 |
Next Article 
Volume 16, Number 18,
Issue of September 15, 1996
pp. 5567-5582
Copyright ©1996 Society for Neuroscience
Multiple Channel Types Contribute to the Low-Voltage-Activated
Calcium Current in Hippocampal CA3 Pyramidal Neurons
Received April 18, 1996; revised June 17, 1996; accepted June 18, 1996.
Robert B. Avery and
Daniel Johnston
Division of Neuroscience, Baylor College of Medicine, Houston,
Texas 77030
Hippocampal neurons exhibit low-voltage-activated (LVA) and
high-voltage-activated (HVA) calcium currents. We characterized the LVA
current by recording whole-cell Ca2+ currents from acutely
isolated rat hippocampal CA3 pyramidal neurons in 2 m
Ca2+.
Long depolarizing steps to 50 mV revealed two components to the LVA
current: transient and sustained. The transient phase had a fast decay
time constant of 59 msec. The sustained phase persisted throughout the
depolarization, even for steps lasting several seconds. The transient
current was inhibited by the classic T-type channel antagonists
Ni2+ and amiloride. The anticonvulsant phenytoin
preferentially blocked the sustained phase, but ethosuximide had no
effect. Steady-state inactivation of the transient component was
half-maximal at 80 mV.
Nimodipine, an L-type channel antagonist, partly inhibited the
sustained current. BayK-8644, an L-type channel agonist, potentiated
the sustained current. Calciseptine, another L-type channel antagonist,
inhibited the sustained component. -Conotoxin-MVIIC, a nonselective
toxin for HVA channels, had no effect on either of the LVA current
components. -Grammotoxin-SIA, another nonselective toxin, partially
inhibited the sustained component. The voltage dependence of activation
of the nimodipine-sensitive current could be fit with a single
Boltzmann, consistent with a homogenous population of L-type channels
in CA3 neurons. Half-maximal activation of the nimodipine-sensitive
current occurred at 30 mV, considerably more negative than the
remaining HVA current.
These results suggest that in physiologic Ca2+ more than
one type of Ca2+ channel contributes to the LVA current in
CA3 neurons. The transient current is carried by T-type channels. The
sustained current is carried, at least in part, by
dihydropyridine-sensitive channels. Thus, the designation
``low-voltage-activated'' should not be limited to T-type channels.
These findings challenge the traditional designation of L-type channels
as exclusively HVA and reveal a possible role in subthreshold
Ca2+ signaling.
Key words:
calcium channels;
hippocampus;
CA3;
whole-cell patch;
low-voltage-activated;
T-type;
L-type;
nimodipine;
ethosuximide;
phenytoin
This article has been cited by other articles:

|
 |

|
 |
 
S. Liu and M. T. Shipley
Multiple Conductances Cooperatively Regulate Spontaneous Bursting in Mouse Olfactory Bulb External Tufted Cells
J. Neurosci.,
February 13, 2008;
28(7):
1625 - 1639.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Inoue and B. W. Strowbridge
Transient Activity Induces a Long-Lasting Increase in the Excitability of Olfactory Bulb Interneurons
J Neurophysiol,
January 1, 2008;
99(1):
187 - 199.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Nikitina, Z.-D. Zhang, A. Kawashima, B. S. Jahromi, V. A. Bouryi, M. Takahashi, A. Xie, and R. L. Macdonald
Voltage-dependent calcium channels of dog basilar artery
J. Physiol.,
April 15, 2007;
580(2):
523 - 541.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Diana, Y. Otsu, G. Maton, T. Collin, M. Chat, and S. Dieudonne
T-Type and L-Type Ca2+ Conductances Define and Encode the Bimodal Firing Pattern of Vestibulocerebellar Unipolar Brush Cells
J. Neurosci.,
April 4, 2007;
27(14):
3823 - 3838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Tai, J. B. Kuzmiski, and B. A. MacVicar
Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons.
