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Department of Computer Science, University of Hull, U.K.. Abstract. The Iowa Gambling Task (IGT) is widely used to assess decision making under conditions of ...
Working Memory Involvement in Emotion-Based Processes Underlying Choosing Advantageously Anna Pecchinenda,1 Michael Dretsch,1 and Paul Chapman2 1

Department of Psychology, University of Hull, U.K. Department of Computer Science, University of Hull, U.K.

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Abstract. The Iowa Gambling Task (IGT) is widely used to assess decision making under conditions of uncertainty in clinical as well as in nonclinical populations. However, there is still debate as to whether normal performance at this task relies on implicit, emotion-based processes that are independent of working memory. To clarify the role of working memory on normal performance on the IGT, participants performed the task under low or high working memory load. We used a modified version of the original task, in which the position of the four decks was randomized between trials. Results showed that only participants performing under low memory load significantly chose more advantageously halfway through the task. In addition, when comparing the number of cards chosen from the two decks with frequent losses, one advantageous and one disadvantageous, only participants performing under low memory load chose more cards from the advantageous deck. The present findings indicate that the processes underlying optimal advantageous performance on the IGT rely on working memory functions. Keywords: Iowa Gambling Task, working memory, decision making

Since Bechara, Damasio, Damasio, and Andersen (1994) introduced the Iowa Gambling Task (IGT) to assess experimentally the decision-making impairment shown by patients who had suffered lesions to the ventromedial frontal lobes, this task has been widely used in a variety of studies with clinical and nonclinical populations. The IGT is based on complex schedules of rewards and punishments and allows studying human decision making under conditions of uncertainty of premises. More specifically, participants are presented with four decks of cards and are asked to make a series of choices aimed at maximizing gains while minimizing losses. They are not informed that each deck is associated with a different schedule of rewards and punishments so that choosing from some decks gives higher immediate gains but even larger future penalties, resulting in loss of play money in the long run. In contrast, although choosing from other decks gives lower immediate gains and smaller future penalties, it results in gains of play money in the long run. The rationale is that by repeated experience of the specific reward and punishment contingencies associated with the outcomes of choosing from the four decks, participants learn which decks are good and which are bad (e.g., Bechara et al., 1994; Bechara, 2004). According to Bechara, Damasio, Tranel, and Damasio (2005), the mechanism underlying choosing advantageously on the IGT is an implicit automatic emotion-based learning that relies on the affective reactions to the consequences of a given choice rather than an explicit learning based on complex computations of cost-benefit ratios linked to the various options. That is, through repeated ex䉷 2006 Hogrefe & Huber Publishers

perience of the affective consequences associated with a given choice, participants develop a “feeling” or an “intuition” of what is good and what is bad, even though an explicit understanding of the complex contingencies may be unavailable. In addition, the development of these intuitions relies on the intact functioning of the ventromedial prefrontal cortex involved in processing the emotional signals used in decision making under uncertainty. The typical finding obtained using the IGT is that normal performance consists of an initial sampling of the four decks. However, halfway through the task (i.e., between trials 41 and 60), participants develop a choice preference for the advantageous decks (or a dislike for the disadvantageous ones), which precedes the explicit knowledge of the gain/loss contingencies that characterize each deck. In contrast, patients with lesions to the ventromedial frontal lobes do not acquire these preferences, and their performance is impaired as they continue to make more choices from the decks that are disadvantageous in the long run (for a review, see Bechara, 2004; Bechara, et al., 2005; for a different viewpoint, see Maia & McClelland, 2004; Bowman, Evans, & Turnbull, 2005). Additional evidence that normal performance on the IGT relies on the intact functioning of the ventromedial prefrontal cortex comes from studies conducted with different populations. Findings show poor IGT performance in individuals with reduced white matter in prefrontal cortex regions, such as in individuals with substance addictions (e.g., Bechara & Damasio, 2002; Bechara, Dolan, & Hindes, 2002) or with psychopathy (e.g., Grant, Contoreggi, & London, 2000). Similarly, differences in advanExperimental Psychology 2006; Vol. 53(3):191–197 DOI 10.1027/1618-3169.53.3.191

