IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52541-w.html
   My bibliography  Save this article

Maintenance and transformation of representational formats during working memory prioritization

Author

Listed:
  • Daniel Pacheco-Estefan

    (Ruhr University Bochum)

  • Marie-Christin Fellner

    (Ruhr University Bochum)

  • Lukas Kunz

    (University Hospital Bonn)

  • Hui Zhang

    (Ruhr University Bochum)

  • Peter Reinacher

    (University of Freiburg
    Fraunhofer Institute for Laser Technology)

  • Charlotte Roy

    (University of Freiburg)

  • Armin Brandt

    (University of Freiburg)

  • Andreas Schulze-Bonhage

    (University of Freiburg)

  • Linglin Yang

    (Zhejiang University)

  • Shuang Wang

    (Zhejiang University)

  • Jing Liu

    (The Hong Kong Polytechnic University)

  • Gui Xue

    (Beijing Normal University)

  • Nikolai Axmacher

    (Ruhr University Bochum
    Beijing Normal University)

Abstract

Visual working memory depends on both material-specific brain areas in the ventral visual stream (VVS) that support the maintenance of stimulus representations and on regions in the prefrontal cortex (PFC) that control these representations. How executive control prioritizes working memory contents and whether this affects their representational formats remains an open question, however. Here, we analyzed intracranial EEG (iEEG) recordings in epilepsy patients with electrodes in VVS and PFC who performed a multi-item working memory task involving a retro-cue. We employed Representational Similarity Analysis (RSA) with various Deep Neural Network (DNN) architectures to investigate the representational format of prioritized VWM content. While recurrent DNN representations matched PFC representations in the beta band (15–29 Hz) following the retro-cue, they corresponded to VVS representations in a lower frequency range (3–14 Hz) towards the end of the maintenance period. Our findings highlight the distinct coding schemes and representational formats of prioritized content in VVS and PFC.

Suggested Citation

  • Daniel Pacheco-Estefan & Marie-Christin Fellner & Lukas Kunz & Hui Zhang & Peter Reinacher & Charlotte Roy & Armin Brandt & Andreas Schulze-Bonhage & Linglin Yang & Shuang Wang & Jing Liu & Gui Xue & , 2024. "Maintenance and transformation of representational formats during working memory prioritization," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52541-w
    DOI: 10.1038/s41467-024-52541-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52541-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-52541-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. Edward K. Vogel & Maro G. Machizawa, 2004. "Neural activity predicts individual differences in visual working memory capacity," Nature, Nature, vol. 428(6984), pages 748-751, April.
    2. Jonathan D. Wallis & Kathleen C. Anderson & Earl K. Miller, 2001. "Single neurons in prefrontal cortex encode abstract rules," Nature, Nature, vol. 411(6840), pages 953-956, June.
    3. Johannes Mehrer & Courtney J. Spoerer & Nikolaus Kriegeskorte & Tim C. Kietzmann, 2020. "Individual differences among deep neural network models," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    4. Greta Tuckute & Aalok Sathe & Shashank Srikant & Maya Taliaferro & Mingye Wang & Martin Schrimpf & Kendrick Kay & Evelina Fedorenko, 2024. "Driving and suppressing the human language network using large language models," Nature Human Behaviour, Nature, vol. 8(3), pages 544-561, March.
    5. 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.
    6. Sanne Ten Oever & Alexander T. Sack & Carina R. Oehrn & Nikolai Axmacher, 2021. "An engram of intentionally forgotten information," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    7. Mikael Lundqvist & Pawel Herman & Melissa R. Warden & Scott L. Brincat & Earl K. Miller, 2018. "Gamma and beta bursts during working memory readout suggest roles in its volitional control," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    8. 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.
    9. D. Pacheco Estefan & M. Sánchez-Fibla & A. Duff & A. Principe & R. Rocamora & H. Zhang & N. Axmacher & P. F. M. J. Verschure, 2019. "Coordinated representational reinstatement in the human hippocampus and lateral temporal cortex during episodic memory retrieval," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    10. Seungdae Baek & Min Song & Jaeson Jang & Gwangsu Kim & Se-Bum Paik, 2021. "Face detection in untrained deep neural networks," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    11. Zachariah M. Reagh & Charan Ranganath, 2023. "Flexible reuse of cortico-hippocampal representations during encoding and recall of naturalistic events," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Pinglei Bao & Liang She & Mason McGill & Doris Y. Tsao, 2020. "A map of object space in primate inferotemporal cortex," Nature, Nature, vol. 583(7814), pages 103-108, July.
    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. 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.
    2. 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.
    3. 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.
    4. Huixin Tan & Xiaoyu Zeng & Jun Ni & Kun Liang & Cuiping Xu & Yanyang Zhang & Jiaxin Wang & Zizhou Li & Jiaxin Yang & Chunlei Han & Yuan Gao & Xinguang Yu & Shihui Han & Fangang Meng & Yina Ma, 2024. "Intracranial EEG signals disentangle multi-areal neural dynamics of vicarious pain perception," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. 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.
    7. 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.
    8. Vasiliki Bougou & Michaël Vanhoyland & Alexander Bertrand & Wim Paesschen & Hans Op De Beeck & Peter Janssen & Tom Theys, 2024. "Neuronal tuning and population representations of shape and category in human visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Georgia Koppe & Hazem Toutounji & Peter Kirsch & Stefanie Lis & Daniel Durstewitz, 2019. "Identifying nonlinear dynamical systems via generative recurrent neural networks with applications to fMRI," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-35, August.
    11. Mark R. Saddler & Ray Gonzalez & Josh H. McDermott, 2021. "Deep neural network models reveal interplay of peripheral coding and stimulus statistics in pitch perception," Nature Communications, Nature, vol. 12(1), pages 1-25, December.
    12. Florian Raudies & Eric A Zilli & Michael E Hasselmo, 2014. "Deep Belief Networks Learn Context Dependent Behavior," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-9, March.
    13. 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.
    14. 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.
    15. Rishi Rajalingham & Aída Piccato & Mehrdad Jazayeri, 2022. "Recurrent neural networks with explicit representation of dynamic latent variables can mimic behavioral patterns in a physical inference task," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Sanne Ten Oever & Alexander T. Sack & Carina R. Oehrn & Nikolai Axmacher, 2021. "An engram of intentionally forgotten information," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    17. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    18. 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.
    19. Jifan Zhou & Jun Yin & Tong Chen & Xiaowei Ding & Zaifeng Gao & Mowei Shen, 2011. "Visual Working Memory Capacity Does Not Modulate the Feature-Based Information Filtering in Visual Working Memory," PLOS ONE, Public Library of Science, vol. 6(9), pages 1-10, September.
    20. Nir Even-Chen & Blue Sheffer & Saurabh Vyas & Stephen I Ryu & Krishna V Shenoy, 2019. "Structure and variability of delay activity in premotor cortex," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-17, February.

    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_s41467-024-52541-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.