Introduction
Schizophrenia is a neurodevelopmental disorder in which cognitive dysfunctions play a central role and are considered among the core symptoms of the disease (Elvevåg and Goldberg 2000; Rund 2018). The neurocognitive performance of individuals with schizophrenia is 1.5 standard deviations below average and contributes to poor clinical outcomes such as unemployment and lower self-sufficiency (McCutcheon et al. 2023). Well-documented cognitive deficits in schizophrenia encompass attention, autobiographical and episodic memory, implicit and associative learning and social cognition (Horan et al. 2008; Diwadkar et al. 2008; Savla et al. 2013; Hoonakker et al. 2017; Kwok et al. 2021). Disruptions in working memory and executive functions play a crucial role in the cognitive functioning of individuals with schizophrenia, resulting in difficulties integrating and processing incoming information (Goldman-Rakic 1994; Rybakowski et al. 2006; Forbes et al. 2009). These deficits are related to disorders of structure and activity of the prefrontal cortex of the brain (Weinberger and Gallhofer 1997). The prefrontal cortex is the most anterior part of the frontal lobe of the brain. Due to its numerous connections with other brain areas, the prefrontal cortex plays an integrating and executive role for its other functions (Friedman and Robbins 2022). The prefrontal cortex is a functionally diverse brain region, and studies on cognitive deficits in schizophrenia have helped identify disorders associated with its specific areas. Well-documented disorders of the dorsolateral prefrontal cortex in schizophrenia lead to deficits in working memory and executive functions (Goldman-Rakic and Salomon 1997; Rybakowski et al. 2006). Deficits of working memory in schizophrenia include problems with storing information in short-term memory, as well as with its manipulation, with more severe disruptions of the latter (Barch 2005). These deficits involve different modalities, with disruption of both visuospatial and verbal working memory (Ichinose and Park 2019). Impairment of executive functions in schizophrenia includes disruption of cognitive flexibility, response inhibition, goal-directed planning, and cognitive control (Polgár et al. 2010; Ettinger et al. 2018; Siddiqui et al. 2019).
Neuroimaging studies have also shown the presence of structural and functional abnormalities of the orbitofrontal cortex in schizophrenia (Hoptman et al. 2006; Isomura et al. 2017). Neuropsychological studies have shown that by integrating cognitive and emotional information, this area enables effective decision-making and learning based on the emotional consequences of previous choices (Damasio 1994; Bechara et al. 1994, 1996, 1997, 2000).
Decision-making deficits in schizophrenia are related to both positive symptoms, such as delusions and hallucinations, and negative symptoms, such as social withdrawal and apathy. Positive symptoms have been related to making choices based on insufficient information, whereas negative symptoms are associated with abnormal reward processing, leading to disrupted estimation of future rewards in guiding of choices (Sterzer et al. 2019).
A frequently used tool for examining decision-making in schizophrenia is the Iowa Gambling Task, developed by Bechara et al. (1997) to assess economic decisions in patients with damage to the orbitofrontal cortex.
As shown in several studies, individuals with schizophrenia tend to make more choices that result in larger financial penalties compared to healthy controls, leading to poorer financial outcomes. It has also been shown that patients are slower to learn the advantageous decisionmaking strategy, which involves avoiding the decks with larger penalties (Beninger et al. 2003; Ritter et al. 2004; Shurman et al. 2005; Lee et al. 2007; Lee et al. 2009; Brown et al. 2015). The results of the studies are, however, ambiguous, as some authors did not find differences between patients and healthy controls (Wilder et al. 1998; Cavallaro et al. 2003; Evans et al. 2005; Rodríguez-Sánchez et al. 2005; Turnbull et al. 2006; Sevy et al. 2007). Possible reasons for these discrepancies are the differences in the intensity of negative symptoms and pharmacotherapy in the patients studied, as well as in different methodology for interpreting the results of the Iowa Gambling Task.
