Striatofrontal Deafferentiation in MSA-P: Evaluation with [18F]FDG Brain PET

Background Although cognitive impairment is not a consistent feature of multiple system atrophy (MSA), increasing evidence suggests that cognitive impairment is common in MSA with predominant parkinsonism (MSA-P). It is assumed that the cognitive impairment in MSA-P is caused by the striatal dysfunction and disruption of striatofrontal connections. The aim of this study was to evaluate the relationship between regional glucose metabolism in the frontal cortex and striatum in patients with MSA-P using [18F]FDG brain PET. Methods Twenty-nine patients with MSA-P and 28 healthy controls underwent [18F]FDG brain PET scan. The [18F]FDG brain PET images were semiquantitatively analyzed on the basis of a template in standard space. The regional glucose metabolism of the cerebral cortex and striatum were compared between MSA-P and healthy control groups. The correlations between age, symptom duration, H&Y stage, UPDRS III score, MMSE score, and glucose metabolism in the cerebellum and striatum to glucose metabolism in the frontal cortex were evaluated by multivariate analysis. Results The glucose metabolism in the frontal cortex and striatum in MSA-P patients were significantly lower than those in healthy controls. Glucose metabolism in the striatum was the most powerful determinant of glucose metabolism in the frontal cortex in MSA-P. Only age and glucose metabolism in the cerebellum were independent variables affecting the glucose metabolism in the frontal cortex in healthy controls. Conclusion The decrease in frontal glucose metabolism in MSA-P is related to the decrease in striatal glucose metabolism. This result provided evidence of striatofrontal deafferentiation in patients with MSA-P.

[1]  G. Cosnard,et al.  Comparison of regional cerebral blood flow and glucose metabolism in the normal brain: effect of aging , 2000, Journal of the Neurological Sciences.

[2]  Yen-Hsiang Chang,et al.  Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration , 2009, European journal of neurology.

[3]  R. Parkkola,et al.  Brain glucose metabolism in neuropathologically confirmed multiple system atrophy , 2013, Journal of Neurology.

[4]  Hitoshi Takahashi,et al.  Multiple system atrophy with severe involvement of the motor cortical areas and cerebral white matter , 1998, Journal of the Neurological Sciences.

[5]  K. Nakashima,et al.  Assessment of dementia in patients with multiple system atrophy , 2009, European journal of neurology.

[6]  Yoon-Hee Cha,et al.  Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome , 2012, PloS one.

[7]  Y. Agid,et al.  Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. , 2010, Brain : a journal of neurology.

[8]  Sid Gilman,et al.  Second consensus statement on the diagnosis of multiple system atrophy , 2008 .

[9]  Joseph Tomasch The numerical capacity of the human cortico-pontocerebellar system. , 1969, Brain research.

[10]  K. Leenders,et al.  Typical cerebral metabolic patterns in neurodegenerative brain diseases , 2010, Movement disorders : official journal of the Movement Disorder Society.

[11]  Ji Hyun Ko,et al.  Parkinson's disease cognitive network correlates with caudate dopamine , 2013, NeuroImage.

[12]  Jae Sung Lee,et al.  Metabolic connectivity by interregional correlation analysis using statistical parametric mapping (SPM) and FDG brain PET; methodological development and patterns of metabolic connectivity in adults , 2008, European Journal of Nuclear Medicine and Molecular Imaging.

[13]  K. Ito,et al.  Cognitive impairments in multiple system atrophy , 2008, Neurology.

[14]  G. Linazasoro,et al.  IMAGING β-AMYLOID BURDEN IN AGING AND DEMENTIA , 2008, Neurology.

[15]  Osama Mawlawi,et al.  Imaging Human Mesolimbic Dopamine Transmission with Positron Emission Tomography: I. Accuracy and Precision of D2 Receptor Parameter Measurements in Ventral Striatum , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[16]  C. Büchel,et al.  Voxel‐based morphometry detects cortical atrophy in the Parkinson variant of multiple system atrophy , 2003, Movement disorders : official journal of the Movement Disorder Society.

