IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49226-9.html
   My bibliography  Save this article

Months-long tracking of neuronal ensembles spanning multiple brain areas with Ultra-Flexible Tentacle Electrodes

Author

Listed:
  • Tansel Baran Yasar

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Peter Gombkoto

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Alexei L. Vyssotski

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Angeliki D. Vavladeli

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Christopher M. Lewis

    (University of Zurich & ETH Zurich
    University of Zurich)

  • Bifeng Wu

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Linus Meienberg

    (ETH Zurich & University of Zurich)

  • Valter Lundegardh

    (ETH Zurich & University of Zurich)

  • Fritjof Helmchen

    (University of Zurich & ETH Zurich
    University of Zurich
    University of Zurich)

  • Wolfger von der Behrens

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

  • Mehmet Fatih Yanik

    (ETH Zurich & University of Zurich
    University of Zurich & ETH Zurich)

Abstract

We introduce Ultra-Flexible Tentacle Electrodes (UFTEs), packing many independent fibers with the smallest possible footprint without limitation in recording depth using a combination of mechanical and chemical tethering for insertion. We demonstrate a scheme to implant UFTEs simultaneously into many brain areas at arbitrary locations without angle-of-insertion limitations, and a 512-channel wireless logger. Immunostaining reveals no detectable chronic tissue damage even after several months. Mean spike signal-to-noise ratios are 1.5-3x compared to the state-of-the-art, while the highest signal-to-noise ratios reach 89, and average cortical unit yields are ~1.75/channel. UFTEs can track the same neurons across sessions for at least 10 months (longest duration tested). We tracked inter- and intra-areal neuronal ensembles (neurons repeatedly co-activated within 25 ms) simultaneously from hippocampus, retrosplenial cortex, and medial prefrontal cortex in freely moving rodents. Average ensemble lifetimes were shorter than the durations over which we can track individual neurons. We identify two distinct classes of ensembles. Those tuned to sharp-wave ripples display the shortest lifetimes, and the ensemble members are mostly hippocampal. Yet, inter-areal ensembles with members from both hippocampus and cortex have weak tuning to sharp wave ripples, and some have unusual months-long lifetimes. Such inter-areal ensembles occasionally remain inactive for weeks before re-emerging.

Suggested Citation

  • Tansel Baran Yasar & Peter Gombkoto & Alexei L. Vyssotski & Angeliki D. Vavladeli & Christopher M. Lewis & Bifeng Wu & Linus Meienberg & Valter Lundegardh & Fritjof Helmchen & Wolfger von der Behrens , 2024. "Months-long tracking of neuronal ensembles spanning multiple brain areas with Ultra-Flexible Tentacle Electrodes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49226-9
    DOI: 10.1038/s41467-024-49226-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49226-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49226-9?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. Carl E. Schoonover & Sarah N. Ohashi & Richard Axel & Andrew J. P. Fink, 2021. "Representational drift in primary olfactory cortex," Nature, Nature, vol. 594(7864), pages 541-546, June.
    2. Mostafa Ghannad-Rezaie & Peter M. Eimon & Yuelong Wu & Mehmet Fatih Yanik, 2019. "Engineering brain activity patterns by neuromodulator polytherapy for treatment of disorders," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Patrick Jendritza & Frederike J. Klein & Pascal Fries, 2023. "Multi-area recordings and optogenetics in the awake, behaving marmoset," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Azahara Oliva & Antonio Fernández-Ruiz & Felix Leroy & Steven A. Siegelbaum, 2020. "Hippocampal CA2 sharp-wave ripples reactivate and promote social memory," Nature, Nature, vol. 587(7833), pages 264-269, November.
    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. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Han Chin Wang & Amy M. LeMessurier & Daniel E. Feldman, 2022. "Tuning instability of non-columnar neurons in the salt-and-pepper whisker map in somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Myung Chung & Katsutoshi Imanaka & Ziyan Huang & Akiyuki Watarai & Mu-Yun Wang & Kentaro Tao & Hirotaka Ejima & Tomomi Aida & Guoping Feng & Teruhiro Okuyama, 2024. "Conditional knockout of Shank3 in the ventral CA1 by quantitative in vivo genome-editing impairs social memory in mice," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. P. Dylan Rich & Stephan Yves Thiberge & Benjamin B. Scott & Caiying Guo & D. Gowanlock R. Tervo & Carlos D. Brody & Alla Y. Karpova & Nathaniel D. Daw & David W. Tank, 2024. "Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Ravi Pancholi & Lauren Ryan & Simon Peron, 2023. "Learning in a sensory cortical microstimulation task is associated with elevated representational stability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Noel Federman & Sebastián A. Romano & Macarena Amigo-Duran & Lucca Salomon & Antonia Marin-Burgin, 2024. "Acquisition of non-olfactory encoding improves odour discrimination in olfactory cortex," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    10. Eunji Kong & Kyu-Hee Lee & Jongrok Do & Pilhan Kim & Doyun Lee, 2023. "Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. Alexandra T. Keinath & Coralie-Anne Mosser & Mark P. Brandon, 2022. "The representation of context in mouse hippocampus is preserved despite neural drift," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    12. Hefei Guan & Steven J. Middleton & Takafumi Inoue & Thomas J. McHugh, 2021. "Lateralization of CA1 assemblies in the absence of CA3 input," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    13. Geoffrey Terral & Evan Harrell & Gabriel Lepousez & Yohan Wards & Dinghuang Huang & Tiphaine Dolique & Giulio Casali & Antoine Nissant & Pierre-Marie Lledo & Guillaume Ferreira & Giovanni Marsicano & , 2024. "Endogenous cannabinoids in the piriform cortex tune olfactory perception," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Elise C. Cope & Samantha H. Wang & Renée C. Waters & Isha R. Gore & Betsy Vasquez & Blake J. Laham & Elizabeth Gould, 2023. "Activation of the CA2-ventral CA1 pathway reverses social discrimination dysfunction in Shank3B knockout mice," Nature Communications, Nature, vol. 14(1), pages 1-16, 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:15:y:2024:i:1:d:10.1038_s41467-024-49226-9. 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.