Compensatory cortical mechanisms in Parkinson's disease evidenced with fMRI during the performance of pre-learned sequential movements

Mallol, Rosella; Barrós‐Loscertales, Alfonso; López, Mario Cantín; Belloch, Vicente; Parcet, Maria Antònia; Ávila, César

doi:10.1016/j.brainres.2007.02.046

Cited by 67 publications

(53 citation statements)

References 32 publications

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“…Alternatively, these findings are also consistent with the hypothesis that hyperactivation represents a deficit regulating activity in a brain structure, which can result in a performance decline (Tinaz, Schendan, & Stern, 2008). This contrasts with most studies that instead interpret hyperactivation as due to compensatory processes that can result in more normal performance (e.g., Mallol et al , 2007). …”

Section: Discussioncontrasting

confidence: 72%

Frontostriatal and mediotemporal lobe contributions to implicit higher-order spatial sequence learning declines in aging and Parkinson's disease.

Schendan¹,

Tinaz²,

Maher³

et al. 2013

Behavioral Neuroscience

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Sequence learning depends on the striatal system, but recent findings also implicate the mediotemporal lobe (MTL) system. Schendan, Searl, Melrose, & Stern (2003) found higher-order associative, learning-related activation in the striatum, dorsolateral prefrontal cortex, and the MTL during the early acquisition phase of both implicit and explicit variants of a serial response time task. This functional magnetic resonance imaging (fMRI) study capitalized on this task to determine how changes in MTL function observed in aging and compromised frontostriatal function characteristic of Parkinson’s disease (PD) patients impacts sequence learning and memory under implicit instructions. Brain activity was compared between “Sequence” and “Random” conditions in 12 non-demented PD patients and education and gender matched healthy control participants of whom 12 were age matched (MC) and 14 were younger (YC). Behaviorally, sequence-specific learning of higher-order associations was reduced with aging and changed further with PD and resulted primarily in implicit knowledge in the older participants. FMRI revealed reduced intensity and extent of sequence learning-related activation in older relative to younger people in frontostriatal circuits and the MTL. This was because signal was greater for the Sequence than Random condition in younger people, whereas older people, especially those with PD, showed the opposite pattern. Both older groups also showed increased activation to the task itself relative to baseline fixation. In addition, right MTL showed hypoactivation and left MTL hyperactivation in PD relative to the MC group. The results suggest changes in frontostriatal and MTL activity occur during aging that affect task-related activity and the initial acquisition phase of implicit higher-order sequence learning. In addition, the results suggest that Parkinson’s disease adversely affects processes in the MTL including sequence learning and memory.

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Section: Discussioncontrasting

confidence: 72%

Frontostriatal and mediotemporal lobe contributions to implicit higher-order spatial sequence learning declines in aging and Parkinson's disease.

Schendan¹,

Tinaz²,

Maher³

et al. 2013

Behavioral Neuroscience

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“…skilled finger movements) (Wu et al, 2010b, Yan et al, 2015) and motor learning (Wu et al, 2010a). These increased connectivity patterns in patients were interpreted as compensatory mechanisms during motor control in PD (Eckert et al, 2006, Katschnig et al, 2011, Mallol et al, 2007, Yu et al, 2007). Likewise, altered functional connectivity during general higher-level planning, such as task-shifting (de Bondt et al, 2016, Helmich et al, 2009) and working memory (Trujillo et al, 2015, Weder et al, 1999), have repeatedly been demonstrated in PD.…”

Section: Discussionmentioning

confidence: 99%

Altered praxis network underlying limb kinetic apraxia in Parkinson's disease - an fMRI study

