specific Large-Conductance Calcium-Activated Potassium Channel Subtype Controls Compartmentalized Ethanol Sensitivity in the Nucleus Accumbens
J. Neurosci.,
July 21, 2004;
24(29):
6563 - 6572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. de Dios Navarro-Lopez, J. C. Alvarado, J. Marquez-Ruiz, M. Escudero, J. M. Delgado-Garcia, and J. Yajeya
A Cholinergic Synaptically Triggered Event Participates in the Generation of Persistent Activity Necessary for Eye Fixation
J. Neurosci.,
June 2, 2004;
24(22):
5109 - 5118.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q. Li, S. Guo-Ross, D. V. Lewis, D. Turner, A. M. White, W. A. Wilson, and H. S. Swartzwelder
Dietary Prenatal Choline Supplementation Alters Postnatal Hippocampal Structure and Function
J Neurophysiol,
April 1, 2004;
91(4):
1545 - 1555.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. S. L. Faber and P. Sah
Opioids Inhibit Lateral Amygdala Pyramidal Neurons by Enhancing a Dendritic Potassium Current
J. Neurosci.,
March 24, 2004;
24(12):
3031 - 3039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. S. Monaghan, D. C. H. Benton, P. K. Bahia, R. Hosseini, Y. A. Shah, D. G. Haylett, and G. W. J. Moss
The SK3 Subunit of Small Conductance Ca2+-activated K+ Channels Interacts with Both SK1 and SK2 Subunits in a Heterologous Expression System
J. Biol. Chem.,
January 9, 2004;
279(2):
1003 - 1009.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. E. Hallworth, C. J. Wilson, and M. D. Bevan
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
J. Neurosci.,
August 20, 2003;
23(20):
7525 - 7542.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. SAH, E. S. L. FABER, M. LOPEZ DE ARMENTIA, and J. POWER
The Amygdaloid Complex: Anatomy and Physiology
Physiol Rev,
July 1, 2003;
83(3):
803 - 834.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. S. L. Faber and P. Sah
Calcium-Activated Potassium Channels: Multiple Contributions to Neuronal Function
Neuroscientist,
June 1, 2003;
9(3):
181 - 194.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
D. G. RAINNIE
Inhibitory and Excitatory Circuitries in Amygdala Nuclei: A Synopsis of Session II
Ann. N.Y. Acad. Sci.,
April 1, 2003;
985(1):
59 - 66.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Sailer, H. Hu, W. A. Kaufmann, M. Trieb, C. Schwarzer, J. F. Storm, and H.-G. Knaus
Regional Differences in Distribution and Functional Expression of Small-Conductance Ca2+-Activated K+ Channels in Rat Brain
J. Neurosci.,
November 15, 2002;
22(22):
9698 - 9707.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|