Increased fronto-striatal reward prediction errors moderate decision making in obsessive–compulsive disorder

Hauser, Tobias U.; Iannaccone, Reto; Dolan, Raymond J.; Ball, Juliane; Hättenschwiler, Josef; Drechsler, Renate; Rufer, Michael; Brandeis, Daniel; Walitza, Susanne; Brem, Silvia

doi:10.1017/s0033291716003305

Cited by 68 publications

(93 citation statements)

References 92 publications

(150 reference statements)

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“…One previous study of reward anticipation (not learning) showed nucleus accumbens dysfunction in OCD (26). Here, we report an overactivation in the nucleus accumbens responses to positive prediction errors in OCD, consistent with prior data showing overactivation in OCD across error tasks and brain regions (38; 39) and in line with results from Hauser and colleagues (31), who showed excessive striatal reward prediction errors in OCD during reversal learning.…”

Section: Discussionsupporting

confidence: 93%

“…We found no significant correlations between anterior cingulate prediction error signals and a general OCD symptom score; this lack of association is in accordance with the results from the only other fMRI study of reward prediction error in OCD (31). However, we did demonstrate an association between anterior cingulate negative prediction error signal with self-perceived 'self-regulation': driven by associations with subcomponents of difficulty in triggering behavioral change, searching for options, and implementing a plan.…”

Section: Discussionsupporting

confidence: 87%

“…The lack of clear prediction errors in controls may have resulted from our procedure containing only 40 reward pair stimuli trials; for comparison, other prior prediction error fMRI studies have included larger numbers of potentially rewarding trials, such as 80 (33) or 90 (11). Pronounced anterior cingulate prediction error signals are consistent with a recent study reporting stronger fronto-striatal reward prediction error signals in OCD, also using a fMRI reinforcement learning paradigm (31). Furthermore, exaggerated responses to errors is a consistent finding in OCD, with a number of prior studies showing an overactivation of frontal responses to error processing in OCD in both fMRI research (38; 39) and EEG Error Related Negativity studies (4; 5).…”

Section: Discussionsupporting

confidence: 80%

“…Both processes involve worse than expected outcome, motivating the study of prediction error signaling in OCD. Recently, Hauser et al (31) reported increased brain signals in response to reward prediction errors in the anterior cingulate cortex and the putamen, indicating an overactivation of the monitoring system. Reward prediction error processing is closely linked to the dopaminergic system (10).…”

Section: Introductionmentioning

confidence: 99%

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

Murray

Knolle

Ersche

et al. 2017

Preprint

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 87%

Section: Discussionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Murray

Knolle

Ersche

et al. 2017

Preprint

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“…Similar to addiction disorders (Curtis and Davis, 2014), compulsive behaviors represent a loss of control over habits, which creates pathological courses of behaviors (Jentsch et al, 2014). Impairment in the reward system can change decision making and learning through the Reward Prediction Error (RPE) that includes the pros and cons of the behavioral outcomes (Benton, 2010; Hauser et al, 2017). The study of Oswald et al (2011) investigated, in rats, the maladaptive situation in which repeated intake of PF occurs along with knowledge that an aversive outcome is likely to follow.…”

Section: Introductionmentioning

confidence: 99%

A Potential Animal Model of Maladaptive Palatable Food Consumption Followed by Delayed Discomfort

2017

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Introduction: Binging is the consumption of larger amounts of food in a briefer period of time than would normally be consumed under similar circumstances. Binging requires palatable food (PF) to trigger abnormal eating, probably reflecting gene × environment interactions. In this study we examined the impact of trait binge eating (BE) and its compulsive nature on the conflict between hedonic eating of PF and anticipation of a delayed aversive effect. We used female rats as an animal model similar to other models of BE. A novel aspect of this model in this paper is the use of a delayed internal aversive effect produced by lactose ingestion. Establishing this model will allow us to better understand the nature of the conflict between immediate reward and its delayed aversive implications. We hypothesized that BE prone (BEP) rats will demonstrate maladaptive decision making, presenting higher motivation toward PF even when this is associated with delayed discomfort.Method: (Phase 1) 52 female adult Wistar rats were divided to two eating profiles: resistant and prone binge eaters (BER/BEP) based on intake of liquid PF (Ensure). Next, all subjects underwent a Lactose Conditioning Protocol (LCP) that included 4 h tests, one baseline and 3 conditioning days (Phase 2), in which solid PF (Oreo cookies) was paired with glucose (control-no internal aversive effect) or lactose, dissolved in liquid PF. Index for PF motivation was PF consumption during the 4 h LCP. To test for memory of lactose conditioning, we performed another LCP with glucose only (anticipation, but no actual lactose-induced discomfort), a week after the last conditioning session.Results: Lactose conditioned BEP showed higher motivation toward PF compared to lactose conditioned BER faced with delayed aversive effects. Only lactose conditioned BER rats devaluated the PF over LCP days, indicating an association between PF and abdominal discomfort. In addition, only lactose conditioned BER presented an adaptive dynamic behavior, by varying PF intake according to consequences. Furthermore, solid PF consumption was predicted by binge size of liquid PF, only for lactose conditioned rats.Conclusions: We established an animal model for a common eating conflict in humans using delayed internal aversive unconditional stimuli.

