Elsevier

NeuroImage

Volume 50, Issue 2, 1 April 2010, Pages 709-716
NeuroImage

The impact of prior risk experiences on subsequent risky decision-making: The role of the insula

https://doi.org/10.1016/j.neuroimage.2009.12.097Get rights and content

Abstract

Risky decision-making is significantly affected by homeostatic states associated with different prior risk experiences, yet the neural mechanisms have not been well understood. Using functional MRI, we examined how gambling decisions and their underlying neural responses were modulated by prior risk experiences, with a focus on the insular cortex since it has been implicated in interoception, emotion and risky decision-making. Fourteen healthy young participants were scanned while performing a gambling task that was designed to simulate daily-life risk taking. Prior risk experience was manipulated by presenting participants with gambles that they were very likely to accept or gambles that they were unlikely to accept. A probe gamble, which was sensitive to individual's risk preference, was presented to examine the effect of prior risk experiences (Risk vs. Norisk) on subsequent risky decisions. Compared to passing on a gamble (Norisk), taking a gamble, especially winning a gamble (Riskwin), was associated with significantly stronger activation in the insular and dorsal medial prefrontal cortices. Decision making after Norisk was more risky and more likely to recruit activation of the insular and anterior cingulate cortices. This insular activity during decision making predicted the extent of risky decisions both within- and across-subjects, and was also correlated with an individual's personality trait of urgency. These findings suggest that the insula plays an important role in activating representations of homeostatic states associated with the experience of risk, which in turn exerts an influence on subsequent decisions.

Introduction

Cumulative evidence has suggested that risky decision-making not only involves cognitive evaluation of reward and risk, but is also modulated by homeostatic signals (Loewenstein et al., 2001, Paulus, 2007). For example, risky decision-making, such as gambling, engenders strong subjective excitement or arousal (Boyd, 1976), which is associated with strong physiological changes in heart rate, blood pressure, electromyogram, cortisol level, skin temperature, and skin conductance response (see Goudriaan et al., 2004 for review). Some form of arousal or excitement is a strong reinforcer of gambling behavior (Anderson and Brown, 1984), and the size of the observed interoceptive increase can explain both normal/regular and pathological gambling (Brown, 1986, Sharpe et al., 1995). Higher arousal is associated with greater persistence (Dickerson and Adcock, 1987) and more withdrawal symptoms when trying to abstain (Wray and Dickerson, 1981).

Convergent evidence from electrophysiology, neuroanatomy, and clinical studies has ascribed a role for the insula in providing interoceptive signals, including those related to pain, temperature, taste and visceral sensation (Craig, 2002, Craig, 2003). On that basis, it has been suggested that the insula contains the fundamental substrates for human awareness of homeostatic states (Craig, 2009). By working together with other brain regions, the insula can trigger bodily states, map bodily states, and represent the relationship between changes in the bodily states and the objects that elicited them (Bechara and Damasio, 2005). The insular cortex contains Von Economo neurons (VENs) that are abundant with Dopamine D3 and Serotonin 2b receptors, and thus is especially suitable to make fast decisions regarding reward and punishment by integrating the “gut feelings” from the visceral organs (Allman et al., 2005). Mounting evidence has suggested that the insula plays an important role in signaling the awareness of the urge for drug addictions (Naqvi and Bechara, 2009).

These findings lead to the hypothesis that the insula is a key region that integrates interoceptive (i.e., bodily) states into conscious feelings that may be subjectively perceived as an urge. In the case of cigarette smoking, for example, such interoceptive signals mediated through the insula can interfere with the decision-making processes that help people resist the urge to smoke (Naqvi and Bechara, 2009). Consistently, the insula is also involved in other types of biological urges, including drug usage (Brody et al., 2002, Garavan et al., 2000; also see Naqvi and Bechara, 2009 for review; Pelchat et al., 2004, Wexler et al., 2001), excessive food consumption (Pelchat et al., 2004), and eye blinking (Lerner et al., 2009).

Considering that both drug use (Naqvi and Bechara, 2009) and gambling (Anderson and Brown, 1984) involve strong interoceptive responses, and that pathological gambling resembles drug addiction in several core respects (Potenza, 2006, Shaffer et al., 2004), one would expect that the insula is also involved in risky decision-making. Indeed, many neuroeconomic studies guided by economic models have found insular activation when subjects make risky decisions involving gains and losses and have implicated the insula in computing different decision parameters, such as monetary losses (Paulus et al., 2003), gains (Izuma et al., 2008) or both (Clark et al., 2009, Elliott et al., 2000), and decision uncertainties (e.g., risk) (Critchley et al., 2001, Preuschoff et al., 2008), as well as risk prediction-errors (Preuschoff et al., 2008). The question we aimed at addressing in the present study is whether the creation of an urge to make a bet or gamble would also engage mechanisms mediated through the insula, which can play a role in influencing decision-making processes that involve risks and rewards.

In the present study, we used functional magnetic resonance imaging (fMRI) and a simple gambling task simulating risky decision-making. By presenting subjects with gambles that they would be very likely to accept or gambles that they would be very likely to reject, we could manipulate the prior risk experiences and neural responses in regions representing homeostatic states, such as the insula. Probe gambles were then used to examine how prior risk experiences would affect their subsequent risky decision-making and the underlying neural mechanisms. Subjects' personal trait of urgency was also measured and correlated with their risk behaviors and insular activation, since this scale has been shown to be predictive of many addictive behaviors, including alcohol abuse (Fischer and Smith, 2008, Whiteside and Lynam, 2003), tobacco craving (Billieux et al., 2007), pathological gambling (Fischer and Smith, 2008), and compulsive buying (Billieux et al., 2008).

Section snippets

Subjects

Fourteen healthy adults participated in this study (7 males and 7 females, mean age of 23.8 years, ranging from 22 to 29). All subjects had normal or corrected-to-normal vision. They were free of neurological or psychiatric history and gave informed consent to the experimental procedure, which was approved by the University of Southern California Institutional Review Board.

The modified cups task

Fig. 1A depicts the Modified Cups Task (Levin et al., 2007) and the experimental design. In each gamble, a number of cups

Gambling decisions were modulated by previous risk experiences

Overall, the relatively young, healthy subjects in the present study were appropriately sensitive to changes in EV (risk rate: RA > FG > RD, F(2,26) = 70.05, p < 0.001). As we had expected, participants made risky choices on most of the RA trials (87%) and seldom risked on the RD trials (11%). No significant sex differences were found in the overall risk rate or in the risk rate for each type of gamble (All p > 0.25). Of particular interest to this study, we found that participants took significantly

Discussion

The centrality of interoceptive processes in addiction and gambling has led to a theoretical model that puts the insula as the key neural structure in decision-making involving reward and risk (Naqvi and Bechara, 2009). According to this model, the insula is a region that integrates interoceptive (i.e. bodily) states into conscious feelings and into decision-making processes that involve uncertain risk and reward. Specifically, the insula represents the interoceptive effects of emotional

Competing interest statement

The authors declare that they have no competing financial interests.

Acknowledgments

This research was supported by the following grants from the National Institute on Drug Abuse (NIDA): DA11779, DA12487, and DA16708, and by the National Science Foundation (NSF) Grant Nos. IIS 04-42586 and SES 03-50984. We wish to thank Dr. Jiancheng Zhuang for his help in fMRI data collection.

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