The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers

A recent study by Maia and McClelland on participants’ knowledge in the Iowa Gambling Task suggests a different interpretation for an experiment we reported in 1997. The authors use their results to question the evidence for the somatic marker hypothesis. Here we consider whether the authors’ conclusions are justified. Maia and McClelland [1] recently repeated part of our 1997 experiment [2] (in normal participants but not in patients) and without the skin conductance response component (see Box 1) in two conditions: one used precisely our method of questioning and replicated our results; another used more probing questioning and revealed that most participants have considerable knowledge of the situation. On this basis, and using selected supporting findings from the literature, they question the evidence for the somatic marker hypothesis (SMH). The significance of Maia and McClelland’s study is twofold: first, it undermines traditional methods for identifyng implicit knowledge, that is, simply asking individuals to declare what they know about a given situation; second, it demonstrates yet again that even in normal participants, adequate knowledge of a situation does not guarantee correct decisions. Maia and McClelland’s study provides fascinating results relevant to any discussion of our 1997 findings (Box 1), but we do not believe they undermine the SMH. Maia and McClelland focus on the amount of conscious knowledge of the situation participants have, whereas the SMH focuses on the presence or absence of an emotionrelated signal, conscious or not, independently of the conscious knowledge of the situation. For example, we have shown that patients whose knowledge of a situation is conscious and adequate can decide quite deficiently [3]. We hypothesize that they do so because an emotionrelated signal, the SM (conscious or not) is missing. The central feature of the SMH is not that non-conscious biases accomplish decisions in the absence of conscious knowledge of a situation, but rather that emotion-related signals assist cognitive processes even when they are non-conscious. It is not clear why a different interpretation for part of our 1997 study, which revolves around the amount of conscious knowledge of the situation available to the players, would undercut ‘one of the main pillars of support’ for the SMH. The main evidence for the SMH comes from neuropsychological studies of patients whose cognitive intelligence was largely intact but whose emotional reactions were impaired, and from experiments in which those patients failed to show emotional reactions to the implied content of social stimuli [4]. The development of the Iowa Gambling Task (IGT) offered further experimental support for the SMH, in ours [2] as well as in others’ hands (e.g. [5–9]). However, the IGT was not the basis for the SMH, let alone was the SMH developed to account for the IGT results, as is surprisingly stated in an editorial following Maia and McClelland’s report [10]. Reversal learning Maia and McClelland suggest that the difficulties of patients with ventromedial prefrontal cortex (VMPC) damage in IGT performance can be explained by an inability to reverse a learned contingency that such patients sometimes exhibit [11]. Learning to reverse a contingency involves inhibition of a previously rewarded response and shifting to a newly rewarded response. Although some VMPC patients have problems with contingency reversal (e.g. those with posterior orbital lesions, as we [12,13] and others have noted [14]), this is not incompatible with the SMH because the difficulty is itself accounted for by the SMH. In order for contingency reversals to occur, a signal is required (a ‘stop’ signal); we have argued that such a signal is emotive, in other words, a somatic marker [15,16]. Moreover, the brain regions associated with reversal learning are the same as those associated with emotional processing, including the VMPC, as shown by Rolls [17]. In short, inhibiting the response is in itself a ‘decision’, albeit at a lower level of processing than the decisions carried out in the IGT. The IGT contains elements of contingency-reversal learning, but at a more complicated level than other tasks used to investigate the phenomenon [18]. Patients who fail contingency-reversal decisions measured by simpler tasks are likely to fail the IGT; however, VMPC patients who perform well in those tasks or in probabilistic reversal learning [18], may or may not fail the IGT. It is of note that normal performance in the Wisconsin Card Sorting Task requires contingencyreversal learning and many VMPC patients perform excellently in this task [3,19]. A behaviorist account in terms of adaptation to contingency reversals does not explain why patients who conceptualize the IGT consciously fail to play advantageously. Besides, VMPC patients do switch away from the Corresponding author: Bechara, A. (). Update TRENDS in Cognitive Sciences Vol.9 No.4 April 2005 bad decks when they are faced with a loss, in the same way that normal participants do, although the patients return to those decks sooner and more often than normal participants. Stout analyzed the results of VMPC patients with an ‘expectancy-valence’ model [20,21], and concluded that their choices are guided by the most recent outcome rather than by outcomes of all past trials, showing that strategy reversal is a common immediate response by these patients. Another issue raised by Maia and McClelland is that IGT impairments appear not only in VMPC patients but also in patients with dorsolateral prefrontal cortex (DLPC) lesions, so the impairments are therefore not specific to VMPC damage [14]. We entirely agree. DLPC patients have defects in working memory and other cognitive processes, which ought to impair IGT performance, albeit for different reasons. Fellows and Farah [14], and Manes and colleagues [22], have demonstrated this, as have we [23,24]. Knowledge of the situation does not guarantee advantageous decisions Maia and McClelland state that the ‘question of precisely why VMPC patients can report the changes in contingencies but perseverate in their behavior is a fascinating one that remains to be fully addressed.’ The SMH addresses this question, by proposing that pure cognitive processes unassisted by emotional signals do not guarantee normal behavior in the face of adequate knowledge. Cognitive processing assisted by emotion-related marker signals, conscious or not, contributes to the proper action being taken. Again, the central issue is the relation to emotion and not the presence or absence of conscious knowledge of the situation. The anticipatory skin conductance responses (SCRs) to the bad decks began to occur in our study at a point at which Maia and McClelland do not claim the presence of ‘adequate knowledge’, only ‘minimal knowledge’ or, in our terminology ‘a hunch’. Maia and McClelland have attempted to dismiss the SCR evidence by suggesting that psychophysiological responses are caused by conscious knowledge of the situation. We disagree, based on the early appearance of anticipatory SCRs for the bad decks in the IGT, and on the time window in which the SCRs become manifest. How do Maia and McClelland explain the uniformly low anticipatory SCRs in the VMPC patients for both decks? If the patients knew what the correct response should be, and anticipatory SCRs are the result of such knowledge, why would they not produce SCRs? If an impairment in reversal learning were Box 1. The somatic marker hypothesis and the Iowa Gambling Task The somatic marker hypothesis (SMH) was developed to address the problems of decision-making encountered in patients with certain kinds of prefrontal damage and with compromised emo