Precision-weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis

Joost Haarsma; Paul Fletcher; Juliet Griffin; Hilde Taverne; Hisham  Ziauddeen; Thomas Spencer; Chantal Miller; Teresa Katthagen; Ian Goodyear; Kelly Diederen; Graham Murray

doi:https://doi.org/10.1038/s41380-020-0803-8

Precision-weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis

Joost Haarsma, Paul Fletcher, Juliet Griffin, Hilde Taverne, Hisham Ziauddeen, Thomas Spencer, Chantal Miller, Teresa Katthagen, Ian Goodyear, Kelly Diederen, Graham Murray

Psychosis Studies

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Abstract

Recent theories of cortical function construe the brain as performing hierarchical Bayesian inference. According to these theories, the precision of prediction errors plays a key role in learning and decision-making, is controlled by dopamine, and contributes to the pathogenesis of psychosis. To test these hypotheses, we studied learning with variable outcome-precision in healthy individuals after dopaminergic modulation with a placebo, a dopamine receptor agonist bromocriptine or a dopamine receptor antagonist sulpiride (dopamine study n=59) and in patients with early psychosis (psychosis study n=74: 20 participants with First Episode Psychosis, 30 healthy controls and 24 participants with At Risk Mental State attenuated psychotic symptoms). Behavioural computational modelling indicated that precision-weighting of prediction errors benefits learning in health and is impaired in psychosis. FMRI revealed coding of unsigned prediction errors, which signal surprise, relative to their precision in superior frontal cortex (replicated across studies, combined n=133), which was perturbed by dopaminergic modulation, impaired in psychosis, and associated with task performance and schizotypy (schizotypy correlation in 86 healthy volunteers). In contrast to our previous work, we did not observe significant precision-weighting of signed prediction errors, which signal valence, in the midbrain and ventral striatum in the healthy controls (or patients) in the psychosis study. We conclude that healthy people, but not patients with first episode psychosis, take into account the precision of the environment when updating beliefs. Precision-weighting of cortical prediction error signals is a key mechanism through which dopamine modulates inference and contributes to the pathogenesis of psychosis.

Original language	English
Pages (from-to)	1-14
Journal	Molecular Psychiatry
Volume	0
Issue number	0
Early online date	24 Jun 2020
DOIs	https://doi.org/10.1038/s41380-020-0803-8
Publication status	Published - 24 Jun 2020

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Haarsma, J., Fletcher, P., Griffin, J., Taverne, H., Ziauddeen, H., Spencer, T., Miller, C., Katthagen, T., Goodyear, I., Diederen, K., & Murray, G. (2020). Precision-weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis. Molecular Psychiatry, 0(0), 1-14. https://doi.org/10.1038/s41380-020-0803-8

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abstract = "Recent theories of cortical function construe the brain as performing hierarchical Bayesian inference. According to these theories, the precision of prediction errors plays a key role in learning and decision-making, is controlled by dopamine, and contributes to the pathogenesis of psychosis. To test these hypotheses, we studied learning with variable outcome-precision in healthy individuals after dopaminergic modulation with a placebo, a dopamine receptor agonist bromocriptine or a dopamine receptor antagonist sulpiride (dopamine study n=59) and in patients with early psychosis (psychosis study n=74: 20 participants with First Episode Psychosis, 30 healthy controls and 24 participants with At Risk Mental State attenuated psychotic symptoms). Behavioural computational modelling indicated that precision-weighting of prediction errors benefits learning in health and is impaired in psychosis. FMRI revealed coding of unsigned prediction errors, which signal surprise, relative to their precision in superior frontal cortex (replicated across studies, combined n=133), which was perturbed by dopaminergic modulation, impaired in psychosis, and associated with task performance and schizotypy (schizotypy correlation in 86 healthy volunteers). In contrast to our previous work, we did not observe significant precision-weighting of signed prediction errors, which signal valence, in the midbrain and ventral striatum in the healthy controls (or patients) in the psychosis study. We conclude that healthy people, but not patients with first episode psychosis, take into account the precision of the environment when updating beliefs. Precision-weighting of cortical prediction error signals is a key mechanism through which dopamine modulates inference and contributes to the pathogenesis of psychosis.",

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Haarsma, J, Fletcher, P, Griffin, J, Taverne, H, Ziauddeen, H, Spencer, T, Miller, C, Katthagen, T, Goodyear, I, Diederen, K & Murray, G 2020, 'Precision-weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis', Molecular Psychiatry, vol. 0, no. 0, pp. 1-14. https://doi.org/10.1038/s41380-020-0803-8

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AU - Fletcher, Paul

AU - Griffin, Juliet

AU - Taverne, Hilde

AU - Ziauddeen, Hisham

AU - Spencer, Thomas

AU - Miller, Chantal

AU - Katthagen, Teresa

AU - Goodyear, Ian

AU - Diederen, Kelly

AU - Murray, Graham

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Precision-weighting of cortical unsigned prediction error signals benefits learning, is mediated by dopamine, and is impaired in psychosis

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