Cited by 249Neuroendocrine regulation and behaviorOlfactory and Sensory Function StudiesNeuropeptides and Animal Physiology

Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons

Open access
Tang, Yan, Benusiglio, Diego, Lefevre, Arthur, Hilfiger, Louis, Althammer, Ferdinand, Bludau, Anna, Hagiwara, Daisuke, Baudon, Angel +15 more·2020·Nature Neuroscience

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.

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Crossref · 10.1038/s41593-020-0674-y

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  • Positive effects of touch from others are likely mediated by increased secretion of oxytocin.

    “positive effects are likely mediated by increased secretion of the neuropeptide oxytocin [6,[16], [17], [18], [19]].”

    From Self-soothing touch and being hugged reduce cortisol responses to stress: A randomized controlled trial on stress, physical touch, and social identity (2021) · cites this paper as [6]

    The indexed Abstract (page unavailable) describes oxytocin release in pain modulation, but does not link touch to increased oxytocin secretion or to its positive effects. Searches for social touch, secretion, and oxytocin release found no passage in our copy establishing that link. (LLM, conf=0.72)

    Experimental — accuracy not yet measured
  • Our finding that receiving hugs from people is effective irrespective of sharing a social identity with them is in line with the benefits of massage therapy and animal studies.

    “Despite these potential explanations, our finding that receiving hugs from people is effective irrespective of sharing a social identity with them is in line with the benefits of massage therapy [4,5] and animal studies (e.g., Ref. [6]).”

    From Self-soothing touch and being hugged reduce cortisol responses to stress: A randomized controlled trial on stress, physical touch, and social identity (2021) · cites this paper as [6]

    The References section names Tang et al.’s social-touch study, but the body passages returned from our copy discuss oxytocin-mediated analgesia in rats rather than benefits of social touch. A search for social touch and its effects did not find a passage establishing the animal-study comparison for which this citation is used. The apparent mismatch between the indexed title and body text prevents verification from our copy. (LLM, conf=0.75)

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  • In rats and mice, several regions provide input to paraventricular oxytocin-expressing cells, including brainstem, thalamic, hypothalamic, and cortical cell populations.

    “In rats and mice, several regions provide input to PVN OXT-expressing cells, including the brainstem, thalamic, hypothalamic, and cortical cell populations (56-58)”
  • OXT neurons are activated in response to social stimuli including social touch, infant cries and mating.

    “Furthermore, OXT neurons are activated in response to social stimuli including social touch 20, infant cries 21 and mating.”
  • PVN oxytocin cells receive projections from many areas of the brain.

    “PVN oxytocin cells receive projections from many areas of the brain”

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References 65 · Cited by 249

Research works printed but not linked: 9

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  2. Knobloch, H S., Charlet, A., Stoop, R. & Grinevich, V. Viral vectors for optogenetics of hypothalamic neuropeptides. Springer Proto- cols (2014).
  3. Chow, L. H., Chen, Y. H., Wu, W. C., Chang, E. P. & Huang, E. Y. Sex difference in oxytocin-induced anti-hyperalgesia at the spinal level in rats with intraplantar carrageenan-induced inflammation. PLoS ONE 11, e0162218 (2016).
  4. Hilfiger, L. et al. A nonpeptide oxytocin receptor agonist for a dur- able relief of inflammatory pain. Sci. Rep. 10, 3017 (2020).
  5. Harris, J. A. et al. Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front Neural Circuits 8, 76 (2014).
  6. Haeussler, M. et al. Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 17, 148 (2016).
  7. Wefers, B. et al. Direct production of mouse disease models by embryo microinjection of TALENs and oligodeoxynucleotides. Proc. Natl Acad. Sci. USA 110, 3782-3787 (2013).
  8. Schonig, K., Schwenk, F., Rajewsky, K. & Bujard, H. Stringent dox- ycycline dependent control of CRE recombinase in vivo. Nucleic Acids Res 30, e134 (2002).
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Authors
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., Leng, G., Neumann, I. D., Charlet, A., & Grinevich, V.
Affiliations
  • Heidelberg University (DE)
  • Centre National de la Recherche Scientifique (FR)
  • Georgia State University (US)
  • University of Regensburg (DE)
  • University of Haifa (IL)
  • Max-von-Pettenkofer-Institut für Hygiene und Medizinische Mikrobiologie (DE)
  • University of Bonn (DE)
  • University of Edinburgh (GB)
Venue
Nature Neuroscience
Published
2020-07-27
Volume
23
Issue
9
Pages
1125-1137
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W3045202423
Cited by
249
References
65
Citations by year
2026: 30 · 2025: 28 · 2024: 36 · 2023: 46 · 2022: 50 · 2021: 48 · 2020: 10 · 2018: 1
FWCI
42.14
Type
journal article
Language
en
Open access
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • HAL (submittedVersion, other-oa)
  • University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
Funders
  • Georgia State University
  • National Alliance for Research on Schizophrenia and Depression (24821)
  • Deutscher Akademischer Austauschdienst (57552337)
  • Deutsche Forschungsgemeinschaft (AL 2466/1-1, GR 3619/16‐1, 3619/16-1, 3619/701, GR 3619/15-1, GR 3619/701, 459051339)
  • Agence Nationale de la Recherche (UPR3212, ANR-17-EURE-, ANR-19-CE16-0011, ANR-17, ANR-17-EURE-0022)
  • Fondation Fyssen
  • Université de Strasbourg (ANR-17-EURE-0022, UPR3212)
  • Centre National de la Recherche Scientifique (ANR‐17‐EURE‐0022, UPR3212)
  • National Institutes of Health
  • Biotechnology and Biological Sciences Research Council (BB/S000224/1)
  • National Heart, Lung, and Blood Institute (R01HL090948, HL090948)
  • National Institute of Neurological Disorders and Stroke (R01NS094640)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords
oxytocin, social touch, somatosensory stimuli, social motivation, social behavior, oxytocin neurons, magnocellular neurons
MeSH terms
Animals, Behavior, Animal, Female, Neurons, Oxytocin, Paraventricular Hypothalamic Nucleus, Social Behavior, Touch, Rats, Wistar, Rats, Touch Perception

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