Characterization of Outward Currents in Neurons of the Avian Nucleus Magnocellularis

Abstract

Characterization of outward currents in neurons of the avian nucleus magnocellularis. J. Neurophysiol. 80: 2824-2835, 1998. Neurons of the nucleus magnocellularis (NM) preserve the timing of auditory signals through the convergence of a variety of voltage- and ligand-gated ion channels. To understand better how these channels interact, we have characterized the kinetics, voltage sensitivity, and pharmacology of outward currents of NM neurons in brain slices. The reversal potential (Erev) of outward currents varied with potassium concentration as expected for currents carried by potassium. However, Erev was consistently more positive than the Nernst potential for potassium (EK). Deviation of Erev from the calculated EK most likely arose from potassium accumulation in extracellular spaces by potassium conductances active at rest and during depolarizing steps. Three outward potassium currents were studied that varied in voltage and pharmacological sensitivity. A tetraethylammonium (TEA)-sensitive, high-threshold current was activated within 1-5 ms of the onset of depolarization, with a half-maximal activation voltage (V1/2) of -19 mV. It was blocked partially by 4-aminopyridine (4-AP) and was the dominant ionic conductance of NM neurons. A dendrotoxin-I (DTX) and 4-AP-sensitive, low-threshold current had a V1/2 of -58 mV, rapid activation kinetics, and only partial inactivation, with decay time constants between 20 and 100 ms. A rapidly inactivating current was observed that was resistant to TEA and DTX and was blocked by intracellular Cs+. The transient current was inactivated almost completely at the resting potential. The onset of inactivation was fastest at potentials negative to those that caused activation. When intracellular K+ was replaced by Cs+, large inward and outward currents were obtained that corresponded respectively to the above-mentioned DTX- and TEA-sensitive currents. Outward, TEA-sensitive current was carried by Cs+, with a PCs/PK of approximately 0.1. In current-clamped neurons, DTX induced repetitive firing and increased membrane time constant near rest but had little effect on action potential duration. These studies indicate that a low-threshold, DTX-sensitive current plays a key role in making NM neurons highly responsive to the onset and offset of synaptic stimuli.

Coding interaural time differences at low best frequencies in the barn owl

“…Voltage sensitive K þ conductances determine the response properties of auditory neurons, and each cell type exhibits a distinct complement of outward K þ currents [3,67,77,123]. At least two K þ conductances underlie phase locked responses in auditory neurons: a low and a high threshold conductance [11,67,90,91,120].…”

“…The high threshold conductance is characterized by an activation threshold around )20 mV and fast kinetics [11,90,121]. These features of the high threshold conductance result in rapid action potential repolarization and brief action potentials.…”

Modeling coincidence detection in nucleus laminaris

“…It presents rapid activation near rest (low threshold), and its deactivation is slow or partial. Conductances and kinetic parameters for K LVA are taken from studies in NM (Rathouz and Trussell 1998), modified to conform to measured behavior in NL (Reyes et al 1996), e.g., activation threshold and voltage change to small current injections. K HVA is believed to be Kv3.1 and is characterized by positively shifted voltage dependencies and very fast deactivation rates Rudy and McBain 2001).…”

“…It is tetraethylammonium (TEA) sensitive. Conductances and kinetic parameters for K LVA are also taken from studies in NM (Rathouz and Trussell 1998), fit to a linear gating model (see Tables 10 and 11 for parameter values).…”

Tonotopic Gradients of Membrane and Synaptic Properties for Neurons of the Chicken Nucleus Magnocellularis

“…In the cochlear nucleus of chicken, Rubel and Parks (1975) demonstrated the tonotopic arrangement in both the NM and NL; NM neurons with lower CF are located in the caudolateral region and those with higher CF in the rostromedial region. The firing properties of NM neurons are determined primarily by the presence of low-voltage threshold dendrotoxin (DTX)-sensitive K ϩ currents (Rathouz and Trussell, 1998), which are probably generated by K ϩ channels Kv1.1, Kv1.2, or Kv1.6 (Hopkins et al, 1994;Harvey, 2001). These serve to shorten the membrane time constant and minimize temporal distortion of signals.…”