This study investigated the relationship between deficits in executive control and verbal list-learning impairments in PDD in contrast to patients with mild AD. Strong support was found for our hypothesis that executive dysfunction is a primary determinant of verbal learning impairment in patients with PDD. We found that measures of executive control (including Word Fluency and CLOX-1) significantly accounted for variance in CVLT-II scores after variance was attributed to overall cognition (measured by DRS total score) and contextual verbal learning (Logical Memory I). Furthermore, the results of this study suggest that list-learning impairments in patients with mild AD are comparatively unrelated to executive dysfunction. In the AD group, the executive measures did not account for significant variance in list-learning scores after the contribution of overall cognition and contextual verbal learning was accounted for.
Previous literature has established that an association exists between executive dysfunction and learning in various populations, which the current study supports. Duff and colleagues (2005)
found measures of executive functioning shared as much as 60% of their variance with a wide array of visual and verbal learning variables in a sample of patients in a neuropsychology clinic. Furthermore, executive measures with a strong visual-spatial component (Trails B and Wisconsin Card Sorting Test) have been shown to be predictive of performance on visual memory tasks (Temple et al., 2006
). Finally, poorer performance on the CVLT has been displayed in mixed samples of neurologic patients with psychometrically documented executive dysfunctions (Tremont et al., 2000
) as well as frontal lobe lesion patients (Alexander, Stuss, & Fansabedian, 2003
The current findings demonstrate that a robust relationship exists between executive function and list learning in patients with PDD. Previous studies have found some evidence for relationships between executive dysfunction and verbal learning in non-demented PD patients (Bondi et al., 1993
; Higginson et al., 2003
). Bondi and colleagues demonstrated that impairments on learning tasks (including word learning, procedural learning, perceptual learning, and continuous verbal recognition) were no longer apparent after using statistical covariation of executive measures, including the Wisconsin Card Sorting Task (WCST), California Sorting Test, and measures of verbal temporal ordering and verbal fluency. Higginson et al. (2003)
utilized a step-wise regression approach to demonstrate that a measure of working memory (Letter-Number Sequencing from the Wechsler Intelligence Scales) predicted CVLT delayed free recall scores. Other executive measures, including WCST, stroop color-word test, digit span, and letter fluency (FAS), did not significantly predict variance in list learning. We found that CLOX-1, a planning and construction task, and word fluency, a search and retrieval task, were the most important predictors of verbal learning in our sample of PDD patients. It is clear that a range of executive functions likely play a role in verbal-learning impairments in patients with PD (both with and without dementia).
Although the current study is one of the first to document an association between verbal learning and executive dysfunction in PDD patients, Levy and colleagues (2002)
demonstrated that impairments in these two cognitive domains are associated with the development of dementia in PD patients. The current study adds to the growing body of evidence, suggesting that the executive dysfunction contributes to the deficits in verbal learning and memory. Given the clinical significance of these cognitive domains in predicting long-term outcomes, it is vital to further explore the relationship between deficits in executive control and memory in the PD population.
Furthermore, our findings provide evidence of comparatively different mechanisms of verbal learning impairment in PDD and mild AD patients. In PDD, executive measures were significantly associated with verbal list-learning after controlling for the contribution of contextual learning. On the other hand, in the AD group, the unique contribution of contextual learning was significant after accounting for the contribution of overall cognition, while the addition of unique variance attributable to the executive measures did not provide a significant contribution in the prediction of variance over that provided by overall cognition and contextual learning. None of the beta coefficients of the executive predictors approached significance levels in the AD patient model. PDD patients typically display poor learning, yet relatively spared cued and recognition memory; whereas AD patients show insufficient registration ability with poor learning, retrieval, and recognition memory (Cummings, 1988
). These patterns suggest a different mechanism of learning deficits in the two populations, which is supported by the current results.
Consistent with previous literature, we found no group differences among patients with AD and PDD, on measures of verbal learning and executive functions (Song, Kim, Yoo, Song, & Lee, 2008
; Starkstein et al., 1996
; Stern et al., 1993
). However, there is little prior support for a link between executive dysfunction and verbal-learning impairment in AD. Baudic et al. (2006)
found significant correlations between scores on the Buschke Selective Reminding Task, a measure of verbal list-learning abilities, and executive measures (number of perseverative errors on Modified Card Sorting Task and WAIS Similarities) in mild AD patients. Unlike the current study, Baudic and colleagues did not account for overall cognition or other measures of verbal learning in their analyses. Furthermore, while their study reported significant correlations, they did not use a multiple regression approach which would help determine the contributions of cognitive processes to learning. Recently, Grober and colleagues (2008)
found memory impairments precede deficits in executive functions by 4–5 years in preclinical AD patients. Therefore, it appears that memory and learning deficits exist independently of executive dysfunctions in mild AD patients.
From our perspective, the literature suggests that several CVLT-II measures may differ between patients with AD and PDD, primarily on the basis of the mnemonic processes that are eroded in these dementias (i.e., encoding, consolidation, retrieval). Our understanding of the literature is that in AD the primary deficit is one of the deficient consolidations of information, such that immediately learned material is rapidly lost and that retrieval cues do not enhance performance. In contrast, we understand memory loss in PDD as representing the prototypical “subcortical” pattern, whereby encoding is impoverished and retrieval is inefficient, such that learning may be slow but that with retrieval cues the information that is learned can be retained. We see this pattern as primarily implicating executive dysfunction. It should be noted that in practice such patterns are relative rather than absolute, and that all aspects of mnemonic function can be impaired in AD, but that consolidation is disproportionately impaired.
There are a number of limitations and weaknesses inherit in this study that suggests avenues for future research. The most prominent weakness lies with the limited sample size. The authors wanted to utilize a well-defined and well-matched sample of PDD and AD patients. This resulted in a more modest sample size due to the rigors of study methods in the diagnostic process. It should also be noted that the specification of PDD patients may not generalize to the dementia with Lewy Bodies or non-demented PD populations. As with any analysis based on correlation, the generalizability of results is of further concern as all regression-based analyses are dependent on the measures used and sample characteristics. The authors chose to utilize widely administered measures of executive functioning and verbal learning, along with highly characterized samples, in order to minimize these concerns. However, replication with other measures and samples is needed.
In summary, this study provides evidence of distinct patterns of list-learning impairment in PDD and AD. This is the first study that we are aware of that specifically compares the influence of executive control on list-learning performance in these two populations using the same measures in a matched sample. The data support the notion that executive dysfunction plays a distinct role in verbal learning impairment in PDD but less of a role in patients with AD. Overall cognition and contextual learning are the key predictors of verbal list-learning performance in AD. More research into comparative cognitive deficits in PDD and AD is strongly desirable to better understand the underlying neurocognitive phenomena behind neuropsychologic impairments in these patient populations.