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Synchronized activity of sensory neurons initiates cortical synchrony in a model of neuropathic pain

Author

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  • Chao Chen

    (Peking 301 Hospital
    First Affiliated Hospital of Southern University of Science and Technology)

  • Linlin Sun

    (Columbia University Medical Center
    Peking University)

  • Avital Adler

    (New York University School of Medicine)

  • Hang Zhou

    (Columbia University Medical Center)

  • Licheng Zhang

    (Peking 301 Hospital)

  • Lihai Zhang

    (Peking 301 Hospital)

  • Junhao Deng

    (Peking 301 Hospital)

  • Yang Bai

    (Shenzhen Bay Laboratory)

  • Jinhui Zhang

    (the Affiliated Southeast Hospital of Xiamen University)

  • Guang Yang

    (Columbia University Medical Center)

  • Wen-Biao Gan

    (Shenzhen Bay Laboratory)

  • Peifu Tang

    (Peking 301 Hospital)

Abstract

Increased low frequency cortical oscillations are observed in people with neuropathic pain, but the cause of such elevated cortical oscillations and their impact on pain development remain unclear. By imaging neuronal activity in a spared nerve injury (SNI) mouse model of neuropathic pain, we show that neurons in dorsal root ganglia (DRG) and somatosensory cortex (S1) exhibit synchronized activity after peripheral nerve injury. Notably, synchronized activity of DRG neurons occurs within hours after injury and 1-2 days before increased cortical oscillations. This DRG synchrony is initiated by axotomized neurons and mediated by local purinergic signaling at the site of nerve injury. We further show that synchronized DRG activity after SNI is responsible for increasing low frequency cortical oscillations and synaptic remodeling in S1, as well as for inducing animals’ pain-like behaviors. In naive mice, enhancing the synchrony, not the level, of DRG neuronal activity causes synaptic changes in S1 and pain-like behaviors similar to SNI mice. Taken together, these results reveal the critical role of synchronized DRG neuronal activity in increasing cortical plasticity and oscillations in a neuropathic pain model. These findings also suggest the potential importance of detection and suppression of elevated cortical oscillations in neuropathic pain states.

Suggested Citation

  • Chao Chen & Linlin Sun & Avital Adler & Hang Zhou & Licheng Zhang & Lihai Zhang & Junhao Deng & Yang Bai & Jinhui Zhang & Guang Yang & Wen-Biao Gan & Peifu Tang, 2023. "Synchronized activity of sensory neurons initiates cortical synchrony in a model of neuropathic pain," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36093-z
    DOI: 10.1038/s41467-023-36093-z
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    References listed on IDEAS

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