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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
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