Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats
The primary somatosensory cortex (S1) plays a key role in the discrimination of somatic sensations. Among subdivisions in S1, the dysgranular zone of rodent S1 (S1DZ) is homologous to Brodmann’s area 3a of primate S1, which is involved in the processing of noxious signals from the body. However, mol...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-07-01
|
| Series: | Biomedicines |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2227-9059/10/7/1633 |
| _version_ | 1797440713342844928 |
|---|---|
| author | Geehoon Chung Yeong-Chan Yun Chae Young Kim Sun Kwang Kim Sang Jeong Kim |
| author_facet | Geehoon Chung Yeong-Chan Yun Chae Young Kim Sun Kwang Kim Sang Jeong Kim |
| author_sort | Geehoon Chung |
| collection | DOAJ |
| description | The primary somatosensory cortex (S1) plays a key role in the discrimination of somatic sensations. Among subdivisions in S1, the dysgranular zone of rodent S1 (S1DZ) is homologous to Brodmann’s area 3a of primate S1, which is involved in the processing of noxious signals from the body. However, molecular changes in this region and their role in the pathological pain state have never been studied. In this study, we identified molecular alteration of the S1DZ in a rat model of neuropathic pain induced by right L5 spinal nerve ligation (SNL) surgery and investigated its functional role in pain symptoms. Brain images acquired from SNL group and control group in our previous study were analyzed, and behaviors were measured using the von Frey test, acetone test, and conditioned place preference test. We found that metabotropic glutamate receptor 5 (mGluR5) levels were significantly upregulated in the S1DZ contralateral to the nerve injury in the SNL group compared to the sham group. Pharmacological deactivation of mGluR5 in S1DZ ameliorated symptoms of neuropathic allodynia, which was shown by a significant increase in the mechanical paw withdrawal threshold and a decrease in the behavioral response to cold stimuli. We further confirmed that this treatment induced relief from the tonic-aversive state of chronic neuropathic pain, as a place preference memory associated with the treatment-paired chamber was formed in rats with neuropathic pain. Our data provide evidence that mGluR5 in the S1DZ is involved in the manifestation of abnormal pain sensations in the neuropathic pain state. |
| first_indexed | 2024-03-09T12:12:17Z |
| format | Article |
| id | doaj.art-f3240ab8a16f47998a2026e3408aa988 |
| institution | Directory Open Access Journal |
| issn | 2227-9059 |
| language | English |
| last_indexed | 2024-03-09T12:12:17Z |
| publishDate | 2022-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Biomedicines |
| spelling | doaj.art-f3240ab8a16f47998a2026e3408aa9882023-11-30T22:50:49ZengMDPI AGBiomedicines2227-90592022-07-01107163310.3390/biomedicines10071633Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in RatsGeehoon Chung0Yeong-Chan Yun1Chae Young Kim2Sun Kwang Kim3Sang Jeong Kim4Department of Physiology, College of Korean Medicine, Kyung Hee University, 26 Kyungheedae-ro, Dongdaemun-gu, Seoul 02447, KoreaDepartment of Physiology, College of Medicine, Seoul National University, 103 Daehak-ro, Jongno-gu, Seoul 03080, KoreaDepartment of Physiology, College of Medicine, Seoul National University, 103 Daehak-ro, Jongno-gu, Seoul 03080, KoreaDepartment of Physiology, College of Korean Medicine, Kyung Hee University, 26 Kyungheedae-ro, Dongdaemun-gu, Seoul 02447, KoreaDepartment of Physiology, College of Medicine, Seoul National University, 103 Daehak-ro, Jongno-gu, Seoul 03080, KoreaThe primary somatosensory cortex (S1) plays a key role in the discrimination of somatic sensations. Among subdivisions in S1, the dysgranular zone of rodent S1 (S1DZ) is homologous to Brodmann’s area 3a of primate S1, which is involved in the processing of noxious signals from the body. However, molecular changes in this region and their role in the pathological pain state have never been studied. In this study, we identified molecular alteration of the S1DZ in a rat model of neuropathic pain induced by right L5 spinal nerve ligation (SNL) surgery and investigated its functional role in pain symptoms. Brain images acquired from SNL group and control group in our previous study were analyzed, and behaviors were measured using the von Frey test, acetone test, and conditioned place preference test. We found that metabotropic glutamate receptor 5 (mGluR5) levels were significantly upregulated in the S1DZ contralateral to the nerve injury in the SNL group compared to the sham group. Pharmacological deactivation of mGluR5 in S1DZ ameliorated symptoms of neuropathic allodynia, which was shown by a significant increase in the mechanical paw withdrawal threshold and a decrease in the behavioral response to cold stimuli. We further confirmed that this treatment induced relief from the tonic-aversive state of chronic neuropathic pain, as a place preference memory associated with the treatment-paired chamber was formed in rats with neuropathic pain. Our data provide evidence that mGluR5 in the S1DZ is involved in the manifestation of abnormal pain sensations in the neuropathic pain state.https://www.mdpi.com/2227-9059/10/7/1633neuropathic painprimary somatosensory cortexdysgranular zonemetabotropic glutamate receptor 5allodyniaspontaneous pain |
| spellingShingle | Geehoon Chung Yeong-Chan Yun Chae Young Kim Sun Kwang Kim Sang Jeong Kim Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats Biomedicines neuropathic pain primary somatosensory cortex dysgranular zone metabotropic glutamate receptor 5 allodynia spontaneous pain |
| title | Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats |
| title_full | Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats |
| title_fullStr | Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats |
| title_full_unstemmed | Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats |
| title_short | Metabotropic Glutamate Receptor 5 in the Dysgranular Zone of Primary Somatosensory Cortex Mediates Neuropathic Pain in Rats |
| title_sort | metabotropic glutamate receptor 5 in the dysgranular zone of primary somatosensory cortex mediates neuropathic pain in rats |
| topic | neuropathic pain primary somatosensory cortex dysgranular zone metabotropic glutamate receptor 5 allodynia spontaneous pain |
| url | https://www.mdpi.com/2227-9059/10/7/1633 |
| work_keys_str_mv | AT geehoonchung metabotropicglutamatereceptor5inthedysgranularzoneofprimarysomatosensorycortexmediatesneuropathicpaininrats AT yeongchanyun metabotropicglutamatereceptor5inthedysgranularzoneofprimarysomatosensorycortexmediatesneuropathicpaininrats AT chaeyoungkim metabotropicglutamatereceptor5inthedysgranularzoneofprimarysomatosensorycortexmediatesneuropathicpaininrats AT sunkwangkim metabotropicglutamatereceptor5inthedysgranularzoneofprimarysomatosensorycortexmediatesneuropathicpaininrats AT sangjeongkim metabotropicglutamatereceptor5inthedysgranularzoneofprimarysomatosensorycortexmediatesneuropathicpaininrats |