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Gamma oscillations in somatosensory cortex recruit prefrontal and descending serotonergic pathways in aversion and nociception

Author

Listed:
  • Linette Liqi Tan

    (Medical Faculty Heidelberg)

  • Manfred Josef Oswald

    (Medical Faculty Heidelberg)

  • Céline Heinl

    (Medical Faculty Heidelberg)

  • Oscar Andrés Retana Romero

    (Medical Faculty Heidelberg)

  • Sanjeev Kumar Kaushalya

    (Medical Faculty Heidelberg)

  • Hannah Monyer

    (Medical Faculty Heidelberg and German Cancer Research Center)

  • Rohini Kuner

    (Medical Faculty Heidelberg)

Abstract

In humans, gamma-band oscillations in the primary somatosensory cortex (S1) correlate with subjective pain perception. However, functional contributions to pain and the nature of underlying circuits are unclear. Here we report that gamma oscillations, but not other rhythms, are specifically strengthened independently of any motor component in the S1 cortex of mice during nociception. Moreover, mice with inflammatory pain show elevated resting gamma and alpha activity and increased gamma power in response to sub-threshold stimuli, in association with behavioral nociceptive hypersensitivity. Inducing gamma oscillations via optogenetic activation of parvalbumin-expressing inhibitory interneurons in the S1 cortex enhances nociceptive sensitivity and induces aversive avoidance behavior. Activity mapping identified a network of prefrontal cortical and subcortical centers whilst morphological tracing and pharmacological studies demonstrate the requirement of descending serotonergic facilitatory pathways in these pain-related behaviors. This study thus describes a mechanistic framework for modulation of pain by specific activity patterns in the S1 cortex.

Suggested Citation

  • Linette Liqi Tan & Manfred Josef Oswald & Céline Heinl & Oscar Andrés Retana Romero & Sanjeev Kumar Kaushalya & Hannah Monyer & Rohini Kuner, 2019. "Gamma oscillations in somatosensory cortex recruit prefrontal and descending serotonergic pathways in aversion and nociception," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08873-z
    DOI: 10.1038/s41467-019-08873-z
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    Cited by:

    1. 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.
    2. Longyu Ma & Lupeng Yue & Shuting Liu & Shi Xu & Jifu Tong & Xiaoyan Sun & Li Su & Shuang Cui & Feng-Yu Liu & You Wan & Ming Yi, 2024. "A distinct neuronal ensemble of prelimbic cortex mediates spontaneous pain in rats with peripheral inflammation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Daniel G. Taub & Qiufen Jiang & Francesca Pietrafesa & Junfeng Su & Aloe Carroll & Caitlin Greene & Michael R. Blanchard & Aakanksha Jain & Mahmoud El-Rifai & Alexis Callen & Katherine Yager & Clara C, 2024. "The secondary somatosensory cortex gates mechanical and heat sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Manfred J. Oswald & Yechao Han & Han Li & Samuel Marashli & Deniz Nouri Oglo & Bhavya Ojha & Paul V. Naser & Zheng Gan & Rohini Kuner, 2022. "Cholinergic basal forebrain nucleus of Meynert regulates chronic pain-like behavior via modulation of the prelimbic cortex," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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