Several studies have also demonstrated that individuals with schizophrenia are more likely to choose decks that contain more frequent losses (Wilder et al. 1998; Shurman et al. 2005; Rodríguez-Sánchez et al. 2005). The number of studies observing this phenomenon may be larger; however, not all authors presented their results in a manner that allows for the assessment of the number of draws from individual card sets.
Some of the above studies attempted to assess the relationship between decision-making in the Iowa Gambling Task and performance on tests assessing working memory and executive functions. Some studies have confirmed a link between poorer working memory and executive functions and the more frequent use of decks that generate both larger and more frequent losses (Lee et al. 2009; Shurman et al. 2005; Rodríguez-Sánchez et al. 2005). These results suggest that due to impaired working memory and executive functions, patients may have difficulty making beneficial decisions, because of the problems in assessing both the size and frequency of the losses incurred (Rodríguez-Sánchez et al. 2005; Brown et al. 2015).
As in the abovementioned analyses, here too there are discrepancies in the way the results of the Iowa Gambling Task were calculated. This makes it difficult to assess how many cases such a relationship would have demonstrated if the results had been reported for individual card sets, rather than for the aggregated presentation of decks containing high losses.
A detailed assessment of the performance of the Iowa Gambling Task in individuals with schizophrenia may help to better understand the way they make their decisions. Together with the assessment of working memory and executive functions, it may add to diagnosing cognitive deficits, which are potentially related to poorer functional outcome.
The aim of this study was to assess decisionmaking in the Iowa Gambling Task by individuals with schizophrenia. In the assessment of decision-making, the influence of both the size and frequency of losses on the decisions made was considered. To the authors’ knowledge, only a few studies have addressed this so far, and the results of the present study may contribute to resolving the discrepancies in the existing literature. The second aim was to assess the efficacy of working memory and executive functions in individuals with schizophrenia, and the relationships between decision-making, working memory and executive functions.
Material and methods
Subjects
Thirty individuals with schizophrenia (18 male and 12 female) aged 21-57 years (mean 34 ±9), participated in the study. Twenty-six of them were stable inpatients, recruited from the Department of Adult Psychiatry, Poznan University of Medical Sciences and the Gizinscy Medical Centre in Bydgoszcz, Poland. The other 4 were outpatients recruited from the Neuropsychiatry Outpatient Clinic of the University Hospital in Bydgoszcz. All patients were in symptomatic remission at the time of the study. The diagnosis of schizophrenia was made by a psychiatrist, using ICD-10 diagnostic criteria. The exclusion criteria were substance abuse, or co-occurring psychiatric, neurological and somatic illnesses, related to a decline in cognitive functioning. All patients were taking some form of anti-psychotic medication, 26 patients atypical antipsychotics, and the remaining 4 typical antipsychotics at the time of the study. Schizophrenic symptoms were assessed with the Positive and Negative Syndrome Scale (PANSS). The global as well as the negative symptoms subscale scores were analyzed in this study. All schizophrenic individuals gave their written consent to participate in the study after the nature of the procedures had been explained to them. The control group consisted of 30 healthy volunteers (10 male and 20 female), aged 21-69 years (mean 34 ±13). The possibility of their suffering from some form of psychological disorder was ruled out using the MINI-International Neuropsychiatric Interview (Sheehan et al. 1998).
