Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain

Yu Shin Kim, Michael Anderson, Kyoungsook Park, Qin Zheng, Amit Agarwal, Catherine Gong, Saijilafu, Le Anne Young, Shaoqiu He, Pamela Colleen LaVinka, Fengquan Zhou, Dwight Bergles, Menachem Hanani, Yun Guan, David C. Spray, Xinzhong Dong

Research output: Contribution to journalArticle

54 Citations (Scopus)

Abstract

Primary sensory neurons in the DRG play an essential role in initiating pain by detecting painful stimuli in the periphery. Tissue injury can sensitize DRG neurons, causing heightened pain sensitivity, often leading to chronic pain. Despite the functional importance, how DRG neurons function at a population level is unclear due to the lack of suitable tools. Here we developed an imaging technique that allowed us to simultaneously monitor the activities of >1,600 neurons/DRG in live mice and discovered a striking neuronal coupling phenomenon that adjacent neurons tend to activate together following tissue injury. This coupled activation occurs among various neurons and is mediated by an injury-induced upregulation of gap junctions in glial cells surrounding DRG neurons. Blocking gap junctions attenuated neuronal coupling and mechanical hyperalgesia. Therefore, neuronal coupling represents a new form of neuronal plasticity in the DRG and contributes to pain hypersensitivity by “hijacking” neighboring neurons through gap junctions.

Original languageEnglish (US)
Pages (from-to)1085-1096
Number of pages12
JournalNeuron
Volume91
Issue number5
DOIs
StatePublished - Sep 7 2016
Externally publishedYes

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Sensory Receptor Cells
Diagnosis-Related Groups
Chronic Pain
Neurons
Gap Junctions
Pain
Wounds and Injuries
Electrical Synapses
Neuronal Plasticity
Hyperalgesia
Neuroglia
Hypersensitivity
Up-Regulation
Population

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Kim, Y. S., Anderson, M., Park, K., Zheng, Q., Agarwal, A., Gong, C., ... Dong, X. (2016). Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain. Neuron, 91(5), 1085-1096. https://doi.org/10.1016/j.neuron.2016.07.044

Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain. / Kim, Yu Shin; Anderson, Michael; Park, Kyoungsook; Zheng, Qin; Agarwal, Amit; Gong, Catherine; Saijilafu; Young, Le Anne; He, Shaoqiu; LaVinka, Pamela Colleen; Zhou, Fengquan; Bergles, Dwight; Hanani, Menachem; Guan, Yun; Spray, David C.; Dong, Xinzhong.

In: Neuron, Vol. 91, No. 5, 07.09.2016, p. 1085-1096.

Research output: Contribution to journalArticle

Kim, YS, Anderson, M, Park, K, Zheng, Q, Agarwal, A, Gong, C, Saijilafu, Young, LA, He, S, LaVinka, PC, Zhou, F, Bergles, D, Hanani, M, Guan, Y, Spray, DC & Dong, X 2016, 'Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain', Neuron, vol. 91, no. 5, pp. 1085-1096. https://doi.org/10.1016/j.neuron.2016.07.044
Kim YS, Anderson M, Park K, Zheng Q, Agarwal A, Gong C et al. Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain. Neuron. 2016 Sep 7;91(5):1085-1096. https://doi.org/10.1016/j.neuron.2016.07.044
Kim, Yu Shin ; Anderson, Michael ; Park, Kyoungsook ; Zheng, Qin ; Agarwal, Amit ; Gong, Catherine ; Saijilafu ; Young, Le Anne ; He, Shaoqiu ; LaVinka, Pamela Colleen ; Zhou, Fengquan ; Bergles, Dwight ; Hanani, Menachem ; Guan, Yun ; Spray, David C. ; Dong, Xinzhong. / Coupled Activation of Primary Sensory Neurons Contributes to Chronic Pain. In: Neuron. 2016 ; Vol. 91, No. 5. pp. 1085-1096.
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