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tageous decision making have been linked to developmental changes in prefrontal functions, and poor performance on the IGT has been observed in adolescents (e.g., Overman, Frassrand, Ansel, Trawalter, Bies, & Redmond, 2004) and in older individuals (e.g., Denburg, Tranel, & Bechara, 2005). In spite of the wide body of evidence gathered using this task, the issue of whether advantageous performance on the IGT relies on purely emotion-based processes or whether other cognitive factors may also play a role is still the subject of debate. This is in part due to the fact that the IGT is a complex task that requires inhibiting response tendencies toward immediate gains but delayed losses; it involves reversal learning as well as holding online information of the outcomes of past choices and of which decks are associated with gains and losses (for a recent discussion, see Maia & McClelland, 2005; Bechara et al., 2005). Even though Bechara and collaborators have shown an asymmetrical dissociation between memory functions and advantageous performance on the IGT (e.g., Bechara, Damasio, Tranel, & Anderson, 1998; Bechara et al., 2005), recent empirical evidence offers a rather unclear picture, leading some authors to argue that normal performance at this task depends on working memory and central executive functions. More specifically, Fellows and Farah (2005) have recently shown that the abnormal performance on the IGT observed in patients with lesions to the ventromedial prefrontal cortex is due to impairment in executive functions underlying reversal learning. They argued that because in the original IGT the four decks occupy fixed positions and the sequence of cards is constant within each deck, an initial preference toward the disadvantageous decks develops because mostly gains are encountered during the first 10 choices, and disadvantageous decks have higher gains. Indeed, by using the original and a variant of the IGT, in which the sequence of cards was reshuffled, they found that disadvantageous decision making in patients with lesions to the ventromedial prefrontal cortex occurred only with the original IGT but not with the reshuffled version. In addition, Hinson and collaborators (e.g., Hinson, Jameson, & Whitney, 2002, 2003; Jameson, Hinson, & Whitney, 2004) have argued that working memory functions may play a role in normal performance on the IGT. In a series of studies, they used an ad hoc card-task similar to the IGT, although it was designed to be more challenging in that of the four decks, one had small gains and even smaller losses; one was neutral; and two were bad decks. Therefore, the difference in the ratio of gains/losses between decks was more subtle than in the original IGT. Participants performed the card-task together with secondary tasks that loaded working memory (e.g., digit maintenance) or specific components of working memory, such as the central executive (e.g., random numbers generation) or the verbal buffer (e.g., articulatory suppression). Findings showed that participants made more disadvantageous choices when the secondary task loaded working memory and the central executive, but not when it loaded the verbal buffer. In contrast, Busemeyer and Stout (2002), have analyzed Experimental Psychology 2006; Vol. 53(3):191–197

