IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43081-w.html
   My bibliography  Save this article

Emergence of task-related spatiotemporal population dynamics in transplanted neurons

Author

Listed:
  • Harman Ghuman

    (University of California, San Francisco)

  • Kyungsoo Kim

    (University of California, San Francisco)

  • Sapeeda Barati

    (University of California, San Francisco)

  • Karunesh Ganguly

    (University of California, San Francisco
    San Francisco Veterans Affairs Medical Center)

Abstract

Loss of nervous system tissue after severe brain injury is a main determinant of poor functional recovery. Cell transplantation is a promising method to restore lost tissue and function, yet it remains unclear if transplanted neurons can demonstrate the population level dynamics important for movement control. Here we present a comprehensive approach for long-term single neuron monitoring and manipulation of transplanted embryonic cortical neurons after cortical injury in adult male mice performing a prehension task. The observed patterns of population activity in the transplanted network strongly resembled that of healthy networks. Specifically, the task-related spatiotemporal activity patterns of transplanted neurons could be represented by latent factors that evolve within a low dimensional manifold. We also demonstrate reliable modulation of the transplanted networks using minimally invasive epidural stimulation. Our approach may allow greater insight into how restoration of cell-type specific network dynamics in vivo can restore motor function.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43081-w
    DOI: 10.1038/s41467-023-43081-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43081-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43081-w?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. Anli Liu & Mihály Vöröslakos & Greg Kronberg & Simon Henin & Matthew R. Krause & Yu Huang & Alexander Opitz & Ashesh Mehta & Christopher C. Pack & Bart Krekelberg & Antal Berényi & Lucas C. Parra & Lu, 2018. "Immediate neurophysiological effects of transcranial electrical stimulation," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    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. Peter Carmeliet & Rakesh K. Jain, 2000. "Angiogenesis in cancer and other diseases," Nature, Nature, vol. 407(6801), pages 249-257, September.
    4. Henrik Lindén & Peter C. Petersen & Mikkel Vestergaard & Rune W. Berg, 2022. "Movement is governed by rotational neural dynamics in spinal motor networks," Nature, Nature, vol. 610(7932), pages 526-531, October.
    5. Andrew J. Peters & Simon X. Chen & Takaki Komiyama, 2014. "Emergence of reproducible spatiotemporal activity during motor learning," Nature, Nature, vol. 510(7504), pages 263-267, June.
    6. Madeline A. Lancaster & Magdalena Renner & Carol-Anne Martin & Daniel Wenzel & Louise S. Bicknell & Matthew E. Hurles & Tessa Homfray & Josef M. Penninger & Andrew P. Jackson & Juergen A. Knoblich, 2013. "Cerebral organoids model human brain development and microcephaly," Nature, Nature, vol. 501(7467), pages 373-379, September.
    7. Mark M. Churchland & John P. Cunningham & Matthew T. Kaufman & Justin D. Foster & Paul Nuyujukian & Stephen I. Ryu & Krishna V. Shenoy, 2012. "Neural population dynamics during reaching," Nature, Nature, vol. 487(7405), pages 51-56, July.
    8. Omer Revah & Felicity Gore & Kevin W. Kelley & Jimena Andersen & Noriaki Sakai & Xiaoyu Chen & Min-Yin Li & Fikri Birey & Xiao Yang & Nay L. Saw & Samuel W. Baker & Neal D. Amin & Shravanti Kulkarni &, 2022. "Maturation and circuit integration of transplanted human cortical organoids," Nature, Nature, vol. 610(7931), pages 319-326, October.
    9. Susanne Falkner & Sofia Grade & Leda Dimou & Karl-Klaus Conzelmann & Tobias Bonhoeffer & Magdalena Götz & Mark Hübener, 2016. "Transplanted embryonic neurons integrate into adult neocortical circuits," Nature, Nature, vol. 539(7628), pages 248-253, November.
