Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes
Introduction
The Wisconsin Card Sorting test (WCST) has been considered a key measure in the diagnosis of frontal lobe dysfunction [6], [7], [15], [27], [39], [40]. This view of the WCST as a specific measure of impairment in the frontal lobes has also been seriously questioned. Reviews and published research stressed that some patients with definite frontal lobe damage performed well on the WCST, or that impairment on the task could be found after lesions in many regions of the brain [1], [2], [3], [10], [16], [19], [24], [43], [46], [52], [56], [70], [71]. As the WCST remains one of the most widely used of neuropsychological tests [50], investigation of its usefulness as a measure of frontal lobe dysfunction is highly relevant. Furthermore, the WCST is often used as a correlative index of ‘frontal functions’ in studies with neurologically intact individuals [11], [30], [49]. Validation of this relationship is required.
Understanding the brain-behavior relationships tapped by the WCST requires careful analysis of patients with brain disease. In particular, the comparison of patients with focal frontal to those with focal nonfrontal lesions is essential. Only a small number of studies have done this [2], [40]. While such a complex multifactorial test as the WCST is unlikely to be sensitive only to the functions of the frontal lobe, analysis of the cognitive processes involved can be helpful in understanding why and how individuals with lesions in different brain regions may be impaired on this test. A corollary of this process analysis is that the WCST may indeed be a reasonable index of frontal lobe functioning, if there is control of some of the ‘nonfrontal’ processes involved in the performance of the WCST. The study of patients with different lesions may dissociate how different brain regions are involved during the completion of this complex task. Imaging research has already suggested that multiple regions are active during the performance of the WCST [5], [44] but such studies cannot normally analyze the different processes required for such a complex task. Studies of lesion patients serve as an important validation for such imaging studies, but more importantly, they extend the localization results. Dissociation of processes and lesion location within the frontal lobe would also provide greater evidence for the separation of frontal lobe processes that has been postulated [33], [56], [61], [62], [65], [67].
The studies demonstrating that patients with frontal lobe damage were impaired on the WCST have not been consistent in their designation of the most relevant region within the frontal lobes. Drewe [15] suggested the importance of medial frontal cortex and Stuss et al. [63] noted the sensitivity of the WCST to orbitofrontal lesions (although the deficit in the latter patients was not reflected in an increased number of perseverations but in loss of maintenance of set). These results are in apparent contrast to Milner’s original emphasis on the dorsolateral prefrontal cortex and the subsequent supporting evidence for this localization [9], [35], [40], [51], [74].
How the test is administered is also important. Stuss et al. [63] reported that the frontal lobotomy patients became impaired after they were told the three sorting criteria necessary to complete the task. It was possible that the provision of information made these patients reflect on what they were automatically doing, making the task more ‘supervisory’ in nature. This finding, though fortuitous, could not be fully explored because there was inadequate control over several factors, such as comparison of lesion location, and the length of test administration. The use of additional instructions may also provide information as to the potential value of external support provided by the instructions as a rehabilitative tool in patients with focal frontal lobe lesions [34], [36], [73]. This notion is supported by the fact that several studies have demonstrated that instructions of various kinds had improved the performance of schizophrenics on the WCST [4], [18], [21], [37], [57], [72], [76]. Manipulating WCST instructions might also be useful in differentiating the sensitivity of the test for patients with pathology in different brain regions. For example, in schizophrenic patients performance improved with additional instructions but remained in the impaired range [54]. Comparison of individuals who did and did not improve with additional instruction would indicate the severity of a particular patient’s deficit.
In the present study we examined WCST performance in a large sample of patients with focal single lesions in frontal and nonfrontal regions of the brain, and compared their performance to age- and education-matched control subjects. In addition to extending previous work, we sought to analyze separable cognitive processes required to complete the task, differentiate patients according to intra-frontal lesion location, and assess the effect of test structure (environmental support) on performance. Each subject was administered the full 128 cards with the standard administration [20], [40]. Following this, two sets of 64 cards were administered, each proceeded by different instructions. For the first set of 64 cards (64A), each subject was told the three sorting criteria. For the second set of cards (64B) (not administered to the normal control subjects), each patient was told that the sorting criterion changed after 10 correct responses. The first criterion was verbalised, and the patient was told WHEN the change occurred, but not what the new sorting criterion was. To replicate Stuss et al. [63], in addition to standard measures of categories and perseverative errors, we analyzed ‘set loss’, defined as the number of times the subject obtained at least three correct sorts in a row, followed by an error. We also included a measure of perseveration reflecting consecutive repetition of incorrect sorts.
Section snippets
Participants
Focal lesion participants were recruited from neurosurgery, neurology, and rehabilitation centres in Ontario and Massachusetts, and control participants from the Rotman Research Institute control subject database. All focal lesion participants had a single focal lesion, verified by CT or MRI, confined to frontal, striatal or nonfrontal structures. Patients with unilateral striatal lesions were included because previous research had indicated similarity in performance to patients with
Results
Although the control group had a NART score significantly greater than the SM and IM groups, the results are unaffected if the NART score was used as a covariate. Moreover, there was no pattern of WCST results that was commensurate with IQ level. For example, while the two nonfrontal groups had somewhat lower IQ, their WCST scores were as good if not better than the control group. While the SM and IM groups both had significantly lower IQ scores than the control group, their WCST profiles were
Summary
As can be seen in Fig. 2, Fig. 3 the patients with nonfrontal lesions were not impaired compared to the matched control group on any measure. Further, there were no significant differences between the two nonfrontal groups on any of the measures. The frontal effects were due to perseverative errors and set loss errors. Non-perseverative and unique errors were not indicative of frontal dysfunction. One exception was the 64A condition, where RDL and LDL patients made more of the other errors.
The WCST as a measure of frontal lobe functioning
The presented data support the widely held assumption that the WCST is sensitive to focal frontal brain damage, and that this effect is specific to patients with focal frontal brain damage. There are, however, qualifications. The sensitivity of the WCST depends on which measure is used, reflecting a differentiation of processes/lesion location relationships within the frontal lobes. For the standard measures such as perseverations of the preceding criterion and number of categories achieved,
Conclusion
This is one of a few studies on the WCST that has been completed on patients with documented focal lesions in various regions of the brain. The current data, along with previous lesion data research on WCST performance, provide a framework for understanding the value of the WCST for the assessment of brain-damaged individuals. Certain themes are constant. The WCST is a multifactorial test that requires a distributed neural network. Performance can be impaired on this test for various reasons,
Acknowledgments
We are grateful to the following: D. Franchi and L. Buckle for assistance in testing the patients; M. Binns for statistical advice; A. Savas, S. Bisschop, and S. Paterson for figure preparations. This project was funded by the Medical Research Council of Canada and the Ontario Mental Health Foundation.
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2022, Progress in NeurobiologyCitation Excerpt :This suggests that following an error, the executive control level became unstable in the following trial and therefore the link between the current control level and the performance in the following trials was disrupted in ACC-lesioned and DLPFC-lesioned monkeys. Such an unstable control might lead to a failure in maintaining the cognitive set, which has been seen as ‘set-loss errors’ in patients with prefrontal cortex damage performing the WCST (Axelrod et al., 1996; Figueroa and Youmans, 2013; Greve et al., 1996; Stuss et al., 2000). Previous studies in monkeys have suggested a crucial role for the mid-dorsolateral prefrontal region (closely corresponding to the sdlPFC region, which was lesioned in our study) in monitoring and manipulation of information in working memory (Owen et al., 1999; Petrides, 2000).