Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain

Department of Systems Neuroscience, NeuroImage Nord, University Medical Center Hamburg-Eppendorf, D-20246 Hamburg, Germany.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 10/2006; 26(37):9530-7. DOI: 10.1523/JNEUROSCI.2915-06.2006
Source: PubMed

ABSTRACT Midbrain dopaminergic neurons projecting to the ventral striatum code for reward magnitude and probability during reward anticipation and then indicate the difference between actual and predicted outcome. It has been questioned whether such a common system for the prediction and evaluation of reward exists in humans. Using functional magnetic resonance imaging and a guessing task in two large cohorts, we are able to confirm ventral striatal responses coding both reward probability and magnitude during anticipation, permitting the local computation of expected value (EV). However, the ventral striatum only represented the gain-related part of EV (EV+). At reward delivery, the same area shows a reward probability and magnitude-dependent prediction error signal, best modeled as the difference between actual outcome and EV+. In contrast, loss-related expected value (EV-) and the associated prediction error was represented in the amygdala. Thus, the ventral striatum and the amygdala distinctively process the value of a prediction and subsequently compute a prediction error for gains and losses, respectively. Therefore, a homeostatic balance of both systems might be important for generating adequate expectations under uncertainty. Prevalence of either part might render expectations more positive or negative, which could contribute to the pathophysiology of mood disorders like major depression.

