Increased fractional anisotropy in the motor tracts of Parkinson's disease suggests compensatory neuroplasticity or selective neurodegeneration

AbstractObjectiveTo determine the differences in motor pathways and selected non-motor pathways of the basal ganglia in Parkinson’s disease (PD) patients compared to healthy controls (HCs).MethodsWe analysed diffusion weighted imaging data of 24 PD patients and 26 HCs. We performed deterministic tractography analysis using the spherical deconvolution-based damped Richardson-Lucy algorithm and subcortical volume analysis.ResultsWe found significantly increased fractional anisotropy (FA) in the motor pathways of PD patients: the bilateral corticospinal tract (right; corrected p = 0.0003, left; corrected p = 0.03), bilateral thalamus-motor cortex tract (right; corrected p = 0.02, left; corrected p = 0.004) and the right supplementary area-putamen tract (corrected p = 0.001). We also found significantly decreased FA in the right uncinate fasiculus (corrected p = 0.01) and no differences of FA in the bilateral supero-lateral medial forebrain bundles (p > 0.05) of PD patients compared to HCs. There were no subcortical volume differences (p > 0.05) between the PD patients and HCs.ConclusionThese results can inform biological models of neurodegeneration and neuroplasticity in PD. We suggest that increased FA values in the motor tracts in PD may reflect compensatory reorganization of neural circuits indicative of adaptive or extended neuroplasticity.Key points• Fractional anisotropy was higher in motor pathways of PD patients compared to healthy controls. • Fractional anisotropy was lower in the uncinate fasciculus of PD patients compared to healthy controls. • Increased fractional anisotropy could suggest adaptive neuroplasticity or selective neurodegeneration.

[1]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[2]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[3]  H. Bergman,et al.  Redundant dopaminergic activity may enable compensatory axonal sprouting in Parkinson disease , 2014, Neurology.

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

[5]  P. Bhattacharya.  Diffusion MRI: Theory, methods, and applications, Derek K. Jones (Ed.). Oxford University press (2011), $152.77 , 2012 .

[6]  Derek K. Jones,et al.  Frontotemporal Connections in Episodic Memory and Aging: A Diffusion MRI Tractography Study , 2011, The Journal of Neuroscience.

[7]  G. B. Pike,et al.  Quantitative magnetization transfer and myelin water imaging of the evolution of acute multiple sclerosis lesions , 2010, Magnetic resonance in medicine.

[8]  Dorothee P. Auer,et al.  Diffusion tensor imaging of nigral degeneration in Parkinson's disease: A region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis☆ , 2013, NeuroImage: Clinical.

[9]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[10]  J. Attems,et al.  White matter connections of the supplementary motor area in humans , 2014, Journal of Neurology, Neurosurgery & Psychiatry.

[11]  Derek K. Jones.  Diffusion MRI: Theory, methods, and applications , 2011 .

[12]  Alexander Leemans,et al.  The B‐matrix must be rotated when correcting for subject motion in DTI data , 2009, Magnetic resonance in medicine.

[13]  J. Mink.  THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[14]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[15]  Erwan Bezard,et al.  Presymptomatic compensation in Parkinson's disease is not dopamine-mediated , 2003, Trends in Neurosciences.

[16]  H. Braak,et al.  Stanley Fahn Lecture 2005: The staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered , 2006, Movement disorders : official journal of the Movement Disorder Society.

[17]  Derek K. Jones,et al.  Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time , 2002, Human brain mapping.

[18]  D. Hackney,et al.  Diffusional anisotropy in cranial nerves with maturation: quantitative evaluation with diffusion MR imaging in rats. , 2000, Radiology.

[19]  Luis Concha,et al.  Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients , 2006, NeuroImage.

[20]  N. Intrator,et al.  Free water elimination and mapping from diffusion MRI , 2009, Magnetic resonance in medicine.

[21]  Roger A. Barker,et al.  White matter pathology in Parkinson's disease: The effect of imaging protocol differences and relevance to executive function , 2012, NeuroImage.

[22]  B. Bloem,et al.  Update on diffusion MRI in Parkinson's disease and atypical parkinsonism , 2013, Journal of the Neurological Sciences.

[23]  Derek K. Jones,et al.  Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging , 2013, Human brain mapping.

[24]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[25]  Derek K. Jones,et al.  Cingulum Microstructure Predicts Cognitive Control in Older Age and Mild Cognitive Impairment , 2012, The Journal of Neuroscience.

[26]  Yaniv Assaf,et al.  Can we use diffusion MRI as a bio-marker of neurodegenerative processes? , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[28]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[29]  J. Frank,et al.  The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. , 2011, Brain : a journal of neurology.

[30]  C Caltagirone,et al.  The Corticospinal Tract in Huntington's Disease. , 2015, Cerebral cortex.

[31]  Christopher Bishop,et al.  Critical involvement of the motor cortex in the pathophysiology and treatment of Parkinson's disease , 2013, Neuroscience & Biobehavioral Reviews.

[32]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[33]  I. Olson,et al.  Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. , 2013, Brain : a journal of neurology.

[34]  Hartwig R. Siebner,et al.  Abnormal dopaminergic modulation of striato-cortical networks underlies levodopa-induced dyskinesias in humans , 2015, Brain : a journal of neurology.

[35]  Volker A Coenen,et al.  Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression. , 2012, The Journal of neuropsychiatry and clinical neurosciences.

[36]  G. Winston.  The physical and biological basis of quantitative parameters derived from diffusion MRI. , 2012, Quantitative imaging in medicine and surgery.

[37]  D. Jones,et al.  Hedonic tone is associated with left supero-lateral medial forebrain bundle microstructure , 2014, Psychological Medicine.

[38]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

[39]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.