 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 17, Number 9, Issue of May 1, 1997 pp. 3136-3147
Copyright ©1997 Society for NeuroscienceDifferential Expression of K4-AP Currents and Kv3.1 Potassium Channel Transcripts in Cortical Neurons that Develop Distinct Firing Phenotypes
Received Nov. 26, 1996; revised Feb. 12, 1997; accepted Feb. 14, 1997.
Jennifer L. Massengill, Martin A. Smith, Dong Ik Son, and Diane K. O'Dowd Departments of Anatomy and Neurobiology and Developmental and Cell Biology, University of California, Irvine, California 92697-1280
Maturation of electrical excitability during early postnatal development is critical to formation of functional neural circuitry in the mammalian neocortex. Little is known, however, about the changes in gene expression underlying the development of firing properties that characterize different classes of cortical neurons. Here we describe the development of cortical neurons with two distinct firing phenotypes, regular-spiking (RS) and fast-spiking (FS), that appear to emerge from a population of immature multiple-spiking (IMS) neurons during the first two postnatal weeks, both in vivo (within layer IV) and in vitro. We report the expression of a slowly inactivating, 4-AP-sensitive potassium current (K4-AP) at significantly higher density in FS compared with RS neurons. The same current is expressed at intermediate levels in IMS neurons. The kinetic, voltage-dependent, and pharmacological properties of the K4-AP current are similar to those observed by heterologous expression of Kv3.1 potassium channel mRNA. Single-cell RT-PCR analysis demonstrates that PCR products representing Kv3.1 transcripts are amplified more frequently from FS than RS neurons, with an intermediate frequency of Kv3.1 detection in neurons with immature firing properties. Taken together, these data suggest that the Kv3.1 gene encodes the K4-AP current and that expression of this gene is regulated in a cell-specific manner during development. Analysis of the effects of 4-AP on firing properties suggests that the K4-AP current is important for rapid action potential repolarization, fast after-hyperpolarization, brief refractory period, and high firing frequency characteristic of FS GABAergic interneurons.
Key words: Kv3.1 mRNA; potassium currents; cortical neurons; development; single cell RT-PCR; fast spiking; regular spiking; mouse somatosensory cortex; firing properties
This article has been cited by other articles:
Q.-Q. Sun
Experience-Dependent Intrinsic Plasticity in Interneurons of Barrel Cortex Layer IV
J Neurophysiol, November 1, 2009; 102(5): 2955 - 2973.
[Abstract] [Full Text] [PDF]
D. L. Jones and S. C. Baraban
Inhibitory Inputs to Hippocampal Interneurons Are Reorganized in Lis1 Mutant Mice
J Neurophysiol, August 1, 2009; 102(2): 648 - 658.
[Abstract] [Full Text] [PDF]
F. V. Chirila, K. C. Rowland, J. M. Thompson, and G. A. Spirou
Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature
J. Physiol., October 1, 2007; 584(1): 167 - 190.
[Abstract] [Full Text] [PDF]
A. H. Gittis and S. du Lac
Firing Properties of GABAergic Versus Non-GABAergic Vestibular Nucleus Neurons Conferred by a Differential Balance of Potassium Currents
J Neurophysiol, June 1, 2007; 97(6): 3986 - 3996.
[Abstract] [Full Text] [PDF]
C. Itami, F. Kimura, and S. Nakamura
Brain-Derived Neurotrophic Factor Regulates the Maturation of Layer 4 Fast-Spiking Cells after the Second Postnatal Week in the Developing Barrel Cortex
J. Neurosci., February 28, 2007; 27(9): 2241 - 2252.
[Abstract] [Full Text] [PDF]
M. Martina, A. E. Metz, and B. P. Bean
Voltage-Dependent Potassium Currents During Fast Spikes of Rat Cerebellar Purkinje Neurons: Inhibition by BDS-I Toxin
J Neurophysiol, January 1, 2007; 97(1): 563 - 571.
[Abstract] [Full Text] [PDF]
A. Burkhalter, Y. Gonchar, R. L. Mellor, and J. M. Nerbonne
Differential Expression of IA Channel Subunits Kv4.2 and Kv4.3 in Mouse Visual Cortical Neurons and Synapses.
J. Neurosci., November 22, 2006; 26(47): 12274 - 12282.
[Abstract] [Full Text] [PDF]
M. M. Huntsman and J. R. Huguenard
Fast IPSCs in rat thalamic reticular nucleus require the GABAA receptor {beta}1 subunit
J. Physiol., April 15, 2006; 572(2): 459 - 475.
[Abstract] [Full Text] [PDF]
W. J. Moody and M. M. Bosma
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells
Physiol Rev, July 1, 2005; 85(3): 883 - 941.
