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


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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    • "Many studies have identified a vast region of the vmPFC, anterior to the genu of the corpus callosum and extending ventrally toward the orbitofrontal cortex, which encodes outcome value (Bartra et al., 2013). This includes both primary rewards, such as pleasant odors (Gottfried et al., 2003), juice (O'Doherty et al., 2002), or attractive faces (Bray and O'Doherty, 2007) and secondary rewards, such as money or points/tokens (Kringelbach and Rolls, 2004;Kuhnen and Knutson, 2005;Oya et al., 2005;Daw et al., 2006;Yacubian et al., 2006;Chib et al., 2009;Haber and Knutson, 2010;Levy et al., 2010;Levy and Glimcher, 2012), compatible with the activation pattern we report here in the more dorsal vmPFC focus. Notably, we observed a monotonic representation of reward value in the outcome phase in the vmPFC ROI generated from a meta-analysis of a large number of human fMRI studies on decision-making (Bartra et al., 2013). "
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    ABSTRACT: Decision-making studies have implicated the ventromedial prefrontal cortex (vmPFC) in tracking the value of rewards and punishments. At the same time, fear-learning studies have pointed to a role of the same area in updating previously learned cue–outcome associations. To disentangle these accounts, we used a reward reversal-learning paradigm in a functional magnetic resonance imaging study in 18 human participants. Participants first learned that one of two colored squares (color A) was associated with monetary reward, whereas the other (color B) was not, and then had to learn that these contingencies reversed. Consistent with value representation, activity of a dorsal region of vmPFC was positively correlated with reward magnitude. Conversely, a more ventral region of vmPFC responded more to color A than to color B after contingency reversal, compatible with a role of inhibiting the previously learned response that was no longer appropriate. Moreover, the response strength was correlated with subjects’ behavioral learning strength. Our findings provide direct evidence for the spatial dissociation of value representation and affective response inhibition in the vmPFC.
    Full-text · Article · Dec 2015
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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.
    Full-text · Article · Jul 2015 · Human Brain Mapping
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    • "However, an alternative explanation to these findings could be driven by the expectancy of a reward, so the invigorating effect could emerge as a result of the momentarily increase of expectancy of winning before the occurrence of a near-miss and be masked by the low temporal resolution of the BOLD fMRI response. Indeed, similar brain regions engaged during the delivery of reward (especially ventral striatum) are also recruited in its anticipation (Knutson et al., 2003; Knutson and Cooper, 2005; Yacubian et al., 2006; Diekhof et al., 2012). Expectation of winning might therefore play a key role in near-miss events. "
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    ABSTRACT: Near-miss events are situations in which an action yields a negative result but is very close to being successful. They are known to influence behavior, especially in gambling scenarios. Previous neuroimaging studies have described an "anomalous" activity of brain reward areas following these events. The goal of the present research was to study electrophysiological correlates of near-misses in the expectation and outcome phases. EEG was recorded while participants were playing a simplified version of a slot machine. Four possible outcomes (gain, near-miss, loss and no-information) were presented in a pseudorandom order to ensure fixed proportions. Results from the time-frequency analysis for the theta (4-8 Hz), alpha (9-13 Hz), low beta (15-22 Hz) and beta-gamma (25-35 Hz) frequency-bands presented larger power increases for wins and near-misses compared to losses. In the anticipation phase, power changes were lower than in the resolution phase. The current results are in agreement with previous studies showing that near-miss events recruit brain areas of the reward network. Likewise, the oscillatory activity in near-misses is very similar to the one elicited in the gain condition. In addition, present findings suggest that oscillatory activity in the expectation phase does not play a crucial role in near-miss events. © The Author (2015). Published by Oxford University Press. For Permissions, please email:
    Full-text · Article · Mar 2015 · Social Cognitive and Affective Neuroscience
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