IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48489-6.html
   My bibliography  Save this article

Optogenetic activation of dorsal raphe serotonin neurons induces brain-wide activation

Author

Listed:
  • Hiro Taiyo Hamada

    (Okinawa Institute of Science and Technology Graduate University
    Araya Inc)

  • Yoshifumi Abe

    (Keio University School of Medicine)

  • Norio Takata

    (Keio University School of Medicine)

  • Masakazu Taira

    (Okinawa Institute of Science and Technology Graduate University)

  • Kenji F. Tanaka

    (Keio University School of Medicine)

  • Kenji Doya

    (Okinawa Institute of Science and Technology Graduate University)

Abstract

Serotonin is a neuromodulator that affects multiple behavioral and cognitive functions. Nonetheless, how serotonin causes such a variety of effects via brain-wide projections and various receptors remains unclear. Here we measured brain-wide responses to optogenetic stimulation of serotonin neurons in the dorsal raphe nucleus (DRN) of the male mouse brain using functional MRI with an 11.7 T scanner and a cryoprobe. Transient activation of DRN serotonin neurons caused brain-wide activation, including the medial prefrontal cortex, the striatum, and the ventral tegmental area. The same stimulation under anesthesia with isoflurane decreased brain-wide activation, including the hippocampal complex. These brain-wide response patterns can be explained by DRN serotonergic projection topography and serotonin receptor expression profiles, with enhanced weights on 5-HT1 receptors. Together, these results provide insight into the DR serotonergic system, which is consistent with recent discoveries of its functions in adaptive behaviors.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48489-6
    DOI: 10.1038/s41467-024-48489-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48489-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48489-6?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. Jacqueline Scholl & Nils Kolling & Natalie Nelissen & Michael Browning & Matthew F S Rushworth & Catherine J Harmer, 2017. "Beyond negative valence: 2-week administration of a serotonergic antidepressant enhances both reward and effort learning signals," PLOS Biology, Public Library of Science, vol. 15(2), pages 1-30, February.
    2. Eran Lottem & Dhruba Banerjee & Pietro Vertechi & Dario Sarra & Matthijs oude Lohuis & Zachary F. Mainen, 2018. "Activation of serotonin neurons promotes active persistence in a probabilistic foraging task," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Kiyohito Iigaya & Madalena S. Fonseca & Masayoshi Murakami & Zachary F. Mainen & Peter Dayan, 2018. "An effect of serotonergic stimulation on learning rates for rewards apparent after long intertrial intervals," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    4. Yi Li & Weixin Zhong & Daqing Wang & Qiru Feng & Zhixiang Liu & Jingfeng Zhou & Chunying Jia & Fei Hu & Jiawei Zeng & Qingchun Guo & Ling Fu & Minmin Luo, 2016. "Serotonin neurons in the dorsal raphe nucleus encode reward signals," Nature Communications, Nature, vol. 7(1), pages 1-15, April.
    5. 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.
    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. Shuancheng Ren & Cai Zhang & Faguo Yue & Jinxiang Tang & Wei Zhang & Yue Zheng & Yuanyuan Fang & Na Wang & Zhenbo Song & Zehui Zhang & Xiaolong Zhang & Han Qin & Yaling Wang & Jianxia Xia & Chenggang , 2024. "A midbrain GABAergic circuit constrains wakefulness in a mouse model of stress," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Payam Piray & Nathaniel D Daw, 2020. "A simple model for learning in volatile environments," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-26, July.
    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. 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.
    5. Drew C. Schreiner & Christian Cazares & Rafael Renteria & Christina M. Gremel, 2022. "Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. 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.
    7. I. Hachen & S. Reinartz & R. Brasselet & A. Stroligo & M. E. Diamond, 2021. "Dynamics of history-dependent perceptual judgment," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    8. 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.
    9. Huanyuan Zhou & KongFatt Wong-Lin & Da-Hui Wang, 2018. "Parallel Excitatory and Inhibitory Neural Circuit Pathways Underlie Reward-Based Phasic Neural Responses," Complexity, Hindawi, vol. 2018, pages 1-20, April.
    10. Andrew Mah & Shannon S. Schiereck & Veronica Bossio & Christine M. Constantinople, 2023. "Distinct value computations support rapid sequential decisions," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Weiwei Guo & Sijia Fan & Dan Xiao & Hui Dong & Guangwei Xu & Zhikun Wan & Yuqian Ma & Zhen Wang & Tian Xue & Yifeng Zhou & Yulong Li & Wei Xiong, 2021. "A Brainstem reticulotegmental neural ensemble drives acoustic startle reflexes," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    12. 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.
    13. Weihua Ding & Liuyue Yang & Eleanor Shi & Bowon Kim & Sarah Low & Kun Hu & Lei Gao & Ping Chen & Wei Ding & David Borsook & Andrew Luo & Jee Hyun Choi & Changning Wang & Oluwaseun Akeju & Jun Yang & C, 2023. "The endocannabinoid N-arachidonoyl dopamine is critical for hyperalgesia induced by chronic sleep disruption," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. 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.
    15. Jing Huang & Weijun Huang & Junzhe Yi & Yiwen Deng & Ruijie Li & Jieying Chen & Jiahao Shi & Yuan Qiu & Tao Wang & Xiaoyong Chen & Xiaoran Zhang & Andy Peng Xiang, 2023. "Mesenchymal stromal cells alleviate depressive and anxiety-like behaviors via a lung vagal-to-brain axis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Milošević, Marija, 2022. "Stochastic serotonin model with discontinuous drift," Mathematics and Computers in Simulation (MATCOM), Elsevier, vol. 198(C), pages 359-374.
    17. Michael J. Colwell & Hosana Tagomori & Fei Shang & Hoi Iao Cheng & Chloe E. Wigg & Michael Browning & Philip J. Cowen & Susannah E. Murphy & Catherine J. Harmer, 2024. "Direct serotonin release in humans shapes aversive learning and inhibition," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Yan Zhang & Jiayi Shen & Famin Xie & Zhiwei Liu & Fangfang Yin & Mingxiu Cheng & Liang Wang & Meiting Cai & Herbert Herzog & Ping Wu & Zhi Zhang & Cheng Zhan & Tiemin Liu, 2024. "Feedforward inhibition of stress by brainstem neuropeptide Y neurons," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. Seth R. Batten & Dan Bang & Brian H. Kopell & Arianna N. Davis & Matthew Heflin & Qixiu Fu & Ofer Perl & Kimia Ziafat & Alice Hashemi & Ignacio Saez & Leonardo S. Barbosa & Thomas Twomey & Terry Lohre, 2024. "Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange," Nature Human Behaviour, Nature, vol. 8(4), pages 718-728, April.

    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_s41467-024-48489-6. 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.