Motor activation in multiple system atrophy and Parkinson disease

Background: Multiple system atrophy (MSA) is an atypical parkinsonian syndrome including cerebellar impairment and poor response to levodopa. We assessed right hand motor activation in patients with MSA before and after an acute levodopa challenge in comparison with patients with PD and healthy volunteers (HVs). Methods: Eighteen patients with MSA, 8 patients with PD, and 10 age-matched HVs were included. Regional cerebral blood flow measurements with H215O PET were performed at rest and during a right hand movement. Statistical parametric mapping was used to analyze motor vs rest in OFF and ON conditions and the effect of levodopa on motor activation. Results: Before levodopa, patients with MSA activated most known cerebral motor areas. Compared with HVs, patients with MSA exhibited less bilateral cerebellar activation and greater left superior parietal activation. They also had less bilateral cerebellar and greater supplementary motor and left superior parietal activation than patients with PD. Conversely, patients with PD had greater activation than HVs in the right cerebellum and less in the supplementary motor cortex. After levodopa, patients with MSA exhibited reduced activation in anterior cingulate, whereas patients with PD had greater activation in the right cerebellum. Conclusion: Patients with MSA and patients with PD recruited different motor networks. Patients with PD preferentially activated cerebellar pathways, possibly to compensate for basal ganglia dysfunction. This was not observed in patients with MSA, probably because of cerebellar dysfunction; other frontoparietal cortical areas were recruited.

[1]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[2]  W Fernandez,et al.  Impaired activation of the supplementary motor area in Parkinson's disease is reversed when akinesia is treated with apomorphine , 1992, Annals of neurology.

[3]  I Litvan,et al.  Consensus statement on the diagnosis of multiple system atrophy , 1998, Journal of the Neurological Sciences.

[4]  M. Hallett,et al.  A PET study of sequential finger movements of varying length in patients with Parkinson's disease. , 1999, Brain : a journal of neurology.

[5]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[6]  P. Lantos,et al.  Multiple system atrophy (MSA): topographic distribution of the alpha-synuclein-associated pathological changes. , 2006, Parkinsonism & related disorders.

[7]  Richard S. J. Frackowiak,et al.  Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease , 1997, Annals of neurology.

[8]  F. Chollet,et al.  The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. , 1997, Brain : a journal of neurology.

[9]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[10]  N. Quinn,et al.  Multiple system atrophy: A review of 203 pathologically proven cases , 1997, Movement disorders : official journal of the Movement Disorder Society.

[11]  F. Tison,et al.  Routine MRI for the differential diagnosis of Parkinson's disease, MSA, PSP, and CBD , 2003, Journal of Neural Transmission.

[12]  M. Hallett,et al.  International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome , 1997, Journal of the Neurological Sciences.

[13]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[14]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[15]  D. Brooks,et al.  In vivo and in vitro studies of the dopaminergic system in movement disorders. , 1992, Cerebrovascular and brain metabolism reviews.

[16]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[17]  F. Chollet,et al.  Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. , 2000, Brain : a journal of neurology.

[18]  D. Goldstein,et al.  The α-synuclein gene in multiple system atrophy , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[19]  Hong Yu,et al.  Role of hyperactive cerebellum and motor cortex in Parkinson's disease , 2007, NeuroImage.

[20]  K. Nagata,et al.  Primary involvement of the motor area in association with the nigrostriatal pathway in multiple system atrophy: neuropathological and morphometric evaluations , 2000, Acta Neuropathologica.

[21]  U Sabatini,et al.  Supplementary and primary sensory motor area activity in Parkinson's disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. , 1992, Archives of neurology.

[22]  Kyum-Yil Kwon,et al.  Diagnostic value of brain MRI and 18F‐FDG PET in the differentiation of parkinsonian type multiple system atrophy from Parkinson’s disease , 2008, European journal of neurology.

[23]  P. Strick,et al.  The cerebellum communicates with the basal ganglia , 2005, Nature Neuroscience.

[24]  M. Sasaki,et al.  Differentiating between multiple system atrophy and Parkinson’s disease by positron emission tomography with18F-dopa and18F-FDG , 1997, Annals of nuclear medicine.

[25]  B. Choe,et al.  Voxel based comparison of glucose metabolism in the differential diagnosis of the multiple system atrophy using statistical parametric mapping , 2005, Neuroscience Research.

[26]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[27]  Pierre Payoux,et al.  Subthalamic nucleus stimulation reduces abnormal motor cortical overactivity in Parkinson disease. , 2004, Archives of neurology.

[28]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[29]  A. Bol,et al.  Decreased glucose utilization in the striatum and frontal lobe in probable striatonigral degeneration , 1989, Annals of neurology.

[30]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[31]  L. Defebvre,et al.  Motor‐related circuit dysfunction in MSA‐P: Usefulness of combined whole‐brain imaging analysis , 2009, Movement disorders : official journal of the Movement Disorder Society.

[32]  A. Bonnet,et al.  [The Unified Parkinson's Disease Rating Scale]. , 2000, Revue neurologique.