We studied 32 patients with LBSD to determine whether and to what extent this syndrome disrupts the organization of narrative discourse. We assessed the ability of speakers to communicate a narrative effectively in the task of telling a complex story. The story was presented to the subject as a series of detailed drawings that were easily and accurately interpreted by healthy seniors, and the narrative was performed while the subjects were looking at the pictures to minimize the impact of memory difficulty on narrative performance. A detailed quantitative analysis revealed a significant narrative production deficit in non-aphasic patients with LBSD. This deficit was most evident in the DLB/PDD subgroup of LBSD patients. Difficulty with narrative organization in the DLB/PDD subgroup was related to impairments on measures of executive functioning and speech fluency, while other measures of language and cognitive functioning were unrelated to their narrative production. A regression analysis related the deficit for narrative organization in LBSD patients to gray matter atrophy in ventral frontal and anterior cingulate regions. We discuss each of these issues below.
We examined the narratives produced by LBSD patients and healthy seniors to assess the communicative competence of the patients, and we related the organization of their narratives to language-specific attributes of their speech, neuropsychological measures of executive functioning, and imaging studies in order to elucidate the basis for their narrative impairment. LBSD patients demonstrated significant deficits in their narratives. These included an impairment in connecting one scene to the next over the course of the story, poor ability to maintain the search theme throughout the narrative, and difficulty appreciating the resolution of the story. These aspects of the narrative do not involve processing at the level of a single word or sentence, but instead appear to depend largely on a higher-level organizational component (Farag et al., 2010
; Mar, 2004
). Several previous studies have emphasized the contribution of executive resources to organizational aspects of a narrative. Non-aphasic patients with behavioral variant frontotemporal dementia have shown a significant deficit in the production of an organized narrative (Ash et al., 2006
). A study of narrative comprehension revealed that these patients were impaired at judging errors in the ordering of events in a brief script, although they were relatively unimpaired at identifying semantically anomalous single events in a script (Cosentino, Chute, Libon, Moore, & Grossman, 2006
). In a follow-up study, we examined whether there was a higher-level organizational deficit or difficulty ordering events in a narrative, and we found that non-aphasic behavioral variant frontotemporal dementia patients were impaired at assessing the top-down organization of brief narratives (Farag et al., 2010
). In all of these studies, impairments on measures of narrative organization were related to deficits on neuropsychological measures of executive control.
Inspection of the data in the present study revealed that the narrative deficit in LBSD is attributable largely to the DLB/PDD subgroup of LBSD patients. This subgroup has a progressive dementia involving executive functioning, memory, and visuospatial processing (Emre et al., 2007
; McKeith et al., 2005
). Indeed, the DLB/PDD patients participating in this study were impaired on neuropsychological measures in these cognitive domains. It is important to point out, however, that non-specific dementia may not be an adequate explanation for the discourse deficit in DLB/PDD. While some measures showing impaired neuropsychological functioning were correlated with deficits in the organization of the narrative, other measures were not correlated, such as visual-perceptual functioning. Patients with Alzheimer's disease appear to have difficulty with lengthy narratives because of their memory impairment, but a study investigating brief narratives showed that Alzheimer's disease patients do not differ from controls in their processing of narrative organization (Farag et al., 2010
Our findings support the contention that executive resources play a central role in the ability of DLB/PDD patients to organize their production of a narrative. The two features of narrative performance that entail the greatest executive resource demands are local connectedness and maintenance of the search theme. These require the storyteller to keep the present and immediately past elements of the story in working memory, to keep in mind the continuing theme of the story, and to embed these events in an appropriate context that is governed by top-down organization. The demand on executive resources is shown by the correlations of local connectedness and search theme maintenance in DLB/PDD with tests of mental organization, working memory, and inhibitory control (). As far as we are aware, this is the first study to demonstrate a role for executive resources in the narrative discourse deficits of patients with DLB/PDD.
We also found that narrative organization is more impaired in DLB than PDD with regard to both local connectedness and search theme. Although only small numbers of patients were examined with each of these clinical phenotypes, this observation is in line with the findings of previous reports of poorer executive functioning in mild DLB than in mild PDD (Aarsland et al., 2003
; Downes et al., 1998
). These authors interpret their findings as evidence that involvement of the frontal cortex occurs earlier in DLB than in PDD. This is consistent with our view that while DLB and PDD may differ in the progression of impairment, they represent a single spectrum of disease. Longitudinal studies of these patients are needed to evaluate this hypothesis empirically.
The DLB/PDD patients were not clinically aphasic, but they were significantly impaired on some language-specific measures of speech production, including the amount and rate of speech output, the proportions of grammatical and syntactically complex utterances, and the frequency of speech sound errors. The only correlation of a language measure with features of narrative production was the correlation of speech rate, in words per minute, with local connectedness and search theme. Speech rate is a very general measure that depends on many factors, such as motor control, attention, grammatical facility, and access to the lexicon. Speech rate may be reduced for different reasons in different patient groups (Ash et al., 2009
), so by itself, this finding only signals some unspecified disruption of speech production. Speech rate in DLB/PDD appears to be correlated with motor functioning as well. This observation merits further study, though it is outside the scope of the present report.
Previous work has demonstrated a deficit of grammatical processing in LBSD, although this work has concentrated on non-demented LBSD patients with PD. This prior work has also emphasized the role of executive resources in processing grammatically demanding sentences. For example, correlation studies have related the comprehension of complex grammatical sentences to measures of executive functioning such as working memory and information processing speed, and on-line studies of grammatical processing have demonstrated the contribution of executive resources to grammatical processing in PD that is independent of task-related performance demands (Grossman, 1999
). The present study found a deficit in grammatical competence in the narrative production of DLB/PDD patients, but we did not find a significant correlation between syntax and narrative organization. Previous studies of grammatical processing in LBSD have focused largely on comprehension, while the present study assessed the production of syntax and narrative, which may draw on different resources from those involved in comprehension. While executive resources may contribute independently to grammatical comprehension, grammatical production, and narrative production, the nature of these resources may differ depending on the specific aspect of language that is being processed.
Phonological features of speech production were impaired in these patients as well, but this did not correlate with the narrative deficit. Speech sound errors in LBSD may be due in part to a motor disorder that interferes with articulatory clarity (Skodda, Visser, & Schlegel, 2010
), although additional work is needed to determine whether all errors of speech sound production are due to a motor disorder in these patients. Taken together, these observations imply that deficits in the structuring of narrative speech in LBSD are not related to an undifferentiated impairment of speech and language, but depend in part on working memory and other executive resources which appear to play a role in organizing a narrative.
We found further that organizational components of narrative discourse are correlated with motor functioning. As an extension of the motor theory of speech perception, recent work based on the hypothesized mirror neuron system has implicated a motor disorder in deficits of many aspects of speech and language (Hauk, Johnsrude, & Pulvermuller, 2004
; Liberman, Cooper, Shankweiler, & Studdert-Kennedy, 1967
; Liberman & Mattingly, 1985
). Other work has related greater difficulty with action verbs than object nouns in PD to the motor deficit of these patients (Boulenger et al., 2008
). However, this line of reasoning must be interpreted cautiously (Hickok, 2010
). Evidence against a role for the mirror neuron system in narrative organization comes from the finding that, although the subgroup of patients with PD has an equally prominent motor disorder, PD patients have minimal difficulty with narrative discourse. Additional work is needed to determine the basis for the association of a motor impairment with impaired organization of narrative discourse in DLB/PDD.
