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

Takeda, Masatoshi; Tanimoto, Tsuyoshi; Ikeda, Mizuho; Nasu, Masanori; Kadoi, Jun; Yoshida, Shinki; Matsumoto, Shigeji

doi:10.1016/j.neuroscience.2005.11.024

Cited by 58 publications

(53 citation statements)

References 49 publications

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“…Also, after injury, the maximal K ϩ current is reduced by 52% by a significant decrease in 2/3 types of their K ϩ currents (Everill et al 1998, cited by Ishikawa et al 1999). This has been partially corroborated by more recent work showing that, after injury (transection of the sciatic nerve), voltage-gated K ϩ current is downregulated (Abdulla and Smith 2001;Takeda et al 2006). Unfortunately, all of these studies have focused on injured afferents and few on intact afferents.…”

Section: Psnl-induced Changes In the Electrical Properties Of L 4mentioning

confidence: 81%

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Boada

Gutiérrez

Aschenbrenner

et al. 2015

Journal of Neurophysiology

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Boada MD, Gutierrez S, Aschenbrenner CA, Houle TT, Hayashida K, Ririe DG, Eisenach JC. Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents. J Neurophysiol 113: 100 -109, 2015. First published October 1, 2014 doi:10.1152/jn.00506.2014.-Chronic pain after nerve injury is often accompanied by hypersensitivity to mechanical stimuli, yet whether this reflects altered input, altered processing, or both remains unclear. Spinal nerve ligation or transection results in hypersensitivity to mechanical stimuli in skin innervated by adjacent dorsal root ganglia, but no previous study has quantified the changes in receptive field properties of these neurons in vivo. To address this, we recorded intracellularly from L 4 dorsal root ganglion neurons of anesthetized young adult rats, 1 wk after L 5 partial spinal nerve ligation (pSNL) or sham surgery. One week after pSNL, hindpaw mechanical withdrawal threshold in awake, freely behaving animals was decreased in the L 4 distribution on the nerve-injured side compared with sham controls. Electrophysiology revealed that highthreshold mechanoreceptive cells of A-fiber conduction velocity in L 4 were sensitized, with a seven-fold reduction in mechanical threshold, a seven-fold increase in receptive field area, and doubling of maximum instantaneous frequency in response to peripheral stimuli, accompanied by reductions in after-hyperpolarization amplitude and duration. Only a reduction in mechanical threshold (minimum von Frey hair producing neuronal activity) was observed in C-fiber conduction velocity high-threshold mechanoreceptive cells. In contrast, low-threshold mechanoreceptive cells were desensitized, with a 13-fold increase in mechanical threshold, a 60% reduction in receptive field area, and a 40% reduction in instantaneous frequency to stimulation. No spontaneous activity was observed in L 4 ganglia, and the likelihood of recording from neurons without a mechanical receptive field was increased after pSNL. These data suggest massively altered input from undamaged sensory afferents innervating areas of hypersensitivity after nerve injury, with reduced tactile and increased nociceptive afferent response. These findings differ importantly from previous preclinical studies, but are consistent with clinical findings in most patients with chronic neuropathic pain. chronic pain model; in vivo electrophysiology; sensory neurons; spinal nerve ligation IN HUMANS, NEUROPATHIC PAIN includes both spontaneous and evoked pain, often accompanied by hypersensitivity to normal nociceptive stimuli (hyperalgesia) and normally nonnociceptive stimuli (allodynia). This pathological condition is also sometimes accompanied by dysesthesias and paresthesias (von Hehn et al. 2012), suggesting that both tactile and nociceptive information channels and/or processing are disrupted.

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Section: Psnl-induced Changes In the Electrical Properties Of L 4mentioning

confidence: 81%

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Boada

Gutiérrez

Aschenbrenner

et al. 2015

Journal of Neurophysiology

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“…There are several possible mechanisms for the extinction-induced increase in bursting. Neuronal excitability can be enhanced by closing large-conductance Ca 2 -activated K potassium channels (Shao et al, 1999;Traub et al, 2003;Brenner et al, 2005) or A-type potassium channels (Perez et al, 2006;Takeda et al, 2006;Wang and Schreurs, 2006), both of which are expressed in cortical neurons (Jin et al, 2000;Dong and White, 2003) and have been linked to increased bursting (Magee and Carruth, 1999;Jin et al, 2000;Traub et al, 2003;Gu et al, 2007). Interestingly, a decrease in A-type currents has been correlated with invertebrate learning (Yamoah et al, 2005) and hippocampal long-term potentiation (Frick et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Fear Conditioning and Extinction Differentially Modify the Intrinsic Excitability of Infralimbic Neurons