[Abstract] [Full Text] [PDF]
S. P. Brandt
Microgenomics: gene expression analysis at the tissue-specific and single-cell levels
J. Exp. Bot., February 1, 2005; 56(412): 495 - 505.
[Abstract] [Full Text] [PDF]
R. Corlew, M. M Bosma, and W. J Moody
Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones
J. Physiol., October 15, 2004; 560(2): 377 - 390.
[Abstract] [Full Text] [PDF]
M. T. Perez-Garcia, O. Colinas, E. Miguel-Velado, A. Moreno-Dominguez, and J. R. Lopez-Lopez
Characterization of the Kv channels of mouse carotid body chemoreceptor cells and their role in oxygen sensing
J. Physiol., June 1, 2004; 557(2): 457 - 471.
[Abstract] [Full Text] [PDF]
M. F. Kramer, W. J. Cook, F. P. Roth, J. Zhu, H. Holman, D. M. Knipe, and D. M. Coen
Latent Herpes Simplex Virus Infection of Sensory Neurons Alters Neuronal Gene Expression
J. Virol., September 1, 2003; 77(17): 9533 - 9541.
[Abstract] [Full Text] [PDF]
X. Jin, H. Hu, P. H. Mathers, and A. Agmon
Brain-Derived Neurotrophic Factor Mediates Activity-Dependent Dendritic Growth in Nonpyramidal Neocortical Interneurons in Developing Organotypic Cultures
J. Neurosci., July 2, 2003; 23(13): 5662 - 5673.
[Abstract] [Full Text] [PDF]
H. L. Picken Bahrey and W. J. Moody
Early Development of Voltage-Gated Ion Currents and Firing Properties in Neurons of the Mouse Cerebral Cortex
J Neurophysiol, April 1, 2003; 89(4): 1761 - 1773.
[Abstract] [Full Text] [PDF]
I. Fukui and H. Ohmori
Developmental changes in membrane excitability and morphology of neurons in the nucleus angularis of the chicken
J. Physiol., April 1, 2003; 548(1): 219 - 232.
[Abstract] [Full Text] [PDF]
D. M. Porcello, C. S. Ho, R. H. Joho, and J. R. Huguenard
Resilient RTN Fast Spiking in Kv3.1 Null Mice Suggests Redundancy in the Action Potential Repolarization Mechanism
J Neurophysiol, March 1, 2002; 87(3): 1303 - 1310.
[Abstract] [Full Text] [PDF]
M. Martin-Caraballo and S. E. Dryer
Activity- and Target-Dependent Regulation of Large-Conductance Ca2+-Activated K+ Channels in Developing Chick Lumbar Motoneurons
J. Neurosci., January 1, 2002; 22(1): 73 - 81.
[Abstract] [Full Text] [PDF]
J. M. Bekkers and A. J. Delaney
Modulation of Excitability by {alpha}-Dendrotoxin-Sensitive Potassium Channels in Neocortical Pyramidal Neurons
J. Neurosci., September 1, 2001; 21(17): 6553 - 6560.
[Abstract] [Full Text] [PDF]
F. Espinosa, A. McMahon, E. Chan, S. Wang, C. S. Ho, N. Heintz, and R. H. Joho
Alcohol Hypersensitivity, Increased Locomotion, and Spontaneous Myoclonus in Mice Lacking the Potassium Channels Kv3.1 and Kv3.3
J. Neurosci., September 1, 2001; 21(17): 6657 - 6665.
[Abstract] [Full Text] [PDF]
X. Jin, P. H. Mathers, G. Szabo, Z. Katarova, and A. Agmon
Vertical Bias in Dendritic Trees of Non-pyramidal Neocortical Neurons Expressing GAD67-GFP In Vitro
Cereb Cortex, July 1, 2001; 11(7): 666 - 678.
[Abstract] [Full Text] [PDF]
G. J. Murphy and S. Du Lac
Postnatal Development of Spike Generation in Rat Medial Vestibular Nucleus Neurons
J Neurophysiol, May 1, 2001; 85(5): 1899 - 1906.
[Abstract] [Full Text] [PDF]
S. Parameshwaran, C. E. Carr, and T. M. Perney
Expression of the Kv3.1 Potassium Channel in the Avian Auditory Brainstem
J. Neurosci., January 15, 2001; 21(2): 485 - 494.
[Abstract] [Full Text] [PDF]
N. Lemon and R. W. Turner
Conditional Spike Backpropagation Generates Burst Discharge in a Sensory Neuron
J Neurophysiol, September 1, 2000; 84(3): 1519 - 1530.
[Abstract] [Full Text] [PDF]
J. M Bekkers
Properties of voltage-gated potassium currents in nucleated patches from large layer 5 cortical pyramidal neurons of the rat
J. Physiol., June 15, 2000; 525(3): 593 - 609.
[Abstract] [Full Text] [PDF]
T. Aoki and S. C. Baraban
Properties of a Calcium-Activated K+ Current on Interneurons in the Developing Rat Hippocampus
J Neurophysiol, June 1, 2000; 83(6): 3453 - 3461.
[Abstract] [Full Text] [PDF]
O. N. Osipenko, R. J. Tate, and A. M. Gurney
Potential Role for Kv3.1b Channels as Oxygen Sensors
Circ. Res., March 17, 2000; 86(5): 534 - 540.