    10. Madison N. Wilson & Martin Thunemann & Xin Liu & Yichen Lu & Francesca Puppo & Jason W. Adams & Jeong-Hoon Kim & Mehrdad Ramezani & Donald P. Pizzo & Srdjan Djurovic & Ole A. Andreassen & Abed AlFatah, 2022. "Multimodal monitoring of human cortical organoids implanted in mice reveal functional connection with visual cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Britton A. Sauerbrei & Jian-Zhong Guo & Jeremy D. Cohen & Matteo Mischiati & Wendy Guo & Mayank Kabra & Nakul Verma & Brett Mensh & Kristin Branson & Adam W. Hantman, 2020. "Cortical pattern generation during dexterous movement is input-driven," Nature, Nature, vol. 577(7790), pages 386-391, 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. Leslie J. Sibener & Alice C. Mosberger & Tiffany X. Chen & Vivek R. Athalye & James M. Murray & Rui M. Costa, 2025. "Dissociable roles of distinct thalamic circuits in learning reaches to spatial targets," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    2. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Sanaya N. Shroff & Eric Lowet & Sudiksha Sridhar & Howard J. Gritton & Mohammed Abumuaileq & Hua-An Tseng & Cyrus Cheung & Samuel L. Zhou & Krishnakanth Kondabolu & Xue Han, 2023. "Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. 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.
    5. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Honghui Zheng & Yilin Feng & Jiyuan Tang & Feifei Yu & Zitian Wang & Jiani Xu & Cheng Hai & Mingyue Jiang & Yifan Cheng & Zhicheng Shao & Ning Ma & Peter E. Lobie & Shaohua Ma, 2025. "Astrocyte-secreted cues promote neural maturation and augment activity in human forebrain organoids," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    7. Cong Zheng & Qifan Wang & He Cui, 2025. "Continuous sensorimotor transformation enhances robustness of neural dynamics to perturbation in macaque motor cortex," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    8. Naohiko Okabe & Xiaofei Wei & Farah Abumeri & Jonathan Batac & Mary Hovanesyan & Weiye Dai & Srbui Azarapetian & Jesus Campagna & Nadia Pilati & Agostino Marasco & Giuseppe Alvaro & Martin J. Gunthorp, 2025. "Parvalbumin interneurons regulate rehabilitation-induced functional recovery after stroke and identify a rehabilitation drug," Nature Communications, Nature, vol. 16(1), pages 1-25, December.
    9. Nan Hu & Jian-Xin Shi & Chong Chen & Hai-Huan Xu & Zhe-Han Chang & Peng-Fei Hu & Di Guo & Xiao-Wang Zhang & Wen-Wei Shao & Xiu Fan & Jia-Chen Zuo & Dong Ming & Xiao-Hong Li, 2024. "Constructing organoid-brain-computer interfaces for neurofunctional repair after brain injury," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Bin Wu & Haixiang Wu & Xiaoyan Liu & Houwen Lin & Jin Li, 2014. "Ranibizumab versus Bevacizumab for Ophthalmic Diseases Related to Neovascularisation: A Meta-Analysis of Randomised Controlled Trials," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-8, July.
    11. Aviv Segev & Sukhwan Jung, 2023. "Common knowledge processing patterns in networks of different systems," PLOS ONE, Public Library of Science, vol. 18(10), pages 1-18, October.
    12. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    13. Jonathan M Werner & Jesse Gillis, 2024. "Meta-analysis of single-cell RNA sequencing co-expression in human neural organoids reveals their high variability in recapitulating primary tissue," PLOS Biology, Public Library of Science, vol. 22(12), pages 1-34, December.
    14. 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.
    15. Shan Yu & Andreas Klaus & Hongdian Yang & Dietmar Plenz, 2014. "Scale-Invariant Neuronal Avalanche Dynamics and the Cut-Off in Size Distributions," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-12, June.
    16. repec:plo:pone00:0075954 is not listed on IDEAS
    17. Ian S Howard & David W Franklin, 2015. "Neural Tuning Functions Underlie Both Generalization and Interference," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-21, June.
    18. Laura Empl & Alexandra Chovsepian & Maryam Chahin & Wing Yin Vanessa Kan & Julie Fourneau & Valérie Steenbergen & Sanofer Weidinger & Maite Marcantoni & Alexander Ghanem & Peter Bradley & Karl Klaus C, 2022. "Selective plasticity of callosal neurons in the adult contralesional cortex following murine traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. Elizabeth A. Werren & Geneva R. LaForce & Anshika Srivastava & Delia R. Perillo & Shaokun Li & Katherine Johnson & Safa Baris & Brandon Berger & Samantha L. Regan & Christian D. Pfennig & Sonja Munnik, 2024. "TREX tetramer disruption alters RNA processing necessary for corticogenesis in THOC6 Intellectual Disability Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    20. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    21. Adrian M Haith & David M Huberdeau & John W Krakauer, 2015. "Hedging Your Bets: Intermediate Movements as Optimal Behavior in the Context of an Incomplete Decision," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-21, March.

    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_s41467-023-43081-w. 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.