Kaplan, Raphael Samuel Matthew; Schuster, Bianca A.; Sowden, Sophie; Rybicki, Alicia J.; Fraser, Dagmar S.; Press, Clare; Hickman, Lydia; Holland, Peter and Cook, Jennifer L.. 2024. Disruption of dopamine D2/D3 system function impairs the human ability to understand the mental states of other people. PLOS Biology, 22(6), e3002652. ISSN 1545-7885 [Article]

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Abstract or Description

Difficulties in reasoning about others’ mental states (i.e., mentalising/Theory of Mind) are highly prevalent among disorders featuring dopamine dysfunctions (e.g., Parkinson’s disease) and significantly affect individuals’ quality of life. However, due to multiple confounding factors inherent to existing patient studies, currently little is known about whether these sociocognitive symptoms originate from aberrant dopamine signalling or from psychosocial changes unrelated to dopamine. The present study, therefore, investigated the role of dopamine in modulating mentalising in a sample of healthy volunteers. We used a double-blind, placebo-controlled procedure to test the effect of the D2/D3 antagonist haloperidol on mental state attribution, using an adaptation of the Heider and Simmel (1944) animations task. On 2 separate days, once after receiving 2.5 mg haloperidol and once after receiving placebo, 33 healthy adult participants viewed and labelled short videos of 2 triangles depicting mental state (involving mentalistic interaction wherein 1 triangle intends to cause or act upon a particular mental state in the other, e.g., surprising) and non-mental state (involving reciprocal interaction without the intention to cause/act upon the other triangle’s mental state, e.g., following) interactions. Using Bayesian mixed effects models, we observed that haloperidol decreased accuracy in labelling both mental and non-mental state animations. Our secondary analyses suggest that dopamine modulates inference from mental and non-mental state animations via independent mechanisms, pointing towards 2 putative pathways underlying the dopaminergic modulation of mental state attribution: action representation and a shared mechanism supporting mentalising and emotion recognition. We conclude that dopaminergic pathways impact Theory of Mind, at least indirectly. Our results have implications for the neurochemical basis of sociocognitive difficulties in patients with dopamine dysfunctions and generate new hypotheses about the specific dopamine-mediated mechanisms underlying social cognition.

Item Type:	Article
Identification Number (DOI):	https://doi.org/10.1371/journal.pbio.3002652
Additional Information:	Funding: This work was supported by the European Union’s Horizon 2020 Research and Innovation Program (https://erc.europa.eu/faqprogramme/horizon-europe-horizon) under ERC2017-STG Grant Agreement No. 757583 (Brain2Bee, awarded to J.L.C.) The funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Data Access Statement:	All data and code files are publicly available on OSF via the link https://osf. io/xm7ty/ (DOI 10.17605/OSF.IO/XM7TY).
Departments, Centres and Research Units:	Psychology
Dates:	Date Event 1 May 2024 Accepted 13 June 2024 Published
Item ID:	37367
Date Deposited:	19 Jul 2024 11:17
Last Modified:	19 Jul 2024 11:21
Peer Reviewed:	Yes, this version has been peer-reviewed.
URI:	https://research.gold.ac.uk/id/eprint/37367

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