[Abstract] [Full Text] [PDF]
P Wahle, T Gorba, M. Wirth, and K Obst-Pernberg
Specification of neuropeptide Y phenotype in visual cortical neurons by leukemia inhibitory factor
Development, January 5, 2000; 127(9): 1943 - 1951.
[Abstract] [PDF]
D. D. Dunning, C. L. Hoover, I. Soltesz, M. A. Smith, and D. K. O'Dowd
GABAA Receptor-Mediated Miniature Postsynaptic Currents and alpha -Subunit Expression in Developing Cortical Neurons
J Neurophysiol, December 1, 1999; 82(6): 3286 - 3297.
[Abstract] [Full Text] [PDF]
T. Gorba, O. Klostermann, and P. Wahle
Development of Neuronal Activity and Activity-dependent Expression of Brain-derived Neurotrophic Factor mRNA in Organotypic Cultures of Rat Visual Cortex
Cereb Cortex, December 1, 1999; 9(8): 864 - 877.
[Abstract] [Full Text] [PDF]
J. Mu, S.-y. Zhuang, M. T. Kirby, R. E. Hampson, and S. A. Deadwyler
Cannabinoid Receptors Differentially Modulate Potassium A and D Currents in Hippocampal Neurons in Culture
J. Pharmacol. Exp. Ther., November 1, 1999; 291(2): 893 - 902.
[Abstract] [Full Text]
R. H. Joho, C. S. Ho, and G. A. Marks
Increased gamma - and Decreased delta -Oscillations in a Mouse Deficient for a Potassium Channel Expressed in Fast-Spiking Interneurons
J Neurophysiol, October 1, 1999; 82(4): 1855 - 1864.
[Abstract] [Full Text] [PDF]
M. C. Angulo, J. Rossier, and E. Audinat
Postsynaptic Glutamate Receptors and Integrative Properties of Fast-Spiking Interneurons in the Rat Neocortex
J Neurophysiol, September 1, 1999; 82(3): 1295 - 1302.
[Abstract] [Full Text] [PDF]
R. Hernandez-Pineda, A. Chow, Y. Amarillo, H. Moreno, M. Saganich, E. V.-S. de Miera, A. Hernandez-Cruz, and B. Rudy
Kv3.1-Kv3.2 Channels Underlie a High-Voltage-Activating Component of the Delayed Rectifier K+ Current in Projecting Neurons From the Globus Pallidus
J Neurophysiol, September 1, 1999; 82(3): 1512 - 1528.
[Abstract] [Full Text] [PDF]
G. Baranauskas, T. Tkatch, and D. J. Surmeier
Delayed Rectifier Currents in Rat Globus Pallidus Neurons Are Attributable to Kv2.1 and Kv3.1/3.2 K+ Channels
J. Neurosci., August 1, 1999; 19(15): 6394 - 6404.
[Abstract] [Full Text] [PDF]
F. K. Skinner, L. Zhang, J. L. P. Velazquez, and P. L. Carlen
Bursting in Inhibitory Interneuronal Networks: A Role for Gap-Junctional Coupling
J Neurophysiol, March 1, 1999; 81(3): 1274 - 1283.
[Abstract] [Full Text] [PDF]
M. D. Whim and L. K. Kaczmarek
Heterologous Expression of the Kv3.1 Potassium Channel Eliminates Spike Broadening and the Induction of a Depolarizing Afterpotential in the Peptidergic Bag Cell Neurons
J. Neurosci., November 15, 1998; 18(22): 9171 - 9180.
[Abstract] [Full Text] [PDF]
S.-q. J. Liu and L. K. Kaczmarek
Depolarization Selectively Increases the Expression of the Kv3.1 Potassium Channel in Developing Inferior Colliculus Neurons
J. Neurosci., November 1, 1998; 18(21): 8758 - 8769.
[Abstract] [Full Text] [PDF]
M. Martina, J. H. Schultz, H. Ehmke, H. Monyer, and P. Jonas
Functional and Molecular Differences between Voltage-Gated K+ Channels of Fast-Spiking Interneurons and Pyramidal Neurons of Rat Hippocampus
J. Neurosci., October 15, 1998; 18(20): 8111 - 8125.
[Abstract] [Full Text] [PDF]
R. Delgado, R. Davis, M. R. Bono, R. Latorre, and P. Labarca
Outward Currents in Drosophila Larval Neurons: dunce Lacks a Maintained Outward Current Component Downregulated by cAMP
J. Neurosci., February 15, 1998; 18(4): 1399 - 1407.
[Abstract] [Full Text] [PDF]
D. J. Baro, R. M. Levini, M. T. Kim, A. R. Willms, C. C. Lanning, H. E. Rodriguez, and R. M. Harris-Warrick
Quantitative Single-Cell-Reverse Transcription-PCR Demonstrates That A-Current Magnitude Varies as a Linear Function of shal Gene Expression in Identified Stomatogastric Neurons
J. Neurosci., September 1, 1997; 17(17): 6597 - 6610.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|