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Impaired planning in Parkinson's disease is reflected by reduced brain activation and connectivity.

ABSTRACT: OBJECTIVE:Parkinson's disease (PD) often entails impairments of executive functions, such as planning. Although widely held that these impairments arise from dopaminergic denervation of the striatum, not all executive functions are affected early on, and the underlying neural dynamics are not fully understood. In a combined longitudinal and cross-sectional study, we investigated how planning deficits progress over time in the early stages of PD compared to matched healthy controls. We used functional magnetic resonance imaging (fMRI) to identify accompanying neural dynamics. METHODS:Seventeen PD patients and 20 healthy controls performed a parametric Tower of London task at two time points separated by ?3 years (baseline and follow-up). We assessed task performance longitudinally in both groups; at follow-up, a subset of participants (14 patients, 19 controls) performed a parallel version of the task during fMRI. We performed meta-analyses to localize regions-of-interest (ROIs), that is, the bilateral dorsolateral prefrontal cortex (DLPFC), inferior parietal cortex, and caudate nucleus, and performed group-by-task analyses and within-group regression analyses of planning-related neural activation. We studied task-related functional connectivity of seeds in the DLPFC and caudate nucleus. RESULTS:PD patients, compared with controls, showed impaired task performance at both time-points, while both groups showed similar performance reductions from baseline to follow-up. Compared to controls, patients showed lower planning-related brain activation together with decreased functional connectivity. CONCLUSION:These findings support the notion that planning is affected early in the PD disease course, and that this impairment in planning is accompanied by decreases in both task-related brain activity and connectivity.

SUBMITTER: Trujillo JP

PROVIDER: S-EPMC5033031 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Impaired planning in Parkinson's disease is reflected by reduced brain activation and connectivity.

Trujillo James P JP Gerrits Niels J H M NJ Vriend Chris C Berendse Henk W HW van den Heuvel Odile A OA van der Werf Ysbrand D YD

Human brain mapping 20150610 9

<h4>Objective</h4>Parkinson's disease (PD) often entails impairments of executive functions, such as planning. Although widely held that these impairments arise from dopaminergic denervation of the striatum, not all executive functions are affected early on, and the underlying neural dynamics are not fully understood. In a combined longitudinal and cross-sectional study, we investigated how planning deficits progress over time in the early stages of PD compared to matched healthy controls. We us ...[more]

PMID: 26096737

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Project description:The identification of reliable biomarkers for early diagnosis and progression tracking of neurodegenerative diseases has become an important objective in clinical neuroscience in the last years. The P3a event-related potential, considered as the neurophysiological hallmark of novelty detection, has been shown to be reduced in Parkinson's disease (PD) and proposed as a sensitive measure for illness duration and severity. Our aim for this study was to explore for the first time whether impaired novelty detection could be observed through phase- and time-locked brain oscillatory activity at early PD. Twenty-seven patients with idiopathic PD at early stages (disease duration <5 years and Hoehn and Yahr stage <3) were included. A healthy control group (n = 24) was included as well. All participants performed an auditory involuntary attention task including frequent and deviant tones while a digital EEG was obtained. A neuropsychological battery was administered as well. Time-frequency representations of power and phase-locked oscillations and P3a amplitudes were compared between groups. We found a significant reduction of power and phase locking of slow oscillations (3-7 Hz) for deviant tones in the PD group compared to controls in the P3a time range (300-550 ms). Also, reduced modulation of late induced (not phase locked) alpha-beta oscillations (400-650 ms, 8-25 Hz) was observed in the PD group after deviant tones onset. The P3a amplitude was predicted by years of evolution in the PD group. Finally, while phase-locked slow oscillations were associated with task behavioral distraction effects, induced alpha-beta activity was related to cognitive flexibility performance. Our results show that novelty detection impairment can be identified in neurophysiological terms from very early stages of PD, and such impairment increases linearly as the disease progresses. Also, induced alpha-beta oscillations underlying novelty detection are related to executive functioning.

Project description:ObjectiveTo use a multimodal approach to assess brain structural pathways and resting state (RS) functional connectivity abnormalities in patients with Parkinson's disease and freezing of gait (PD-FoG).MethodsT1-weighted, diffusion tensor (DT) MRI and RS functional MRI (fMRI) were obtained from 22 PD-FoG patients and 35 controls on a 3.0 T MR scanner. Patients underwent clinical, motor, and neuropsychological evaluations. Gray matter (GM) volumes and white matter (WM) damage were assessed using voxel based morphometry and tract-based spatial statistics, respectively. The pedunculopontine tract (PPT) was studied using tractography. RS fMRI data were analyzed using a model free approach investigating the main sensorimotor and cognitive brain networks. Multiple regression models were performed to assess the relationships between structural, functional, and clinical/cognitive variables. Analysis of GM and WM structural abnormalities was replicated in an independent sample including 28 PD-FoG patients, 25 PD patients without FoG, and 30 healthy controls who performed MRI scans on a 1.5 T scanner.ResultsCompared with controls, no GM atrophy was found in PD-FoG cases. PD-FoG patients showed WM damage of the PPT, corpus callosum, corticospinal tract, cingulum, superior longitudinal fasciculus, and WM underneath the primary motor, premotor, prefrontal, orbitofrontal, and inferior parietal cortices, bilaterally. In PD-FoG, right PTT damage was associated with a greater disease severity. Analysis on the independent PD sample showed similar findings in PD-FoG patients relative to controls as well as WM damage of the genu and body of the corpus callosum and right parietal WM in PD-FoG relative to PD no-FoG patients. RS fMRI analysis showed that PD-FoG is associated with a decreased functional connectivity of the primary motor cortex and supplementary motor area bilaterally in the sensorimotor network, frontoparietal regions in the default mode network, and occipital cortex in the visual associative network.ConclusionsThis study suggests that FoG in PD can be the result of a poor structural and functional integration between motor and extramotor (cognitive) neural systems.

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Impaired planning in Parkinson's disease is reflected by reduced brain activation and connectivity.

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Impaired planning in Parkinson's disease is reflected by reduced brain activation and connectivity.

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