whether the source of abnormal performance on the IGT is cognitive, emotional-motivational, or linked to response processes. In line with the findings provided by Bechara and collaborators (2000, 2005), they found that whereas the abnormal performance of patients with Huntington’s disease—who show learning impairments and progressive dementia—is due to memory and learning deficits, that of cocaine abusers—who show myopic behavior and disadvantageous decision making similar to that of patients with ventromedial lesions—is due to emotional and choice-consistency factors (Stout, Busemeyer, Lin, Grant, & Bonson, 2004). Finally, in a recent study, Turnbull, Evans, Bunce, Carzolio, and O’Connor (2005) have argued that if the emotion-based processes underlying normal performance on the IGT are automatic, then they should be independent of processing resources. In their study, participants performed the original IGT, either without any secondary tasks or with a secondary task that loaded the central executive (e.g., random number generation) or the verbal buffer of working memory (e.g., articulatory suppression). Results showed normal performance on the IGT regardless of the type of secondary task. Whereas these findings indicate that performance at this task relies on implicit, emotional-based learning that is independent of working memory functions, and as such are in line with the findings reported by Busemeyer and collaborators (2002; Stout et al., 2004), they are clearly at odds with the findings reported by Fellows and Farah (2005) and by Hinson and collaborators (Hinson, et al., 2002, 2003; Jameson et al., 2004). However, some important points need to be considered that may explain this pattern of results. Firstly, Hinson and collaborators (Hinson, et al., 2002, 2003; Jameson, et al., 2004) used a cardtask that differed in various aspects from the original IGT; whereas Turnbull et al. (2005) and Fellows and Farah (2005) used the original IGT. Therefore, one could argue that differences in the tasks used, such as reducing the difference in the ratio of gains and losses between some decks, may explain the different findings. Secondly, in all the above studies, the position of the four decks was fixed, although in Fellows and Farah’s study (2005), the sequence of cards within each deck was shuffled. This would allow participants to use different strategies to perform the task, such as maintaining online information of the spatial position of the decks, which would rely on working memory functions. It becomes evident then that a clear test of whether normal performance on the IGT relies on processes that are independent of working memory functions can be obtained by randomizing the spatial location of the four decks throughout the task and loading working memory. The present study used this strategy as we assessed participants’ performance at a modified version of the IGT under working memory load. The rationale being that by removing the fixed spatial position of the four decks throughout the task and by maintaining all the other characteristics of the original task (i.e., number of choices, ratios of gains and losses associated with each deck, etc.), if the mechanism underlying normal performance on the IGT 䉷 2006 Hogrefe & Huber Publishers

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is implicit learning of what is good or bad, then loading working memory with a secondary task should not affect participants’ performance. In addition, because the four decks vary with regard to the frequency of occurrence of negative events (i.e., Decks A and C have frequent penalties, with 5 penalties over 10 trials;, whereas Decks B and D have infrequent penalties, with 1 penalty over 10 trials), working memory load could affect participants’ ability to maintain online information of the costs and benefits associated with choosing a card from a given deck (for instance, if participants maintained a rough running average of the gains for each deck). Obviously, such a possibility would be less detrimental for the two decks with infrequent penalties, because there are fewer and therefore more distinctive events to take into account over 20 trials (i.e., the 2 big penalties per block). Therefore, we assessed whether working memory load affects the capacity to retain online information about multiple events such as frequent penalties. We compared participants’ performance on the two decks that share a schedule of frequent losses (Decks A and C), although Deck A is disadvantageous (i.e., the losses outweigh the wins), whereas deck C is advantageous in the long run. If the process underlying normal performance on the IGT does not depend on working memory resources to retain information about multiple events, then high and low memory load should affect participants’ choices from these two decks in similar ways.

Method Participants Sixty-eight undergraduates (40 women and 18 men; age: M ⳱ 20.7; SD ⳱ 3.8) were randomly assigned to performing the IGT under low (N ⳱ 34) or high memory load conditions.

Materials and Procedure The study employed a dual-task procedure in which the modified version of the computerized IGT (Bechara, Damasio, Damasio, & Andersen, 1994; Bechara, 1997) and a memory task were combined. For the modified IGT, the spatial position of the four decks was randomized across trials while all other characteristics were kept constant (i.e., appearance, decks’ labels, schedule of gains/losses, etc.). As in the original computerized version of the IGT, participants were presented with four decks of cards (labeled A, B, C, and D) on the computer monitor and were given a loan of £2,000 of play money. They were asked to accumulate as much play money as possible by choosing cards from any of the four decks, using the computer mouse. Participants were informed that whereas the position of the decks would change after each card-choice, the sequence of cards within each deck and the label of each deck would remain constant throughout the task. More specifically, whereas the four spatial locations occupied by the decks were as in the original version of the computerized IGT 䉷 2006 Hogrefe & Huber Publishers

