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

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Gelens, Frank; Aijala, Julio; Roberts, Louis; Komatsu, Misako; Uran, Cem; Jensen, Michael A.; Miller, Kai J.; Ince, Robin A.A.; Garagnani, M.; Vinck, Martin and Canales-Johnson, Andres. 2024. Distributed representations of prediction error signals across the cortical hierarchy are synergistic. Nature Communications, 15, 3941. ISSN 2041-1723 [Article]

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Official URL: https://www.nature.com/articles/s41467-024-48329-7

Abstract or Description

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 during 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 the distributed representations of PE signals across the cortical hierarchy can be highly synergistic.

Item Type:

Article

Identification Number (DOI):

https://doi.org/10.1038/s41467-024-48329-7

Data Access Statement:

Data availability: The original raw data of marmosets Fr, Kr, and Go used in this study is publicly available at: http://www.www.neurotycho.org/auditory-oddball-task. The original raw data of marmosets Ji and Nr used in this study is publicly available at: https://datadryad.org/stash/dataset/doi:10.5061/dryad.j3tx95xfp Source data are provided with this paper. Code availability: The MATLAB/Python toolbox GCMI (Gaussian Copula Mutual Information) used in this study is publicly available at: https://github.com/robince/gcmi.

Departments, Centres and Research Units:

Computing

Dates: