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A persistent prefrontal reference frame across time and task rules

Author

Listed:
  • Hannah Muysers

    (Albert-Ludwigs-University Freiburg
    Albert-Ludwigs-University Freiburg)

  • Hung-Ling Chen

    (Albert-Ludwigs-University Freiburg)

  • Johannes Hahn

    (Goethe University Frankfurt)

  • Shani Folschweiller

    (Albert-Ludwigs-University Freiburg
    Albert-Ludwigs-University Freiburg
    Inselspital, Bern University Hospital, University of Bern)

  • Torfi Sigurdsson

    (Goethe University Frankfurt)

  • Jonas-Frederic Sauer

    (Albert-Ludwigs-University Freiburg)

  • Marlene Bartos

    (Albert-Ludwigs-University Freiburg)

Abstract

Behavior can be remarkably consistent, even over extended time periods, yet whether this is reflected in stable or ‘drifting’ neuronal responses to task features remains controversial. Here, we find a persistently active ensemble of neurons in the medial prefrontal cortex (mPFC) of mice that reliably maintains trajectory-specific tuning over several weeks while performing an olfaction-guided spatial memory task. This task-specific reference frame is stabilized during learning, upon which repeatedly active neurons show little representational drift and maintain their trajectory-specific tuning across long pauses in task exposure and across repeated changes in cue-target location pairings. These data thus suggest a ‘core ensemble’ of prefrontal neurons forming a reference frame of task-relevant space for the performance of consistent behavior over extended periods of time.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46350-4
    DOI: 10.1038/s41467-024-46350-4
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    References listed on IDEAS

    as
    1. Hugo Malagon-Vina & Stephane Ciocchi & Johannes Passecker & Georg Dorffner & Thomas Klausberger, 2018. "Fluid network dynamics in the prefrontal cortex during multiple strategy switching," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Tyler D. Marks & Michael J. Goard, 2021. "Author Correction: Stimulus-dependent representational drift in primary visual cortex," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    3. 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.
    4. Hiroshi T. Ito & Sheng-Jia Zhang & Menno P. Witter & Edvard I. Moser & May-Britt Moser, 2015. "A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation," Nature, Nature, vol. 522(7554), pages 50-55, June.
    5. Timothy Spellman & Mattia Rigotti & Susanne E. Ahmari & Stefano Fusi & Joseph A. Gogos & Joshua A. Gordon, 2015. "Hippocampal–prefrontal input supports spatial encoding in working memory," Nature, Nature, vol. 522(7556), pages 309-314, June.
    6. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    7. Jung Won Bae & Huijeong Jeong & Young Ju Yoon & Chan Mee Bae & Hyeonsu Lee & Se-Bum Paik & Min Whan Jung, 2021. "Parallel processing of working memory and temporal information by distinct types of cortical projection neurons," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    8. Thomas Hainmueller & Marlene Bartos, 2018. "Parallel emergence of stable and dynamic memory engrams in the hippocampus," Nature, Nature, vol. 558(7709), pages 292-296, June.
    9. Tyler D. Marks & Michael J. Goard, 2021. "Stimulus-dependent representational drift in primary visual cortex," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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