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task, each deck of cards appeared an equal number of times in each of the four possible spatial locations. A trial started with the four decks presented on screen, one adjacent to the other (i.e., A B C D), and the message “pick a card” underneath the four decks. Immediately after a card had been selected from any of the four decks, the information concerning the reward was presented on screen (for 1,500 ms), followed—if applicable—by the information concerning the punishment (for 1,500 ms). This was followed by a screen showing the four decks occupying different spatial locations among the four possible (i.e., B D C A) and the message “please wait” underneath the four decks (for 5,000 ms). Finally, a new trial started when the message “pick a card” appeared underneath the four decks presented on screen (see Figure 1). For the memory task, a memory set consisting of a series of four digits (from 1 to 5) was presented acoustically. Under low memory load, the sequence of digits (i.e., the memory set) was numerical (i.e., 1 2 3 4 5); whereas under high memory load, the sequence of digits was random (i.e., 3 1 4 5 2). Participants were required to retain the memory set until a probe consisting of a single digit from the original memory set was presented (i.e., 4). The participant’s task was to verbally report the digit following the probe in the original memory set (i.e., in the example above, 2 is the correct answer for the random sequence, and 5 for the numerical sequence). This task has been successfully used to load working memory in past research (e.g., de Fockert, Rees, Frith, & Lavie, 2001; Jameson et al., 2004; Lavie, Hirst, de Fockert, & Viding, 2004), as performance on the low memory load task is known to require very few working memory resources given that only the information that the memory set is in numerical order needs to be maintained. In contrast, performance on the high memory load task depends heavily on working memory resources because the entire sequence of digits of the memory set needs to be maintained. In addition, to make sure that low memory load is really low, working memory load is manipulated between-subjects rather than using intermixed trials within-subjects. A total of 25 memory sets was presented after a variable number of card choices on the IGT, 5 memory sets in each block of 20 trials of the IGT.

Data Reduction and Analyses As in previous studies, participants’ performance on the IGT was quantified by dividing the 100 trials in five blocks of 20 trials each. The number of cards selected from each of the four decks over 20 consecutive trials was then computed. A net performance score was obtained for each participant by subtracting the number of cards selected from the advantageous decks (C and D) from the number of cards selected from the disadvantageous ones (A and B) for each individual block. A negative score indicates more disadvantageous choices, whereas a positive score indicates more advantageous choices. For the memory task, the correct number of responses was computed for each of the five blocks of the IGT. Data were first analyzed using a 2 (Memory Load: Low Experimental Psychology 2006; Vol. 53(3):191–197

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Figure 1. Schematic diagram representing the sequence of events during the modified version of the computerized Iowa Gambling Task (IGT).

vs. High) by 5 (Blocks) mixed-factorial ANOVA, with Memory Load as the between-subjects factor. In addition, to assess the impact of frequent losses on participants’ performance under memory load, data were further analyzed using a 2 by 5 by 2 mixed-factorial ANOVA, with Memory Load as the between-subject factor, and Block and Decks (Decks A and C) as the within-subject factors. The two decks considered share the characteristic of having the same number of losses over 10 trials, although one is advantageous (Deck C), whereas the other is disadvantageous (Deck A) in the long run. Experimental Psychology 2006; Vol. 53(3):191–197

Results Memory Load Manipulation Results showed a significant main effect of Memory Load, F(1, 66) ⳱ 51.14, MSE ⳱ 1.33, p ⳱ .000. Participants reported less correct responses under High Memory Load (M ⳱ 4.11, SE ⳱ .09) than under Low Memory Load (M ⳱ 5.00, SE ⳱ .09). The effect of Blocks, F(4, 264) ⳱ 1.65, ns, and the interaction was not significant, F(4, 264) ⳱ 1.67, ns. 䉷 2006 Hogrefe & Huber Publishers

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Net Performance on Modified IGT Overall, participants under High Memory Load chose more disadvantageously (M ⳱ ⳮ2.31) than participants under Low Memory Load (M ⳱ 1.05), F(1, 66) ⳱ 12.5, MSE ⳱ 77.06, p ⳱ .001. The main effect of Block was significant, F(4, 264) ⳱ 9.06, MSE ⳱ 45.59, p ⳱ .000. Because performance on the original IGT normally improves over blocks obeying a linear relationship (i.e., less disadvantageous and/or more advantageous choices over blocks), a linear trend is expected. Indeed, overall a significant linear trend was observed, F(1, 66) ⳱ 19.48, p ⳱ .000. The two-way interaction did not reach statistical significance, F(4, 264) ⬍ 1.5, ns. However, when testing whether participants’ performance on each block was significantly different from zero (i.e., whether participants significantly chose more advantageously or less disadvantageously), only participants under Low Memory Load chose more advantageously on Block 3 (M ⳱ 1.08), t(33) ⳱ 2.47, p ⳱ .019]; Block 4 (M ⳱ 3.47), t(33) ⳱ 2.58, p ⳱ .014; and Block 5 (M ⳱ 4.41), t(33) ⳱ 3.14, p ⳱ .004. In contrast, participants under High Memory Load did not start to chose more advantageously from Block 3 onward, t’s(33) ⬍ 1, ns (see Figure 2).