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    • "rd atlas ( probability threshold 50% ) . In addi - tion , due to the ventral striatums ' role in coding delayed reward signals [ Miedl et al . , 2014 ] and emotional aspects of autobiographical memories [ Speer et al . , 2014 ] , 8mm - sphreres were centred around established coordinates : x , y , z : 614 , 8 , 28 mm [ O ' Doherty et al . , 2004 ; Yacubian et al . , 2006 ] . The threshold of small volume corrections was set to P < 0 . 05 corrected for multiple comparisons using the family wise error rate ( FWE < 0 . 05 ) . Other regions were reported when passing a whole - brain cor - rected cluster - threshold of FWE < 0 . 05 ( cluster forming threshold P < 0 . 005 uncorrected ) ."
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    ABSTRACT: Imagining future events while performing an intertemporal choice task can attenuate the devaluation of future rewards. Here, we investigated whether this effect and its neural basis depend on the degree of personal prior experience associated with the simulated future scenarios. Functional magnetic resonance imaging was combined with a modified intertemporal choice task in which the delayed options were either purely monetary, or linked with a social event. Subject-specific events differed regarding familiarity, that is, meeting a close, familiar person or a celebrity in a café. In line with recent hypotheses on episodic construction, the simulation of future familiar and unfamiliar events equally attenuated delay discounting behavior in comparison with the control condition and both were imagined with similar richness. Imaging data, however, indicate that these results rely on differential neural activation patterns. The hippocampus was particularly involved in the simulation of unfamiliar future scenarios, probably reflecting enhanced construction processes when personal experience with similar past events is lacking. Consequently, functional coupling of the hippocampus with neural valuation signals in the anterior cingulate cortex predicted the subjective value only of rewards offered in the unfamiliar context. In contrast, valuation of rewards in a familiar context was predicted by activation in key nodes of emotional and autobiographical memory retrieval and dynamically modulated by frontal-striatal connectivity. The present data emphasize that the mechanisms underlying neural valuation of prospective rewards largely depend on the pre-experience with the context in which they are offered. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Human Brain Mapping 07/2015; DOI:10.1002/hbm.22912 · 5.97 Impact Factor
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    • "The nucleus accumbens, part of the ventral striatum , has been shown to code both probability and delay features of rewards indiscriminately, pointing towards a common 'neural currency' (Peters and Bü chel, 2009). This region responds preferentially to (i) low-probability rewards that are betterthan-expected and so more subjectively gratifying (Yacubian et al., 2006; Smith et al., 2009); and (ii) immediate rewards over those that are superior in the longer-term (McClure et al., 2004). In contrast, activity in dorsofrontal structures, most notably the dorsolateral prefrontal cortex (PFC), is associated with mediating behaviour in the direction of safer over risky prospects (Campbell-Meiklejohn et al., 2008) and with delaying gratification in favour of superior but delayed rewards (McClure et al., 2004). "
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    ABSTRACT: Bipolar disorder is characterized by impaired decision-making captured in impulsivity and risk-taking. We sought to determine whether this is driven by a failure to effectively weight the lower-order goal of obtaining a strongly desired reward in relation to higher-order goals, and how this relates to trait impulsivity and risk-taking. We hypothesized that in bipolar disorder the weighting of valuation signals converging on ventromedial prefrontal cortex are more heavily weighted towards ventral striatum inputs (lower-order), with less weighting of dorsolateral prefrontal cortex inputs (higher-order). Twenty euthymic patients with bipolar disorder not in receipt of antipsychotic medication and 20 case-matched controls performed a roulette task during functional magnetic resonance imaging. Activity in response to high-probability ('safe') and low-probability ('risky') prospects was measured during both anticipation, and outcome. In control subjects, anticipatory and outcome-locked activity in dorsolateral prefrontal cortex was greater for safe than risky reward prospects. The bipolar disorder group showed the opposite pattern with preferential response to risky rewards. This group also showed increased anticipatory and outcome-locked activity in ventral striatum in response to rewards. In control subjects, however, ventromedial prefrontal activation was positively associated with both ventral striatum and dorsolateral prefrontal activity; patients evidenced a strong positive association with ventral striatum, but a negative association with dorsolateral prefrontal cortex. Response to high-probability rewards in dorsolateral prefrontal cortex was inversely associated with trait impulsivity and risk-taking in the bipolar disorder group. Our findings suggest that clinically impulsive and risky decision-making are related to subjective valuation that is biased towards lower-order preference, with diminished integration of higher-order goals. The findings extend a functional neuroanatomical account of disorders characterized by clinically impulsive decision-making, and provide targets for evaluating interventions that foster self-control.
    Brain 07/2014; 137(8). DOI:10.1093/brain/awu152 · 9.20 Impact Factor
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    • "There seems to be a specialization within dopamine projection sites in relation to monetary reward: anticipation of monetary reward increases activation in the VStr, which includes the nucleus accumbens, while rewarding outcomes increase activation in the ventral medial prefrontal cortex, dorsal striatum, and posterior cingulate, with deactivation in the aforementioned regions during reward omission (Elliott et al., 2000; Breiter et al., 2001; Knutson et al., 2001b; Tricomi et al., 2004). Neuroimaging experiments in humans suggest that VStr activity strongly correlates with expected value, as well as magnitude and probability (Breiter et al., 2001; Knutson et al., 2001a, 2005; Abler et al., 2006; Yacubian et al., 2006; Rolls et al., 2008). Work by D’Ardenne et al. (2008) supports a role for the mesolimbic dopamine system in monetary RPE signaling. "
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    ABSTRACT: An influential model suggests that dopamine signals the difference between predicted and experienced reward. In this way, dopamine can act as a learning signal that can shape behaviors to maximize rewards and avoid punishments. Dopamine is also thought to invigorate reward seeking behavior. Loss of dopamine signaling is the major abnormality in Parkinson's disease. Dopamine agonists have been implicated in the occurrence of impulse control disorders in Parkinson's disease patients, the most common being pathological gambling, compulsive sexual behavior, and compulsive buying. Recently, a number of functional imaging studies investigating impulse control disorders in Parkinson's disease have been published. Here we review this literature, and attempt to place it within a decision-making framework in which potential gains and losses are evaluated to arrive at optimum choices. We also provide a hypothetical but still incomplete model on the effect of dopamine agonist treatment on these value and risk assessments. Two of the main brain structures thought to be involved in computing aspects of reward and loss are the ventral striatum (VStr) and the insula, both dopamine projection sites. Both structures are consistently implicated in functional brain imaging studies of pathological gambling in Parkinson's disease.
    Frontiers in Behavioral Neuroscience 05/2014; 8:196. DOI:10.3389/fnbeh.2014.00196 · 3.27 Impact Factor
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