Journal Article

Activity‐dependent redistribution of Kv2.1 ion channels on rat spinal motoneurons

Romer, Shannon H., Deardorff, Adam S., Fyffe, Robert E. W.

2016

Overview

Homeostatic plasticity occurs through diverse cellular and synaptic mechanisms, and extensive investigations over the preceding decade have established Kv2.1 ion channels as key homeostatic regulatory elements in several central neuronal systems. As in these cellular systems, Kv2.1 channels in spinal motoneurons (MNs) localize within large somatic membrane clusters. However, their role in regulating motoneuron activity is not fully established in vivo. We have previously demonstrated marked Kv2.1 channel redistribution in MNs following in vitro glutamate application and in vivo peripheral nerve injury (Romer et al., 2014, Brain Research, 1547:1–15). Here, we extend these findings through the novel use of a fully intact, in vivo rat preparation to show that Kv2.1 ion channels in lumbar MNs rapidly and reversibly redistribute throughout the somatic membrane following 10 min of electrophysiological sensory and/or motor nerve stimulation. These data establish that Kv2.1 channels are remarkably responsive in vivo to electrically evoked and synaptically driven action potentials in MNs, and strongly implicate motoneuron Kv2.1 channels in the rapid homeostatic response to altered neuronal activity. Delayed rectifier Kv2.1 ion channels are key homeostatic regulatory elements in several neuronal systems, but the functional implications of large Kv2.1 channel clusters in spinal motoneurons (MNs) are not well established. Here, for the first time, we demonstrate that both motor and sensory nerve activity rapidly influence Kv2.1 clustering in spinal MNs in vivo and suggest that Kv2.1 channels contribute to the homeostatic regulation of motoneuron firing properties. These data provide important mechanistic insight into the prominent and puzzling Kv2.1 cluster dynamics that have been observed in spinal MNs.

• Publisher: John Wiley & Sons, Inc,John Wiley and Sons Inc
• Subject: Action Potentials - physiology / Animals / Cellular and Molecular Neuroscience / Central Nervous System / C‐boutons / Data processing / Female / Glutamic Acid - metabolism / Homeostasis - physiology / Homeostatic plasticity / Hypotheses / Ion Channel Gating - physiology / Ion Channels / Kv2.1 / Laboratory animals / Membrane Physiology / Motor Control / Motor neurons / Motor Neurons - metabolism / Motor Neurons - physiology / Nervous system / Original Research / Pathology / Physiology / Potassium channels (voltage-gated) / Rats / Rats, Sprague-Dawley / Regulatory sequences / Shab Potassium Channels - metabolism / Spinal Nerves - metabolism / Spinal Nerves - physiology / Spinal plasticity / Synaptic plasticity / voltage‐gated ion channels, activity dependent / α‐motoneuron