IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47255-y.html
   My bibliography  Save this article

Dopamine control of social novelty preference is constrained by an interpeduncular-tegmentum circuit

Author

Listed:
  • Susanna Molas

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB
    University of Colorado Boulder 1480 30th St
    University of Colorado Boulder 1905 Colorado Ave)

  • Timothy G. Freels

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Rubing Zhao-Shea

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Timothy Lee

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Pablo Gimenez-Gomez

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Melanie Barbini

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Gilles E. Martin

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

  • Andrew R. Tapper

    (Brudnick Neuropsychiatric Research Institute University of Massachusetts Chan Medical School 364 Plantation St, LRB)

Abstract

Animals are inherently motivated to explore social novelty cues over familiar ones, resulting in a novelty preference (NP), although the behavioral and circuit bases underlying NP are unclear. Combining calcium and neurotransmitter sensors with fiber photometry and optogenetics in mice, we find that mesolimbic dopamine (DA) neurotransmission is strongly and predominantly activated by social novelty controlling bout length of interaction during NP, a response significantly reduced by familiarity. In contrast, interpeduncular nucleus (IPN) GABAergic neurons that project to the lateral dorsal tegmentum (LDTg) were inhibited by social novelty but activated during terminations with familiar social stimuli. Inhibition of this pathway during NP increased interaction and bout length with familiar social stimuli, while activation reduced interaction and bout length with novel social stimuli via decreasing DA neurotransmission. These data indicate interest towards novel social stimuli is encoded by mesolimbic DA which is dynamically regulated by an IPN→LDTg circuit to control NP.

Suggested Citation

  • Susanna Molas & Timothy G. Freels & Rubing Zhao-Shea & Timothy Lee & Pablo Gimenez-Gomez & Melanie Barbini & Gilles E. Martin & Andrew R. Tapper, 2024. "Dopamine control of social novelty preference is constrained by an interpeduncular-tegmentum circuit," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47255-y
    DOI: 10.1038/s41467-024-47255-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47255-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47255-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Shuo Chen & Linmeng He & Arthur J. Y. Huang & Roman Boehringer & Vincent Robert & Marie E. Wintzer & Denis Polygalov & Adam Z. Weitemier & Yanqiu Tao & Mingxiao Gu & Steven J. Middleton & Kana Namiki , 2020. "A hypothalamic novelty signal modulates hippocampal memory," Nature, Nature, vol. 586(7828), pages 270-274, October.
    2. Christie D. Fowler & Qun Lu & Paul M. Johnson & Michael J. Marks & Paul J. Kenny, 2011. "Habenular α5 nicotinic receptor subunit signalling controls nicotine intake," Nature, Nature, vol. 471(7340), pages 597-601, March.
    3. Sebastiano Bariselli & Hanna Hörnberg & Clément Prévost-Solié & Stefano Musardo & Laetitia Hatstatt-Burklé & Peter Scheiffele & Camilla Bellone, 2018. "Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    4. Shannon L. Wolfman & Daniel F. Gill & Fili Bogdanic & Katie Long & Ream Al-Hasani & Jordan G. McCall & Michael R. Bruchas & Daniel S. McGehee, 2018. "Nicotine aversion is mediated by GABAergic interpeduncular nucleus inputs to laterodorsal tegmentum," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    5. Bárbara Coimbra & Carina Soares-Cunha & Nivaldo A P Vasconcelos & Ana Verónica Domingues & Sónia Borges & Nuno Sousa & Ana João Rodrigues, 2019. "Role of laterodorsal tegmentum projections to nucleus accumbens in reward-related behaviors," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    6. Xin Jin & Rui M. Costa, 2010. "Start/stop signals emerge in nigrostriatal circuits during sequence learning," Nature, Nature, vol. 466(7305), pages 457-462, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Clément Solié & Alessandro Contestabile & Pedro Espinosa & Stefano Musardo & Sebastiano Bariselli & Chieko Huber & Alan Carleton & Camilla Bellone, 2022. "Superior Colliculus to VTA pathway controls orienting response and influences social interaction in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Andrew C. Harris & John R. Smethells & Mary Palumbo & Maciej Goniewicz & Mark G. LeSage, 2020. "Comparison of the Relative Abuse Liability of Electronic Cigarette Aerosol Extracts and Nicotine Alone in Adolescent Rats: A Behavioral Economic Analysis," IJERPH, MDPI, vol. 17(3), pages 1-12, January.
    3. Hiroyuki Kawai & Youcef Bouchekioua & Naoya Nishitani & Kazuhei Niitani & Shoma Izumi & Hinako Morishita & Chihiro Andoh & Yuma Nagai & Masashi Koda & Masako Hagiwara & Koji Toda & Hisashi Shirakawa &, 2022. "Median raphe serotonergic neurons projecting to the interpeduncular nucleus control preference and aversion," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    4. Francesco Paolo Ulloa Severino & Oluwadamilola O. Lawal & Kristina Sakers & Shiyi Wang & Namsoo Kim & Alexander David Friedman & Sarah Anne Johnson & Chaichontat Sriworarat & Ryan H. Hughes & Scott H., 2023. "Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Nima Khalighinejad & Neil Garrett & Luke Priestley & Patricia Lockwood & Matthew F. S. Rushworth, 2021. "A habenula-insular circuit encodes the willingness to act," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Zengpeng Han & Nengsong Luo & Wenyu Ma & Xiaodong Liu & Yuxiang Cai & Jiaxin Kou & Jie Wang & Lei Li & Siqi Peng & Zihong Xu & Wen Zhang & Yuxiang Qiu & Yang Wu & Chaohui Ye & Kunzhang Lin & Fuqiang X, 2023. "AAV11 enables efficient retrograde targeting of projection neurons and enhances astrocyte-directed transduction," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Qingtao Sun & Jianping Zhang & Anan Li & Mei Yao & Guangcai Liu & Siqi Chen & Yue Luo & Zhi Wang & Hui Gong & Xiangning Li & Qingming Luo, 2022. "Acetylcholine deficiency disrupts extratelencephalic projection neurons in the prefrontal cortex in a mouse model of Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    8. Stefano Nardone & Roberto Luca & Antonino Zito & Nataliya Klymko & Dimitris Nicoloutsopoulos & Oren Amsalem & Cory Brannigan & Jon M. Resch & Christopher L. Jacobs & Deepti Pant & Molly Veregge & Hari, 2024. "A spatially-resolved transcriptional atlas of the murine dorsal pons at single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    9. Stefano Garofalo & Germana Cocozza & Alessandro Mormino & Giovanni Bernardini & Eleonora Russo & Donald Ielpo & Diego Andolina & Rossella Ventura & Katiuscia Martinello & Massimiliano Renzi & Sergio F, 2023. "Natural killer cells and innate lymphoid cells 1 tune anxiety-like behavior and memory in mice via interferon-γ and acetylcholine," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Ruy Gómez-Ocádiz & Massimiliano Trippa & Chun-Lei Zhang & Lorenzo Posani & Simona Cocco & Rémi Monasson & Christoph Schmidt-Hieber, 2022. "A synaptic signal for novelty processing in the hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Elise C. Cope & Samantha H. Wang & Renée C. Waters & Isha R. Gore & Betsy Vasquez & Blake J. Laham & Elizabeth Gould, 2023. "Activation of the CA2-ventral CA1 pathway reverses social discrimination dysfunction in Shank3B knockout mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47255-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.