Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation

doi:10.1016/j.neuroscience.2005.11.024

Neuroscience

Volume 138, Issue 2, 2006, Pages 621-630

https://doi.org/10.1016/j.neuroscience.2005.11.024 Get rights and content

Abstract

The aim of the present study was to investigate the effect of temporomandibular joint inflammation on the excitability of trigeminal root ganglion neurons innervating the temporomandibular joint using a perforated patch-clamp technique. Inflammation was induced by injection of complete Freund’s adjuvant into the rat temporomandibular joint. The threshold for escape from mechanical stimulation in the temporomandibular joint-inflamed rats was significantly lower than that in control rats. Fluorogold labeling was used to identify the trigeminal root ganglion neurons innervating the site of inflammation. When voltage-clamp (V_h=−60 mV) conditions were applied to these Fluorogold-labeled small diameter trigeminal root ganglion neurons (<30 μm), voltage-dependent transient K⁺ current densities were significantly reduced in the inflamed rats compared with controls. In addition, the voltage-dependence of inactivation of the voltage-dependent transient K⁺ current was negatively shifted in the labeled temporomandibular joint-inflamed trigeminal root ganglion neurons. Furthermore, temporomandibular joint inflammation significantly reduced the threshold current and significantly increased action potential firings evoked at two-fold threshold in the Fluorogold-labeled small trigeminal root ganglion neurons. Application of 4-aminopyridine (0.5mM) to control trigeminal root ganglion neurons mimicked the changes in the firing properties observed after complete Freund’s adjuvant treatment. Together, these results suggest that temporomandibular joint inflammation increases the excitability of trigeminal root ganglion neurons innervating temporomandibular joint by suppressing voltage-dependent transient K⁺ current via a leftward shift in the inactivation curve. These changes may contribute to trigeminal inflammatory allodynia in temporomandibular joint disorder.

Section snippets

Experimental procedures

The experiments were approved by the animal use and care committee of Nippon Dental University and were consistent with the ethical guidelines of the International Association for the Study of Pain (Zimmermann, 1983). Double-blind experiments were carried out and all possible efforts were made to minimize the number of animals used and their suffering.

Induction of TMJ inflammation and allodynia

After CFA injection, the animals were tested for abnormal pain sensation by probing the injected site and/or the orofacial skin with von Frey filaments. In the TMJ-inflamed rats, the threshold for escape from mechanical stimulation applied to the whisker pad area was significantly reduced from 51.3±6.3 mN to 19.1±2.1 mN at 48 h after CFA injection (n=18, P<0.05). No significant changes in the contralateral threshold in the whisker pad area were observed in either group (control vs. inflamed;

Discussion

The results presented herein provide evidence that TMJ inflammation potentiates the excitability of small-diameter TRG neurons innervating TMJ, by suppressing A-currents via a leftward, hyperpolarizing, shift in the inactivation curve without any changes in the activation curve. The I_A suppression of the TRG neuron innervating TMJ may contribute to trigeminal inflammatory allodynia in the TMJ disorder.

Acknowledgments

This study was supported by a grant from the Ministry of Education, Science and Culture of Japan (No.15591980).

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Citation Excerpt :
Kv channels are involved in several important functions in the nervous system including setting the resting membrane potential, setting action potential shape, neuronal repolarization, and neurotransmitter release (Ficker and Heinemann, 2001; Pearce and Duchen, 1994; Hille, 2001; Lawson, 2006) via slow-inactivating sustained (K-current; IK) and fast-inactivating transient (A-current; IA) channels. Takeda et al. (2006) previously observed that a reduction in IA density, but not in dominant sustained current (Ik), contributes to the increased excitability of small-diameter TG neuron in intact rats. In fact, applying an A-type potassium channel blocker to TG neurons in vivo also enhances Aδ/C-TG neuronal activities innervating the temporomandibular joint (TMJ) region in intact rats (Hara et al., 2012).
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Pain mechanismEnhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation

Abstract

Section snippets

Experimental procedures

Induction of TMJ inflammation and allodynia

Discussion

Acknowledgments

Neuroscience

Pain

Neurosci Lett

Pain

Brain Res

Neurosci Lett

Prog Neurobiol

Neuroscience

Mol Cells

Neuroscience

Physiol Behav

Neuron

Neuroscience

Neuroscience

Pain

Pain

Neuroscience

Pain

Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neuronsthe role of voltage-gated ion channels

Neurogastroenterol Motil

Brain-derived neurotrophic factor (BDNF) contributes to neuronal dysfunction in a model of allergic airway inflammation

Br J Pharmacol

Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus

J Neurosci

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Am J Physiol Gastrointest Liver Physiol

Morphologically identified cutaneous afferent DRG neurons express three different potassium currents in varying properties

J Neurophysiol

Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy

J Neurophysiol

Slow and fast transient potassium currents in cultured rat hippocampus cells

J Physiol (Lond)

Pain mechanism
Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation