IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50717-y.html
   My bibliography  Save this article

Prefrontal neuronal dynamics in the absence of task execution

Author

Listed:
  • Shusen Pu

    (Vanderbilt University
    University of West Florida)

  • Wenhao Dang

    (Vanderbilt University)

  • Xue-Lian Qi

    (Wake Forest School of Medicine)

  • Christos Constantinidis

    (Vanderbilt University
    Vanderbilt University
    Vanderbilt University Medical Center)

Abstract

Prefrontal cortical activity represents stimuli in working memory tasks in a low-dimensional manifold that transforms over the course of a trial. Such transformations reflect specific cognitive operations, so that, for example, the rotation of stimulus representations is thought to reduce interference by distractor stimuli. Here we show that rotations occur in the low-dimensional activity space of prefrontal neurons in naïve male monkeys (Macaca mulatta), while passively viewing familiar stimuli. Moreover, some aspects of these rotations remain remarkably unchanged after training to perform working memory tasks. Significant training effects are still present in population dynamics, which further distinguish correct and error trials during task execution. Our results reveal automatic functions of prefrontal neural circuits allow transformations that may aid cognitive flexibility.

Suggested Citation

  • Shusen Pu & Wenhao Dang & Xue-Lian Qi & Christos Constantinidis, 2024. "Prefrontal neuronal dynamics in the absence of task execution," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50717-y
    DOI: 10.1038/s41467-024-50717-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50717-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50717-y?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. Mitchell R. Riley & Xue-Lian Qi & Xin Zhou & Christos Constantinidis, 2018. "Anterior-posterior gradient of plasticity in primate prefrontal cortex," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    2. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    3. Matthew F. Panichello & Timothy J. Buschman, 2021. "Shared mechanisms underlie the control of working memory and attention," Nature, Nature, vol. 592(7855), pages 601-605, April.
    4. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    5. Gregor Rainer & Wael F. Asaad & Earl K. Miller, 1998. "Selective representation of relevant information by neurons in the primate prefrontal cortex," Nature, Nature, vol. 393(6685), pages 577-579, June.
    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. Atsushi Kikumoto & Apoorva Bhandari & Kazuhisa Shibata & David Badre, 2024. "A transient high-dimensional geometry affords stable conjunctive subspaces for efficient action selection," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. 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.
    4. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Mikael Lundqvist & Scott L. Brincat & Jonas Rose & Melissa R. Warden & Timothy J. Buschman & Earl K. Miller & Pawel Herman, 2023. "Working memory control dynamics follow principles of spatial computing," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    9. Kiyohito Iigaya & Sanghyun Yi & Iman A. Wahle & Sandy Tanwisuth & Logan Cross & John P. O’Doherty, 2023. "Neural mechanisms underlying the hierarchical construction of perceived aesthetic value," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    10. Takuya Ito & Guangyu Robert Yang & Patryk Laurent & Douglas H. Schultz & Michael W. Cole, 2022. "Constructing neural network models from brain data reveals representational transformations linked to adaptive behavior," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    11. 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.
    12. Daniel Durstewitz, 2017. "A state space approach for piecewise-linear recurrent neural networks for identifying computational dynamics from neural measurements," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-33, June.
    13. Kaushik J. Lakshminarasimhan & Eric Avila & Xaq Pitkow & Dora E. Angelaki, 2023. "Dynamical latent state computation in the male macaque posterior parietal cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    14. J. L. Amengual & F. Di Bello & S. Ben Hadj Hassen & Suliann Ben Hamed, 2022. "Distractibility and impulsivity neural states are distinct from selective attention and modulate the implementation of spatial attention," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Laura E. Suárez & Agoston Mihalik & Filip Milisav & Kenji Marshall & Mingze Li & Petra E. Vértes & Guillaume Lajoie & Bratislav Misic, 2024. "Connectome-based reservoir computing with the conn2res toolbox," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    16. Arno Onken & Jue Xie & Stefano Panzeri & Camillo Padoa-Schioppa, 2019. "Categorical encoding of decision variables in orbitofrontal cortex," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-27, October.
    17. Qianli Yang & Edgar Walker & R. James Cotton & Andreas S. Tolias & Xaq Pitkow, 2021. "Revealing nonlinear neural decoding by analyzing choices," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    18. Márton Albert Hajnal & Duy Tran & Zsombor Szabó & Andrea Albert & Karen Safaryan & Michael Einstein & Mauricio Vallejo Martelo & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2024. "Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex in mice during decision making," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    19. Gabriele Di Antonio & Sofia Raglio & Maurizio Mattia, 2024. "A geometrical solution underlies general neural principle for serial ordering," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    20. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, 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_s41467-024-50717-y. 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.