 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, May 15, 1998, 18(10):3574-3588
Dendritic Low-Threshold Calcium Currents in Thalamic Relay Cells
Alain Destexhe1, Mike Neubig1, Daniel Ulrich2, and John Huguenard2 1 Laboratoire de Neurophysiologie, Faculté de Médecine, Université Laval, Quebec G1K 7P4, Canada, and 2 Department of Neurology and Neurological Sciences, Stanford University Medical Center, Stanford, California 94305
The low-threshold calcium current (IT) underlies burst generation in thalamocortical (TC) relay cells and plays a central role in the genesis of synchronized oscillations by thalamic circuits. Here we have combined in vitro recordings and computational modeling techniques to investigate the consequences of dendritically located IT in TC cells. Simulations of a reconstructed TC cell were compared with the recordings obtained in the same cell to constrain the values of its passive parameters. T-current densities in soma and proximal dendrites were then estimated by matching the model to voltage-clamp recordings obtained in dissociated TC cells, which lack most of the dendrites. The distal dendritic T-current density was constrained by recordings in intact TC cells, which show 5-14 times larger peak T-current amplitudes compared with dissociated cells. Comparison of the model with the recordings of the same cell constrained further the T-current density in dendrites, which had to be 4.5-7.6 times higher than in the soma to reproduce all experimental results. Similar conclusions were reached using a simplified three-compartment model. Functionally, the model shows that the same amount of T-channels can lead to different bursting behaviors if they are exclusively somatic or distributed throughout the dendrites. In conclusion, this combination of models and experiments shows that dendritic T-currents are necessary to reproduce low-threshold calcium electrogenesis in TC cells. Dendritic T-current may also have significant functional consequences, such as an efficient modulation of thalamic burst discharges by corticothalamic feedback.
Key words: computational models; voltage clamp; bursting; oscillations; low-threshold spikes; dendritic calcium currents
Copyright © 1998 Society for Neuroscience 0270-6474/98/18103574-15$05.00/0
This article has been cited by other articles:
Y. Guo, J. E. Rubin, C. C. McIntyre, J. L. Vitek, and D. Terman
Thalamocortical Relay Fidelity Varies Across Subthalamic Nucleus Deep Brain Stimulation Protocols in a Data-Driven Computational Model
J Neurophysiol, March 1, 2008; 99(3): 1477 - 1492.
[Abstract] [Full Text] [PDF]
M. J. Birdno, S. E. Cooper, A. R. Rezai, and W. M. Grill
Pulse-to-Pulse Changes in the Frequency of Deep Brain Stimulation Affect Tremor and Modeled Neuronal Activity
J Neurophysiol, September 1, 2007; 98(3): 1675 - 1684.
[Abstract] [Full Text] [PDF]
C. J. Lacey, J. P. Bolam, and P. J. Magill
Novel and Distinct Operational Principles of Intralaminar Thalamic Neurons and Their Striatal Projections
J. Neurosci., April 18, 2007; 27(16): 4374 - 4384.
[Abstract] [Full Text] [PDF]
J. J. Lawrence, F. Saraga, J. F. Churchill, J. M. Statland, K. E. Travis, F. K. Skinner, and C. J. McBain
Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons.
J. Neurosci., November 22, 2006; 26(47): 12325 - 12338.
[Abstract] [Full Text] [PDF]
A. V. M. Herz, T. Gollisch, C. K. Machens, and D. Jaeger
Modeling single-neuron dynamics and computations: a balance of detail and abstraction.
Science, October 6, 2006; 314(5796): 80 - 85.
[Abstract] [Full Text] [PDF]
M. Miyata and K. Imoto
Different composition of glutamate receptors in corticothalamic and lemniscal synaptic responses and their roles in the firing responses of ventrobasal thalamic neurons in juvenile mice
J. Physiol., August 15, 2006; 575(1): 161 - 174.
[Abstract] [Full Text] [PDF]
H. Khosravani and G. W. Zamponi
Voltage-gated calcium channels and idiopathic generalized epilepsies.
Physiol Rev, July 1, 2006; 86(3): 941 - 966.
[Abstract] [Full Text] [PDF]
A. Traboulsie, J. Chemin, E. Kupfer, J. Nargeot, and P. Lory
T-Type Calcium Channels Are Inhibited by Fluoxetine and Its Metabolite Norfluoxetine
Mol. Pharmacol., June 1, 2006; 69(6): 1963 - 1968.
