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Identification of touch neurons underlying dopaminergic pleasurable touch and sexual receptivity

Leah Middleton, Melanie Schaffler, Isabella Succi, William Foster, Mark Gradwell, Manon Bohic, Lindsay Ejoh, Victoria Abraira, View ORCID ProfileIshmail Abdus-Saboor
doi: https://doi.org/10.1101/2021.09.22.461355
Leah Middleton
1Zuckerman Mind Brain Behavior Institute and Department of Biological Sciences, Columbia University, New York, New York, United States of America
2Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, PA, USA
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Melanie Schaffler
1Zuckerman Mind Brain Behavior Institute and Department of Biological Sciences, Columbia University, New York, New York, United States of America
2Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, PA, USA
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Isabella Succi
1Zuckerman Mind Brain Behavior Institute and Department of Biological Sciences, Columbia University, New York, New York, United States of America
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William Foster
1Zuckerman Mind Brain Behavior Institute and Department of Biological Sciences, Columbia University, New York, New York, United States of America
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Mark Gradwell
3Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
4W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
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Manon Bohic
3Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
4W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
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Lindsay Ejoh
2Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, PA, USA
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Victoria Abraira
3Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
4W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, United States of America
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Ishmail Abdus-Saboor
1Zuckerman Mind Brain Behavior Institute and Department of Biological Sciences, Columbia University, New York, New York, United States of America
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  • ORCID record for Ishmail Abdus-Saboor
  • For correspondence: ia2458@columbia.edu
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Abstract

Pleasurable touch during social behavior is the key to building familial bonds and meaningful connections. One form of social touch occurs during sex. Although sexual behavior is initiated in part by touch, and touch is ongoing throughout copulation, the identity and role of sensory neurons that transduce sexual touch remain unknown. A population of sensory neurons labeled by the G-protein coupled receptor Mrgprb4 detect stroking touch in mice1,2. Here, we study the social relevance of this population by genetically engineering mice to allow activation or ablation of Mrgprb4-lineage neurons and reveal that these neurons are required for sexual receptivity and sufficient to activate reward circuitry. Even in social isolation, optogenetic stimulation of Mrgprb4-lineage neurons through the back skin is sufficient to induce a conditioned place preference and a striking dorsoflexion resembling the lordotic copulatory posture in females. In the absence of Mrgprb4-lineage neurons, female mice no longer find male mounts rewarding: sexual receptivity is supplanted by aggression and a coincident decline in dopaminergic release in the mesolimbic reward pathway. In addition to sexual behavior, Mrgprb4-lineage neurons are also required for social postures induced by female-to-female back touch. Together, these findings establish that Mrgprb4-lineage neurons are the first neurons of a skin-to-brain circuit encoding the rewarding quality of social touch.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 22, 2021.
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Identification of touch neurons underlying dopaminergic pleasurable touch and sexual receptivity
Leah Middleton, Melanie Schaffler, Isabella Succi, William Foster, Mark Gradwell, Manon Bohic, Lindsay Ejoh, Victoria Abraira, Ishmail Abdus-Saboor
bioRxiv 2021.09.22.461355; doi: https://doi.org/10.1101/2021.09.22.461355
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Identification of touch neurons underlying dopaminergic pleasurable touch and sexual receptivity
Leah Middleton, Melanie Schaffler, Isabella Succi, William Foster, Mark Gradwell, Manon Bohic, Lindsay Ejoh, Victoria Abraira, Ishmail Abdus-Saboor
bioRxiv 2021.09.22.461355; doi: https://doi.org/10.1101/2021.09.22.461355

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