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Visuospatial and Visuoperceptual Impairment and Its Structural Correlates As Measures of Cognitive Decline in Parkinson’S Disease

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Visuospatial and Visuoperceptual Impairment and Its Structural Correlates As Measures of Cognitive Decline in Parkinson’S Disease Visuospatial and visuoperceptual impairment and its structural correlates as measures of cognitive decline in Parkinson’s disease Anna Isabel Garcia Diaz Aquesta tesi doctoral està subjecta a la llicència Reconeixement- NoComercial – SenseObraDerivada 3.0. Espanya de Creative Commons. Esta tesis doctoral está sujeta a la licencia Reconocimiento - NoComercial – SinObraDerivada 3.0. España de Creative Commons. This doctoral thesis is licensed under the Creative Commons Attribution-NonCommercial- NoDerivs 3.0. Spain License. Visuospatial and visuoperceptual impairment and its structural correlates as measures of cognitive decline in Parkinson's disease Anna Isabel Garcia Diaz Unitat de Psicologia Mèdica · Departament de Medicina Facultat de Medicina i Ciències de la Salut Universitat de Barcelona 2018 Visuospatial and visuoperceptual impairment and its structural correlates as measures of cognitive decline in Parkinson’s disease Thesis presented by: Anna Isabel Garcia Diaz To obtain the degree of Doctor from Universitat de Barcelona Supervised by: Dra. Carme Junqué i Plaja Dra. Bàrbara Segura i Fàbregas Unitat de Psicologia Mèdica · Departament de Medicina Facultat de Medicina i Ciències de la Salut Universitat de Barcelona 2018 “It did make the throwaway assumption that the mind was simply the operation of the brain, an idea that struck me with force; it startled my naïve understanding of the world. […] Literature provided a rich account of human meaning; the brain, then, was the machinery that somehow enabled it. It seemed like magic.” Paul Kalanithi- When breath becomes air Als meus pares A la meva germana Dr. Carme Junqué i Plaja and Dr. Bàrbara Segura i Fàbregas, professors at the Universitat de Barcelona, CERTIFY that they have guided and supervised the doctoral thesis entitled ‘Visuospatial and visuoperceptual impairment and its structural correlates as measures of cognitive decline in Parkinson’s disease’ presented by Anna Isa- bel Garcia Diaz. They hereby assert that this thesis fulfills the requirements to present her defense to be granted the title of doctor. Signatures, Dr. Carme Junqué i Plaja Dr. Bàrbara Segura i Fàbregas The present work has been carried out at the Neuropsicologia team (IDIBAPS) and financially supported by the Spanish Ministry of Economy and Competi- tiveness (PSI2013-41393-P), by Generalitat de Catalunya (2014SGR 98) and by Fundació La Marató de TV3 (20142310). CONTENTS Foreword III Glossary of abbreviations V CHAPTER 1. GENERAL INTRODUCTION 1 A general view of Parkinson’s disease 1 Cognitive spectrum in Parkinson’s disease 2 Neurobiological basis of cognitive impairment in Parkinson’s disease 8 Neuropathology and neurobiological mechanisms 8 Neuropathology 8 Neurobiological mechanisms 9 Genetic variations and risk of cognitive impairment 9 Structural neuroimaging in Parkinson’s disease 10 Gray matter degeneration 10 White matter integrity 12 Visual cognition in Parkinson’s disease 14 A foreword on the healthy visual system pathways 14 From the retina to the cortex 14 Vision pathways. The case for functionally specialized visual projections 15 Face recognition 19 Visuoconstructive functions 19 Ocular and visual dysfunction in Parkinson’s disease 20 Visual fields and glaucomatous disturbances 20 Visual acuity 21 Contrast sensitivity 21 Color vision 21 Pupil reactivity 22 Saccades, oculomotor disturbances and convergence 22 Blinking and blink reflex 23 Retinal involvement 24 Visuospatial, visuoperceptual and visuoconstructive impairment in Parkinson’s disease 24 