Elsevier

NeuroImage

Volume 19, Issue 4, August 2003, Pages 1674-1685
NeuroImage

Regular article
Context-dependent cortical activation in response to financial reward and penalty: an event-related fMRI study

https://doi.org/10.1016/S1053-8119(03)00250-7Get rights and content

Abstract

An event-related fMRI technique was used to assess neural responses to financial reward and penalty during a simple gambling task. We attempted to determine whether brain activities are dependent on the unique context of an event sequence. Thirty-six healthy volunteers participated in the study. The task was to guess the color of the suit of a card on each trial and to respond by pressing a button. Every correct response (“win”) and incorrect response (“loss”) was associated with financial reward and penalty, respectively. The magnitude of reward or penalty in each trial did not change; however, the subjects' self-reported emotional arousal was significantly higher for the events of “the fourth win of four wins in a row” and “the fourth loss of four losses in a row.” We also found that the bilateral anterior cingulate and medial prefrontal cortices were specifically activated when the subjects experienced “the fourth win of four wins in a row” and “the fourth loss of four losses in a row. ”When the subjects experienced “a win following four losses in a row” or “a loss following four wins in a row, ”the right dorsolateral prefrontal cortex was specifically activated. Our data indicate that there exist brain activities associated with the event-sequence context in which abstract reward or penalty is received. These context-dependent activities appear to be crucial for adapting oneself to new circumstances and may account for clinical symptoms of various mental illnesses in which dysfunction of these regions has been reported.

Introduction

Receiving rewards or penalties is not a simply passive behavior. Animals should predict potential rewards/penalties, distinguish their nature, and respond appropriately by changing their attentional or arousal level for successful adaptive behavior. Single-unit studies of nonhuman primates revealed the brain structures that are related to rewards and penalties. In the monkey, midbrain dopamine neurons were reported to be activated by the occurrence of rewards after their presentation and visual or auditory stimuli that predict rewards Schultz, 1986, Romo and Schultz, 1990, Schultz and Romo, 1990, Ljungberg et al., 1992. Dopamine neurons also encode an error in the temporal prediction of rewards; the dopamine activity is enhanced by surprising rewards and it is depressed by the omission of predicted rewards Ljungberg et al., 1992, Mirenowicz and Schultz, 1994. Other neurons in the ventral striatum Apicella et al., 1991, Shidara et al., 1998 and orbitofrontal cortex (Niki et al., 1972) also respond to the delivery of rewards. Furthermore, neurons within the orbitofronal cortex not only discriminate rewards and penalties (Thorpe et al., 1983), but also respond to reward expectancy Tremblay and Schultz, 1999, Tremblay and Schultz, 2000. Reward expectation neurons are also found in the striatum Shidara et al., 1998, Schultz et al., 1992. Neurons in the lateral prefrontal cortex were reported to be sensitive to the presence or absence of expected rewards Watanabe, 1990, Watanabe, 1992 and play an important role in coding the discrepancy between the expectancy of a specific reward and the response outcome (Watanabe, 1996).

On the other hand, imaging studies revealed that human brain activities are associated with the cognition of abstract rewards and penalties. In particular, the “gambling task” has been recently used as a laboratory model for investigating brain activities in response to abstract types of reward and punishment (e.g., monetary reward or penalty) in normal subjects. A previous positron emission tomography (PET) study revealed that the human orbitofrontal cortex can be activated with monetary reward (Thut et al., 1997). A functional magnetic resonance imaging (fMRI) study supports this finding, demonstrating that an increase in the activity of the medial orbitofrontal cortex is related to the subjects' receipt of monetary reward and deactivation following punishments (O'Doherty et al., 2001). The authors recorded the converse pattern of activation in the lateral orbitofrontal cortex (activation following punishments, deactivation following rewards). Moreover, in these areas, the authors found a correlation between the magnitude of brain activation and that of rewards and punishments received.