Santini

Quirk²,

Porter³

2008

J. Neurosci.

242

265

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Extinction of conditioned fear is an active learning process involving inhibition of fear expression. It has been proposed that fear extinction potentiates neurons in the infralimbic (IL) prefrontal cortex, but the cellular mechanisms underlying this potentiation remain unknown. It is also not known whether this potentiation occurs locally in IL neurons as opposed to IL afferents. To determine whether extinction enhances the intrinsic excitability of IL pyramidal neurons in layers II/III and V, we performed whole-cell patch-clamp recordings in slices from naive, conditioned, or conditioned-extinguished rats. We observed that conditioning depressed IL excitability compared with slices from naive animals, as evidenced by a decreased number of spikes evoked by injected current and an increase in the slow afterhyperpolarizing potential (sAHP). Extinction reversed these conditioning-induced effects. Furthermore, IL neurons from extinguished rats showed increased burst spiking compared with naive rats, which was correlated with extinction recall. These changes were specific to IL prefrontal cortex and were not observed in prelimbic prefrontal cortex. Together, these findings suggest that IL intrinsic excitability is reduced to allow for expression of conditioning memory and enhanced for expression of extinction memory through the modulation of Ca 2ϩ -gated K ϩ channels underlying the sAHP. Inappropriate modulation of these intrinsic mechanisms may underlie anxiety disorders, characterized by exaggerated fear and deficient extinction.

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“…NMDA treatment induces opposite changes in I A suggesting that the increased excitability seen in the early stage of sensitization is not an activity-dependent change but may depend on a more specific signal. Changes in A-type currents have been shown to follow inflammation in dorsal root ganglion cells suggesting that this is a crucial current to alter the functioning of the nociceptive system (Yoshimura and de Groat, 1999;Stewart et al, 2003;Dang et al, 2004;Takeda et al, 2006;Xu et al, 2006;Wang et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…However, recent evidence indicates that Kv4.2 channels underlay A-type currents in mice dorsal horn neurons and that the genetic elimination of this channel prevents a normal hyperalgesic response to inflammatory stimuli (Hu et al, 2006). Transient and sustained potassium currents (A-type and delayed rectifier type currents) influence membrane excitability and are modulated by activity-dependent mechanisms (Desai et al, 1999;Yoshimura and de Groat, 1999;Stewart et al, 2003;Dang et al, 2004;Misonou et al, 2004;Takeda et al, 2006;van Welie et al, 2006;Xu et al, 2006;Wang et al, 2007;Lei et al, 2008;Shen et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Changes in Membrane Excitability and Potassium Currents in Sensitized Dorsal Horn Neurons of Mice Pups

Rivera-Arconada¹,

López-García²

2010

J. Neurosci.

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Rationally, an increased intrinsic excitability of dorsal horn neurons could be a factor contributing to alter the gain of the nociceptive system during central sensitization, however direct evidence is scarce. Here we have examined this hypothesis using current and voltageclamp recordings from dorsal horn neurons in the spinal cord in vitro preparation obtained from mice pups of either sex. Cords were extracted from carrageenan-pretreated and control animals to allow for comparison. Dorsal horn neurons from treated animals showed significantly larger and faster synaptic responses. Synaptic changes started developing shortly after inflammation (1 h) and developed further after a longer-term inflammation (20 h). However, these neurons showed biphasic changes in membrane excitability with an increase shortly after inflammation and a decrease in the longer term. Concomitant changes were observed in transient (I A ) and sustained potassium currents (I DR ). Prolonged superfusion of naive spinal cords with NMDA led to a decreased neuronal excitability and to increased potassium currents.Results suggest that excitability plays a role more complex than expected during the process of central sensitization of dorsal horn neurons and that modulation of potassium currents may contribute to shape the changing states of excitability. The decreased excitability observed after long-term inflammation is interpreted as a homeostatic correction to an abnormal state of synaptic activity.

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

Cited by 58 publications

References 49 publications

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Nerve injury induces a new profile of tactile and mechanical nociceptor input from undamaged peripheral afferents

Fear Conditioning and Extinction Differentially Modify the Intrinsic Excitability of Infralimbic Neurons

Changes in Membrane Excitability and Potassium Currents in Sensitized Dorsal Horn Neurons of Mice Pups

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