The impact of localized grey matter damage on neighboring connectivity: posterior cortical atrophy and the visual network

Posterior cortical atrophy (PCA), a localized neurodegenerative syndrome involving the occipito-parietal cortices, can serve as a good model to elaborate on the consequence of a localized damage on the anatomical and functional connectivity within an affected system. Ten PCA patients and 14 aged-matched controls were enrolled. Structural connectivity was measured via Diffusion Tensor Imaging (DTI) and probabilistic tractography. The optic tracts and radiations and the splenial fibers were delineated and their microstructural properties were evaluated. Functional connectivity was measured by resting state functional MRI (rsfMRI). Voxel-based morphometry (VBM) was used to assess atrophy. Dorsal stream visual functions were tested and correlation between these behavioral data, volume measures, white matter integrity and connectivity were examined. Impaired white matter integrity was evident in patients’ optic radiations and occipito-callosal fibers, in the segments located in close proximity to the occipital cortex, suggesting a localized damage. Degeneration did not proceed to the optic tracts, opposing trans-synaptic changes. rsfMRI revealed reduced connectivity within the visual network and between the visual and other related areas such as the frontal eye field. Correlations were found between grey matter volume and spatial perception abilities and between the integrity of the affected fibers and motion perception. White matter involvement in PCA seems to be grey matter dependent. Functional connectivity, on the other hand, showed a more diffuse pattern of damage. Correlations were found between the integrity of the affected fibers and patients’ visual abilities suggesting that fiber integrity plays a role in determining behavioral manifestation.

[1]  Cindee M. Madison,et al.  Loss of functional connectivity is greater outside the default mode network in nonfamilial early-onset Alzheimer's disease variants , 2015, Neurobiology of Aging.

[2]  J. Liberman,et al.  Rater agreement for the Rey-Osterrieth Complex Figure Test. , 1994, Journal of clinical psychology.

[3]  Ó. Gonçalves,et al.  Posterior cortical atrophy and Alzheimer’s disease: a meta-analytic review of neuropsychological and brain morphometry studies , 2013, Brain Imaging and Behavior.

[4]  Elisabetta Coppi,et al.  Brain changes within the visuo-spatial attentional network in posterior cortical atrophy. , 2014, Journal of Alzheimer's disease : JAD.

[5]  Jun Soo Kwon,et al.  Clinical and empirical applications of the Rey–Osterrieth Complex Figure Test , 2006, Nature Protocols.

[6]  K. Greve,et al.  Construct Validity and Predictive Value of the Hooper Visual Organization Test in Stroke Rehabilitation , 2000 .

[7]  E. S. Gollin,et al.  Developmental Studies of Visual Recognition of Incomplete Objects , 1960 .

[8]  Robert I. Reid,et al.  Characterizing White Matter Tract Degeneration in Syndromic Variants of Alzheimer's Disease: A Diffusion Tensor Imaging Study. , 2015, Journal of Alzheimer's disease : JAD.

[9]  Massimo Filippi,et al.  Ventral and dorsal visual streams in posterior cortical atrophy: A DT MRI study , 2012, Neurobiology of Aging.

[10]  Kiralee M. Hayashi,et al.  The topography of grey matter involvement in early and late onset Alzheimer's disease. , 2007, Brain : a journal of neurology.

[11]  V. Kiviniemi,et al.  The Effect of Gray Matter ICA and Coefficient of Variation Mapping of BOLD Data on the Detection of Functional Connectivity Changes in Alzheimer’s Disease and bvFTD , 2017, Front. Hum. Neurosci..

[12]  F Lhermitte,et al.  Cognitive slowing in Parkinson's disease fails to respond to levodopa treatment , 1989, Neurology.

[13]  G. Bartzokis Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease , 2004, Neurobiology of Aging.

[14]  Heidi Johansen-Berg,et al.  Behavioural relevance of variation in white matter microstructure. , 2010, Current opinion in neurology.

[15]  N. Raz,et al.  Focal demyelinative damage and neighboring white matter integrity: an optic neuritis study , 2015, Multiple sclerosis.