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Association of Environmental Uncertainty With Altered Decision-making and Learning Mechanisms in Youths With Obsessive-Compulsive Disorder

Marzuki

Tomić

et al. 2021

JAMA Netw Open

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IMPORTANCE Adults with obsessive-compulsive disorder (OCD) display perseverative behavior in stable environments but exhibit vacillating choice when payoffs are uncertain. These findings may be associated with intolerance of uncertainty and compulsive behaviors; however, little is known about the mechanisms underlying learning and decision-making in youths with OCD because research into this population has been limited. OBJECTIVE To investigate cognitive mechanisms associated with decision-making in youths withOCD by using executive functioning tasks and computational modeling. DESIGN, SETTING, AND PARTICIPANTSIn this cross-sectional study, 50 youths with OCD (patients) and 53 healthy participants (controls) completed a probabilistic reversal learning (PRL) task between January 2014 and March 2020. A separate sample of 27 patients and 46 controls completed the Wisconsin Card Sorting Task (WCST) between January 2018 and November 2020. The study took place at the University of Cambridge in the UK. MAIN OUTCOMES AND MEASURES Decision-making mechanisms were studied by fitting hierarchical bayesian reinforcement learning models to the 2 data sets and comparing model parameters between participant groups. Model parameters included reward and punishment learning rates (feedback sensitivity), reinforcement sensitivity and decision consistency (exploitation), and stickiness (perseveration). Associations of receipt of serotonergic medication with performance were assessed. RESULTS In total, 50 patients (29 female patients [58%]; median age, 16.6 years [IQR, 15.3-18.0 years]) and 53 controls (30 female participants [57%]; median age, 16.4 years [IQR, 14.8-18.0 years]) completed the PRL task. A total of 27 patients (18 female patients [67%]; median age, 16.1 years [IQR, 15.2-17.2 years]) and 46 controls (28 female participants [61%]; median age, 17.2 [IQR, 16.3-17.6 years]) completed the WCST. During the reversal phase of the PRL task, patients made fewer correct responses (mean [SD] proportion: 0.83 [0.16] for controls and 0.61 [0.31] for patients; 95% CI, −1.31 to −0.64) and switched choices more often following false-negative feedback (mean [SD] proportion: 0.09 [0.16] for controls vs 0.27 [0.34] for patients; 95% CI, 0.60-1.26) and true-positive feedback (mean [SD] proportion: 0.93 [0.17] for controls vs 0.73 [0.34] for patients; 95% CI, −2.17 to −1.31). Computational modeling revealed that patients displayed enhanced reward learning rates (mean difference [MD], 0.21; 95% highest density interval [HDI], 0.04-0.38) but decreased punishment learning rates (MD, −0.29; 95% HDI, −0.39 to −0.18), reinforcement sensitivity (MD, −4.91; 95% HDI, −9.38 to −1.12), and stickiness (MD, −0.35; 95% HDI, −0.57 to −0.11) compared with controls. There were no group differences on standard WCST measures and computational model parameters. However, patients who received serotonergic medication showed slower response times (mean [SD], 1420.49 [279.71] milliseconds for controls, 1471.42 [212.81] milliseconds for (continued) Key Points Questio...

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Increased fronto-striatal reward prediction errors moderate decision making in obsessive–compulsive disorder

Abstract: Background: Obsessive-compulsive disorder (OCD) has been linked to functional

Cited by 68 publications

References 92 publications

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

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

A Potential Animal Model of Maladaptive Palatable Food Consumption Followed by Delayed Discomfort

Association of Environmental Uncertainty With Altered Decision-making and Learning Mechanisms in Youths With Obsessive-Compulsive Disorder

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