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Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder. / Murray, Graham; Knolle, Franziska; Ersche, Karen D; Craig, Kevin J; Abbott, Sanja; Shabbir, Shaila S; Fineberg, Naomi; Suckling, John ; Sahakian, Barbara J.; Bullmore, Edward T.; Robbins, Trevor W.

In: Psychopharmacology, Vol. 236, No. 8, 01.08.2019, p. 2325-2336.

Research output: Contribution to journalArticlepeer-review

Harvard

Murray, G, Knolle, F, Ersche, KD, Craig, KJ, Abbott, S, Shabbir, SS, Fineberg, N, Suckling, J, Sahakian, BJ, Bullmore, ET & Robbins, TW 2019, 'Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder', Psychopharmacology, vol. 236, no. 8, pp. 2325-2336. https://doi.org/10.1007/s00213-019-05292-2

APA

Murray, G., Knolle, F., Ersche, K. D., Craig, K. J., Abbott, S., Shabbir, S. S., Fineberg, N., Suckling, J., Sahakian, B. J., Bullmore, E. T., & Robbins, T. W. (2019). Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder. Psychopharmacology, 236(8), 2325-2336. https://doi.org/10.1007/s00213-019-05292-2

Vancouver

Author

Murray, Graham ; Knolle, Franziska ; Ersche, Karen D ; Craig, Kevin J ; Abbott, Sanja ; Shabbir, Shaila S ; Fineberg, Naomi ; Suckling, John ; Sahakian, Barbara J. ; Bullmore, Edward T. ; Robbins, Trevor W. / Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder. In: Psychopharmacology. 2019 ; Vol. 236, No. 8. pp. 2325-2336.

Bibtex

@article{87636b09c0a54b3d8ab5ddfc15100ed1,
title = "Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder",
abstract = "Rationale: Patients with obsessive-compulsive disorder (OCD) have been found to show exaggerated error responses and prediction error learning signals in a variety of EEG and fMRI tasks, with data converging on the anterior cingulate cortex as a key locus of dysfunction. Considerable evidence has linked prediction error processing to dopaminergic function. Objective: In this study, we investigate potential dopaminergic dysfunction during reward processing in the context of OCD. Methods: We studied OCD patients (n = 18) and controls (n = 18) whilst they learned probabilistic associations between abstract stimuli and monetary rewards in the fMRI scanner involving administration (on separate visits) of a dopamine receptor agonist, pramipexole 0.5 mg; a dopamine receptor antagonist, amisulpride 400 mg; and placebo. We fitted a Q-learning computational model to fMRI prediction error responses; group differences were examined in anterior cingulate and nucleus accumbens regions of interest. Results: There were no significant group, drug, or interaction effects in the number of correct choices; computational modeling suggested a marginally significant difference in learning rates between groups (p = 0.089, partial ƞ 2 = 0.1). In the imaging results, there was a significant interaction of group by drug (p = 0.013, partial ƞ 2 = 0.13). OCD patients showed abnormally strong cingulate signaling of prediction errors during omission of an expected reward, with unexpected reduction by both pramipexole and amisulpride (p = 0.014, partial ƞ 2 = 0.26, 1-β error probability = 0.94). Exaggerated cingulate prediction error signaling to omitted reward in placebo was related to trait subjective difficulty in self-regulating behavior in OCD. Conclusions: Our data support cingulate dysfunction during reward processing in OCD, and bidirectional remediation by dopaminergic modulation, suggesting that exaggerated cingulate error signals in OCD may be of dopaminergic origin. The results help to illuminate the mechanisms through which dopamine receptor antagonists achieve therapeutic benefit in OCD. Further research is needed to disentangle the different functions of dopamine receptor agonists and antagonists during bidirectional modulation of cingulate activation. ",
keywords = "Amisulpride, Anterior cingulate, Computational model, Nucleus accumbens, Obsessive-compulsive disorder, Pramipexole, Prediction error, Reward learning",
author = "Graham Murray and Franziska Knolle and Ersche, {Karen D} and Craig, {Kevin J} and Sanja Abbott and Shabbir, {Shaila S} and Naomi Fineberg and John Suckling and Sahakian, {Barbara J.} and Bullmore, {Edward T.} and Robbins, {Trevor W.}",
note = "{\textcopyright} The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.",
year = "2019",
month = aug,
day = "1",
doi = "10.1007/s00213-019-05292-2",
language = "English",
volume = "236",
pages = "2325--2336",
journal = "Psychopharmacology",
issn = "0033-3158",
publisher = "Springer Verlag",
number = "8",

}

RIS

TY - JOUR

T1 - Dopaminergic drug treatment remediates exaggerated cingulate prediction error responses in obsessive-compulsive disorder

AU - Murray, Graham

AU - Knolle, Franziska

AU - Ersche, Karen D

AU - Craig, Kevin J

AU - Abbott, Sanja

AU - Shabbir, Shaila S

AU - Fineberg, Naomi

AU - Suckling, John

AU - Sahakian, Barbara J.