Number of Cards Selected From Decks A and C Overall, participants under High Memory Load chose more cards from these two decks (M ⳱ 4.37) than participants under Low Memory Load (M ⳱ 3.54), F(1, 66) ⳱ 10.99,

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MSE ⳱ 5.21, p ⳱ .001. This main effect was qualified by a significant Memory Load by Deck interaction, F(1, 66) ⳱ 11.83, MSE ⳱ 12.18, p ⳱ .001 (see Figure 3), indicating that whereas participants performing under Low Memory Load chose more cards from the advantageous deck than from the disadvantageous one, t(33) ⳱ 3.42, p ⳱ .002, this was not the case for participants performing under High Memory Load, t(33) ⳱ 1.68, ns. This resulted in a significant difference in the number of cards chosen from the disadvantageous deck between participants performing under High Memory Load (M ⳱ 4.72) and participants performing under Low Memory Load (M ⳱ 2.98), t(66) ⳱ 5.41, p ⳱ .000. The Deck by Block interaction was significant, F(4, 264) ⳱ 5.69, MSE ⳱ 6.39, p ⳱ .000. Follow-up analyses showed a significant linear trend for the disadvantageous deck, F(1, 66) ⳱ 19.12, p ⳱ .000, but not for the advantageous one, F(1, 66) ⬍ 1, ns. That is, regardless of memory load, participants progressively chose fewer cards from the disadvantageous deck over the five blocks. Finally, the three-way interaction did not reach statistical significance, F(4, 264) ⬍ 1, ns.

Performance Comparison With the Original IGT One could argue that changing the spatial location of the four decks between trials rather than working memory load could affect participants’ performance on the modified IGT. If this were the case, then participants performing the modified IGT under Low Memory Load should chose more

Figure 2. Mean net performance (and SE) on the Iowa Gambling Task (IGT) over the five blocks as a function of Memory Load. A negative score indicates more selections from the disadvantageous decks than from the advantageous ones. 䉷 2006 Hogrefe & Huber Publishers

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Figure 3. Mean number of cards (and SE) selected from the two decks with frequent penalties as a function of Memory Load. disadvantageously (or less advantageously) than participants performing the original IGT. To check for this possibility, we compared participants’ performance on the modified IGT with that of a group of participants (N ⳱ 24 undergraduate students; 6 men and 19 women, age M ⳱ 21.5, SD ⳱ 3.0) who had performed the original computerized IGT in a separate study conducted in our laboratory. Participants’ performance on the original IGT showed a significant linear trend over the five blocks, F(1, 24) ⳱ 13.82, MSE ⳱ 66.14, p ⳱ .001, indicating that they progressively chose more advantageously. In line with findings reported in the literature, participants made more advantageous choices on Block 3 (M ⳱ 2.72, SD ⳱ .83) than on Block 2 (M ⳱ .32, SD ⳱ 1.4), t(24) ⳱ 2.05, p ⳱ .05. Considering that in both studies participants started to choose more advantageously from Block 3 onward, we compared the net score of participants performing the modified IGT under Low and High Memory Load on Block 3 with that of participants performing the original IGT. Results showed no significant difference between the net scores of participants performing the modified IGT under Low Memory Load (M ⳱ 1.08, SE ⳱ .44) and the net scores of participants performing the original IGT, t(57) ⳱ 1.86, ns. In contrast, the net score of participants performing the modified IGT under High Memory Load was significantly lower (M ⳱ ⳮ.79, SE ⳱ .61) than that of participants performing the original IGT, t(57) ⳱ 3.49, p ⳱ .001.