[Abstract] [Full Text] [PDF]
P. A Rhodes and R. Llinas
A model of thalamocortical relay cells
J. Physiol., June 15, 2005; 565(3): 765 - 781.
[Abstract] [Full Text] [PDF]
I. Vitko, Y. Chen, J. M. Arias, Y. Shen, X.-R. Wu, and E. Perez-Reyes
Functional Characterization and Neuronal Modeling of the Effects of Childhood Absence Epilepsy Variants of CACNA1H, a T-Type Calcium Channel
J. Neurosci., May 11, 2005; 25(19): 4844 - 4855.
[Abstract] [Full Text] [PDF]
R. D. Traub, D. Contreras, M. O. Cunningham, H. Murray, F. E. N. LeBeau, A. Roopun, A. Bibbig, W. B. Wilent, M. J. Higley, and M. A. Whittington
Single-Column Thalamocortical Network Model Exhibiting Gamma Oscillations, Sleep Spindles, and Epileptogenic Bursts
J Neurophysiol, April 1, 2005; 93(4): 2194 - 2232.
[Abstract] [Full Text] [PDF]
H. J. Alitto, T. G. Weyand, and W. M. Usrey
Distinct Properties of Stimulus-Evoked Bursts in the Lateral Geniculate Nucleus
J. Neurosci., January 12, 2005; 25(2): 514 - 523.
[Abstract] [Full Text] [PDF]
P. Isope and T. H. Murphy
Low threshold calcium currents in rat cerebellar Purkinje cell dendritic spines are mediated by T-type calcium channels
J. Physiol., January 1, 2005; 562(1): 257 - 269.
[Abstract] [Full Text] [PDF]
J. Murbartian, J. M. Arias, and E. Perez-Reyes
Functional Impact of Alternative Splicing of Human T-Type Cav3.3 Calcium Channels
J Neurophysiol, December 1, 2004; 92(6): 3399 - 3407.
[Abstract] [Full Text] [PDF]
J. H. Goldberg, C. O. Lacefield, and R. Yuste
Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting
J. Physiol., July 15, 2004; 558(2): 465 - 478.
[Abstract] [Full Text] [PDF]
Y. Zhang, A. P. Vilaythong, D. Yoshor, and J. L. Noebels
Elevated Thalamic Low-Voltage-Activated Currents Precede the Onset of Absence Epilepsy in the SNAP25-Deficient Mouse Mutant Coloboma
J. Neurosci., June 2, 2004; 24(22): 5239 - 5248.
[Abstract] [Full Text] [PDF]
I. Song, D. Kim, S. Choi, M. Sun, Y. Kim, and H.-S. Shin
Role of the {alpha}1G T-Type Calcium Channel in Spontaneous Absence Seizures in Mutant Mice
J. Neurosci., June 2, 2004; 24(22): 5249 - 5257.
[Abstract] [Full Text] [PDF]
A. Massaux, G. Dutrieux, N. Cotillon-Williams, Y. Manunta, and J.-M. Edeline
Auditory Thalamus Bursts in Anesthetized and Non-Anesthetized States: Contribution to Functional Properties
J Neurophysiol, May 1, 2004; 91(5): 2117 - 2134.
[Abstract] [Full Text] [PDF]
C. C. McIntyre, W. M. Grill, D. L. Sherman, and N. V. Thakor
Cellular Effects of Deep Brain Stimulation: Model-Based Analysis of Activation and Inhibition
J Neurophysiol, April 1, 2004; 91(4): 1457 - 1469.
[Abstract] [Full Text] [PDF]
R. Ruscheweyh, H. Ikeda, B. Heinke, and J. Sandkuhler
Distinctive membrane and discharge properties of rat spinal lamina I projection neurones in vitro
J. Physiol., March 1, 2004; 555(2): 527 - 543.
[Abstract] [Full Text] [PDF]
A. DESTEXHE and T. J. SEJNOWSKI
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations
Physiol Rev, October 1, 2003; 83(4): 1401 - 1453.
[Abstract] [Full Text] [PDF]
A. T. Schaefer, M. E. Larkum, B. Sakmann, and A. Roth
Coincidence Detection in Pyramidal Neurons Is Tuned by Their Dendritic Branching Pattern
J Neurophysiol, June 1, 2003; 89(6): 3143 - 3154.
