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Brain mechanisms of reversible symbolic reference: a potential singularity of the human brain

View ORCID ProfileTimo van Kerkoerle, Louise Pape, View ORCID ProfileMilad Ekramnia, Xiaoxia Feng, View ORCID ProfileJordy Tasserie, Morgan Dupont, Xiaolian Li, Bechir Jarraya, View ORCID ProfileWim Vanduffel, View ORCID ProfileStanislas Dehaene, View ORCID ProfileGhislaine Dehaene-Lambertz
doi: https://doi.org/10.1101/2023.03.04.531109
Timo van Kerkoerle
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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  • For correspondence: ghislaine.dehaene@cea.fr timo@neuroscience.visio
Louise Pape
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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Milad Ekramnia
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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Xiaoxia Feng
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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Jordy Tasserie
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
2Center for Brain Circuit Therapeutics Department of Neurology Brigham & Women’s Hospital, Harvard Medical School, Boston, MA, USA
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Morgan Dupont
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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Xiaolian Li
3Department of Neurosciences, Laboratory of Neuro- and Psychophysiology, KU Leuven Medical School, Leuven 3000, Belgium
4Leuven Brain Institute, KU Leuven, Leuven 3000, Belgium
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Bechir Jarraya
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
4Leuven Brain Institute, KU Leuven, Leuven 3000, Belgium
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Wim Vanduffel
3Department of Neurosciences, Laboratory of Neuro- and Psychophysiology, KU Leuven Medical School, Leuven 3000, Belgium
4Leuven Brain Institute, KU Leuven, Leuven 3000, Belgium
6Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA 02129, USA
7Department of Radiology, Harvard Medical School, Boston, MA 02144, USA
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Stanislas Dehaene
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
8Collège de France, Université Paris-Sciences-Lettres (PSL), 11 Place Marcelin Berthelot, 75005 Paris, France
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Ghislaine Dehaene-Lambertz
1Cognitive Neuroimaging Unit, CEA, INSERM, Université Paris-Saclay, NeuroSpin center, 91191 Gif/Yvette, France
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  • For correspondence: ghislaine.dehaene@cea.fr timo@neuroscience.visio
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Abstract

The emergence of symbolic thinking has been proposed as a dominant cognitive criterion to distinguish humans from other primates during hominization. Although the proper definition of a symbol has been the subject of much debate, one of its simplest features is bidirectional attachment: the content is accessible from the symbol, and vice versa. Behavioral observations scattered over the past four decades suggest that this criterion might not be met in non-human primates, as they fail to generalize an association learned in one temporal order (A to B) to the reverse order (B to A). Here, we designed an implicit fMRI test to investigate the neural mechanisms of arbitrary audio-visual and visual-visual pairing in monkeys and humans and probe their spontaneous reversibility. After learning a unidirectional association, humans showed surprise signals when this learned association was violated. Crucially, this effect occurred spontaneously in both learned and reversed directions, within an extended network of high-level brain areas, including, but also going beyond the language network. In monkeys, by contrast, violations of association effects occurred solely in the learned direction and were largely confined to sensory areas. We propose that a human-specific brain network may have evolved the capacity for reversible symbolic reference.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 04, 2023.
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Brain mechanisms of reversible symbolic reference: a potential singularity of the human brain
Timo van Kerkoerle, Louise Pape, Milad Ekramnia, Xiaoxia Feng, Jordy Tasserie, Morgan Dupont, Xiaolian Li, Bechir Jarraya, Wim Vanduffel, Stanislas Dehaene, Ghislaine Dehaene-Lambertz
bioRxiv 2023.03.04.531109; doi: https://doi.org/10.1101/2023.03.04.531109
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Brain mechanisms of reversible symbolic reference: a potential singularity of the human brain
Timo van Kerkoerle, Louise Pape, Milad Ekramnia, Xiaoxia Feng, Jordy Tasserie, Morgan Dupont, Xiaolian Li, Bechir Jarraya, Wim Vanduffel, Stanislas Dehaene, Ghislaine Dehaene-Lambertz
bioRxiv 2023.03.04.531109; doi: https://doi.org/10.1101/2023.03.04.531109

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