However, neural responses related to human reward systems under different psychological contexts are studied less extensively. On this issue, some groups focused on the context of anticipation of abstract rewards and punishments. They demonstrated that whereas anticipation of increasing rewards elicited nucleus accumbens activation Breiter et al., 2001, Knutson et al., 2001a, the anticipation of increasing punishment did not activate the nucleus accumbens (Knutson et al., 2001a). Nucleus accumbens activation correlated with individual differences in self-reported happiness elicited by the reward cues (Knutson et al., 2001a). On the other hand, Elliott and colleagues (2000) focused on the psychological context of a winning or losing streak. They demonstrated that brain activities in the bilateral globus pallidus, thalamus, and subgenual cingulate are associated with rewards in the context of winning streak. They also showed that responses to both rewards occurring as part of a winning streak and penalties as part of a losing streak are observed in the caudate, insula, and ventral prefrontal cortex. This is consistent with the findings that the medial orbitofrontal and ventromedial prefrontal cortices are involved in the representation of rewards and risk Bechara et al., 1994, Bechara et al., 1996, Bechara et al., 1997, Rolls et al., 1994.

Taking these results into account, a prior emotional experience with streaks of rewards/penalties appears to shape the subjective “feeling” of an incoming expected reward/penalty or an unexpected one for that matter. Moreover, there seems to be dissociable neural responses that are dependent on the psychological context in which abstract rewards and penalties are received in the human brain. Therefore, based on the study by Elliott et al., we would like to determine the relationship between subjective feelings and the context of winning/losing streaks and how these context are expressed in the human brain. In this experiment, an event-related fMRI technique was used to assess neural responses to financial reward and penalty during a gambling task whose paradigm was based on the study by Elliott and Critchely (Critchley et al., 2000). Our aim is to determine whether subjective feelings and brain activities are dependent on the unique context of an event sequence, that is, four wins in a row, four losses in a row, a win following four losses in a row, or a loss following four wins in a row. On the basis of previous studies, we hypothesize that:

  • 1.

    The medial prefrontal cortex is activated by risk-tasking and emotionally salient events, such as the context of a winning or losing streak.

  • 2.

    The lateral prefrontal cortex is activated by the discrepancy between the expectancy and the outcome of rewards/penalties, such as the context of switching from a winning or losing streak to the opposite event.

Section snippets

Subjects

Thirty-six healthy volunteers (19 men and 17 women), whose mean age was 20.8 years (SD = 2.98), participated in this study. All were native Japanese speakers and right-handed, as assessed by the Edinburgh Handedness Inventory. Subjects with a history of psychiatric, neurological, or other serious physical illnesses; drug or alcohol abuse; or second-degree relatives with a history of major psychiatric disorders were excluded.

Approval to carry out this experiment was obtained from Ethics

Subjects' ratings

Two-way ANOVA (analysis of variance) and post hoc Tukey's tests were performed. Examination of the subjects' self-reported ratings indicated that W4 was a significantly more pleasant/happier event than W1 (mean ± SD, W1, 1.58 ± 0.87; W4, 4.5 ± 0.78, P < 0.000001), and L4 was a significantly more unpleasant/unhappier event than L1 (mean ± SD, L1, −1.28 ± 1.03; L4, −4.17 ± 1.36, P < 0.000001) (Fig. 2).

However, there was no significant difference between W1 and SW (mean ± SD, L1, 1.58 ± 0.87; SW,

Discussion

In this study, using a simple gambling task, we demonstrated brain activities associated with the event-sequence context in which abstract reward or penalty is received.

The most significant findings in our study are as follows:

  • 1.

    The magnitude of each reward or penalty was the same across the whole events; however, psychological data demonstrated that subjective emotional experiences are different because of the context in which reward or penalty is received, that is, the sequence of each

Conclusion

In conclusion, we demonstrated that there exist brain activities associated with the event-sequence context in which abstract reward or penalty is received. Our data also suggest that information regarding this context is dissociably represented in the human brain, regardless of the nature of event (i.e., reward-related or penalty-related). The anterior cingulate cortex, the medial aspect of the prefrontal cortex, and the right dorsolateral prefrontal cortex appear to have an important role in

Acknowledgements

We thank Y. Satoh, O. Imaizumi, and A. Nosaka for support in fMRI data acquisition and K. Satoh, A. Harada, M. Fujikawa, M. Kubota, F. Hashimoto, and T. Satoh for help in data analysis. This study was supported by JST/RISTEX, R&D promotion scheme for regional proposals promoted by TAO, a Grant-Aid for Scientific Research on Priority areas (C)–Advanced Brain Science Project–from MEXT, and the 21st Century Center of Excellence (COE) Program (Ministry of Education, Culture, Sports, Science and

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