IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33843-3.html
   My bibliography  Save this article

Reward and aversion processing by input-defined parallel nucleus accumbens circuits in mice

Author

Listed:
  • Kuikui Zhou

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions
    University of Health and Rehabilitation Sciences)

  • Hua Xu

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions)

  • Shanshan Lu

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions
    University of Chinese Academy of Sciences)

  • Shaolei Jiang

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions
    University of Shanghai for Science and Technology)

  • Guoqiang Hou

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions)

  • Xiaofei Deng

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions)

  • Miao He

    (Fudan University)

  • Yingjie Zhu

    (Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

Abstract

The nucleus accumbens (NAc) is critical in mediating reward seeking and is also involved in negative emotion processing, but the cellular and circuitry mechanisms underlying such opposing behaviors remain elusive. Here, using the recently developed AAV1-mediated anterograde transsynaptic tagging technique in mice, we show that NAc neurons receiving basolateral amygdala inputs (NAcBLA) promote positive reinforcement via disinhibiting dopamine neurons in the ventral tegmental area (VTA). In contrast, NAc neurons receiving paraventricular thalamic inputs (NAcPVT) innervate GABAergic neurons in the lateral hypothalamus (LH) and mediate aversion. Silencing the synaptic output of NAcBLA neurons impairs reward seeking behavior, while silencing of NAcPVT or NAcPVT→LH pathway abolishes aversive symptoms of opiate withdrawal. Our results elucidate the afferent-specific circuit architecture of the NAc in controlling reward and aversion.

