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Agent-specific learning signals for self–other distinction during mentalising

Ereira, S; Dolan, R; Kurth-Nelson, Z; (2018) Agent-specific learning signals for self–other distinction during mentalising. PLOS Biology , 16 (4) , Article e2004752. 10.1371/journal.pbio.2004752. Green open access

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Abstract

Humans have a remarkable ability to simulate the minds of others. How the brain distinguishes between mental states attributed to self and mental states attributed to someone else is unknown. Here, we investigated how fundamental neural learning signals are selectively attributed to different agents. Specifically, we asked whether learning signals are encoded in agent-specific neural patterns or whether a self–other distinction depends on encoding agent identity separately from this learning signal. To examine this, we tasked subjects to learn continuously 2 models of the same environment, such that one was selectively attributed to self and the other was selectively attributed to another agent. Combining computational modelling with magnetoencephalography (MEG) enabled us to track neural representations of prediction errors (PEs) and beliefs attributed to self, and of simulated PEs and beliefs attributed to another agent. We found that the representational pattern of a PE reliably predicts the identity of the agent to whom the signal is attributed, consistent with a neural self–other distinction implemented via agent-specific learning signals. Strikingly, subjects exhibiting a weaker neural self–other distinction also had a reduced behavioural capacity for self–other distinction and displayed more marked subclinical psychopathological traits. The neural self–other distinction was also modulated by social context, evidenced in a significantly reduced decoding of agent identity in a nonsocial control task. Thus, we show that self–other distinction is realised through an encoding of agent identity intrinsic to fundamental learning signals. The observation that the fidelity of this encoding predicts psychopathological traits is of interest as a potential neurocomputational psychiatric biomarker.

Type: Article
Title: Agent-specific learning signals for self–other distinction during mentalising
Open access status: An open access version is available from UCL Discovery
DOI: 10.1371/journal.pbio.2004752
Publisher version: https://doi.org/10.1371/journal.pbio.2004752
Language: English
Additional information: Copyright © 2018 Ereira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Keywords: Learning, Magnetoencephalography, Behavior, Games, Human learning, Random walk, Decision making, Neuroimaging
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Imaging Neuroscience
URI: https://discovery.ucl.ac.uk/id/eprint/10045534
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