J. Neurosci.,
June 7, 2006;
26(23):
6249 - 6258.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. D. Helton, W. Xu, and D. Lipscombe
Neuronal L-Type Calcium Channels Open Quickly and Are Inhibited Slowly
J. Neurosci.,
November 2, 2005;
25(44):
10247 - 10251.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Chen, C. Yue, and Y. Yaari
A transitional period of Ca2+-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells
J. Physiol.,
August 15, 2005;
567(1):
79 - 93.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Olson, T. Tkatch, S. Hernandez-Lopez, S. Ulrich, E. Ilijic, E. Mugnaini, H. Zhang, I. Bezprozvanny, and D. J. Surmeier
G-Protein-Coupled Receptor Modulation of Striatal CaV1.3 L-Type Ca2+ Channels Is Dependent on a Shank-Binding Domain
J. Neurosci.,
February 2, 2005;
25(5):
1050 - 1062.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Power and P. Sah
Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials
J. Physiol.,
January 15, 2005;
562(2):
439 - 453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Lipscombe, T. D. Helton, and W. Xu
L-Type Calcium Channels: The Low Down
J Neurophysiol,
November 1, 2004;
92(5):
2633 - 2641.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. Jackson, G. L. Yao, and B. P. Bean
Mechanism of Spontaneous Firing in Dorsomedial Suprachiasmatic Nucleus Neurons
J. Neurosci.,
September 15, 2004;
24(37):
7985 - 7998.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Maravall, E. A. Stern, and K. Svoboda
Development of Intrinsic Properties and Excitability of Layer 2/3 Pyramidal Neurons During a Critical Period for Sensory Maps in Rat Barrel Cortex
J Neurophysiol,
July 1, 2004;
92(1):
144 - 156.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Zhou, S.-A. Kim, E. A. Kirk, A. L. Tippens, H. Sun, F. Haeseleer, and A. Lee
Ca2+-Binding Protein-1 Facilitates and Forms a Postsynaptic Complex with Cav1.2 (L-Type) Ca2+ Channels
J. Neurosci.,
May 12, 2004;
24(19):
4698 - 4708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. R. Johnson, P. Kloppenburg, and R. M. Harris-Warrick
Dopamine Modulation of Calcium Currents in Pyloric Neurons of the Lobster Stomatogastric Ganglion
J Neurophysiol,
August 1, 2003;
90(2):
631 - 643.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Habermann, B. J. O'Brien, H. Wassle, and D. A. Protti
AII Amacrine Cells Express L-Type Calcium Channels at Their Output Synapses
J. Neurosci.,
July 30, 2003;
23(17):
6904 - 6913.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Frick, J. Magee, H. J. Koester, M. Migliore, and D. Johnston
Normalization of Ca2+ Signals by Small Oblique Dendrites of CA1 Pyramidal Neurons
J. Neurosci.,
April 15, 2003;
23(8):
3243 - 3250.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Isaacson and H. Vitten
GABAB Receptors Inhibit Dendrodendritic Transmission in the Rat Olfactory Bulb
J. Neurosci.,
March 15, 2003;
23(6):
2032 - 2039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Perez-Reyes
Molecular Physiology of Low-Voltage-Activated T-type Calcium Channels
Physiol Rev,
January 1, 2003;
83(1):
117 - 161.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Sukhareva, S. V. Smith, D. Maric, and J. L. Barker
Functional Properties of Ryanodine Receptors in Hippocampal Neurons Change During Early Differentiation in Culture
J Neurophysiol,
September 1, 2002;
88(3):
1077 - 1087.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-F. Zhang, D. C. Cooper, and F. J. White
Repeated Cocaine Treatment Decreases Whole-Cell Calcium Current in Rat Nucleus Accumbens Neurons
J. Pharmacol. Exp. Ther.,
June 1, 2002;
301(3):
1119 - 1125.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Su, D. Sochivko, A. Becker, J. Chen, Y. Jiang, Y. Yaari, and H. Beck
Upregulation of a T-Type Ca2+ Channel Causes a Long-Lasting Modification of Neuronal Firing Mode after Status Epilepticus
J. Neurosci.,
May 1, 2002;
22(9):
