Elsevier

Neuropsychologia

Volume 47, Issue 1, January 2009, Pages 50-58
Neuropsychologia

Decision making in patients with temporal lobe epilepsy

https://doi.org/10.1016/j.neuropsychologia.2008.08.014Get rights and content

Abstract

The mesiotemporal lobe is involved in decision making processes because bilateral amygdala damage can cause impairments in decision making that is mainly based on the processing of emotional feedback. In addition to executive functions, previous studies have suggested the involvement of feedback processing in decision making under risk when explicit information about consequences and their probabilities is provided. In the current study, we investigated whether unilateral mesiotemporal damage, comprising of the hippocampus and/or the amygdala, results in alterations of both kinds of decision making. For this purpose, we preoperatively examined 20 patients with refractory unilateral mesiotemporal lobe epilepsy (TLE) and a comparison group (CG) of 20 healthy volunteers with the Iowa Gambling Task to assess decision making based on feedback processing, the Game of Dice Task to assess decision making under risk, and with a neuropsychological test battery. Results indicate that TLE patients performed normally in decision making under risk, but can exhibit disturbances in decision making on the Iowa Gambling Task. A subgroup analysis revealed that those patients with a preference for the disadvantageous alternatives performed worse on executive subcomponents and had seizure onset at an earlier age in comparison to the patient subgroup without disadvantageous decision making. Furthermore, disadvantageous decision making can emerge in patients with selective hippocampal sclerosis not extended to the amygdala. Thus, our results demonstrate for the first time that presurgical patients with TLE can have selective reductions in decision making and that these deficits can result from hippocampal lesions without structural amygdala abnormalities.

Introduction

Decision making is an everyday life function and disturbances of this ability can lead to severe problems in various scopes of life. To date, from a neuroscientific perspective, at least two types of decision making have been differentiated—most frequently termed decision making under ambiguity and decision making under risk (e.g. Bechara, 2004; Brand, Labudda, & Markowitsch, 2006). These types of decision making vary in terms of the degree of available information provided about consequences and their probabilities. In decision making situations in which consequences and their probabilities are implicit (often referred to as decision making under ambiguity or feedback-based decision making) the decision maker has to initially figure out the options’ qualities by processing feedback of previous decisions. The Iowa Gambling Task (IGT, Bechara, Damasio, Damasio, & Anderson, 1994; Bechara, Tranel, & Damasio, 2000) is a task most frequently used to assess decision making under these implicit conditions. In this task, subjects have to maximise a fictitious amount of money by successively choosing cards from four different card decks. After each card selection, subjects are awarded a sum of money; occasionally however, some selections lead to monetary losses. Subjects are unaware of the amount of cards they need to select and also which card decks are advantageous (i.e. leading to a positive outcome balance in the long run) or disadvantageous (i.e. leading to a negative outcome balance in the long run), respectively. Thus, subjects have to learn to avoid the disadvantageous options by processing emotional feedback, in terms of gains and losses, following their decisions. This type of decision making seems to particularly depend on the integrity of the medial frontal lobe as shown in numerous studies with neurological and psychiatric patients (e.g. Bark, Dieckmann, Bogerts, & Northoff, 2005; Bechara & Damasio, 2002; Bechara et al., 1994; Bechara & Martin, 2004; Bechara, Tranel, Damasio, & Damasio, 1996; Bolla et al., 2003; Cavedini, Riboldi, D’Annucci et al., 2002; Cavedini, Riboldi, Keller, D’Annucci, & Bellodi, 2002; Pagonabarraga et al., 2007; for an overview see Dunn, Dalgleish, & Lawrence, 2006) as well as in several neuroimaging studies (Bolla et al., 2003; Bolla, Eldreth, Matochik, & Cadet, 2005; Fukui, Murai, Fukuyama, Hayashi, & Hanakawa, 2005; Tanabe et al., 2007; Thiel et al., 2003). Furthermore, the amygdala was proposed as another key structure involved in decision making processes under implicit conditions. According to the somatic marker hypothesis, the amygdala is assumed to be essential for the generation of an automatic emotional state, e.g. in response to a gain/loss in the context of decision making (Damasio, Tranel, & Damasio, 1991). In a subsequent associative process – mainly dependent on the integrity of the medial prefrontal cortex – amygdala induced emotional responses are linked to different decision options. Based on the latter process, somatic markers (often described as a diffuse physiological arousal associated with a ‘hunch’ before the selection of an option) guides the decision making process, e.g. by leading to the avoidance of disadvantageous alternatives. Although the somatic marker hypothesis and its implications for the explanation of feedback-based decision making processes have been discussed controversially (see Hinson, Jameson, & Whitney, 2002; Jameson, Hinson, & Whitney, 2004; Maia & McClelland, 2004), the importance of the amygdala for this kind of decision making has been supported by some patient studies. For instance, Bechara, Damasio, Damasio, and Lee (1999) examined five patients with bilateral amygdala lesions with the IGT. These patients showed decision making impairments in the sense of a preference for the disadvantageous card decks. The results of a recent study by Brand, Grabenhorst, Starcke, Vandekerckhove, and Markowitsch (2007) also support the suggested role of the amygdala in decision making measured with the IGT. The authors studied three patients suffering from Urbach-Wiethe disease. This very rare syndrome leads to selective bilateral calcification within the amygdalae. In accordance with the results of Bechara et al. (1999), all patients had impaired decision making on the IGT which was associated with reduced anticipatory as well as feedback SCRs. Thus, bilateral amygdala pathology might hamper the generation of emotional reactions in response to task immanent reward and punishment and with that leading to a disturbance of the subsequent emotion-driven process of forming associations between options and their consequences.

