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The Journal of Neuroscience, January 12, 2005, 25(2):363-371; doi:10.1523/JNEUROSCI.3950-04.2005

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Cellular/Molecular
High-Threshold K⁺ Current Increases Gain by Offsetting a Frequency-Dependent Increase in Low-Threshold K⁺ Current

Fernando R. Fernandez, ^* W. Hamish Mehaffey, ^* Michael L. Molineux, and Ray W. Turner

Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 4N1

High-frequency firing neurons are found in numerous central systems, including the auditory brainstem, thalamus, hippocampus, and neocortex. The kinetics of high-threshold K⁺ currents (IK_HT) from the Kv3 subfamily has led to the proposal that these channels offset cumulative Na⁺ current inactivation and stabilize tonic high-frequency firing. However, all high-frequency firing neurons, examined to date, also express low-threshold K⁺ currents (IK_LT) that have slower kinetics and play an important role in setting the subthreshold and filtering properties of the neuron. IK_LT has also been shown to dampen excitability and is therefore likely to oppose high-frequency firing. In this study, we examined the role of IK_HT in pyramidal cells of the electrosensory lobe of weakly electric fish, which are characterized by high-frequency firing, a very wide frequency range, and high levels of IK_HT. In particular, we examined the mechanisms that allow IK_HT to set the gain of the F-I relationship by interacting with another low-threshold K⁺ current. We found that IK_HT increases the gain of the F-I relationship and influences spike waveform almost exclusively in the high-frequency firing range. The frequency dependence arises from IK_HT influencing both the IK_LT and Na⁺ currents. IK_HT thus plays a significant role in stabilizing high-frequency firing by preventing a steady-state accumulation of IK_LT that is as important as preventing Na⁺ current inactivation.

Key words: high-threshold K⁺ current; low-threshold K⁺ current; frequency-current relationship; Kv3; Na⁺ current inactivation; gain

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Received Sep 23, 2004; revised November 2, 2004; accepted November 17, 2004.

This article has been cited by other articles:

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