3645 - 3655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Isomura, Y. Fujiwara-Tsukamoto, M. Imanishi, A. Nambu, and M. Takada
Distance-Dependent Ni2+-Sensitivity of Synaptic Plasticity in Apical Dendrites of Hippocampal CA1 Pyramidal Cells
J Neurophysiol,
February 1, 2002;
87(2):
1169 - 1174.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Yamakage and A. Namiki
Calcium channels - basic aspects of their structure, function and gene encoding; anesthetic action on the channels - a review: [Revue : notions de base sur la structure, la fonction et l'encodage genetique des canaux calciques et action des anesthesiques sur ces canaux]
Can J Anesth,
February 1, 2002;
49(2):
151 - 164.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Gomora, A. N. Daud, M. Weiergraber, and E. Perez-Reyes
Block of Cloned Human T-Type Calcium Channels by Succinimide Antiepileptic Drugs
Mol. Pharmacol.,
November 1, 2001;
60(5):
1121 - 1132.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Xu and D. Lipscombe
Neuronal CaV1.3{alpha}1 L-Type Channels Activate at Relatively Hyperpolarized Membrane Potentials and Are Incompletely Inhibited by Dihydropyridines
J. Neurosci.,
August 15, 2001;
21(16):
5944 - 5951.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-P. Fan, E. M. Horn, and T. G. Waldrop
Biophysical Characterization of Rat Caudal Hypothalamic Neurons: Calcium Channel Contribution to Excitability
J Neurophysiol,
December 1, 2000;
84(6):
2896 - 2903.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Shah and D. G. Haylett
Ca2+ Channels Involved in the Generation of the Slow Afterhyperpolarization in Cultured Rat Hippocampal Pyramidal Neurons
J Neurophysiol,
May 1, 2000;
83(5):
2554 - 2561.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. G. Mermelstein, H. Bito, K. Deisseroth, and R. W. Tsien
Critical Dependence of cAMP Response Element-Binding Protein Phosphorylation on L-Type Calcium Channels Supports a Selective Response to EPSPs in Preference to Action Potentials
J. Neurosci.,
January 1, 2000;
20(1):
266 - 273.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Larkum, K. M. M. Kaiser, and B. Sakmann
Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials
PNAS,
December 7, 1999;
96(25):
14600 - 14604.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Magee and M. Carruth
Dendritic Voltage-Gated Ion Channels Regulate the Action Potential Firing Mode of Hippocampal CA1 Pyramidal Neurons
J Neurophysiol,
October 1, 1999;
82(4):
1895 - 1901.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Morisset and F. Nagy
Ionic Basis for Plateau Potentials in Deep Dorsal Horn Neurons of the Rat Spinal Cord
J. Neurosci.,
September 1, 1999;
19(17):
7309 - 7316.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Bianchi, S. R. Young, and R. K. S. Wong
Group I mGluR Activation Causes Voltage-Dependent and -Independent Ca2+ Rises in Hippocampal Pyramidal Cells
J Neurophysiol,
June 1, 1999;
81(6):
2903 - 2913.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. M. DAVILA
Molecular and Functional Diversity of Voltage-Gated Calcium Channels
Ann. N.Y. Acad. Sci.,
April 30, 1999;
868(1):
102 - 117.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. PEREZ-REYES, J.-H. LEE, and L. L. CRIBBS
Molecular Characterization of Two Members of the T-Type Calcium Channel Family
Ann. N.Y. Acad. Sci.,
April 30, 1999;
868(1):
131 - 143.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. N. Coogan, D. M. O'Leary, and J. J. O'Connor
P42/44 MAP Kinase Inhibitor PD98059 Attenuates Multiple Forms of Synaptic Plasticity in Rat Dentate Gyrus In Vitro
J Neurophysiol,
January 1, 1999;
81(1):
103 - 110.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. S. McDowell, J. J. Pancrazio, P. Q. Barrett, and C. Lynch III
Volatile Anesthetic Sensitivity of T-Type Calcium Currents in Various Cell Types
Anesth. Analg.,
January 1, 1999;
88(1):
168 - 173.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. N. Urban, D. A. Henze, and G. Barrionuevo