In contrast to decision making with implicit probabilities, many real life decisions are made based on explicit information about the potential consequences of different options and their subsequent probabilities. This type of decision making is termed decision making under risk conditions. Brand et al. developed a task – the Game of Dice Task (GDT, Brand, Fujiwara et al., 2005) – to measure this type of decision making. In this task, subjects are asked to maximise a fictitious starting capital within 18 trials by guessing which number of a single die will be thrown by the computer. Subjects can choose among different options (i.e. single numbers or combinations of two, three or four numbers) to receive a certain amount of money when the number or one number of a combination chosen is thrown with the single die. Subjects lose the same amount of money when the number or any number of the combination chosen is not thrown. Some options are risky or disadvantageous because they have high potential gains/losses but low winning probabilities. Other options are non-risky or advantageous because of their lower potential gains/losses but higher winning probabilities. Based on several studies in which the GDT was used in various neurological and psychiatric patients (Brand, Franke-Sievert, Jacoby, Markowitsch, & Tuschen-Caffier, 2007; Brand, Fujiwara et al., 2005; Brand, Kalbe et al., 2005; Brand et al., 2004; Delazer, Sinz, Zamarian, & Benke, 2007; Drechsler, Rizzo, & Steinhausen, 2008; Labudda, Wolf, Markowitsch, & Brand, 2007; Lee et al., 2007), Brand et al. (2006) suggested that there might be two interacting routes that can guide decision making under risk: an emotional route, in which feedback in terms of gains and losses is processed, and a cognitive route, in which information about consequences and probabilities is integrated and utilised before a decision is made. In agreement with the assumed cognitive route, decision making under explicit conditions has been shown to correlate with executive functions, such as set-shifting, cognitive flexibility and categorisation (cf. studies cited above). The impact of executive functions is most likely due to the explicitness of given information that can be used to plan and modify decision making behaviour. In accordance with the neuropsychological results cited, we recently demonstrated that the deliberation phase in which subjects can integrate explicit information is associated with increased activation within brain structures, such as the lateral prefrontal cortex, the posterior parietal cortex and the anterior cingulate gyrus, which mainly underlie executive processes (Labudda et al., 2008). In correspondence with the proposed emotional route, decision making performance on the GDT is correlated with the use of feedback. Subjects who use negative feedback, in terms of losses, to modify their decision making, appear to select the disadvantageous alternatives less frequently than those who ignored receiving losses (Brand, 2008; Brand, Kalbe et al., 2005; Brand et al., 2004).

Although feedback processing in the context of decision making based on implicit conditions might depend on the integrity of the amygdala, little is known about the role of mesiotemporal structures in decision making under risk. Only Brand, Grabenhorst et al. (2007) have investigated decision making under risk conditions by examining patients with bilateral amygdala damage with the GDT (in addition to decision making measured with the IGT, see above). A strong preference for risky choices was revealed in two of the three patients. Both patients had reduced anticipatory and feedback SCRs, indicating decreased emotional responsiveness, and both patients exhibited executive dysfunctions. The patient who showed advantageous decision making under risk was unimpaired on tasks of executive functions. The results suggest that disturbances within one of the two proposed routes might be compensated by the other; however the deterioration of both routes seems to result in disadvantageous decision making.

