IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36808-2.html
   My bibliography  Save this article

Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice

Author

Listed:
  • M. E. Flanigan

    (University of North Carolina School of Medicine)

  • O. J. Hon

    (University of North Carolina School of Medicine
    University of North Carolina School of Medicine)

  • S. D’Ambrosio

    (University of North Carolina School of Medicine)

  • K. M. Boyt

    (University of North Carolina School of Medicine)

  • L. Hassanein

    (University of North Carolina School of Medicine)

  • M. Castle

    (University of North Carolina School of Medicine)

  • H. L. Haun

    (University of North Carolina School of Medicine)

  • M. M. Pina

    (University of North Carolina School of Medicine)

  • T. L. Kash

    (University of North Carolina School of Medicine
    University of North Carolina School of Medicine)

Abstract

Binge alcohol consumption induces discrete social and arousal disturbances in human populations that promote increased drinking and accelerate the progression of Alcohol Use Disorder. Here, we show in a mouse model that binge alcohol consumption disrupts social recognition in females and potentiates sensorimotor arousal in males. These negative behavioral outcomes were associated with sex-specific adaptations in serotonergic signaling systems within the lateral habenula (LHb) and the bed nucleus of the stria terminalis (BNST), particularly those related to the receptor 5HT2c. While both BNST and LHb neurons expressing this receptor display potentiated activation following binge alcohol consumption, the primary causal mechanism underlying the effects of alcohol on social and arousal behaviors appears to be excessive activation of LHb5HT2c neurons. These findings may have valuable implications for the development of sex-specific treatments for mood and alcohol use disorders targeting the brain’s serotonin system.

Suggested Citation

  • M. E. Flanigan & O. J. Hon & S. D’Ambrosio & K. M. Boyt & L. Hassanein & M. Castle & H. L. Haun & M. M. Pina & T. L. Kash, 2023. "Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36808-2
    DOI: 10.1038/s41467-023-36808-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36808-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36808-2?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. Gül Dölen & Ayeh Darvishzadeh & Kee Wui Huang & Robert C. Malenka, 2013. "Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin," Nature, Nature, vol. 501(7466), pages 179-184, September.
    2. Catherine A. Marcinkiewcz & Christopher M. Mazzone & Giuseppe D’Agostino & Lindsay R. Halladay & J. Andrew Hardaway & Jeffrey F. DiBerto & Montserrat Navarro & Nathan Burnham & Claudia Cristiano & Cay, 2016. "Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala," Nature, Nature, vol. 537(7618), pages 97-101, September.
    3. Olivia B. Levine & Mary Jane Skelly & John D. Miller & Jean K. Rivera-Irizarry & Sydney A. Rowson & Jeffrey F. DiBerto & Jennifer A. Rinker & Todd E. Thiele & Thomas L. Kash & Kristen E. Pleil, 2021. "The paraventricular thalamus provides a polysynaptic brake on limbic CRF neurons to sex-dependently blunt binge alcohol drinking and avoidance behavior in mice," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    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. Andrea Bonassi & Ilaria Cataldo & Giulio Gabrieli & Moses Tandiono & Jia Nee Foo & Bruno Lepri & Gianluca Esposito, 2022. "The Interaction between Serotonin Transporter Allelic Variation and Maternal Care Modulates Instagram Sociability in a Sample of Singaporean Users," IJERPH, MDPI, vol. 19(9), pages 1-15, April.
    2. Yang Zhao & Chun-Xiao Huang & Yiming Gu & Yacong Zhao & Wenjie Ren & Yutong Wang & Jinjin Chen & Na N. Guan & Jianren Song, 2024. "Serotonergic modulation of vigilance states in zebrafish and mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Henry W. Kietzman & Gracy Trinoskey-Rice & Sarah A. Blumenthal & Jidong D. Guo & Shannon L. Gourley, 2022. "Social incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Hyosang Kim & Doyoun Kim & Yisul Cho & Kyungdeok Kim & Junyeop Daniel Roh & Yangsik Kim & Esther Yang & Seong Soon Kim & Sunjoo Ahn & Hyun Kim & Hyojin Kang & Yongchul Bae & Eunjoon Kim, 2022. "Early postnatal serotonin modulation prevents adult-stage deficits in Arid1b-deficient mice through synaptic transcriptional reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Masafumi Tsurutani & Teppei Goto & Mitsue Hagihara & Satsuki Irie & Kazunari Miyamichi, 2024. "Selective vulnerability of parvocellular oxytocin neurons in social dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Nihaad Paraouty & Justin D. Yao & Léo Varnet & Chi-Ning Chou & SueYeon Chung & Dan H. Sanes, 2023. "Sensory cortex plasticity supports auditory social learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Hiro Taiyo Hamada & Yoshifumi Abe & Norio Takata & Masakazu Taira & Kenji F. Tanaka & Kenji Doya, 2024. "Optogenetic activation of dorsal raphe serotonin neurons induces brain-wide activation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Ashim Gupta & Abdalla Bowirrat & Luis Llanos Gomez & David Baron & Igor Elman & John Giordano & Rehan Jalali & Rajendra D. Badgaiyan & Edward J. Modestino & Mark S. Gold & Eric R. Braverman & Anish Ba, 2022. "Hypothesizing in the Face of the Opioid Crisis Coupling Genetic Addiction Risk Severity (GARS) Testing with Electrotherapeutic Nonopioid Modalities Such as H-Wave Could Attenuate Both Pain and Hedonic," IJERPH, MDPI, vol. 19(1), pages 1-12, January.
    10. Jennifer Isaac & Sonia Corbett Karkare & Hymavathy Balasubramanian & Nicholas Schappaugh & Jarildy Larimar Javier & Maha Rashid & Malavika Murugan, 2024. "Sex differences in neural representations of social and nonsocial reward in the medial prefrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    11. Kansai Fukumitsu & Misato Kaneko & Teppo Maruyama & Chihiro Yoshihara & Arthur J. Huang & Thomas J. McHugh & Shigeyoshi Itohara & Minoru Tanaka & Kumi O. Kuroda, 2022. "Amylin-Calcitonin receptor signaling in the medial preoptic area mediates affiliative social behaviors in female mice," Nature Communications, Nature, vol. 13(1), pages 1-19, 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:14:y:2023:i:1:d:10.1038_s41467-023-36808-2. 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.