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Primary somatosensory cortex bidirectionally modulates sensory gain and nociceptive behavior in a layer-specific manner

Author

Listed:
  • Katharina Ziegler

    (Heidelberg University)

  • Ross Folkard

    (Heidelberg University)

  • Antonio J. Gonzalez

    (Heidelberg University)

  • Jan Burghardt

    (Heidelberg University)

  • Sailaja Antharvedi-Goda

    (Heidelberg University)

  • Jesus Martin-Cortecero

    (Heidelberg University)

  • Emilio Isaías-Camacho

    (Heidelberg University)

  • Sanjeev Kaushalya

    (Heidelberg University)

  • Linette Liqi Tan

    (Heidelberg University)

  • Thomas Kuner

    (Heidelberg University)

  • Claudio Acuna

    (Heidelberg University)

  • Rohini Kuner

    (Heidelberg University)

  • Rebecca Audrey Mease

    (Heidelberg University)

  • Alexander Groh

    (Heidelberg University)

Abstract

The primary somatosensory cortex (S1) is a hub for body sensation of both innocuous and noxious signals, yet its role in somatosensation versus pain is debated. Despite known contributions of S1 to sensory gain modulation, its causal involvement in subjective sensory experiences remains elusive. Here, in mouse S1, we reveal the involvement of cortical output neurons in layers 5 (L5) and 6 (L6) in the perception of innocuous and noxious somatosensory signals. We find that L6 activation can drive aversive hypersensitivity and spontaneous nocifensive behavior. Linking behavior to neuronal mechanisms, we find that L6 enhances thalamic somatosensory responses, and in parallel, strongly suppresses L5 neurons. Directly suppressing L5 reproduced the pronociceptive phenotype induced by L6 activation, suggesting an anti-nociceptive function for L5 output. Indeed, L5 activation reduced sensory sensitivity and reversed inflammatory allodynia. Together, these findings reveal a layer-specific and bidirectional role for S1 in modulating subjective sensory experiences.

Suggested Citation

  • Katharina Ziegler & Ross Folkard & Antonio J. Gonzalez & Jan Burghardt & Sailaja Antharvedi-Goda & Jesus Martin-Cortecero & Emilio Isaías-Camacho & Sanjeev Kaushalya & Linette Liqi Tan & Thomas Kuner , 2023. "Primary somatosensory cortex bidirectionally modulates sensory gain and nociceptive behavior in a layer-specific manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38798-7
    DOI: 10.1038/s41467-023-38798-7
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    References listed on IDEAS

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    1. Arghya Mukherjee & Norman H. Lam & Ralf D. Wimmer & Michael M. Halassa, 2021. "Thalamic circuits for independent control of prefrontal signal and noise," Nature, Nature, vol. 600(7887), pages 100-104, December.
    2. Shawn R. Olsen & Dante S. Bortone & Hillel Adesnik & Massimo Scanziani, 2012. "Gain control by layer six in cortical circuits of vision," Nature, Nature, vol. 483(7387), pages 47-52, March.
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    Cited by:

    1. 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.

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