Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study.

Jason A Martin,Nadine Zimmermann,Jakob Jankowski,Thomas Klockgether,Sebastian Paus,Hans H Schild,Henning Boecker,Lukas Scheef

doi:10.1016/j.nicl.2019.101784

Jason A Martin, Nadine Zimmermann + Show 6 more

Open Access

https://doi.org/10.1016/j.nicl.2019.101784

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Abstract

Many studies have used functional magnetic resonance imaging to unravel the neuronal underpinnings of motor system abnormalities in Parkinson's disease, indicating functional inhibition at the level of basal ganglia-thalamo-cortical motor networks. The study aim was to extend the characterization of functional motor changes in Parkinson's Disease by dissociating between two phases of action (i.e. motor planning and motor execution) during an automated unilateral finger movement sequence with the left and right hand, separately. In essence, we wished to identify neuronal dysfunction and potential neuronal compensation before (planning) and during (execution) automated sequential motor behavior in unmedicated early stage Parkinson's Disease patients. Twenty-two Parkinson's Disease patients (14 males; 53 ± 11 years; Hoehn and Yahr score 1.4 ± 0.6; UPDRS (part 3) motor score 16 ± 6) and 22 healthy controls (14 males; 49 ± 12 years) performed a pre-learnt four finger sequence (index, ring, middle and little finger, in order), either self-initiated (FREE) or externally triggered (REACT), within an 8-second time window. Findings were most pronounced during FREE with the clinically most affected side, where motor execution revealed significant underactivity of contralateral primary motor cortex, contralateral posterior putamen (sensorimotor territory), ipsilateral anterior cerebellum / cerebellar vermis, along with underactivity in supplementary motor area (based on ROI analyses only), corroborating previous findings in Parkinson's Disease. During motor planning, Parkinson's Disease patients showed a significant relative overactivity in dorsolateral prefrontal cortex (DLPFC), suggesting a compensatory overactivity. To a variable extent this relative overactivity in the DLPFC went along with a relative overactivity in the precuneus and the ipsilateral anterior cerebellum/cerebellar vermis Our study illustrates that a refined view of disturbances in motor function and compensatory processes can be gained from experimental designs that try to dissociate motor planning from motor execution, emphasizing that compensatory mechanisms are triggered in Parkinson's Disease when voluntary movements are conceptualized for action.

Highlights

Parkinson's disease is a progressive neurodegenerative disorder caused by loss of striatal dopaminergic projections originating from the substantia nigra (Lees et al, 2009)
To a variable extent this relative overactivity in the dorsolateral prefrontal cortex (DLPFC) went along with a relative overactivity in the precuneus and the ipsilateral anterior cerebellum/cerebellar vermis Our study illustrates that a refined view of disturbances in motor function and compensatory processes can be gained from experimental designs that try to dissociate motor planning from motor execution, emphasizing that compensatory mechanisms are triggered in Parkinson's
Activation for the preparation and motor execution of self-initiated action are shown in the top half of the figure (FREEPLAN and FREEMOTOR, respectively)

Summary

Introduction

Parkinson's disease is a progressive neurodegenerative disorder caused by loss of striatal dopaminergic projections originating from the substantia nigra (Lees et al, 2009). Cardinal motor symptoms in Parkinson's disease include rigidity, tremor, and hypokinesia/akinesia, the latter being a characteristic inability to properly initiate movements at precise temporal and spatial scales that is thought to result from. We aimed to extend the characterization of motorrelated changes in Parkinson's disease, with a specific focus on the conceptualization and planning phase of a forthcoming movement. We employed a sequential motor task that allows the disentanglement of motor planning and motor execution (Boecker et al, 2008; Jankowski et al, 2013), i.e. separately measuring the neural activity during the planning and execution of a pre-learnt sequence of finger movements, either self-initiated (FREE) or externally triggered (REACT) with either the affected or the non-affected hand.

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