Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons

Yan Tang; Diego Benusiglio; Arthur Lefevre; Louis Hilfiger; Ferdinand Althammer; Anna Bludau; Daisuke Hagiwara; Angel Baudon; Pascal Darbon; Jonas Schimmer; Matthew K. Kirchner; Ranjan K. Roy; Shiyi Wang; Marina Eliava; Shlomo Wagner; Martina Oberhuber; Karl K. Conzelmann; Martin Schwarz; Javier E. Stern; Gareth Leng; Inga D. Neumann; Alexandre Charlet; Valery Grinevich

doi:10.1038/s41593-020-0674-y

Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons

Yan Tang, Diego Benusiglio, Arthur Lefevre, Louis Hilfiger, Ferdinand Althammer, Anna Bludau, Daisuke Hagiwara, Angel Baudon, Pascal Darbon, Jonas Schimmer, Matthew K. Kirchner, Ranjan K. Roy, Shiyi Wang, Marina Eliava, Shlomo Wagner, Martina Oberhuber, Karl K. Conzelmann, Martin Schwarz, Javier E. Stern, Gareth LengInga D. Neumann, Alexandre Charlet, Valery Grinevich

Department of Neurobiology

Research output: Contribution to journal › Article › peer-review

Abstract

Oxytocin (OT) is a great facilitator of social life but, although its effects on socially relevant brain regions have been extensively studied, OT neuron activity during actual social interactions remains unexplored. Most OT neurons are magnocellular neurons, which simultaneously project to the pituitary and forebrain regions involved in social behaviors. In the present study, we show that a much smaller population of OT neurons, parvocellular neurons that do not project to the pituitary but synapse onto magnocellular neurons, is preferentially activated by somatosensory stimuli. This activation is transmitted to the larger population of magnocellular neurons, which consequently show coordinated increases in their activity during social interactions between virgin female rats. Selectively activating these parvocellular neurons promotes social motivation, whereas inhibiting them reduces social interactions. Thus, parvocellular OT neurons receive particular inputs to control social behavior by coordinating the responses of the much larger population of magnocellular OT neurons.

Original language	English
Pages (from-to)	1125-1137
Number of pages	13
Journal	Nature Neuroscience
Volume	23
Issue number	9
DOIs	https://doi.org/10.1038/s41593-020-0674-y
State	Published - 1 Sep 2020

Bibliographical note

Funding Information:
We thank T. Grund and X. Liu for initial contribution to this study, R. Stoop for valuable comments on the manuscript, J. Müller for packaging viral vectors, E. Kremer for the canine virus, J. Maicos-Roya for contributing to the modeling of OT release, S. Netser for his comments on the manuscript, C. Pitzer and the Interdisciplinary Neurobehavioral Core Facility of Heidelberg University for some of the behavioral experiments performed there, and T. Splettstoesser (www.scistyle.com) for composing Extended Data Fig. 10. The work was supported by Chinese Scholarship Council No. 201406140043 (to Y.T.), the German Research Foundation (DFG) within the Collaborative Research Center (SFB) 1158 seed grant for young researchers and Fyssen Foundation (to A.L.), DFG postdoctoral fellowship AL 2466/1-1 (to F.A.), Alexander von Humboldt research fellowship (to D.H.), Human Frontier Science Program RGP0019/2015 (to V.G. and S.W.), Israel Science Foundation (grant nos. 1350/12 and 1361/17), Milgrom Foundation and the Ministry of Science, Technology and Space of Israel (grant no. 3-12068, to S.W.), NIH grant (no. R01NS094640, to J.E.S.), BBSRC grant (no. BB/S000224/1, to G.L.), DFG grant (nos. NE 465/27, NE 465/31 and NE 465/34, to I.D.N.), ANR-DFG grant and PICS grant (no. GR 3619/701 and no. GR 07882, to A.C. and V.G.), NARSAD Young Investigator grant (no. 24821) and ANR JCJC grant (no. GR 19-CE16-0011-01, to A.C.), DFG grant (no. GR 3619/4-1), SFB 1158, SNSF-DFG grant (no. GR 3619/8-1) and Fritz Thyssen Foundation grant (no. 10.16.2.018 MN) (all to V.G.).

Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

ASJC Scopus subject areas

Neuroscience (all)

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10.1038/s41593-020-0674-y

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Tang, Y., Benusiglio, D., Lefevre, A., Hilfiger, L., Althammer, F., Bludau, A., Hagiwara, D., Baudon, A., Darbon, P., Schimmer, J., Kirchner, M. K., Roy, R. K., Wang, S., Eliava, M., Wagner, S., Oberhuber, M., Conzelmann, K. K., Schwarz, M., Stern, J. E., ... Grinevich, V. (2020). Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons. Nature Neuroscience, 23(9), 1125-1137. https://doi.org/10.1038/s41593-020-0674-y

@article{b2578abac4844bd791ba3fae15929c51,

title = "Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons",

abstract = "Oxytocin (OT) is a great facilitator of social life but, although its effects on socially relevant brain regions have been extensively studied, OT neuron activity during actual social interactions remains unexplored. Most OT neurons are magnocellular neurons, which simultaneously project to the pituitary and forebrain regions involved in social behaviors. In the present study, we show that a much smaller population of OT neurons, parvocellular neurons that do not project to the pituitary but synapse onto magnocellular neurons, is preferentially activated by somatosensory stimuli. This activation is transmitted to the larger population of magnocellular neurons, which consequently show coordinated increases in their activity during social interactions between virgin female rats. Selectively activating these parvocellular neurons promotes social motivation, whereas inhibiting them reduces social interactions. Thus, parvocellular OT neurons receive particular inputs to control social behavior by coordinating the responses of the much larger population of magnocellular OT neurons.",

author = "Yan Tang and Diego Benusiglio and Arthur Lefevre and Louis Hilfiger and Ferdinand Althammer and Anna Bludau and Daisuke Hagiwara and Angel Baudon and Pascal Darbon and Jonas Schimmer and Kirchner, {Matthew K.} and Roy, {Ranjan K.} and Shiyi Wang and Marina Eliava and Shlomo Wagner and Martina Oberhuber and Conzelmann, {Karl K.} and Martin Schwarz and Stern, {Javier E.} and Gareth Leng and Neumann, {Inga D.} and Alexandre Charlet and Valery Grinevich",

note = "Funding Information: We thank T. Grund and X. Liu for initial contribution to this study, R. Stoop for valuable comments on the manuscript, J. M{\"u}ller for packaging viral vectors, E. Kremer for the canine virus, J. Maicos-Roya for contributing to the modeling of OT release, S. Netser for his comments on the manuscript, C. Pitzer and the Interdisciplinary Neurobehavioral Core Facility of Heidelberg University for some of the behavioral experiments performed there, and T. Splettstoesser (www.scistyle.com) for composing Extended Data Fig. 10. The work was supported by Chinese Scholarship Council No. 201406140043 (to Y.T.), the German Research Foundation (DFG) within the Collaborative Research Center (SFB) 1158 seed grant for young researchers and Fyssen Foundation (to A.L.), DFG postdoctoral fellowship AL 2466/1-1 (to F.A.), Alexander von Humboldt research fellowship (to D.H.), Human Frontier Science Program RGP0019/2015 (to V.G. and S.W.), Israel Science Foundation (grant nos. 1350/12 and 1361/17), Milgrom Foundation and the Ministry of Science, Technology and Space of Israel (grant no. 3-12068, to S.W.), NIH grant (no. R01NS094640, to J.E.S.), BBSRC grant (no. BB/S000224/1, to G.L.), DFG grant (nos. NE 465/27, NE 465/31 and NE 465/34, to I.D.N.), ANR-DFG grant and PICS grant (no. GR 3619/701 and no. GR 07882, to A.C. and V.G.), NARSAD Young Investigator grant (no. 24821) and ANR JCJC grant (no. GR 19-CE16-0011-01, to A.C.), DFG grant (no. GR 3619/4-1), SFB 1158, SNSF-DFG grant (no. GR 3619/8-1) and Fritz Thyssen Foundation grant (no. 10.16.2.018 MN) (all to V.G.). Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2020",

month = sep,

day = "1",

doi = "10.1038/s41593-020-0674-y",

language = "English",

volume = "23",

pages = "1125--1137",

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Tang, Y, Benusiglio, D, Lefevre, A, Hilfiger, L, Althammer, F, Bludau, A, Hagiwara, D, Baudon, A, Darbon, P, Schimmer, J, Kirchner, MK, Roy, RK, Wang, S, Eliava, M, Wagner, S, Oberhuber, M, Conzelmann, KK, Schwarz, M, Stern, JE, Leng, G, Neumann, ID, Charlet, A & Grinevich, V 2020, 'Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons', Nature Neuroscience, vol. 23, no. 9, pp. 1125-1137. https://doi.org/10.1038/s41593-020-0674-y

TY - JOUR

T1 - Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons

AU - Tang, Yan

AU - Benusiglio, Diego

AU - Lefevre, Arthur

AU - Hilfiger, Louis

AU - Althammer, Ferdinand

AU - Bludau, Anna

AU - Hagiwara, Daisuke

AU - Baudon, Angel

AU - Darbon, Pascal

AU - Schimmer, Jonas

AU - Kirchner, Matthew K.

