IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31072-2.html
   My bibliography  Save this article

Brain-wide reconstruction of inhibitory circuits after traumatic brain injury

Author

Listed:
  • Jan C. Frankowski

    (University of California)

  • Alexa Tierno

    (University of California)

  • Shreya Pavani

    (University of California)

  • Quincy Cao

    (University of California)

  • David C. Lyon

    (University of California)

  • Robert F. Hunt

    (University of California
    University of California
    University of California
    University of California, Irvine)

Abstract

Despite the fundamental importance of understanding the brain’s wiring diagram, our knowledge of how neuronal connectivity is rewired by traumatic brain injury remains remarkably incomplete. Here we use cellular resolution whole-brain imaging to generate brain-wide maps of the input to inhibitory neurons in a mouse model of traumatic brain injury. We find that somatostatin interneurons are converted into hyperconnected hubs in multiple brain regions, with rich local network connections but diminished long-range inputs, even at areas not directly damaged. The loss of long-range input does not correlate with cell loss in distant brain regions. Interneurons transplanted into the injury site receive orthotopic local and long-range input, suggesting the machinery for establishing distant connections remains intact even after a severe injury. Our results uncover a potential strategy to sustain and optimize inhibition after traumatic brain injury that involves spatial reorganization of the direct inputs to inhibitory neurons across the brain.

