Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers

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Abstract

A decision-making instrument known as the ‘gambling task’ was used, which has been shown to be sensitive to the decision-making impairment of patients with bilateral lesions of the ventromedial prefrontal cortex (VM). Three groups of subjects were tested, substance dependent individuals (SD) (n=41), normal controls (n=40), and VM patients (n=5). All SD met the DSM-IV criteria for dependence, with either alcohol or stimulants (metamphetamine or cocaine) as the primary substance of choice. The results revealed a significant impairment in the performance of SD relative to normal controls. A significantly high proportion of SD (61 vs. only 32.5% of normal controls) performed within the range of the VM patients, while the rest performed within the range of normal controls. General demographic factors such as age, sex, and level of education could not explain these differences in performance. As well, differences in performance were not explained by intelligence (IQ), memory, or performance on standard executive function/frontal lobe tests. Performance on the gambling task was best predicted by a combination of factors, including duration of abstinence, years of abuse, relapses and times in treatment, and the ability to hold gainful employment. The results support the hypothesis that impairment in decision-making linked to a dysfunctional VM cortex is associated with at least a sub-group of SD.

Introduction

Patients with bilateral lesions of the ventromedial prefrontal cortex (VM) and substance dependents (SD) show similar behaviors: (1) they often deny, or they are not aware, that they have a problem; (2) when faced with the choice to pursue a course of action that brings an immediate reward, at the risk of incurring future negative consequences, including the loss of reputation, job, home, and family, they choose the immediate reward and ignore the future consequences.

A decision-making instrument known as the ‘gambling task’ has been shown to be sensitive to the detection of the decision-making impairment of VM patients [4], [7], [9]. Using this gambling task, studies have shown that cocaine [23], opiate [39], and alcohol abusers [36] perform abnormally on this task. With a decision-making instrument that is similar, but not identical, to the gambling task, studies have shown that VM patients, cocaine, and opiate abusers also perform abnormally on this task [41]. Although SD do not have an abnormal VM cortex as revealed on a structural MR, functional neuroimaging studies do reveal abnormalities in cocaine [47], [51] and alcohol [27] abusers. Thus, both the neuropsychological and functional neuroimaging data suggest that a decision-making impairment linked to a dysfunctional VM cortex may be at the core of the problem of addiction to substances.

The principal aim of this study was to test the hypothesis that SD suffer from a decision-making impairment as measured by the ‘gambling task’, an instrument which simulates real-life decisions in the way it factors uncertainty, reward, and punishment [4], [7], [9]. The unique advantage of the gambling task is that several lines of studies have linked performance on this task to activity in the VM cortex. First, lesion studies show that damage to the VM, but not the dorsolateral, sector of the prefrontal cortex impairs performance on the gambling task [8]. Second, functional neurolmaging studies using positron emission tomography (PET) indicate that the VM area is active during the performance of the gambling task [23]. Third, electrophysiological studies in patients with implanted electrodes in the VM area, prior to undergoing neurosurgery for intractable seizure disorder, reveal increased electrophysiological activity in the VM area, especially during the period before selecting a card, i.e. during the period the patient is pondering from which deck to choose [1]. These studies suggest that the gambling task taxes the decision-making function mediated by the VM cortex. Using this task, studies have shown that cocaine [23], opiate [39], and alcohol abusers [36] perform abnormally. With a decision-making instrument that is similar, but not identical, to the gambling task, studies have shown that VM patients, cocaine, and opiate abusers also perform abnormally [41]. Although SD do not have an abnormal VM cortex as revealed on a structural MR, functional neuroimaging studies do reveal abnormalities in cocaine [47], [51] and alcohol [27] abusers. Thus, both the neuropsychological and functional neuroimaging data suggest that a decision-making impairment linked to a dysfunctional VM cortex could be a contributing factor to the problem of addiction to substances. In addition to the principal aim of the study, which tends to corroborate the findings of previous studies cited above, there were several new issues that were addressed and tested in the current study.

First, one addressed the issue of whether cognitive abilities, including intelligence (IQ) and memory, or performance on standard executive (frontal lobe) function tests, including the Wisconsin Card Sorting Test (WCST), The Stroop, and The Tower of Hanoi, would predict performance on the gambling task in SD. Based on studies in VM patients showing impairments in decision-making despite normal intelligence and neuropsychological profiles [4], [14], it was hypothesized that the performance of SD on these standard neuropsychological tests would not predict their decision-making impairment as measured by the gambling task.

Second, SD often suffer from a variety of co-morbid psychopathologies, including psychopathy, depression, and/or anxiety [30]. Therefore, it is important to disentangle the contribution of the dependence on substances from the contribution of each of these psychological traits to the impairment in decision-making. Such psychological issues become very pertinent in light of recent evidence indicating that psychopathy could influence performance on the gambling task [36]. Similarly, it has been suggested that mood states such as anxiety improve performance on the gambling task [44]. Therefore, in the current study a variety of measures of psychological states were obtained, including psychopathy, depression, and anxiety. One tested whether the decision-making impairment in SD can be explained by the co-existence of another psychopathology. It was hypothesized that addiction to substances alone, independent of co-morbid psychopathologies, is associated with impairment in decision-making.

Finally, one focused on factors that best predict the poor decision-making in SD. General demographic factors such as age, gender, and education were considered. Most important, demographic factors that are unique to substance abuse, such as the drug of choice, the number of years of abuse, the duration of abstinence, and the number of cycles of relapse and return to treatment were considered. The ability to hold gainful employment was also considered. This factor is generally overlooked in studies of SD. However, in patients with bilateral VM lesions, or lesions restricted to the right VM region, the inability to hold gainful employment is one of the cardinal signs of their decision-making impairment. Interestingly, VM patients with lesions restricted mostly to the left VM cortex tend to continue to be able to hold a job, and their performance on the gambling task is within the normal range. Therefore, one looked at the relationship between employment and performance on the gambling task. Most important, it was reasoned that impairment in decision-making in SD could not be predicted by a single factor, but rather by a combination of these factors. The prediction index was formulated simply on the basis of signs that reflect improved judgment of SD in real life. For instance, the ability to remain abstinent for a long period of time, having fewer years of abuse, fewer cycles of relapse and return to treatment, and the ability to maintain employment are all signs of good decision and success in real-life. It was hypothesized that the longer the duration of abstinence, the shorter the number of years of abuse, the lower the number of cycles of relapse and treatment, combined with the ability to keep employment, the less severe the decision-making impairment would be. It was predicted that abstinence (in days), divided by the number of years of abuse, times the number of return to treatment, multiplied by a factor of employment would be the best prediction index of performance on the gambling task.

Section snippets

Methods

Normal controls were recruited through local advertisement, and were paid for their participation. SD were recruited while undergoing treatment at the Mid-Eastern Center for Chemical Abuse (MECCA) or they were brought back after they had completed treatment at MECCA. SD were paid for their participation in the study in gift certificates an hourly rate identical to that earned by normal controls. Patients with VM lesions (n=5) were selected from the Patient Registry of the University of Iowa's

Results

All the statistical analyses of the data presented below were conducted using the software STATISTICA 4.1 for the MacIntosh of Statsoft, Inc.

  • Demographic Data: These data from the participating subjects are shown in Table 1.

  • Total N: Number of subjects in the SD and normal control groups is almost equal. However, many fewer VM patients were studied because such patients are relatively rare. A figure illustrating the extent of the lesions in these patients can be found in another study [6].

  • Age:

Discussion

The results of this study support the main hypothesis that addiction to substances is associated with impairment in decision-making, and confirm prior demonstrations of impairment on the gambling task in cocaine [23], opiate [39], and alcohol [36] abusers. These results corroborate parallel lines of studies using similar decision-making tasks [41], and thus reinforce the notion that a sub-group of SD suffers from a decision-making impairment akin to that seen in patients with bilateral VM

Acknowledgements

This study was supported by NIDA DA11779-02.

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    A preliminary report of this study was presented at the 29th Annual Meeting of the Society for Neuroscience in Miami, FL, 1999.

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