AU - Roy, Ranjan K.

AU - Wang, Shiyi

AU - Eliava, Marina

AU - Wagner, Shlomo

AU - Oberhuber, Martina

AU - Conzelmann, Karl K.

AU - Schwarz, Martin

AU - Stern, Javier E.

AU - Leng, Gareth

AU - Neumann, Inga D.

AU - Charlet, Alexandre

AU - Grinevich, Valery

N1 - Funding Information: We thank T. Grund and X. Liu for initial contribution to this study, R. Stoop for valuable comments on the manuscript, J. Müller for packaging viral vectors, E. Kremer for the canine virus, J. Maicos-Roya for contributing to the modeling of OT release, S. Netser for his comments on the manuscript, C. Pitzer and the Interdisciplinary Neurobehavioral Core Facility of Heidelberg University for some of the behavioral experiments performed there, and T. Splettstoesser (www.scistyle.com) for composing Extended Data Fig. 10. The work was supported by Chinese Scholarship Council No. 201406140043 (to Y.T.), the German Research Foundation (DFG) within the Collaborative Research Center (SFB) 1158 seed grant for young researchers and Fyssen Foundation (to A.L.), DFG postdoctoral fellowship AL 2466/1-1 (to F.A.), Alexander von Humboldt research fellowship (to D.H.), Human Frontier Science Program RGP0019/2015 (to V.G. and S.W.), Israel Science Foundation (grant nos. 1350/12 and 1361/17), Milgrom Foundation and the Ministry of Science, Technology and Space of Israel (grant no. 3-12068, to S.W.), NIH grant (no. R01NS094640, to J.E.S.), BBSRC grant (no. BB/S000224/1, to G.L.), DFG grant (nos. NE 465/27, NE 465/31 and NE 465/34, to I.D.N.), ANR-DFG grant and PICS grant (no. GR 3619/701 and no. GR 07882, to A.C. and V.G.), NARSAD Young Investigator grant (no. 24821) and ANR JCJC grant (no. GR 19-CE16-0011-01, to A.C.), DFG grant (no. GR 3619/4-1), SFB 1158, SNSF-DFG grant (no. GR 3619/8-1) and Fritz Thyssen Foundation grant (no. 10.16.2.018 MN) (all to V.G.). Publisher Copyright: © 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2020/9/1

Y1 - 2020/9/1

N2 - Oxytocin (OT) is a great facilitator of social life but, although its effects on socially relevant brain regions have been extensively studied, OT neuron activity during actual social interactions remains unexplored. Most OT neurons are magnocellular neurons, which simultaneously project to the pituitary and forebrain regions involved in social behaviors. In the present study, we show that a much smaller population of OT neurons, parvocellular neurons that do not project to the pituitary but synapse onto magnocellular neurons, is preferentially activated by somatosensory stimuli. This activation is transmitted to the larger population of magnocellular neurons, which consequently show coordinated increases in their activity during social interactions between virgin female rats. Selectively activating these parvocellular neurons promotes social motivation, whereas inhibiting them reduces social interactions. Thus, parvocellular OT neurons receive particular inputs to control social behavior by coordinating the responses of the much larger population of magnocellular OT neurons.

AB - Oxytocin (OT) is a great facilitator of social life but, although its effects on socially relevant brain regions have been extensively studied, OT neuron activity during actual social interactions remains unexplored. Most OT neurons are magnocellular neurons, which simultaneously project to the pituitary and forebrain regions involved in social behaviors. In the present study, we show that a much smaller population of OT neurons, parvocellular neurons that do not project to the pituitary but synapse onto magnocellular neurons, is preferentially activated by somatosensory stimuli. This activation is transmitted to the larger population of magnocellular neurons, which consequently show coordinated increases in their activity during social interactions between virgin female rats. Selectively activating these parvocellular neurons promotes social motivation, whereas inhibiting them reduces social interactions. Thus, parvocellular OT neurons receive particular inputs to control social behavior by coordinating the responses of the much larger population of magnocellular OT neurons.

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DO - 10.1038/s41593-020-0674-y

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VL - 23

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JO - Nature Neuroscience

JF - Nature Neuroscience

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ER -

Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons

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