Pain-related neuronal ensembles in the primary somatosensory cortex contribute to hyperalgesia and anxiety

Ishikawa, Tatsuya; Murata, Katsumi; Okuda, Hiromichi; Potapenko, Ilia; Hori, Keiichi; Furuyama, Takafumi; Yamamoto, Ryo; Ono, Munenori; Kato, Nobuo; Fukazawa, Yugo; Ozaki, Noriyuki

doi:10.1016/j.isci.2023.106332

Cited by 9 publications

(4 citation statements)

References 45 publications

(69 reference statements)

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“…The results of previous reports including our studies suggest that plastic changes in S1 cortex contributed to chronic pain or inflammatory pain. [5][6][7][8][9][10][11]25,27) Therefore, to investigate the interaction between neuronal activity in S1 and change of mechanical threshold of hind paw by above combined experiment may play important role to further understand the mechanism of causing chronic pain.…”

Section: Discussionmentioning

confidence: 99%

Combined Experiments with <i>in Vivo</i> Fiber Photometry and Behavior Tests Can Facilitate the Measurement of Neuronal Activity in the Primary Somatosensory Cortex and Hyperalgesia in an Inflammatory Pain Mice Model

Ishikawa,

Uta,

Okuda

et al. 2024

Biological & Pharmaceutical Bulletin

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The pain matrix, which includes several brain regions that respond to pain sensation, contribute to the development of chronic pain. Thus, it is essential to understand the mechanism of causing chronic pain in the pain matrix such as anterior cingulate (ACC), or primary somatosensory (S1) cortex. Recently, combined experiment with the behavior tests and in vivo calcium imaging using fiber photometry revealed the interaction between the neuronal function in deep brain regions of the pain matrix including ACC and the phenotype of chronic pain. However, it remains unclear whether this combined experiment can identify the interaction between neuronal activity in S1, which receive pain sensation, and pain behaviors such as hyperalgesia or allodynia. In this study, to examine whether the interaction between change of neuronal activity in S1 and hyperalgesia in hind paw before and after causing inflammatory pain was detected from same animal, the combined experiment of in vivo fiber photometry system and von Frey hairs test was applied. This combined experiment detected that amplitude of calcium responses in S1 neurons increased and the mechanical threshold of hind paw decreased from same animals which have an inflammatory pain. Moreover, we found that the values between amplitude of calcium responses and mechanical thresholds were shifted to negative correlation after causing inflammatory pain. Thus, the combined experiment with fiber photometry and the behavior tests has a possibility that can simultaneously consider the interaction between neuronal activity in pain matrix and pain induced behaviors and the effects of analgesics or pain treatments.

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Section: Discussionmentioning

confidence: 99%

Combined Experiments with <i>in Vivo</i> Fiber Photometry and Behavior Tests Can Facilitate the Measurement of Neuronal Activity in the Primary Somatosensory Cortex and Hyperalgesia in an Inflammatory Pain Mice Model

Ishikawa,

Uta,

Okuda

et al. 2024

Biological & Pharmaceutical Bulletin

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“…As evidenced by a number of clinical parameters, either combined/multimodal anesthesia techniques 165 or use of higher doses of intraoperative analgesia are associated with decreased levels of chronic pain as well as analgesic use; 166 (2) prevention of central sensitization at the time of injury (an unusual opportunity or circumstance in the chronic pain domain) may contribute to the decrease of the acute to chronic pain transition. 167 , 168 Such changes may have a neurobiological underpinning in preventing “neuronal ensembles” from becoming dysfunctional and contribute to enhanced processes in the acute to chronic pain transition (e.g., hyperaglgesia and anxiety); 169 (3) premorbid conditions (e.g., catastrophizing) defined prior to surgery are known to predict poorer outcomes. Such conditions may enhance brain responsivity to trauma during the surgical procedure as well as pain levels immediately following surgery ( Fig.…”

Section: Clinical Use – Adoption Process Using Biomarker Standardsmentioning

confidence: 99%

Machines, mathematics, and modules: the potential to provide real-time metrics for pain under anesthesia

Peng,

Karunakaran,

Green

et al. 2024

Neurophoton.