Discussion The present study investigated whether normal or optimal performance on the IGT relies on working memory functions. To this aim, participants performed a modified version of the IGT, which was in all respects like the original task, except that the spatial location of the four decks was randomized across trials, under either low or high working memory load. Consistent with past findings from nonclinical populations, participants in both working memory load conditions showed learning throughout the task as they progressively made fewer disadvantageous choices. However, only parExperimental Psychology 2006; Vol. 53(3):191–197

ticipants performing the task under low working memory load chose more advantageously from Block 3 onward; whereas, participants performing under high working memory load never started to consistently choose advantageously. Therefore, the present findings show that indeed optimal performance on the IGT relies on working memory functions. As such, they are in line with past findings (e.g., Hinson et al., 2003; Jameson et al., 2004; Fellows et al., 2005) showing an involvement of working memory functions in performing complex tasks, such as the IGT and its variants, which require pondering over different alternatives under conditions of uncertainty of premises. In contrast, the present findings are at odds with those reported by Turnbull et al. (2005) that show no effects of memory load on IGT performance. An interesting question is whether the lack of an effect of the secondary task on IGT performance in their study is due to the nature of the secondary task used. For instance, if participants could perform the random numbers generation task and the articulatory suppression task at their own pace, they could have slowed down at the secondary task whenever the IGT required more working memory resources. If this were the case, then the lack of an effect of memory load could be due to task switching and memory load not being constant throughout the IGT task. In the present study, it was not possible to adopt such a strategy, because to make sure that they maintained the memory set presented in the secondary task throughout the various phases of the IGT, the memory probes were presented after a variable number of card selections. This made the memory probe presentation somewhat unpredictable and, therefore, assured memory load was constant during the various stages of the IGT. Because the modified version of the IGT used in the present study was in all aspects similar to the original, except for the randomized spatial location of the four decks, the present findings cannot be explained by differences in the level of difficulty between the present version of the task and the original one. In fact, an obvious effect of increased task difficulty is a slower learning trend of what is good and what is bad. Instead, in the present study participants performing under low memory load started to choose advantageously from Block 3 onward, which is consistent with findings reported in the literature using the original IGT. In addition, a direct comparison of the net scores obtained on Block 3 by participants playing the modified IGT under low memory load with those obtained by participants playing the original IGT showed no statistically reliable differences. Therefore, the present findings cannot be explained by increased task difficulty due to changing the spatial location of the four decks between trials. Furthermore, because the spatial location of the four decks was not fixed, the fact that memory load manipulation affected participants performance cannot be explained by participants relying on memory functions to maintain online information of the spatial location of the decks. Similarly, an explanation calling on the involvement of executive functions underlying reversal learning processes is less likely. Finally, as the four decks vary with regard to the frequency of occurrence of losses, one could argue that work䉷 2006 Hogrefe & Huber Publishers

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ing memory load affects participants’ ability to maintain online information about the relative goodness/badness of each deck, for instance if participants were keeping a rough running average of the costs/benefits associated with choosing a card from each deck. If this were the case, then participants under high memory load would be less able to discriminate between the good and the bad deck when the two decks share frequent losses. Indeed, participants under high memory load did not differentiate between the two decks with frequent losses; whereas participants performing under low memory load did so and chose more cards from the advantageous deck. Hence, this finding suggests that possibly because of the complex schedules of gains and losses, the implicit learning of what is good and bad underlying normal or, as in the case of the present findings, optimal performance on the IGT relies on working memory resources to retain information about multiple events associated with the various decks. The present findings are particularly important in the context of the recent debate on whether the implicit learning of what is good and bad as assessed by the IGT is independent of working memory functions, as they show that optimal performance on the IGT is disrupted by working memory load. Acknowledgments The present study was part of the second author’s work for the MPhil course.

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Anna Pecchinenda Department of Psychology University of Hull Hull HU6 7RX UK E-mail [email protected]

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