[17]  Y. Hashizume,et al.  Multiple system atrophy with remarkable frontal lobe atrophy , 1999, Acta Neuropathologica.

[18]  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.

[19]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[20]  Michael Schocke,et al.  Progression of brain atrophy in multiple system atrophy , 2007, Journal of Neurology.

[21]  Nick C Fox,et al.  Longitudinal MRI in progressive supranuclear palsy and multiple system atrophy: rates and regions of atrophy. , 2006, Brain : a journal of neurology.

[22]  M. S. Lee,et al.  Effects of disease duration on the clinical features and brain glucose metabolism in patients with mixed type multiple system atrophy. , 2008, Brain : a journal of neurology.

[23]  V. Dhawan,et al.  Differential diagnosis of parkinsonian syndromes using F-18 fluorodeoxyglucose positron emission tomography , 2013, Neuroradiology.

[24]  Dae Hyuk Moon,et al.  Subregional Patterns of Preferential Striatal Dopamine Transporter Loss Differ in Parkinson Disease, Progressive Supranuclear Palsy, and Multiple-System Atrophy , 2012, The Journal of Nuclear Medicine.

[25]  V. Dhawan,et al.  Changes in network activity with the progression of Parkinson's disease. , 2007, Brain : a journal of neurology.

[26]  Young Eun Kim,et al.  Clinical and imaging characteristics of dementia in multiple system atrophy. , 2013, Parkinsonism & related disorders.

[27]  A. Formiconi,et al.  Brain metabolic correlates of dopaminergic degeneration in de novo idiopathic Parkinson’s disease , 2010, European Journal of Nuclear Medicine and Molecular Imaging.

[28]  P. Lantos,et al.  A quantitative study of the pathological changes in white matter in multiple system atrophy , 2007, Neuropathology : official journal of the Japanese Society of Neuropathology.

[29]  L Junck,et al.  A Relationship between Metabolism in Frontal Lobes and Cerebellum in Normal Subjects Studied with PET , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  E. Tolosa,et al.  A cross-sectional multicenter study of cognitive and behavioural features in multiple system atrophy patients of the parkinsonian and cerebellar type , 2013, Journal of Neural Transmission.

[31]  Karsten Specht,et al.  Voxel-based morphometry and voxel-based relaxometry in multiple system atrophy—A comparison between clinical subtypes and correlations with clinical parameters , 2007, NeuroImage.

[32]  Leanne M Williams,et al.  Preservation of limbic and paralimbic structures in aging , 2005, Human brain mapping.

[33]  W. Poewe,et al.  Cognitive impairment in multiple system atrophy: A position statement by the neuropsychology task force of the MDS multiple system atrophy (MODIMSA) study group , 2014, Movement disorders : official journal of the Movement Disorder Society.

[34]  Jong-Min Lee,et al.  Topographic distribution of cortical thinning in subtypes of multiple system atrophy. , 2013, Parkinsonism & related disorders.

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

[36]  Karl Zilles,et al.  Developmental hemispheric asymmetry of interregional metabolic correlation of the auditory cortex in deaf subjects , 2003, NeuroImage.

[37]  Niall P Quinn,et al.  The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. , 2004, Brain : a journal of neurology.

[38]  Christine Bastin,et al.  Relationships between brain metabolism decrease in normal aging and changes in structural and functional connectivity , 2013, NeuroImage.

[39]  J. Baron,et al.  Relationships between striatal dopamine denervation and frontal executive tests in Parkinson's disease , 1999, Neuroscience Letters.

[40]  P. Lantos,et al.  The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. , 1994, Brain : a journal of neurology.

[41]  T. Révész,et al.  Neuropathological features of multiple system atrophy with cognitive impairment , 2014, Movement disorders : official journal of the Movement Disorder Society.