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Intracortical recordings reveal vision-to-action cortical gradients driving human exogenous attention

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  • Tal Seidel Malkinson

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière
    Université de Lorraine, CNRS, IMoPA, F-54000)

  • Dimitri J. Bayle

    (Licae Lab, Université Paris Ouest-La Défense)

  • Brigitte C. Kaufmann

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière)

  • Jianghao Liu

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière
    Dassault Systèmes)

  • Alexia Bourgeois

    (University of Geneva)

  • Katia Lehongre

    (CENIR - Centre de Neuro-Imagerie de Recherche, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière)

  • Sara Fernandez-Vidal

    (CENIR - Centre de Neuro-Imagerie de Recherche, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière)

  • Vincent Navarro

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière
    AP-HP, Epilepsy and EEG Units, Pitié-Salpêtrière Hospital
    Reference center of rare epilepsies, EpiCare, Pitié-Salpêtrière Hospital)

  • Virginie Lambrecq

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière
    AP-HP, Epilepsy and EEG Units, Pitié-Salpêtrière Hospital
    Reference center of rare epilepsies, EpiCare, Pitié-Salpêtrière Hospital)

  • Claude Adam

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière
    AP-HP, Epilepsy and EEG Units, Pitié-Salpêtrière Hospital
    Reference center of rare epilepsies, EpiCare, Pitié-Salpêtrière Hospital)

  • Daniel S. Margulies

    (Université de Paris)

  • Jacobo D. Sitt

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière)

  • Paolo Bartolomeo

    (Sorbonne Université, Inserm UMRS 1127, CNRS UMR 7225, Paris Brain Institute, ICM, Hôpital de la Pitié-Salpêtrière)

Abstract

Exogenous attention, the process that makes external salient stimuli pop-out of a visual scene, is essential for survival. How attention-capturing events modulate human brain processing remains unclear. Here we show how the psychological construct of exogenous attention gradually emerges over large-scale gradients in the human cortex, by analyzing activity from 1,403 intracortical contacts implanted in 28 individuals, while they performed an exogenous attention task. The timing, location and task-relevance of attentional events defined a spatiotemporal gradient of three neural clusters, which mapped onto cortical gradients and presented a hierarchy of timescales. Visual attributes modulated neural activity at one end of the gradient, while at the other end it reflected the upcoming response timing, with attentional effects occurring at the intersection of visual and response signals. These findings challenge multi-step models of attention, and suggest that frontoparietal networks, which process sequential stimuli as separate events sharing the same location, drive exogenous attention phenomena such as inhibition of return.

Suggested Citation

  • Tal Seidel Malkinson & Dimitri J. Bayle & Brigitte C. Kaufmann & Jianghao Liu & Alexia Bourgeois & Katia Lehongre & Sara Fernandez-Vidal & Vincent Navarro & Virginie Lambrecq & Claude Adam & Daniel S., 2024. "Intracortical recordings reveal vision-to-action cortical gradients driving human exogenous attention," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46013-4
    DOI: 10.1038/s41467-024-46013-4
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    References listed on IDEAS

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    1. Tirin Moore & Katherine M. Armstrong, 2003. "Selective gating of visual signals by microstimulation of frontal cortex," Nature, Nature, vol. 421(6921), pages 370-373, January.
    2. D. F. Wasmuht & E. Spaak & T. J. Buschman & E. K. Miller & M. G. Stokes, 2018. "Intrinsic neuronal dynamics predict distinct functional roles during working memory," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Ilaria Sani & Heiko Stemmann & Bradley Caron & Daniel Bullock & Torsten Stemmler & Manfred Fahle & Franco Pestilli & Winrich A. Freiwald, 2021. "The human endogenous attentional control network includes a ventro-temporal cortical node," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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