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Primary Somatosensory Cortex Bidirectionally Modulates Sensory Gain and Nociceptive Behavior in a Layer-Specific Manner

Katharina Ziegler, Jan Burghardt, Ross Folkard, Antonio J Gonzalez, Sailaja Antharvedi-Goda, View ORCID ProfileJesus Martin-Cortecero, Emilio Isaías-Camacho, Sanjeev Kaushalya, Linette Liqi Tan, Thomas Kuner, View ORCID ProfileRohini Kuner, Rebecca Mease, View ORCID ProfileAlexander Groh
doi: https://doi.org/10.1101/2022.08.02.502350
Katharina Ziegler
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Jan Burghardt
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Ross Folkard
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Antonio J Gonzalez
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Sailaja Antharvedi-Goda
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Jesus Martin-Cortecero
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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  • ORCID record for Jesus Martin-Cortecero
Emilio Isaías-Camacho
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Sanjeev Kaushalya
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA
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Linette Liqi Tan
3Institute for Pharmacology, Heidelberg University, Germany
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Thomas Kuner
4Institute for Anatomy, Heidelberg University, Germany
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Rohini Kuner
3Institute for Pharmacology, Heidelberg University, Germany
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Rebecca Mease
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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Alexander Groh
1Medical Biophysics, Institute for Physiology and Pathophysiology, Heidelberg University, Germany
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  • ORCID record for Alexander Groh
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Abstract

The primary somatosensory cortex (S1) is the 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. Unspecific bulk manipulations of S1 activity have not disambiguated the precise role of the S1 in nociception and pain. Here, using cell-type-specific manipulations in mouse S1 we reveal the involvement of two major cortical output neuron types in layers 5 (L5) and 6 (L6) in the perception of innocuous and noxious somatosensory signals. We find that L6 neurons can drive aversive hypersensitivity and spontaneous nocifensive behavior. L6 downstream effects revealed enhanced thalamic somatosensory responses, and in parallel, strong suppression of L5 neurons, pointing towards an antinociceptive function of L5 output. Indeed, targeted L5 activation reduced sensory sensitivity and normalized inflammatory allodynia, thus revealing a layer-specific and bidirectional role for S1 in modulating subjective sensory experiences.

Competing Interest Statement

The authors have declared no competing interest.

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Posted August 03, 2022.
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Primary Somatosensory Cortex Bidirectionally Modulates Sensory Gain and Nociceptive Behavior in a Layer-Specific Manner
Katharina Ziegler, Jan Burghardt, Ross Folkard, Antonio J Gonzalez, Sailaja Antharvedi-Goda, Jesus Martin-Cortecero, Emilio Isaías-Camacho, Sanjeev Kaushalya, Linette Liqi Tan, Thomas Kuner, Rohini Kuner, Rebecca Mease, Alexander Groh
bioRxiv 2022.08.02.502350; doi: https://doi.org/10.1101/2022.08.02.502350
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Primary Somatosensory Cortex Bidirectionally Modulates Sensory Gain and Nociceptive Behavior in a Layer-Specific Manner
Katharina Ziegler, Jan Burghardt, Ross Folkard, Antonio J Gonzalez, Sailaja Antharvedi-Goda, Jesus Martin-Cortecero, Emilio Isaías-Camacho, Sanjeev Kaushalya, Linette Liqi Tan, Thomas Kuner, Rohini Kuner, Rebecca Mease, Alexander Groh
bioRxiv 2022.08.02.502350; doi: https://doi.org/10.1101/2022.08.02.502350

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