Measures
Assessment of decision making
Iowa Gambling Task
Decision making was assessed by means of the Iowa Gambling Task (IGT) (Bechara et al. 1997). During the test, the subject selects cards from four decks (A’, B’, C’, and D’). Selecting a card leads to gaining a certain amount of money; however, it may simultaneously lead to losing a certain amount. The subject’s task is to finish the game with the highest possible financial balance. Selecting cards from decks A’ and B’ leads to large wins, but also to large losses, so using them for a longer period of time results in a negative balance. In contrast, sets C’ and D’ generate smaller profits, but the losses incurred are also smaller, so that using them throughout the task results in a positive balance. The decks also differ in the frequency of losses in such a way that A’ and C’ contain more frequent losses than B’ and D’. The present study involved analysis of both the number of cards selected from each of the four individual decks and the overall net scores, expressed as the number of cards selected from decks involving high penalties (A’ and B’), subtracted from the number of cards selected from decks involving low penalties (C’ and D’). The number of cards selected from decks involving frequent penalties (A’ and C’) subtracted from the number of cards selected from decks involving less frequent penalties (B’ and D’) was also recorded. Such analyses enabled the assessment of decision making in the context of the magnitude as well as the frequency of losses.
Assessment of working memory and executive functions
Wisconsin Card Sorting Test
The Wisconsin Card Sorting Test (WCST) consists of 4 stimulus cards and 128 response cards, marked with figures of different forms, colors and numbers (Heaton et al. 1993). The subject is instructed to match response cards that appear on the computer screen to the stimulus cards displayed above. The task of the subject is to match cards according to three rules: form, color and figure. The only information given to the subject during the test is whether each of his responses was right or wrong. After a specified number of consecutive correct matches, the sorting principle changes without any warning being given to the subject. As the test proceeds, a number of shifts in sorting principle take place. The test finishes after all categories have been completed or after all 128 response cards have been used. This study involves analysis of the percentage of perseverative and non-perseverative errors, number of categories completed, percentage of conceptual level responses and number of cards used to complete the first category. The Wisconsin Card Sorting Test assesses executive functions such as set shifting and performance monitoring, as well as the ability to maintain the proper performance criterion in working memory.
Trail Making Test
The Trail Making Test (TMT) (Reitan 1958) consists of two parts. In the first part, a subject is asked to connect points with numbers 1-25 on a chart, in an ascending order, as quickly as possible. In the second part, a subject is asked to match points with numbers 1-13 and letters A-L in alternating, ascending order (1-A-2-B, etc.). Time (in seconds) required for completion of each part was analyzed in this study. The Trail Making Test assesses the visuospatial and verbal working memory as well as set shifting ability.
Statistical analysis
The statistical analysis was carried out with the PS IMAGO 9.0 program. Normality of variable distribution was assessed by means of the Kolmogorov-Smirnov test. A repeated measures ANOVA was applied for analysis of IGT performance in individual decks of cards. To evaluate differences between the schizophrenic and control groups, Student’s t test was applied. Between-variable correlations were assessed with Spearman’s rho coefficient.
Results
Sociodemographic and clinical data
Sociodemographic and clinical data are presented in Table 1. No differences were observed between the patient and control groups regarding age and years of education. The number of male subjects was higher in the patient group than the control group.
Decision making
The first statistical analysis provided was the assessment of between-group differences, regarding the performance in IGT. Male and female subjects did not differ in terms of number of cards selected from individual decks or in the number of choices from “low penalty” minus “high-penalty” decks. This was observed in the whole tested sample, as well as in both schizophrenic and control groups. Also, there were no significant differences between individuals with schizophrenia taking typical and atypical antipsychotics regarding their performance in all neuropsychological tests. Differences between schizophrenic and healthy control groups in the number of selections from individual decks of cards were assessed with 2 (group) × 4 (deck) repeated measures ANOVA (Table 2). A main effect of deck, F(1, 84) = 22.50, p = 0.001, but not group was observed. However, a group by deck interaction effect approached significance, F(1, 93) = 4.45, p = 0.06. The performance of participants in individual decks of IGT was further explored with between-group comparisons, using Student’s t-test. Descriptive statistics for number of choices from individual decks in the IGT are presented in Table 2. Individuals with schizophrenia made more choices from decks A’ and C’ and fewer choices from deck D’ than the healthy controls. There were no between-group differences in number of choices from deck B’. Both groups were next compared regarding the number of choices from the groups of decks, divided with regard to the magnitude of gains and losses which appear. The net score was the number of cards selected from “low-penalty” minus “high-penalty” decks ((C + D) – (A + B)). As shown in Table 1, there were no differences between individuals with schizophrenia and the healthy controls regarding their net scores.
