A longitudinal evaluation of personalized intrinsic network topography and cognitive decline in Parkinson's disease

Resting state functional MRI (R-fMRI) offers insight into how synchrony within and between brain networks is altered in disease states. Individual and disease-related variability in intrinsic connectivity networks may influence our interpretation of R-fMRI data. We used a personalized approach designed to account for individual variation in the spatial location of correlation maxima to evaluate R-fMRI differences between Parkinson's disease (PD) patients who showed cognitive decline, those who remained cognitively stable, and cognitively stable controls. We compared fMRI data from these participant groups, studied at baseline and 18 months later, using both Network-based Statistics (NBS) and calculations of mean inter- and intra-network connectivity within pre-defined functional networks. The NBS analysis showed that PD participants who remained cognitively stable showed exclusively (at baseline) or predominantly (at follow-up) increased intra-network connectivity, whereas decliners showed exclusively reduced intra-network and inter- (ventral attention and default mode) connectivity, in comparison to the control group. Evaluation of mean connectivity between all ROIs within a priori networks showed that decliners had consistently reduced inter-network connectivity for ventral attention, somatomotor, visual, and striatal networks, and reduced intra-network connectivity for ventral attention network to striatum and cerebellum. These findings suggest that specific functional connectivity covariance patterns differentiate PD cognitive subtypes and may predict cognitive decline. Further, increased intra and internetwork synchrony may support cognitive function in the face of PD-related network disruptions.

[1]  L. Defebvre,et al.  Resting‐State Functional Connectivity in Frontostriatal and Posterior Cortical Subtypes in Parkinson's Disease‐Mild Cognitive Impairment , 2021, Movement disorders : official journal of the Movement Disorder Society.

[2]  M. Tittgemeyer,et al.  The default mode network and cognition in Parkinson's disease: A multimodal resting‐state network approach , 2021, Human brain mapping.

[3]  H. Berendse,et al.  Functional connectivity between resting-state networks reflects decline in executive function in Parkinson’s disease: A longitudinal fMRI study , 2020, NeuroImage: Clinical.

[4]  M. Filippi,et al.  Longitudinal brain connectivity changes and clinical evolution in Parkinson’s disease , 2020, Molecular Psychiatry.

[5]  W. He,et al.  Functional Connectivity in Parkinson’s Disease Patients with Mild Cognitive Impairment , 2020, International journal of general medicine.

[6]  H. Jacobs,et al.  Resting-state fMRI in Parkinson's disease patients with cognitive impairment: A meta-analysis. , 2019, Parkinsonism & related disorders.

[7]  Matthew F. Glasser,et al.  Ciftify: A framework for surface-based analysis of legacy MR acquisitions , 2018, NeuroImage.

[8]  Hai-long Lin,et al.  Abnormal resting‐state functional connectivity in posterior cingulate cortex of Parkinson's disease with mild cognitive impairment and dementia , 2018, CNS neuroscience & therapeutics.

[9]  Sterling C. Johnson,et al.  Longitudinal white matter microstructural change in Parkinson's disease , 2018, Human brain mapping.

[10]  A. Strafella,et al.  Dynamic functional connectivity in Parkinson's disease patients with mild cognitive impairment and normal cognition , 2017, NeuroImage: Clinical.

[11]  Erin W. Dickie,et al.  Personalized Intrinsic Network Topography Mapping and Functional Connectivity Deficits in Autism Spectrum Disorder , 2017, Biological Psychiatry.

[12]  L. Calvó-Perxas,et al.  The Trail Making Test , 2017, Assessment (Odessa, Fla.).

[13]  Ludovica Griffanti,et al.  Challenges in the reproducibility of clinical studies with resting state fMRI: An example in early Parkinson's disease , 2016, NeuroImage.

[14]  C. Junqué,et al.  Resting‐State Functional Brain Networks in Parkinson's Disease , 2015, CNS neuroscience & therapeutics.

[15]  D. Lulé,et al.  To rise and to fall: functional connectivity in cognitively normal and cognitively impaired patients with Parkinson's disease , 2015, Neurobiology of Aging.

[16]  D. Eidelberg,et al.  Brain network markers of abnormal cerebral glucose metabolism and blood flow in Parkinson’s disease , 2014, Neuroscience Bulletin.

[17]  T. Robbins,et al.  The CamPaIGN study of Parkinson's disease: 10-year outlook in an incident population-based cohort , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[18]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[19]  Fabrizio Esposito,et al.  Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease , 2012, Neurology.

[20]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[21]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[22]  G. Halliday,et al.  Visual misperceptions and hallucinations in Parkinson's disease: Dysfunction of attentional control networks? , 2011, Movement disorders : official journal of the Movement Disorder Society.

[23]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[24]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[25]  H. Vankova Mini Mental State , 2010 .

[26]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[27]  D. Eidelberg Metabolic brain networks in neurodegenerative disorders: a functional imaging approach , 2009, Trends in Neurosciences.

[28]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[29]  Paolo Calabresi,et al.  Dopamine-mediated regulation of corticostriatal synaptic plasticity , 2007, Trends in Neurosciences.

[30]  R. Nudo Postinfarct Cortical Plasticity and Behavioral Recovery , 2007, Stroke.

[31]  David Eidelberg,et al.  Metabolic brain networks associated with cognitive function in Parkinson's disease , 2007, NeuroImage.

[32]  A. Dagher,et al.  Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. , 2006, Cerebral cortex.

[33]  K. Greve The WCST-64: A Standardized Short-Form of the Wisconsin Card Sorting Test , 2001, The Clinical neuropsychologist.

[34]  W. Rosen,et al.  Verbal fluency in aging and dementia , 1980 .

[35]  I. T. Draper THE ASSESSMENT OF APHASIA AND RELATED DISORDERS , 1973 .

[36]  G. H. Freeman,et al.  Note on an exact treatment of contingency, goodness of fit and other problems of significance. , 1951, Biometrika.

[37]  D. A. Grant,et al.  A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. , 1948, Journal of experimental psychology.

[38]  F. Esposito,et al.  Resting-state functional connectivity associated with mild cognitive impairment in Parkinson’s disease , 2014, Journal of Neurology.

[39]  K A Sigvardt,et al.  Resting state functional connectivity is associated with cognitive dysfunction in non-demented people with Parkinson's disease. , 2014, Journal of Parkinson's disease.

[40]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[41]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[42]  J. Brandt The Hopkins Verbal Learning Test: Development of a new memory test with six equivalent forms. , 1991 .

[43]  S. Fahn Unified Parkinson's Disease Rating Scale , 1987 .

[44]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.