AU - Bullmore, Edward T.

AU - Robbins, Trevor W.

N1 - © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

PY - 2019/8/1

Y1 - 2019/8/1

N2 - Rationale: Patients with obsessive-compulsive disorder (OCD) have been found to show exaggerated error responses and prediction error learning signals in a variety of EEG and fMRI tasks, with data converging on the anterior cingulate cortex as a key locus of dysfunction. Considerable evidence has linked prediction error processing to dopaminergic function. Objective: In this study, we investigate potential dopaminergic dysfunction during reward processing in the context of OCD. Methods: We studied OCD patients (n = 18) and controls (n = 18) whilst they learned probabilistic associations between abstract stimuli and monetary rewards in the fMRI scanner involving administration (on separate visits) of a dopamine receptor agonist, pramipexole 0.5 mg; a dopamine receptor antagonist, amisulpride 400 mg; and placebo. We fitted a Q-learning computational model to fMRI prediction error responses; group differences were examined in anterior cingulate and nucleus accumbens regions of interest. Results: There were no significant group, drug, or interaction effects in the number of correct choices; computational modeling suggested a marginally significant difference in learning rates between groups (p = 0.089, partial ƞ 2 = 0.1). In the imaging results, there was a significant interaction of group by drug (p = 0.013, partial ƞ 2 = 0.13). OCD patients showed abnormally strong cingulate signaling of prediction errors during omission of an expected reward, with unexpected reduction by both pramipexole and amisulpride (p = 0.014, partial ƞ 2 = 0.26, 1-β error probability = 0.94). Exaggerated cingulate prediction error signaling to omitted reward in placebo was related to trait subjective difficulty in self-regulating behavior in OCD. Conclusions: Our data support cingulate dysfunction during reward processing in OCD, and bidirectional remediation by dopaminergic modulation, suggesting that exaggerated cingulate error signals in OCD may be of dopaminergic origin. The results help to illuminate the mechanisms through which dopamine receptor antagonists achieve therapeutic benefit in OCD. Further research is needed to disentangle the different functions of dopamine receptor agonists and antagonists during bidirectional modulation of cingulate activation.

AB - Rationale: Patients with obsessive-compulsive disorder (OCD) have been found to show exaggerated error responses and prediction error learning signals in a variety of EEG and fMRI tasks, with data converging on the anterior cingulate cortex as a key locus of dysfunction. Considerable evidence has linked prediction error processing to dopaminergic function. Objective: In this study, we investigate potential dopaminergic dysfunction during reward processing in the context of OCD. Methods: We studied OCD patients (n = 18) and controls (n = 18) whilst they learned probabilistic associations between abstract stimuli and monetary rewards in the fMRI scanner involving administration (on separate visits) of a dopamine receptor agonist, pramipexole 0.5 mg; a dopamine receptor antagonist, amisulpride 400 mg; and placebo. We fitted a Q-learning computational model to fMRI prediction error responses; group differences were examined in anterior cingulate and nucleus accumbens regions of interest. Results: There were no significant group, drug, or interaction effects in the number of correct choices; computational modeling suggested a marginally significant difference in learning rates between groups (p = 0.089, partial ƞ 2 = 0.1). In the imaging results, there was a significant interaction of group by drug (p = 0.013, partial ƞ 2 = 0.13). OCD patients showed abnormally strong cingulate signaling of prediction errors during omission of an expected reward, with unexpected reduction by both pramipexole and amisulpride (p = 0.014, partial ƞ 2 = 0.26, 1-β error probability = 0.94). Exaggerated cingulate prediction error signaling to omitted reward in placebo was related to trait subjective difficulty in self-regulating behavior in OCD. Conclusions: Our data support cingulate dysfunction during reward processing in OCD, and bidirectional remediation by dopaminergic modulation, suggesting that exaggerated cingulate error signals in OCD may be of dopaminergic origin. The results help to illuminate the mechanisms through which dopamine receptor antagonists achieve therapeutic benefit in OCD. Further research is needed to disentangle the different functions of dopamine receptor agonists and antagonists during bidirectional modulation of cingulate activation.

KW - Amisulpride

KW - Anterior cingulate

KW - Computational model

KW - Nucleus accumbens

KW - Obsessive-compulsive disorder

KW - Pramipexole

KW - Prediction error

KW - Reward learning

UR - http://www.scopus.com/inward/record.url?scp=85067789621&partnerID=8YFLogxK

U2 - 10.1007/s00213-019-05292-2

DO - 10.1007/s00213-019-05292-2

M3 - Article

VL - 236

SP - 2325

EP - 2336

JO - Psychopharmacology

JF - Psychopharmacology

SN - 0033-3158

IS - 8

ER -