Amplification of Perforant-Path EPSPs in CA3 Pyramidal Cells by LVA Calcium and Sodium Channels
J Neurophysiol,
September 1, 1998;
80(3):
1558 - 1561.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. H. Lee and C. J. Heckman
Bistability in Spinal Motoneurons In Vivo: Systematic Variations in Persistent Inward Currents
J Neurophysiol,
August 1, 1998;
80(2):
583 - 593.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kapur, M. F. Yeckel, R. Gray, and D. Johnston
L-Type Calcium Channels Are Required for One Form of Hippocampal Mossy Fiber LTP
J Neurophysiol,
April 1, 1998;
79(4):
2181 - 2190.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. Todorovic and C. J. Lingle
Pharmacological Properties of T-Type Ca2+ Current in Adult Rat Sensory Neurons: Effects of Anticonvulsant and Anesthetic Agents
J Neurophysiol,
January 1, 1998;
79(1):
240 - 252.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Kollmar, L. G. Montgomery, J. Fak, L. J. Henry, and A. J. Hudspeth
Predominance of the alpha 1D subunit in L-type voltage-gated Ca2+ channels of hair cells in the chicken's cochlea
PNAS,
December 23, 1997;
94(26):
14883 - 14888.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. S. Piedras-Renteria, C.-C. Chen, and P. M. Best
Antisense oligonucleotides against rat brain alpha 1E DNA and its atrial homologue decrease T-type calcium current in atrial myocytes
PNAS,
December 23, 1997;
94(26):
14936 - 14941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Wang, M. J. Rowan, and R. Anwyl
LTP Induction Dependent on Activation of Ni2+-Sensitive Voltage-Gated Calcium Channels, but not NMDA Receptors, in the Rat Dentate Gyrus In Vitro
J Neurophysiol,
November 1, 1997;
78(5):
2574 - 2581.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Margeta-Mitrovic, J. J. Grigg, K. Koyano, Y. Nakajima, and S. Nakajima
Neurotensin and Substance P Inhibit Low- and High-Voltage-Activated Ca2+ Channels in Cultured Newborn Rat Nucleus Basalis Neurons
J Neurophysiol,
September 1, 1997;
78(3):
1341 - 1352.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Svirskis and J. Hounsgaard
Depolarization-Induced Facilitation of a Plateau-Generating Current in Ventral Horn Neurons in the Turtle Spinal Cord
J Neurophysiol,
September 1, 1997;
78(3):
1740 - 1742.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. T. Kavalali, K. S. Hwang, and M. R. Plummer
cAMP-Dependent Enhancement of Dihydropyridine-Sensitive Calcium Channel Availability in Hippocampal Neurons
J. Neurosci.,
July 15, 1997;
17(14):
5334 - 5348.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Hernandez-Lopez, J. Bargas, D. J. Surmeier, A. Reyes, and E. Galarraga
D1 Receptor Activation Enhances Evoked Discharge in Neostriatal Medium Spiny Neurons by Modulating an L-Type Ca2+ Conductance
J. Neurosci.,
May 1, 1997;
17(9):
3334 - 3342.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Gillessen and C. Alzheimer
Amplification of EPSPs by Low Ni2+- and Amiloride-Sensitive Ca2+ Channels in Apical Dendrites of Rat CA1 Pyramidal Neurons
J Neurophysiol,
March 1, 1997;
77(3):
1639 - 1643.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. R. Christie, L. K. Schexnayder, and D. Johnston
Contribution of Voltage-Gated Ca2+ Channels to Homosynaptic Long-Term Depression in the CA1 Region In Vitro
J Neurophysiol,
March 1, 1997;
77(3):
1651 - 1655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. B. Avery and D. Johnston
Ca2+ Channel Antagonist U-92032 Inhibits Both T-Type Ca2+ Channels and Na+ Channels in Hippocampal CA1 Pyramidal Neurons
J Neurophysiol,
February 1, 1997;
77(2):
1023 - 1028.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Koschak, D. Reimer, I. Huber, M. Grabner, H. Glossmann, J. Engel, and J. Striessnig
alpha 1D (Cav1.3) Subunits Can Form L-type Ca2+ Channels Activating at Negative Voltages
J. Biol. Chem.,
June 15, 2001;
276(25):
22100 - 22106.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|