[Abstract] [Full Text] [PDF]
M. Rudolph and A. Destexhe
A Fast-Conducting, Stochastic Integrative Mode for Neocortical Neurons InVivo
J. Neurosci., March 15, 2003; 23(6): 2466 - 2476.
[Abstract] [Full Text] [PDF]
D. M. Porcello, S. D. Smith, and J. R. Huguenard
Actions of U-92032, a T-Type Ca2+ Channel Antagonist, Support a Functional Linkage Between IT and Slow Intrathalamic Rhythms
J Neurophysiol, January 1, 2003; 89(1): 177 - 185.
[Abstract] [Full Text] [PDF]
B. Doiron, L. Noonan, N. Lemon, and R. W. Turner
Persistent Na+ Current Modifies Burst Discharge By Regulating Conditional Backpropagation of Dendritic Spikes
J Neurophysiol, January 1, 2003; 89(1): 324 - 337.
[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]
Y. Zhang, M. Mori, D. L. Burgess, and J. L. Noebels
Mutations in High-Voltage-Activated Calcium Channel Genes Stimulate Low-Voltage-Activated Currents in Mouse Thalamic Relay Neurons
J. Neurosci., August 1, 2002; 22(15): 6362 - 6371.
[Abstract] [Full Text] [PDF]
S. S. Sidach and I. M. Mintz
Kurtoxin, A Gating Modifier of Neuronal High- and Low-Threshold Ca Channels
J. Neurosci., March 15, 2002; 22(6): 2023 - 2034.
[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]
H.-y. Jung, N. P. Staff, and N. Spruston
Action Potential Bursting in Subicular Pyramidal Neurons Is Driven by a Calcium Tail Current
J. Neurosci., May 15, 2001; 21(10): 3312 - 3321.
[Abstract] [Full Text] [PDF]
C. Gutierrez, C. L. Cox, J. Rinzel, and S. M. Sherman
Dynamics of Low-Threshold Spike Activation in Relay Neurons of the Cat Lateral Geniculate Nucleus
J. Neurosci., February 1, 2001; 21(3): 1022 - 1032.
[Abstract] [Full Text] [PDF]
X. J. Zhan, C. L. Cox, and S. M. Sherman
Dendritic Depolarization Efficiently Attenuates Low-Threshold Calcium Spikes in Thalamic Relay Cells
J. Neurosci., May 15, 2000; 20(10): 3909 - 3914.
[Abstract] [Full Text] [PDF]
B. S. Mleux and L. E. Moore
Active Dendritic Membrane Properties of Xenopus Larval Spinal Neurons Analyzed With a Whole Cell Soma Voltage Clamp
J Neurophysiol, March 1, 2000; 83(3): 1381 - 1393.
[Abstract] [Full Text] [PDF]
S. R. Williams and G. J. Stuart
Action Potential Backpropagation and Somato-dendritic Distribution of Ion Channels in Thalamocortical Neurons
J. Neurosci., February 15, 2000; 20(4): 1307 - 1317.
[Abstract] [Full Text] [PDF]
L. E. Moore, N. Chub, J. Tabak, and M. O'Donovan
NMDA-Induced Dendritic Oscillations during a Soma Voltage Clamp of Chick Spinal Neurons
J. Neurosci., October 1, 1999; 19(19): 8271 - 8280.
[Abstract] [Full Text] [PDF]
X. J. Zhan, C. L. Cox, J. Rinzel, and S. M. Sherman
Current Clamp and Modeling Studies of Low-Threshold Calcium Spikes in Cells of the Cat's Lateral Geniculate Nucleus
J Neurophysiol, May 1, 1999; 81(5): 2360 - 2373.
[Abstract] [Full Text] [PDF]
E. M. Talley, L. L. Cribbs, J.-H. Lee, A. Daud, E. Perez-Reyes, and D. A. Bayliss
Differential Distribution of Three Members of a Gene Family Encoding Low Voltage-Activated (T-Type) Calcium Channels
J. Neurosci., March 15, 1999; 19(6): 1895 - 1911.
[Abstract] [Full Text] [PDF]
V. Gauck, M. Thomann, D. Jaeger, and A. Borst
Spatial Distribution of Low- and High-Voltage-Activated Calcium Currents in Neurons of the Deep Cerebellar Nuclei
J. Neurosci., August 1, 2001; 21(15): RC158 - RC158.
[Abstract] [Full Text] [PDF]
J. Chemin, A. Monteil, E. Perez-Reyes, E. Bourinet, J. Nargeot, and P. Lory
Specific contribution of human T-type calcium channel isotypes (alpha1G, alpha1H and alpha1I) to neuronal excitability
J. Physiol., April 1, 2002; 540(1): 3 - 14.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|