Mechanisms of Sustained High Firing Rates in Two Classes of Vestibular Nucleus Neurons: Differential Contributions of Resurgent Na, Kv3, and BK Currents
Open Access
- 1 September 2010
- journal article
- research article
- Published by American Physiological Society in Journal of Neurophysiology
- Vol. 104 (3), 1625-1634
- https://doi.org/10.1152/jn.00378.2010
Abstract
To fire at high rates, neurons express ionic currents that work together to minimize refractory periods by ensuring that sodium channels are available for activation shortly after each action potential. Vestibular nucleus neurons operate around high baseline firing rates and encode information with bidirectional modulation of firing rates up to several hundred Hz. To determine the mechanisms that enable these neurons to sustain firing at high rates, ionic currents were measured during firing by using the action potential clamp technique in vestibular nucleus neurons acutely dissociated from transgenic mice. Although neurons from the YFP-16 line fire at rates higher than those from the GIN line, both classes of neurons express Kv3 and BK currents as well as both transient and resurgent Na currents. In the fastest firing neurons, Kv3 currents dominated repolarization at all firing rates and minimized Na channel inactivation by rapidly transitioning Na channels from the open to the closed state. In slower firing neurons, BK currents dominated repolarization at the highest firing rates and sodium channel availability was protected by a resurgent blocking mechanism. Quantitative differences in Kv3 current density across neurons and qualitative differences in immunohistochemically detected expression of Kv3 subunits could account for the difference in firing range within and across cell classes. These results demonstrate how divergent firing properties of two neuronal populations arise through the interplay of at least three ionic currents.Keywords
This publication has 62 references indexed in Scilit:
- Sodium Entry during Action Potentials of Mammalian Neurons: Incomplete Inactivation and Reduced Metabolic Efficiency in Fast-Spiking NeuronsNeuron, 2009
- Rescue of Motor Coordination by Purkinje Cell-Targeted Restoration of Kv3.3 Channels inKcnc3-Null Mice RequiresKcnc1Journal of Neuroscience, 2009
- Response Linearity of Alert Monkey Non-Eye Movement Vestibular Nucleus Neurons During Sinusoidal Yaw RotationJournal of Neurophysiology, 2009
- Kv3.3 Channels at the Purkinje Cell Soma Are Necessary for Generation of the Classical Complex Spike WaveformJournal of Neuroscience, 2008
- Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert MouseJournal of Neurophysiology, 2007
- BK potassium channels facilitate high‐frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cellsThe Journal of Physiology, 2007
- Transgenic Mouse Lines Subdivide Medial Vestibular Nucleus Neurons into Discrete, Neurochemically Distinct PopulationsJournal of Neuroscience, 2007
- Transformation of Vestibular Signals Into Motor Commands in the Vestibuloocular Reflex Pathways of MonkeysJournal of Neurophysiology, 2006
- Interaction of Kv3 Potassium Channels and Resurgent Sodium Current Influences the Rate of Spontaneous Firing of Purkinje NeuronsJournal of Neuroscience, 2006
- Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neuronsNature Neuroscience, 2005