Kübel

Stegmayer

Vanbellingen

et al. 2017

NeuroImage: Clinical

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Parkinson's disease (PD) patients frequently suffer from dexterous deficits impeding activities of daily living. There is controversy whether impaired fine motor skill may stem from limb kinetic apraxia (LKA) rather than bradykinesia. Based on classical models of limb praxis LKA is thought to result when premotor transmission of time-space information of skilled movements to primary motor representations is interrupted. Therefore, using functional magnetic resonance imaging (fMRI) we tested the hypothesis that dexterous deficits in PD are associated with altered activity and connectivity in left parieto-premotor praxis network. Whole-brain analysis of fMRI activity during a task for LKA (coin rotation) showed increased activation of superior and inferior parietal lobule (SPL, IPL) and ventral premotor cortex (vPM) in PD patients compared to controls. For bradykinesia (assessed by finger tapping) a decreased fMRI activity could be detected in patients. Additionally, psychophysical interaction analysis showed increased functional connectivity between IPL and the posterior hippocampi in patients with PD. By contrast, functional connectivity to the right dorsolateral prefrontal cortex was decreased in patients with PD compared to controls.In conclusion, our data demonstrates that dexterous deficits in PD were associated with enhanced fMRI activation of the left praxis network upstream to primary motor areas, mirroring a neural correlate for the behavioral dissociation of LKA and bradykinesia. Furthermore, the findings suggest that patients recruit temporal areas of motor memory as an attempt to compensate for impaired motor skills. Finally, dysexecutive function may contribute to the deficit.

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“…However, these studies analyzed PD patients in a resting state while we refer to microlesion-related subcortical and cortical hypoactivation during movements in comparison to rest. fMRI studies analyzing movements in PD in the OFF medication state usually found decreased [64], [65], [66], [67], [68], [69] or unchanged [15], [16], [39], [70], [71], [72] activity in basal ganglia with cortical motor regions being variably involved in comparison to control subjects perhaps due to various stages of PD and different aspects of movement tasks. As the control group was missing in our study we can only compare our results with fMRI studies focusing on effects of treatment like DBS or levodopa.…”

Section: Discussionmentioning

confidence: 99%

The Subthalamic Microlesion Story in Parkinson's Disease: Electrode Insertion-Related Motor Improvement with Relative Cortico-Subcortical Hypoactivation in fMRI

et al. 2012

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Electrode implantation into the subthalamic nucleus for deep brain stimulation in Parkinson's disease (PD) is associated with a temporary motor improvement occurring prior to neurostimulation. We studied this phenomenon by functional magnetic resonance imaging (fMRI) when considering the Unified Parkinson's Disease Rating Scale (UPDRS-III) and collateral oedema. Twelve patients with PD (age 55.9± (SD)6.8 years, PD duration 9–15 years) underwent bilateral electrode implantation into the subthalamic nucleus. The fMRI was carried out after an overnight withdrawal of levodopa (OFF condition): (i) before and (ii) within three days after surgery in absence of neurostimulation. The motor task involved visually triggered finger tapping. The OFF/UPDRS-III score dropped from 33.8±8.7 before to 23.3±4.8 after the surgery (p<0.001), correlating with the postoperative oedema score (p<0.05). During the motor task, bilateral activation of the thalamus and basal ganglia, motor cortex and insula were preoperatively higher than after surgery (p<0.001). The results became more enhanced after compensation for the oedema and UPDRS-III scores. In addition, the rigidity and axial symptoms score correlated inversely with activation of the putamen and globus pallidus (p<0.0001). One month later, the OFF/UPDRS-III score had returned to the preoperative level (35.8±7.0, p = 0.4).In conclusion, motor improvement induced by insertion of an inactive electrode into the subthalamic nucleus caused an acute microlesion which was at least partially related to the collateral oedema and associated with extensive impact on the motor network. This was postoperatively manifested as lowered movement-related activation at the cortical and subcortical levels and differed from the known effects of neurostimulation or levodopa. The motor system finally adapted to the microlesion within one month as suggested by loss of motor improvement and good efficacy of deep brain stimulation.

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Compensatory cortical mechanisms in Parkinson's disease evidenced with fMRI during the performance of pre-learned sequential movements

Cited by 67 publications

References 32 publications

Frontostriatal and mediotemporal lobe contributions to implicit higher-order spatial sequence learning declines in aging and Parkinson's disease.

Frontostriatal and mediotemporal lobe contributions to implicit higher-order spatial sequence learning declines in aging and Parkinson's disease.

Altered praxis network underlying limb kinetic apraxia in Parkinson's disease - an fMRI study

The Subthalamic Microlesion Story in Parkinson's Disease: Electrode Insertion-Related Motor Improvement with Relative Cortico-Subcortical Hypoactivation in fMRI

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