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Distributed representations of prediction error signals across the cortical hierarchy are synergistic

Author

Listed:
  • Frank Gelens

    (University of Amsterdam
    University of Cambridge)

  • Juho Äijälä

    (University of Cambridge)

  • Louis Roberts

    (University of Cambridge
    University of London)

  • Misako Komatsu

    (RIKEN Brain Science Institute)

  • Cem Uran

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    Radboud University Nijmegen)

  • Michael A. Jensen

    (Mayo Clinic)

  • Kai J. Miller

    (Mayo Clinic)

  • Robin A. A. Ince

    (University of Glasgow)

  • Max Garagnani

    (University of London
    Freie Universität Berlin)

  • Martin Vinck

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    Radboud University Nijmegen)

  • Andres Canales-Johnson

    (University of Cambridge
    Universidad Católica del Maule)

Abstract

A relevant question concerning inter-areal communication in the cortex is whether these interactions are synergistic. Synergy refers to the complementary effect of multiple brain signals conveying more information than the sum of each isolated signal. Redundancy, on the other hand, refers to the common information shared between brain signals. Here, we dissociated cortical interactions encoding complementary information (synergy) from those sharing common information (redundancy) during prediction error (PE) processing. We analyzed auditory and frontal electrocorticography (ECoG) signals in five common awake marmosets performing two distinct auditory oddball tasks and investigated to what extent event-related potentials (ERP) and broadband (BB) dynamics encoded synergistic and redundant information about PE processing. The information conveyed by ERPs and BB signals was synergistic even at lower stages of the hierarchy in the auditory cortex and between auditory and frontal regions. Using a brain-constrained neural network, we simulated the synergy and redundancy observed in the experimental results and demonstrated that the emergence of synergy between auditory and frontal regions requires the presence of strong, long-distance, feedback, and feedforward connections. These results indicate that distributed representations of PE signals across the cortical hierarchy can be highly synergistic.

Suggested Citation

  • Frank Gelens & Juho Äijälä & Louis Roberts & Misako Komatsu & Cem Uran & Michael A. Jensen & Kai J. Miller & Robin A. A. Ince & Max Garagnani & Martin Vinck & Andres Canales-Johnson, 2024. "Distributed representations of prediction error signals across the cortical hierarchy are synergistic," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48329-7
    DOI: 10.1038/s41467-024-48329-7
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    References listed on IDEAS

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    Cited by:

    1. Antonino Greco & Julia Moser & Hubert Preissl & Markus Siegel, 2024. "Predictive learning shapes the representational geometry of the human brain," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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