Suggested Citation

  • Jan C. Frankowski & Alexa Tierno & Shreya Pavani & Quincy Cao & David C. Lyon & Robert F. Hunt, 2022. "Brain-wide reconstruction of inhibitory circuits after traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31072-2
    DOI: 10.1038/s41467-022-31072-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31072-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-31072-2?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. Matthew E. Larkum & J. Julius Zhu & Bert Sakmann, 1999. "A new cellular mechanism for coupling inputs arriving at different cortical layers," Nature, Nature, vol. 398(6725), pages 338-341, March.
    2. Bingyao Zhu & Jisu Eom & Robert F. Hunt, 2019. "Transplanted interneurons improve memory precision after traumatic brain injury," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Jonas Doerr & Martin Karl Schwarz & Dirk Wiedermann & Anke Leinhaas & Alina Jakobs & Florian Schloen & Inna Schwarz & Michael Diedenhofen & Nils Christian Braun & Philipp Koch & Daniel A. Peterson & U, 2017. "Whole-brain 3D mapping of human neural transplant innervation," Nature Communications, Nature, vol. 8(1), pages 1-7, April.
    4. Christian J. Niedworok & Alexander P. Y. Brown & M. Jorge Cardoso & Pavel Osten & Sebastien Ourselin & Marc Modat & Troy W. Margrie, 2016. "aMAP is a validated pipeline for registration and segmentation of high-resolution mouse brain data," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
    5. XiaoTing Zheng & Kirstie J. Salinas & Dario X. Figueroa Velez & Taylor Nakayama & Xiaoxiao Lin & Dhruba Banerjee & Xiangmin Xu & Sunil P. Gandhi, 2021. "Host interneurons mediate plasticity reactivated by embryonic inhibitory cell transplantation in mouse visual cortex," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Matt Udakis & Victor Pedrosa & Sophie E. L. Chamberlain & Claudia Clopath & Jack R. Mellor, 2020. "Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    7. Adam L Tyson & Charly V Rousseau & Christian J Niedworok & Sepiedeh Keshavarzi & Chryssanthi Tsitoura & Lee Cossell & Molly Strom & Troy W Margrie, 2021. "A deep learning algorithm for 3D cell detection in whole mouse brain image datasets," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-17, May.
    8. Carmen Vivar & Michelle C. Potter & Jiwon Choi & Ji-young Lee & Thomas P. Stringer & Edward M. Callaway & Fred H. Gage & Hoonkyo Suh & Henriette van Praag, 2012. "Monosynaptic inputs to new neurons in the dentate gyrus," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
    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. Simon Weiler & Vahid Rahmati & Marcel Isstas & Johann Wutke & Andreas Walter Stark & Christian Franke & Jürgen Graf & Christian Geis & Otto W. Witte & Mark Hübener & Jürgen Bolz & Troy W. Margrie & Kn, 2024. "A primary sensory cortical interareal feedforward inhibitory circuit for tacto-visual integration," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    2. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    3. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Giulia Faini & Dimitrii Tanese & Clément Molinier & Cécile Telliez & Massilia Hamdani & Francois Blot & Christophe Tourain & Vincent Sars & Filippo Bene & Benoît C. Forget & Emiliano Ronzitti & Valent, 2023. "Ultrafast light targeting for high-throughput precise control of neuronal networks," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Arjun A. Bhaskaran & Théo Gauvrit & Yukti Vyas & Guillaume Bony & Melanie Ginger & Andreas Frick, 2023. "Endogenous noise of neocortical neurons correlates with atypical sensory response variability in the Fmr1−/y mouse model of autism," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Giuseppe Chindemi & Marwan Abdellah & Oren Amsalem & Ruth Benavides-Piccione & Vincent Delattre & Michael Doron & András Ecker & Aurélien T. Jaquier & James King & Pramod Kumbhar & Caitlin Monney & Ro, 2022. "A calcium-based plasticity model for predicting long-term potentiation and depression in the neocortex," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Liang Wang & Jingyi Du & Qilu Liu & Dongshuang Wang & Wenhan Wang & Ming Lei & Keyi Li & Yiwei Li & Aijun Hao & Yuanhua Sang & Fan Yi & Wenjuan Zhou & Hong Liu & Chuanbin Mao & Jichuan Qiu, 2024. "Wrapping stem cells with wireless electrical nanopatches for traumatic brain injury therapy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Adam L Tyson & Charly V Rousseau & Christian J Niedworok & Sepiedeh Keshavarzi & Chryssanthi Tsitoura & Lee Cossell & Molly Strom & Troy W Margrie, 2021. "A deep learning algorithm for 3D cell detection in whole mouse brain image datasets," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-17, May.
    9. Jingtan Zhu & Xiaomei Liu & Zhang Liu & Yating Deng & Jianyi Xu & Kunxing Liu & Ruiying Zhang & Xizhi Meng & Peng Fei & Tingting Yu & Dan Zhu, 2024. "SOLID: minimizing tissue distortion for brain-wide profiling of diverse architectures," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Dongsheng Xiao & Brandon J. Forys & Matthieu P. Vanni & Timothy H. Murphy, 2021. "MesoNet allows automated scaling and segmentation of mouse mesoscale cortical maps using machine learning," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    11. Shan Shen & Xiaolong Jiang & Federico Scala & Jiakun Fu & Paul Fahey & Dmitry Kobak & Zhenghuan Tan & Na Zhou & Jacob Reimer & Fabian Sinz & Andreas S. Tolias, 2022. "Distinct organization of two cortico-cortical feedback pathways," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Etay Hay & Sean Hill & Felix Schürmann & Henry Markram & Idan Segev, 2011. "Models of Neocortical Layer 5b Pyramidal Cells Capturing a Wide Range of Dendritic and Perisomatic Active Properties," PLOS Computational Biology, Public Library of Science, vol. 7(7), pages 1-18, July.
    13. Pierre Yger & Kenneth D Harris, 2013. "The Convallis Rule for Unsupervised Learning in Cortical Networks," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-16, October.
    14. 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.
    15. Matthias Griebel & Dennis Segebarth & Nikolai Stein & Nina Schukraft & Philip Tovote & Robert Blum & Christoph M. Flath, 2023. "Deep learning-enabled segmentation of ambiguous bioimages with deepflash2," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Harman Ghuman & Kyungsoo Kim & Sapeeda Barati & Karunesh Ganguly, 2023. "Emergence of task-related spatiotemporal population dynamics in transplanted neurons," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Li, Xuening & Xie, Ying & Ye, Zhiqiu & Huang, Weifang & Yang, Lijian & Zhan, Xuan & Jia, Ya, 2024. "Chimera-like state in the bistable excitatory-inhibitory cortical neuronal network," Chaos, Solitons & Fractals, Elsevier, vol. 180(C).
    18. Brandon R. Munn & Eli J. Müller & Vicente Medel & Sharon L. Naismith & Joseph T. Lizier & Robert D. Sanders & James M. Shine, 2023. "Neuronal connected burst cascades bridge macroscale adaptive signatures across arousal states," Nature Communications, Nature, vol. 14(1), pages 1-17, 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_s41467-022-31072-2. 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.