IGT performance was also analyzed in the “frequent-infrequent” penalty format. The net score was the number of cards selected from decks involving large but infrequent penalties minus the number of cards from decks involving small but frequent penalties ((B + D) – (A + C)). As shown in Table 3, individuals with schizophrenia selected more cards from the frequent penalty decks than the healthy controls.
Executive functions
Descriptive statistics for the scores in the WCST and TMT are presented in Table 4. Comparison of the performance in WCST and TMT between schizophrenic and healthy groups revealed poorer performance of individuals with schizophrenia in both tests. They committed more perseverative and non-perseverative errors, gave lower conceptual level responses, completed fewer categories and needed more cards to complete the first category in the WCST. They also needed more time to complete both parts of the TMT.
Relationships between decision making and executive functions
The analyses of associations between performance in the IGT and in tasks assessing executive functions performed in the schizophrenic group (Table 5) showed no relationships between the variables.
Discussion
The aim of this study was to assess the difference between individuals with schizophrenia and healthy controls in decision-making, working memory and executive functions. The purpose was also to establish whether preference towards particular decks in a decision-making task is related to the efficacy of working memory and executive functions.
Between-group comparisons, concerning the 4 individual decks of cards, revealed that individuals with schizophrenia made more choices from decks A’ and C’ and fewer choices from deck D’ than the healthy controls. Decks A’ and C’ are characterized by more frequent losses than decks B’ and D’. Therefore, selecting cards from deck A’ generates high and frequent losses, and therefore can be labeled as disadvantageous and may indicate impaired decision-making. Impaired decision making in schizophrenia has been reported in studies using the IGT (Beninger et al. 2003; Ritter et al. 2004; Shurman et al. 2005; Lee et al. 2007; Lee et al. 2009; Brown et al. 2015), as well as other tools (Bark et al. 2005; Zhang et al. 2015; Benke et al. 2021). However, as indicated by the results of the present study, the decision-making deficit in schizophrenia does not resemble the one observed in individuals with damage to the prefrontal cortex. In studies by Bechara et al. (1997, 1999), individuals with damage to the orbitofrontal cortex never learned to avoid the high-penalty decks in IGT, which resulted in higher overall preference towards these decks compared to the healthy participants. In the present study, individuals with schizophrenia did not differ from the healthy controls in the overall preference towards high and low-penalty decks. It is possible that individuals with schizophrenia eventually learn to make advantageous decisions by avoiding high penalties; however, this process is slower than in healthy individuals (Ritter et al. 2004). Compared to the control group, individuals with schizophrenia from the present study made more choices from decks involving more frequent penalties. A similar profile of IGT performance in schizophrenia was observed by Rodríguez-Sánchez et al. (2005) in a study involving 80 individuals in the first episode of schizophrenia. The authors proposed that this pattern of decision-making is linked to deficits in working memory, which hinder the ability to store information about loss frequency and use it to guide subsequent decisions.
In the present study, individuals with schizophrenia performed significantly poorer on all measures of executive functioning and working memory than the healthy controls. This finding is in line with previous studies indicating that executive dysfunction is a core symptom of schizophrenia (Morice 1990; Gold et al. 1997; Saykin et al. 1994; Braff et al. 1991; Raffard and Bayard 2012), which results from the well-documented dysfunction of the dorsolateral prefrontal cortex (Weinberger et al. 1992; Volz et al. 1997; Egan et al. 2003). While we did not observe relationships between IGT performance and measures of working memory and executive functioning, some results require attention and probably further investigation. Relationships between the number of cards selected from deck A’ and the number of perseverative errors in WCST, as well as between the number of choices from the frequent penalty decks and the number of categories completed in WCST, while they did not reach statistical significance, are in line with findings from previous studies, and indicate that decision making in schizophrenia should be considered in the context of the executive dysfunction (Betz et al. 2019). Brown et al. (2015) proposed an interesting viewpoint suggesting that the specific performance in IGT by individuals with schizophrenia results from difficulties in integrating frequency and magnitude information in decision-making, a process hardly separable from the efficacy of working memory and executive functions.
