Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala

<p>Abstract</p> <p>Background</p> <p>Neurons in the capsular part of the central nucleus of the amygdala (CeC), a region also called "nociceptive amygdala," receive nociceptive information from the dorsal horn via afferent pathways relayed from the lateral par...

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Main Authors: Nakao Ayano, Takahashi Yukari, Nagase Masashi, Ikeda Ryo, Kato Fusao
Format: Article
Language:English
Published: SAGE Publishing 2012-07-01
Series:Molecular Pain
Subjects:
Online Access:http://www.molecularpain.com/content/8/1/51
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author Nakao Ayano
Takahashi Yukari
Nagase Masashi
Ikeda Ryo
Kato Fusao
author_facet Nakao Ayano
Takahashi Yukari
Nagase Masashi
Ikeda Ryo
Kato Fusao
author_sort Nakao Ayano
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Neurons in the capsular part of the central nucleus of the amygdala (CeC), a region also called "nociceptive amygdala," receive nociceptive information from the dorsal horn via afferent pathways relayed from the lateral parabrachial nucleus (LPB). As the central amygdala is known to be involved in the acquisition and expression of emotion, this pathway is thought to play central roles in the generation of affective responses to nociceptive inputs. Excitatory synaptic transmission between afferents arising from the LPB and these CeC neurons is potentiated in arthritic, visceral, neuropathic, inflammatory and muscle pain models. In neuropathic pain models following spinal nerve ligation (SNL), in which we previously showed a robust LPB-CeC potentiation, the principal behavioral symptom is tactile allodynia triggered by non-C-fiber low-threshold mechanoreceptor afferents. Conversely, recent anatomical studies have revealed that most of the spinal neurons projecting to the LPB receive C-fiber afferent inputs. Here, we examined the hypothesis that these C-fiber-mediated inputs are necessary for the full establishment of robust synaptic potentiation of LPB-CeC transmission in the rats with neuropathic pain.</p> <p>Results</p> <p>Postnatal capsaicin treatment, which has been shown to denervate the C-fibers expressing transient receptor potential vanilloid type-1 (TRPV1) channels, completely abolished eye-wiping responses to capsaicin eye instillation in rats, but this treatment did not affect mechanical allodynia in the nerve-ligated animals. However, the postnatal capsaicin treatment prevented LPB-CeC synaptic potentiation after SNL, unlike in the vehicle-treated rats, primarily due to the decreased incidence of potentiated transmission by elimination of TRPV1-expressing C-fiber afferents.</p> <p>Conclusions</p> <p>C-fiber-mediated afferents in the nerve-ligated animals may be a required facilitator of the establishment of nerve injury-evoked synaptic potentiation in the CeC. These inputs might play essential roles in the chronic pain-induced plastic changes in the central network linking nociception and negative emotion.</p>
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spelling doaj.art-4c0a5f3b9a7e48cf8df06da629f3d3222022-12-21T21:49:30ZengSAGE PublishingMolecular Pain1744-80692012-07-01815110.1186/1744-8069-8-51Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdalaNakao AyanoTakahashi YukariNagase MasashiIkeda RyoKato Fusao<p>Abstract</p> <p>Background</p> <p>Neurons in the capsular part of the central nucleus of the amygdala (CeC), a region also called "nociceptive amygdala," receive nociceptive information from the dorsal horn via afferent pathways relayed from the lateral parabrachial nucleus (LPB). As the central amygdala is known to be involved in the acquisition and expression of emotion, this pathway is thought to play central roles in the generation of affective responses to nociceptive inputs. Excitatory synaptic transmission between afferents arising from the LPB and these CeC neurons is potentiated in arthritic, visceral, neuropathic, inflammatory and muscle pain models. In neuropathic pain models following spinal nerve ligation (SNL), in which we previously showed a robust LPB-CeC potentiation, the principal behavioral symptom is tactile allodynia triggered by non-C-fiber low-threshold mechanoreceptor afferents. Conversely, recent anatomical studies have revealed that most of the spinal neurons projecting to the LPB receive C-fiber afferent inputs. Here, we examined the hypothesis that these C-fiber-mediated inputs are necessary for the full establishment of robust synaptic potentiation of LPB-CeC transmission in the rats with neuropathic pain.</p> <p>Results</p> <p>Postnatal capsaicin treatment, which has been shown to denervate the C-fibers expressing transient receptor potential vanilloid type-1 (TRPV1) channels, completely abolished eye-wiping responses to capsaicin eye instillation in rats, but this treatment did not affect mechanical allodynia in the nerve-ligated animals. However, the postnatal capsaicin treatment prevented LPB-CeC synaptic potentiation after SNL, unlike in the vehicle-treated rats, primarily due to the decreased incidence of potentiated transmission by elimination of TRPV1-expressing C-fiber afferents.</p> <p>Conclusions</p> <p>C-fiber-mediated afferents in the nerve-ligated animals may be a required facilitator of the establishment of nerve injury-evoked synaptic potentiation in the CeC. These inputs might play essential roles in the chronic pain-induced plastic changes in the central network linking nociception and negative emotion.</p>http://www.molecularpain.com/content/8/1/51Excitatory postsynaptic currentsParabrachial nucleusTactile allodyniaEmotionMinimal stimulationCapsular part of the central nucleus of the amygdala
spellingShingle Nakao Ayano
Takahashi Yukari
Nagase Masashi
Ikeda Ryo
Kato Fusao
Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
Molecular Pain
Excitatory postsynaptic currents
Parabrachial nucleus
Tactile allodynia
Emotion
Minimal stimulation
Capsular part of the central nucleus of the amygdala
title Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
title_full Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
title_fullStr Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
title_full_unstemmed Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
title_short Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala
title_sort role of capsaicin sensitive c fiber afferents in neuropathic pain induced synaptic potentiation in the nociceptive amygdala
topic Excitatory postsynaptic currents
Parabrachial nucleus
Tactile allodynia
Emotion
Minimal stimulation
Capsular part of the central nucleus of the amygdala
url http://www.molecularpain.com/content/8/1/51
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