Suggested Citation

  • Kuikui Zhou & Hua Xu & Shanshan Lu & Shaolei Jiang & Guoqiang Hou & Xiaofei Deng & Miao He & Yingjie Zhu, 2022. "Reward and aversion processing by input-defined parallel nucleus accumbens circuits in mice," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33843-3
    DOI: 10.1038/s41467-022-33843-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33843-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33843-3?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. Yusuke Iino & Takeshi Sawada & Kenji Yamaguchi & Mio Tajiri & Shin Ishii & Haruo Kasai & Sho Yagishita, 2020. "Dopamine D2 receptors in discrimination learning and spine enlargement," Nature, Nature, vol. 579(7800), pages 555-560, March.
    2. Yingjie Zhu & Carl F. R. Wienecke & Gregory Nachtrab & Xiaoke Chen, 2016. "A thalamic input to the nucleus accumbens mediates opiate dependence," Nature, Nature, vol. 530(7589), pages 219-222, February.
    3. Garret D. Stuber & Dennis R. Sparta & Alice M. Stamatakis & Wieke A. van Leeuwen & Juanita E. Hardjoprajitno & Saemi Cho & Kay M. Tye & Kimberly A. Kempadoo & Feng Zhang & Karl Deisseroth & Antonello , 2011. "Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking," Nature, Nature, vol. 475(7356), pages 377-380, July.
    4. D. S. Engelke & X. O. Zhang & J. J. O’Malley & J. A. Fernandez-Leon & S. Li & G. J. Kirouac & M. Beierlein & F. H. Do-Monte, 2021. "A hypothalamic-thalamostriatal circuit that controls approach-avoidance conflict in rats," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Miao Li & Guang Yang, 2024. "A mesocortical glutamatergic pathway modulates neuropathic pain independent of dopamine co-release," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Xin-Yue Wang & Wen-Bin Jia & Xiang Xu & Rui Chen & Liang-Biao Wang & Xiao-Jing Su & Peng-Fei Xu & Xiao-Qing Liu & Jie Wen & Xiao-Yuan Song & Yuan-Yuan Liu & Zhi Zhang & Xin-Feng Liu & Yan Zhang, 2023. "A glutamatergic DRN–VTA pathway modulates neuropathic pain and comorbid anhedonia-like behavior in mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    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. Kelsey M. Vollmer & Lisa M. Green & Roger I. Grant & Kion T. Winston & Elizabeth M. Doncheck & Christopher W. Bowen & Jacqueline E. Paniccia & Rachel E. Clarke & Annika Tiller & Preston N. Siegler & B, 2022. "An opioid-gated thalamoaccumbal circuit for the suppression of reward seeking in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Tadaaki Nishioka & Suthinee Attachaipanich & Kosuke Hamaguchi & Michael Lazarus & Alban Kerchove d’Exaerde & Tom Macpherson & Takatoshi Hikida, 2023. "Error-related signaling in nucleus accumbens D2 receptor-expressing neurons guides inhibition-based choice behavior in mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Huiling Yu & Liping Chen & Huiyang Lei & Guilin Pi & Rui Xiong & Tao Jiang & Dongqin Wu & Fei Sun & Yang Gao & Yuanhao Li & Wenju Peng & Bingyu Huang & Guoda Song & Xin Wang & Jingru Lv & Zetao Jin & , 2022. "Infralimbic medial prefrontal cortex signalling to calbindin 1 positive neurons in posterior basolateral amygdala suppresses anxiety- and depression-like behaviours," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. 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.
    5. Koustav Roy & Xuzhao Zhou & Rintaro Otani & Ping-Chuan Yuan & Shuji Ioka & Kaspar E. Vogt & Tamae Kondo & Nouran H. T. Farag & Haruto Ijiri & Zhaofa Wu & Youhei Chitose & Mao Amezawa & David S. Uygun , 2024. "Optochemical control of slow-wave sleep in the nucleus accumbens of male mice by a photoactivatable allosteric modulator of adenosine A2A receptors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Marie A. Labouesse & Maria Wilhelm & Zacharoula Kagiampaki & Andrew G. Yee & Raphaelle Denis & Masaya Harada & Andrea Gresch & Alina-Măriuca Marinescu & Kanako Otomo & Sebastiano Curreli & Laia Serrat, 2024. "A chemogenetic approach for dopamine imaging with tunable sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    7. Jun Ma & John J. O’Malley & Malaz Kreiker & Yan Leng & Isbah Khan & Morgan Kindel & Mario A. Penzo, 2024. "Convergent direct and indirect cortical streams shape avoidance decisions in mice via the midline thalamus," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Yosuke Yawata & Yu Shikano & Jun Ogasawara & Kenichi Makino & Tetsuhiko Kashima & Keiko Ihara & Airi Yoshimoto & Shota Morikawa & Sho Yagishita & Kenji F. Tanaka & Yuji Ikegaya, 2023. "Mesolimbic dopamine release precedes actively sought aversive stimuli in mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. In Bum Lee & Eugene Lee & Na-Eun Han & Marko Slavuj & Jeong Wook Hwang & Ahrim Lee & Taeyoung Sun & Yehwan Jeong & Ja-Hyun Baik & Jae-Yong Park & Se-Young Choi & Jeehyun Kwag & Bong-June Yoon, 2024. "Persistent enhancement of basolateral amygdala-dorsomedial striatum synapses causes compulsive-like behaviors in mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Matthew T. Birnie & Annabel K. Short & Gregory B. Carvalho & Lara Taniguchi & Benjamin G. Gunn & Aidan L. Pham & Christy A. Itoga & Xiangmin Xu & Lulu Y. Chen & Stephen V. Mahler & Yuncai Chen & Talli, 2023. "Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    11. Lizhu Li & Lihui Lu & Yuqi Ren & Guo Tang & Yu Zhao & Xue Cai & Zhao Shi & He Ding & Changbo Liu & Dali Cheng & Yang Xie & Huachun Wang & Xin Fu & Lan Yin & Minmin Luo & Xing Sheng, 2022. "Colocalized, bidirectional optogenetic modulations in freely behaving mice with a wireless dual-color optoelectronic probe," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Yanjun Sun & Lisa M. Giocomo, 2022. "Neural circuit dynamics of drug-context associative learning in the mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Huan Sheng & Chao Lei & Yu Yuan & Yali Fu & Dongyang Cui & Li Yang & Da Shao & Zixuan Cao & Hao Yang & Xinli Guo & Chenshan Chu & Yaxian Wen & Zhangyin Cai & Ming Chen & Bin Lai & Ping Zheng, 2023. "Nucleus accumbens circuit disinhibits lateral hypothalamus glutamatergic neurons contributing to morphine withdrawal memory in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Charlie H. T. Kwok & Erika K. Harding & Nicole E. Burma & Tamara Markovic & Nicolas Massaly & Nynke J. van den Hoogen & Sierra Stokes-Heck & Eder Gambeta & Kristina Komarek & Hye Jean Yoon & Kathleen , 2024. "Pannexin-1 channel inhibition alleviates opioid withdrawal in rodents by modulating locus coeruleus to spinal cord circuitry," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Li Shen & Guang-Wei Zhang & Can Tao & Michelle B. Seo & Nicole K. Zhang & Junxiang J. Huang & Li I. Zhang & Huizhong W. Tao, 2022. "A bottom-up reward pathway mediated by somatostatin neurons in the medial septum complex underlying appetitive learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. Susanne Prokop & Péter Ábrányi-Balogh & Benjámin Barti & Márton Vámosi & Miklós Zöldi & László Barna & Gabriella M. Urbán & András Dávid Tóth & Barna Dudok & Attila Egyed & Hui Deng & Gian Marco Leggi, 2021. "PharmacoSTORM nanoscale pharmacology reveals cariprazine binding on Islands of Calleja granule cells," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    18. Oliver Barnstedt & Petra Mocellin & Stefan Remy, 2024. "A hippocampus-accumbens code guides goal-directed appetitive behavior," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    19. Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, 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:13:y:2022:i:1:d:10.1038_s41467-022-33843-3. 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.