Journal of Neurophysiology, Vol 76, Issue 2 668-682, Copyright © 1996 by APS

ARTICLES

Layer I neurons of the rat neocortex. II. Voltage-dependent outward currents

F. M. Zhou and J. J. Hablitz
Neurobiology Research Center, University of Alabama at Birmingham 35294, USA.

1. Whole cell patch-clamp techniques, combined with direct visualization of neurons, were used to study voltage-dependent potassium currents in layer 1 neurons and layer II/III pyramidal cells. 2. In the presence of tetrodotoxin, step depolarizations evoked an outward current. This current had a complex waveform and appeared to be a composite of early and late components. The early peak of the composite K+ outward current was larger in layer I neurons. 3. In both layer I and pyramidal cells, the composite outward K+ current could be separated into two components based on kinetic and pharmacological properties. The early component was termed I(A) because it was a transient outward current activating rapidly and then decaying. I(A) was more sensitive to blocking by 4-aminopyridine (4-AP) than tetraethylammonium (TEA). The second component, termed the delayed rectifier or I(DR), activated relatively slowly and did not decay significantly during a 200-ms test pulse. I(DR) was insensitive to blocking by 4-AP at concentrations up to 4 mM and blocked by > 60% by 40-60 mM TEA. 4. I(A) kinetics were examined in the presence of 40-60 mM TEA. Under these conditions, I(A) began to activate between -40 and -30 mV. Half-maximal activation occurred around 0 mV. In both layer I and pyramidal cells, the half-inactivation potential (Vh-inact) was around or more positive than -50 mV. At -60 mV, > 70% of I(A) conductance was available. I(A) decayed along a single exponential time course with a time constant of approximately 15 ms. This decay showed little voltage dependence. 5. In both layer I and pyramidal cells, I(DR) was studied in the presence of 4 mM 4-AP to block I(A) and in saline containing 0.2 mM Ca2+ and 3.6 mM Mg2+ to reduce contributions from Ca2+-dependent K+ currents. Under these conditions, I(DR) began to activate at -35 to -25 mV with Vh-act of 3.6 +/- 4.5 mV (mean +/- SD). The 10-90% rise time of I(DR) was 15 ms at 30 mV. At 2.2 ms after the onset of the command potential to +30 mV, I(DR) could reach a significant amplitude (approximately 1.5 nA in layer I neurons and 2.2 nA in pyramidal cells depending on the cell size). When long test pulses (> or = 1,000 ms) were used, a decay time constant approximately 800 ms at +40 mV was observed. In both layer I and pyramidal cells, steady state inactivation of I(DR) was minimal. 6. These results indicate that I(A) and I(DR) are the two major hyperpolarizing currents in layer I and pyramidal cells. The kinetics and pharmacological properties of I(A) and I(DR) were not significantly different in fast-spiking layer I neurons and regular-spiking layer II/III pyramidal cells. The relatively positive activation threshold (more than or equal to -40 mV) of both I(A) and I(DR) suggest that they do not play a role in neuronal behavior below action potential (AP) threshold and that their properties are more suitable to repolarize AP. The greater density of I(A) in layer I neurons appears responsible for fast spike generation.

This article has been cited by other articles:

				D. Guan, T. Tkatch, D. J. Surmeier, W. E. Armstrong, and R. C. Foehring Kv2 subunits underlie slowly inactivating potassium current in rat neocortical pyramidal neurons J. Physiol., June 15, 2007; 581(3): 941 - 960. [Abstract] [Full Text] [PDF]

				D. Guan, J. C. F. Lee, M. H. Higgs, W. J. Spain, and R. C. Foehring Functional Roles of Kv1 Channels in Neocortical Pyramidal Neurons J Neurophysiol, March 1, 2007; 97(3): 1931 - 1940. [Abstract] [Full Text] [PDF]

				D. Guan, J. C. F. Lee, T. Tkatch, D. J. Surmeier, W. E. Armstrong, and R. C. Foehring Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones J. Physiol., March 1, 2006; 571(2): 371 - 389. [Abstract] [Full Text] [PDF]

				Y. Dong and F. J. White Dopamine D1-Class Receptors Selectively Modulate a Slowly Inactivating Potassium Current in Rat Medial Prefrontal Cortex Pyramidal Neurons J. Neurosci., April 1, 2003; 23(7): 2686 - 2695. [Abstract] [Full Text] [PDF]

				H. L. P. Bahrey and W. J. Moody Voltage-gated Currents, Dye and Electrical Coupling in the Embryonic Mouse Neocortex Cereb Cortex, March 1, 2003; 13(3): 239 - 251. [Abstract] [Full Text] [PDF]

				R. A. DeFazio and S. M. Moenter Estradiol Feedback Alters Potassium Currents and Firing Properties of Gonadotropin-Releasing Hormone Neurons Mol. Endocrinol., October 1, 2002; 16(10): 2255 - 2265. [Abstract] [Full Text] [PDF]

				A. Bordey and H. Sontheimer Differential Inhibition of Glial K+ Currents by 4-AP J Neurophysiol, December 1, 1999; 82(6): 3476 - 3487. [Abstract] [Full Text] [PDF]

				J.-M. Mienville Feature Article: Cajal-Retzius Cell Physiology: Just in Time to Bridge the 20th Century Cereb Cortex, December 1, 1999; 9(8): 776 - 782. [Abstract] [Full Text] [PDF]

				F.-M. Zhou and J. J. Hablitz Metabotropic Glutamate Receptor Enhancement of Spontaneous IPSCs in Neocortical Interneurons J Neurophysiol, November 1, 1997; 78(5): 2287 - 2295. [Abstract] [Full Text] [PDF]