Whether performance in IGT is related to deficits of working memory and executive functions in schizophrenia is a matter of debate. While some authors found no relationship, others made observations that shed some light on the possible mechanism of decision-making in schizophrenia. For example, Yip et al. (2009), in a study of 39 individuals with schizophrenia, found a relationship between higher number of choices from the high penalty decks and number of perseverative errors. Perseveration in WCST is a result of poorer executive functioning, specifically, the set-shifting, reflecting subjects’ ability to adjust the performance to the incoming feedback. This indicates that the inability to shift from the high-magnitude and high-frequency punishments in schizophrenia is related to the so-called stuck-in-set type of performance, whereby a subject is unable to shift from the initial decision-making strategy, even when experiencing large or frequent losses (Paulus et al. 1999a, b). Saperia et al. (2019) offer an alternative explanation of sub-optimal reward-based decision making in schizophrenia, whereby schizophrenic individuals are capable of shifting their choices while facing losses. However, they do not adhere to choices that previously led to financial gains. The authors claim that decision-making in schizophrenia is related to both motivational and cognitive factors.
Between-group differences in IGT performance in the present study should also be reviewed in the context of gender differences, as the number of male subjects in the study group exceeded the number of male subjects in the control group. This may be of significance for the present results, as there are well-documented gender differences in economic decision-making (Fisher and Yao 2017; Lin et al. 2019). It also pertains to the differences in IGT performance, where male subjects tend to select more cards from the low-penalty decks than do females (Zanini et al. 2024).
Findings from the present study encourage some clinical suggestions. Although individuals with schizophrenia learn to make advantageous decisions, they present a specific decision-making style, with different sensitivity to magnitude and frequency of punishments. This may lead to sub-optimal use of information about consequences of previous choices, in guiding further decisions, a phenomenon that psychological interventions aimed at improving the functional outcome of patients should take into account. Working memory and executive functioning should also be considered as a target in pharmacological and psychological therapy, as its deficit, together with poorer decision-making, contributes to worse functional capacities (Cámara et al. 2021).
The present study has its strengths and limitations. It adds to the understanding of how individuals with schizophrenia make decisions by indicating the specific way patients take into account the magnitude and frequency of punishments in their choices. It also confirms the importance of executive dysfunction in the clinical picture of schizophrenia.
Limitations of the present study include the small sample size, which, in some cases, may have led to type 2 errors. Furthermore, the large number of comparisons and correlations performed in in the present study may have led to type 1 errors. It is worth addressing these issues in further studies, by enrolling larger numbers of participants. This will make it possible to avoid type 2 errors and correct for multiple analyses. Furthermore, the unequal number of male and female subjects in patient and control groups may limit the accuracy of between-group comparisons. The wide age range of study participants in both groups may also have influenced the results, as cognitive functions have been found to decrease with age.
Conclusions
Individuals with schizophrenia demonstrate specific way of making decisions, with less sensitivity to the magnitude and frequency of penalties, compared to healthy subjects. This is accompanied by deficits of working memory and executive functions. Both these phenomena can result in difficulties with everyday decision-making, leading to poorer functional outcomes, and thus should be a target in pharmacological and psychological interventions.
Disclosures
The study was financed from the sources of a scientific grant of the Polish Ministry of Science and Higher Education: MNiSW N402 078234.
The study has been approved by the Nicolaus Copernicus University in Torun, Collegium Medicum in Bydgoszcz Bioethics Committee.
The author declares no conflict of interest.
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