Non-demented PD patients do not appear to have a significant impairment of narrative organization. They also have fewer language and cogntive deficits than the DLB/PDD subgroup of patients. Many studies have reported minimal speech deficits in non-demented PD patients, although this has rarely been quantified (Bayles, 1990
; Piatt et al., 1999
). The present report supports this generalization of reasonably preserved language production in PD. In particular, the organization of the narratives of the 18 PD patients in this study did not differ substantially from those of healthy seniors () on either local or global connectedness of the narrative or on maintenance of the search theme. Furthermore, the PD patients did not differ from healthy seniors on several basic measures of linguistic competence in expression, such as speech output, speech rate, syntactic competence, or speech sound errors (). In addition, the PD patients were relatively unimpaired in their performance on neuropsychological measures, including measures of executive resources. One reason for the discrepancy relative to prior work in PD may be that previous assessments of language in PD have focused on comprehension, and the present study examined expression. Another possibility is that a subset of PD patients assessed in prior work demonstrated an executive deficit but were not otherwise demented, while the present study carefully separated LBSD patients with a cognitive deficit from those with essentially normal cognitive performance. With these caveats in mind, we did find a possible deficit in semantic memory in non-demented patients with PD. This has been observed previously (Copland, 2003
) and may be related to factors such as selection and information processing speed that are mediated in part by changes in dopaminergic functioning in the basal ganglia (Chenery, Angwin, & Copland, 2008
; Copland, McMahon, Silburn, & de Zubicaray, 2009
). One study has related a semantic deficit to narrative discourse impairments in PD (Godbout & Doyon, 2000
), although we did not find a correlation between semantic difficulty and narrative impairments. Godbout and Doyon (2000)
did not characterize the narrative impairment in LBSD quantitatively, and additional work is needed to specify the precise contribution of semantic limitations to the narrative deficits of LBSD patients. The imaging results emphasize the contribution of frontal brain regions to narrative organization. Cortical atrophy in LBSD is seen bilaterally in frontal, temporal, and parietal/occipital regions (Burton et al., 2009
; Burton et al., 2004
; Sauer et al., 2006
; Tam et al., 2005
; Whitwell et al., 2007
). We replicated these findings in the present study. Moreover, within this area of atrophy, we observed a specific pattern of gray matter thinning related to narrative organization. While we know that regression analyses related local connectedness to cortical thickness in regions that are not significantly atrophied, we did not interpret these regressions because neither their presence nor their absence can be explained in any clear manner. For example, such a finding in areas of no associated significant atrophy might suggest that the area may become atrophied in the future, that the component of the task related to the area is not central to the task, or that the area plays a marginal role in task performance. Local connectedness was related to atrophy bilaterally in ventral prefrontal regions. This observation suggests a role for ventral frontal cortex in processing narrative production by contributing to maintenance of cohesion within the narrative. In an fMRI study of comprehension, healthy young adults showed greater bilateral ventral frontal activation in judgments of more closely related events compared to less closely related events taken from short scripts (Farag et al., 2010
). In the same study, patients with progressive non-fluent aphasia and behavioral variant frontotemporal dementia (bvFTD) did not distinguish between more and less closely related events, and structural MRI analysis showed that these patients had significantly more atrophy relative to healthy seniors in a region of interest corresponding to the left ventral frontal activation seen in the fMRI study of healthy young adults (Farag et al., 2010
). These results implicate ventral frontal regions in the processing of discourse cohesion. In a study of language production using the same procedure as the present report, significant cortical atrophy was found in right ventral frontal regions in bvFTD patients, and this correlated with poor local connectedness (Ash et al., 2006
). Another investigation used arterial spin labeling perfusion fMRI in healthy young adults performing a story-telling task with the same stimuli. This study found activation bilaterally in ventral frontal regions on the task of narrating a continuous story relative to describing single, unconnected pictures (Troiani et al., 2008
). Independent evidence that these frontal brain regions contribute to executive resources comes from a variety of imaging studies of healthy adults that show activation of these areas during performance of planning, working memory, and decision-making tasks (Ramnani & Owen, 2004
). The involvement of brain regions in the right hemisphere not typically associated with core elements of language processing is consistent with the hypothesis that the executive resource component of narrative organization is not necessarily linguistic. These converging results imply that impaired discourse cohesion in DLB/PDD patients is related to executive and organizational deficits associated with frontal lobe atrophy.
The regression analysis also related local connectedness to atrophy in the anterior cingulate (BA 32). Previous work has suggested that this area is associated with a component of top-down organization involved in response selection (Botvinick et al., 2001
; Botvinick, Cohen, & Carter, 2004
), and selection has been implicated in the language-mediated deficits of PD patients (Copland, 2006
). The present study suggests that response selection mediated by the anterior cingulate may contribute to decisions about narrative organization as well.
A limitation of the study is the variability of the interval between the narrative task and the MRI scan. The average interval for the 11 patients in our sample is about 7 months. Parkinson's disease progresses slowly, with survival often decades long. In this context, an average discrepancy between behavioral study and image acquisition of 7 months is acceptable. Nevertheless, a larger study is needed to help estimate the maximum acceptable difference that allows reasonable inferences about brain-behavior relationships.
In sum, our findings are consistent with a model of narrative discourse that includes both linguistic and non-linguistic components. It appears that a resource-related deficit in planning and organization interferes with narrative discourse in patients with DLB and PDD. Moreover, this pattern of impairment is related to disease affecting frontal brain regions in these patients.