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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
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    References listed on IDEAS

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    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.
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