In summary, decision making depends on emotional feedback processing and associated brain structures such as the ventromedial prefrontal cortex and the amygdala when no information about consequences and their probabilities is provided. Decision making under risk that is based on explicit probabilities depends on executive functions and associated brain regions, as well as on feedback processing. Nevertheless, the impact of unilateral lesions within the mesial temporal lobe on both types of decision making is rather unknown to date.

Patients with temporal lobe epilepsy (TLE), normally suffer from unilateral structural damage within temporal lobe regions mainly comprising of the hippocampus, the parahippocampal gyrus and/or the amygdala (Bernasconi et al., 2003; Bernasconi, Natsume, & Bernasconi, 2005; Bonilha, Kobayashi, Rorden, Cendes, & Li, 2003). In concert with the aforementioned brain alterations, TLE patients can have impairments in affective functions, e.g. the perception and recognition of emotional facial expressions (Benuzzi et al., 2004, McClelland et al., 2006, Meletti et al., 2003; Reynders, Broks, Dickson, Lee, & Turpin, 2005; Shaw et al., 2007). Additionally, some studies suggest that TLE patients can suffer from deficits in executive functioning, including cognitive flexibility, set-shifting and interference susceptibility (Exner et al., 2002, Giovagnoli, 2001; Kim, Lee, Yoo, Kang, & Lee, 2007) whereas others do not (McDonald, Delis, Norman, Tecoma, & Iragui-Madozi, 2005; McDonald, Delis, Norman, Wetter et al., 2005). Thus, patients with TLE can have structural as well as functional abnormalities that are assumed to crucially affect decision making processes. Nevertheless, little is known about potential decision making reductions in patients with TLE. Only Butman et al. (2007) revealed in ten postsurgical TLE patients that they failed to use given feedback in the IGT to develop a tendency for choosing the advantageous alternatives. However, it is unclear whether these decision making deficits already exist preoperatively, or whether they are a consequence of unilateral resection of anterior mesiotemporal structures. Additionally, to our knowledge, nothing is known about decision making under risk conditions in TLE patients. Therefore, the aim of the current study was to investigate potential alterations in both kinds of decision making in presurgical TLE patients. We hypothesised that TLE patients exhibit disadvantageous decision making under implicit conditions which is mainly based on the processing of emotional feedback. Furthermore, we assume that patients with TLE who do not exhibit executive dysfunctions perform comparably to healthy subjects on decisions made under risk conditions. Additionally, as shown in previous studies, we expected that executive subcomponents are associated with decision making under risk conditions.

Section snippets

Subjects

The subjects included 20 patients (14 females and 6 males, aged 18–53 years, see Table 1) diagnosed with intractable unilateral TLE according to EEG monitoring. We examined all patients whilst they were hospitalised for surgical evaluation to treat refractory TLE. All patients were recruited from the Epilepsy Centre Bethel, Bielefeld. Exclusion criteria were current or a history of substance abuse, psychiatric and further neurological disorders, an IQ < 85, and signs of dementia. Sociodemographic

Results

The results of the neuropsychological test battery are summarised in Table 2. In general, the patients’ performance on the neuropsychological tasks was comparable to that of the healthy subjects. Although patients performed significantly worse compared to the healthy participants on two subtests assessing information processing (letter sequencing subtest of the Trail Making Test and the colour naming trial of the Colour Word Interference Test) and on one test assessing short-term memory (digit

Discussion

Our main findings demonstrate that in patients with TLE alterations in decision making selectively occur in ambiguous situations (i.e. when consequences and probabilities are initially implicit), whilst decision making under risk conditions (i.e. when consequences and probabilities are explicit) is normal. As hypothesised, patients selected disadvantageous alternatives on the IGT more frequently than healthy subjects. With regard to the relevance of mesiotemporal structures for decision making

Acknowledgements

We thank Miriam Antoine-Redeker for her assistance with the English wording and Eva Boecker for her help with the figures.

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