Functional activity related to risk anticipation during performance of the Iowa gambling task

Risk anticipation is an important cognitive/emotional component of decision making. The Iowa Gambling Task [Bechara, A., Damasio, A.R., Damasio, H., Anderson, S.W., 1994. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15], which is the most widely used “risk-anticipation task” in clinical studies, has been demonstrated to be sensitive to lesions involving the ventromedial prefrontal cortex or amygdala. However, the critical neural circuitry involved in this complex task has not yet been fully clarified even in healthy subjects. Using a 3-T scanner, we performed an event-related functional magnetic resonance imaging study in 14 healthy subjects performing the task. The statistical parametric mapping showed that the risk anticipation component (risky decisions minus safe decisions) exclusively activated the medial frontal gyrus. Furthermore, we found a significant interindividual correlation between the task performance and the magnitude of brain activity during risky decisions. These results indicate that the Iowa Gambling Task does recruit the neural circuitry that is critical in decision making under uncertainty, particularly when subjects perceive the risk of their decision.

Introduction

Making advantageous decisions by weighing differently on their risks and benefits based upon previous experiences is an important ability for survival; however, this process would rely not only on cognitive but also on emotional substrates. The Iowa Gambling Task (IGT) was developed to simulate real-life financial decisions (Bechara et al., 1994). In contrast to other tasks in which all necessary information is available for making each decision (e.g., Elliott et al., 1999, Paulus et al., 2001, Rogers et al., 1999), the IGT is based on a long exploratory learning process to evaluate long-term risk anticipation in decision making. Moreover, IGT performance is strongly influenced by emotional factors related to rewards and penalties. As a result of these unique properties, the IGT is considered invaluable in investigating various neuropsychiatric conditions (Bechara and Damasio, 2002, Bechara et al., 2001, Best et al., 2002, Blair et al., 2001, Cavedini et al., 2001, Cavedini et al., 2002, Grant et al., 2000, Mazas et al., 2001, Mintzer and Stitzer, 2002, Mitchell et al., 2002, Petry, 2001, van Honk et al., 2002).

Despite the above mentioned properties, the neural underpinning of the IGT has not yet been fully clarified. Poor performance of this task has been associated with lesions involving the ventromedial prefrontal cortex (Bechara et al., 1994, Bechara et al., 1996, Bechara et al., 1999) or amygdala (Bechara et al., 1999, Bechara et al., 2003). Recent lesion studies suggest the involvement of more extensive structures including the dorsolateral prefrontal cortex for the IGT (Clark et al., 2003, Manes et al., 2002). Evidence from neuroimaging studies is limited. Using positron emission tomography (PET), Ernst et al. (2002) demonstrated widespread activations including the orbitofrontal, dorsolateral, prefrontal, and anterior cingulate cortices in healthy subjects. However, PET evaluates the summation of brain activity over a period of time (typically >1 min), during which the IGT requires multiple cognitive components (e.g., working memory) and should elicit complex emotional reactions. Hence, the most important component of the IGT, namely, anticipation of the long-term consequences associated with risky decision making (Bechara et al., 1996), may not be appropriately highlighted by PET.

In the present experiment, an event-related functional magnetic resonance imaging (fMRI) was used to assess neural responses to risk anticipation during the Iowa Gambling Task. We hypothesized that (1) specific regions of the prefrontal cortex would show increased activation during risky decision making, and (2) neural activity in these regions would correlate with the task performance.