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The brain-based assessments under anesthesia have provided the ability to evaluate pain/nociception during surgery and the potential to prevent long-term evolution of chronic pain. Prior studies have shown that the functional near-infrared spectroscopy (fNIRS)-measured changes in cortical regions such as the primary somatosensory and the polar frontal cortices show consistent response to evoked and ongoing pain in awake, sedated, and anesthetized patients. We take this basic approach and integrate it into a potential framework that could provide real-time measures of pain/nociception during the peri-surgical period. This application could have significant implications for providing analgesia during surgery, a practice that currently lacks quantitative evidence to guide patient tailored pain management. Through a simple readout of "pain" or "no pain," the proposed system could diminish or eliminate levels of intraoperative, early post-operative, and potentially, the transition to chronic post-surgical pain. The system, when validated, could also be applied to measures of analgesic efficacy in the clinic.

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“… 1 , 2 , 3 The comorbidity of chronic pain and psychological disorders—a common clinical problem—poses significant challenges for current effective antidepressant and analgesic therapies, which are characterized by a lack of precise intervention targets and unavoidable severe side effects. 4 , 5 , 6 Despite a rapidly growing body of literature focusing on the pathogenesis of the comorbidity of chronic pain and psychological disorders at the neural circuit level, 7 , 8 , 9 , 10 , 11 , 12 , 13 further investigations are required to elucidate its underlying neural molecular mechanisms.…”

Section: Introductionmentioning

confidence: 99%

HCN channels in the lateral habenula regulate pain and comorbid depressive‐like behaviors in mice

Cao,

Zhu,

et al. 2024

CNS Neurosci Ther

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AimsComorbid anxiodepressive‐like symptoms (CADS) in chronic pain are closely related to the overactivation of the lateral habenula (LHb). Hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channels have been implicated to play a key role in regulating neuronal excitability. However, the role of HCN channels in the LHb during CADS has not yet been characterized. This study aimed to investigate the effect of HCN channels in the LHb on CADS during chronic pain.MethodsAfter chronic neuropathic pain induction by spared nerve injury (SNI), mice underwent a sucrose preference test, forced swimming test, tail suspension test, open‐field test, and elevated plus maze test to evaluate their anxiodepressive‐like behaviors. Electrophysiological recordings, immunohistochemistry, Western blotting, pharmacological experiments, and virus knockdown strategies were used to investigate the underlying mechanisms.ResultsEvident anxiodepressive‐like behaviors were observed 6w after the SNI surgery, accompanied by increased neuronal excitability, enhanced HCN channel function, and increased expression of HCN2 isoforms in the LHb. Either pharmacological inhibition or virus knockdown of HCN2 channels significantly reduced LHb neuronal excitability and ameliorated both pain and depressive‐like behaviors.ConclusionOur results indicated that the LHb neurons were hyperactive under CADS in chronic pain, and this hyperactivation possibly resulted from the enhanced function of HCN channels and up‐regulation of HCN2 isoforms.

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Pain-related neuronal ensembles in the primary somatosensory cortex contribute to hyperalgesia and anxiety

Cited by 9 publications

References 45 publications

Combined Experiments with <i>in Vivo</i> Fiber Photometry and Behavior Tests Can Facilitate the Measurement of Neuronal Activity in the Primary Somatosensory Cortex and Hyperalgesia in an Inflammatory Pain Mice Model

Combined Experiments with <i>in Vivo</i> Fiber Photometry and Behavior Tests Can Facilitate the Measurement of Neuronal Activity in the Primary Somatosensory Cortex and Hyperalgesia in an Inflammatory Pain Mice Model

Machines, mathematics, and modules: the potential to provide real-time metrics for pain under anesthesia

HCN channels in the lateral habenula regulate pain and comorbid depressive‐like behaviors in mice

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