Selective frontal neurodegeneration of the inferior fronto-occipital fasciculus in progressive supranuclear palsy (PSP) demonstrated by diffusion tensor tractography

BackgroundThe clinical presentation in progressive supranuclear palsy (PSP), an atypical parkinsonian disorder, includes varying degrees of frontal dysexecutive symptoms. Using diffusion tensor imaging (DTI) and tractography (DTT), we investigated whether diffusion changes and atrophy of the inferior fronto-occipital fasciculus (IFO) occurs in PSP and if these changes correlate with disease stage and clinical phenotype. The corticospinal tract (CST), which is often involved in PSP, was investigated for comparison.MethodsDTI of the whole brain was performed with a 3 T MR scanner using a single shot-EPI sequence with diffusion encoding in 48 directions. Scans were obtained in patients with PSP (n = 13) and healthy age-matched controls (n = 12). DTT of the IFO and CST was performed with the PRIDE fibre tracking tool (Philips Medical System). Fractional anisotropy (FA) and apparent diffusion coefficient (ADC) were calculated and correlated with disease stage and clinical phenotype.ResultsIn patients with PSP, significantly decreased FA and increased ADC was found in the frontal part of IFO compared with the medial and occipital parts of IFO, as well as compared to controls. Four of the thirteen patients with PSP showed a marked decrease in the number of tracked voxels in the frontal part of IFO. These findings were most pronounced in patients with severe frontal cognitive symptoms, such as dysexecutive problems, apathy and personality change. There was a strong correlation (r2 = -0.84; p < 0,001) between disease stage and FA and ADC values in the CST.ConclusionsDTT for identification of neuronal tracts with subsequent measurement of FA and ADC is a useful diagnostic tool for demonstrating patterns of neuronal tract involvement in neurodegenerative disease. In selected tracts, FA and ADC values might act as surrogate markers for disease stage.

[1]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[2]  B. Ardekani,et al.  Diffusion tensor imaging reliably differentiates patients with schizophrenia from healthy volunteers , 2011, Human brain mapping.

[3]  Hugues Duffau,et al.  Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data , 2010, Cortex.

[4]  R. Bronen,et al.  MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. , 2004, AJNR. American journal of neuroradiology.

[5]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[6]  I. Litvan Update on progressive supranuclear palsy , 2004, Current neurology and neuroscience reports.

[7]  M. Catani,et al.  Diffusion-based tractography in neurological disorders: concepts, applications, and future developments , 2008, The Lancet Neurology.

[8]  David R Williams,et al.  Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges , 2009, The Lancet Neurology.

[9]  A. Rajput,et al.  Progressive Supranuclear Palsy , 2001, Drugs & aging.

[10]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[11]  Anders M. Dale,et al.  White matter tracts associated with set-shifting in healthy aging , 2009, Neuropsychologia.

[12]  S. Brockstedt,et al.  Tracking the neurodegeneration of parkinsonian disorders – a pilot study , 2007, Neuroradiology.

[13]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

[14]  Irene Litvan,et al.  Update on epidemiological aspects of progressive supranuclear palsy , 2003, Movement disorders : official journal of the Movement Disorder Society.

[15]  L. Golbe,et al.  A clinical rating scale for progressive supranuclear palsy. , 2007, Brain : a journal of neurology.

[16]  Volkmar Glauche,et al.  Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. , 2004, Brain : a journal of neurology.

[17]  Norbert Schuff,et al.  White matter damage in frontotemporal dementia and Alzheimer's disease measured by diffusion MRI , 2009, Brain : a journal of neurology.

[18]  Osamu Abe,et al.  Diffusion abnormality in posterior cingulate fiber tracts in Alzheimer’s disease: tract-specific analysis , 2008, Radiation Medicine.

[19]  D. Dickson,et al.  Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders: Dickson/Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders , 2011 .

[20]  Byung‐Chul Lee,et al.  Midbrain atrophy in subcortical ischemic vascular dementia , 2009, Journal of Neurology.

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

[22]  J. Olszewski,et al.  Progressive Supranuclear Palsy: A Heterogeneous Degeneration Involving the Brain Stem, Basal Ganglia and Cerebellum With Vertical Gaze and Pseudobulbar Palsy, Nuchal Dystonia and Dementia , 1964 .

[23]  J. Turner Third Symposium on Parkinson's Disease , 1970 .

[24]  Z. Schwab,et al.  Projection technique for evaluating surgery in Parkinson’s disease , 1969 .

[25]  W. Ondo,et al.  Brain magnetic resonance imaging (MRI) in parkinsonian disorders. , 2009, Parkinsonism & related disorders.

[26]  I. McKeith,et al.  SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders , 2003, Movement disorders : official journal of the Movement Disorder Society.

[27]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[28]  Maria Stamelou,et al.  In vivo demonstration of microstructural brain pathology in progressive supranuclear palsy: A DTI study using TBSS , 2010, Movement disorders : official journal of the Movement Disorder Society.

[29]  M. Behen,et al.  Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. , 2010, Cerebral cortex.

[30]  G. Stebbins,et al.  Diffusion Tensor Imaging in Alzheimer’s Disease and Mild Cognitive Impairment , 2009, Behavioural neurology.

[31]  F. M. Vos,et al.  White matter fractional anisotropy correlates with speed of processing and motor speed in young childhood cancer survivors. , 2009, International journal of radiation oncology, biology, physics.

[32]  P. Karunanayaka,et al.  Diffusion Tensor MR Imaging Reveals Persistent White Matter Alteration after Traumatic Brain Injury Experienced during Early Childhood , 2007, American Journal of Neuroradiology.

[33]  D Perani,et al.  Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy , 2005, Journal of Neurology, Neurosurgery & Psychiatry.