[16]  Nick C. Fox,et al.  Consensus classification of posterior cortical atrophy , 2017, Alzheimer's & Dementia.

[17]  Richard J Krauzlis,et al.  Spatial integration by MT pattern neurons: a closer look at pattern-to-component effects and the role of speed tuning. , 2008, Journal of vision.

[18]  B. Wandell,et al.  Tract Profiles of White Matter Properties: Automating Fiber-Tract Quantification , 2012, PloS one.

[19]  D. Marcus,et al.  White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. , 2005, Archives of neurology.

[20]  S. M. de la Monte,et al.  Quantitation of cerebral atrophy in preclinical and end‐stage alzheimer's disease , 1989, Annals of neurology.

[21]  J. Harrison,et al.  Posterior cortical atrophy. , 1989, Clinical and experimental neurology.

[22]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[23]  G. Benedek,et al.  An investigation of the white matter microstructure in motion detection using diffusion MRI , 2014, Brain Research.

[24]  J. Atkinson,et al.  Normal and anomalous development of visual motion processing: motion coherence and ‘dorsal-stream vulnerability’ , 2003, Neuropsychologia.

[25]  Xenophon Papademetris,et al.  More accurate Talairach coordinates for neuroimaging using non-linear registration , 2008, NeuroImage.

[26]  Jitender Saini,et al.  A study of structural and functional connectivity in early Alzheimer's disease using rest fMRI and diffusion tensor imaging , 2015, International journal of geriatric psychiatry.

[27]  Hyunjin Park,et al.  Structural and functional connectional fingerprints in mild cognitive impairment and Alzheimer’s disease patients , 2017, PloS one.

[28]  N. Raz,et al.  Demyelination affects temporal aspects of perception: An optic neuritis study , 2012, Annals of neurology.

[29]  N. Raz,et al.  Functional neural substrates of posterior cortical atrophy patients , 2015, Journal of Neurology.

[30]  Massimo Filippi,et al.  White Matter Degeneration in Atypical Alzheimer Disease. , 2015, Radiology.

[31]  H. Spinnler,et al.  Poppelreuter-Ghent's Overlapping Figures Test: its sensitivity to age, and its clinical use. , 1995, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[32]  Brent A. Vogt,et al.  Atypical form of Alzheimer's disease with prominent posterior cortical atrophy: A review of lesion distribution and circuit disconnection in cortical visual pathways , 1997, Vision Research.

[33]  Christopher P Benton,et al.  The direction of measured face aftereffects. , 2008, Journal of vision.

[34]  Benson Df,et al.  Posterior cortical atrophy. , 1988, Archives of neurology.

[35]  M. Filippi,et al.  Insights into White Matter Damage in Alzheimer's Disease: From Postmortem to in vivo Diffusion Tensor MRI Studies , 2015, Neurodegenerative Diseases.

[36]  Hao Huang,et al.  DTI tractography based parcellation of white matter: Application to the mid-sagittal morphology of corpus callosum , 2005, NeuroImage.

[37]  Timo Grimmer,et al.  Neuro-cognitive mechanisms of simultanagnosia in patients with posterior cortical atrophy. , 2016, Brain : a journal of neurology.

[38]  R. Jacobsen,et al.  Age-related norms for the Hooper Visual Organization Test. , 1984, Journal of clinical psychology.

[39]  G. Frisoni,et al.  Early and late onset Alzheimer's disease patients have distinct patterns of white matter damage , 2012, Neurobiology of Aging.

[40]  James T Becker,et al.  Detection of visuoperceptual deficits in preclinical and mild Alzheimer's disease , 2009, Journal of clinical and experimental neuropsychology.

[41]  Anthony J. Sherbondy,et al.  ConTrack: finding the most likely pathways between brain regions using diffusion tractography. , 2008, Journal of vision.

[42]  Yoav Benjamini,et al.  Identifying differentially expressed genes using false discovery rate controlling procedures , 2003, Bioinform..

[43]  J. Ghika,et al.  Visual signs and symptoms in patients with the visual variant of Alzheimer disease , 2015, BMC Ophthalmology.