General aspects 25 Visuospatial impairment 29 Spatial orientation 29 Mental rotation, visual transformation and visuospatial problem solving 30 Visuoperceptual impairment 31 Face and object visual perception 31 Space and depth perception 33 Motion detection 34 I Visuoconstructive impairment 34 Closing-in 36 Symbol Digit Modalities Test 37 Relationship with disease variables and cognitive progression 42 Basic visual dysfunction 42 Motor phenotype 42 Visual hallucinations 43 Medication 44 Disease progression and evolution to dementia 44 Neuroanatomical correlates of visual cognition in Parkinson’s disease 45 CHAPTER 2. HYPOTHESES AND OBJECTIVES 53 Hypotheses 53 Objectives 54 CHAPTER 3. METHODS 55 Study samples 55 Neuropsychological assessment 56 Structural neuroimaging techniques 58 MRI acquisition 58 Gray matter degeneration 58 White matter degeneration 59 Statistical analyses 59 CHAPTER 4. RESULTS 60 Study 1 61 Study 2 70 Study 3 83 CHAPTER 5. GENERAL DISCUSSION 103 General cognitive status measures 103 Visuospatial and visuoperceptual impairment 106 Structural degeneration in Parkinson’s disease 110 Concluding remarks 111 CHAPTER 6. CONCLUSIONS 112 Abstract 114 Resum 115 Annex 1 117 Annex 2 118 Agraïments 131 Acknowledgements 134 References 137 II FOREWORD The thesis hereby presented to obtain the degree of Doctor by Universitat de Barcelona is the result of the work carried out over a four-year period at the Unitat de Psicologia Mèdica of the Departament de Medici- na, Facultat de Medicina i Ciències de la Salut. Following a format based on published articles, this thesis includes three papers published in peer-reviewed journals as follows: 1. Garcia-Diaz AI, Segura B, Baggio HC, Marti MJ, Valldeoriola F, Compta Y, Vendrell P, Bargallo N, Tolosa E, Junque C. Structural MRI correlates of the MMSE and pentagon copying test in Parkinson's disease. Parkinsonism Relat Disord 2014; 12:1405-10 2. Garcia-Diaz AI, Segura B, Baggio HC, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Uribe C, Campabadal A, Abos A, Junque C. Structural Brain Correlations of Visuospatial and Visuoper- ceptual Tests in Parkinson’s Disease. J Int Neuropsychol Soc 2018; 24:33-44. 3. Garcia-Diaz AI, Segura B, Baggio HC, Uribe C, Campabadal A, Abos A, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Junque C. Cortical thinning correlates of changes in visuospatial and visuoperceptual performance in Parkinson’s disease: A 4-year follow-up. Parkinsonism Relat Dis- ord, 2018; 46:62-8. During this period, the candidate has collaborated in additional related academic works, published as follows: 1. Garcia-Diaz AI, Segura B, Baggio HC, Junque C. Visuospatial and visuoperceptual impairment in relation to global atrophy in Parkinson’s disease. UB J Psychol 2013;2:147-58. 2. Segura B, Baggio HC, Marti MJ, Valldeoriola F, Compta Y, Garcia-Diaz AI, Vendrell P, Bargallo N, Tolosa E, Junque C. Cortical Thinning Associated with Mild Cognitive Impairment in Parkin- son’s Disease. Mov Disord 2014; 29:1495-503. 3. Abós A, Baggio HC, Segura B, Garcia-Diaz AI, Compta Y, Marti MJ, Valldeoriola F, Junque C. Discriminating cognitive status in Parkinson’s disease through functional connectomics and ma- chine learning. Sci Rep 7:45347. 4. Campabadal A, Uribe C, Segura B, Baggio HC, Abos A, Garcia-Diaz AI, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Junque C. Brain correlates of progressive olfactory loss in Parkinson’s disease. Parkinsonism Relat Disord 2017;41:44-50. III 5. Campabadal A, Segura B, Baggio HC, Abos A, Uribe C, Garcia-Diaz AI, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Junque C. The use of the University of Pennsylvania Smell Identifica- tion Test in Parkinson’s disease- diagnostic accuracy and item analysis in a Spanish population (submitted) IV GLOSSARY OF ABBREVIATIONS 3MS Modified Mini-Mental State MAPT Microtubule associated protein tau AD Alzheimer’s disease MCI Mild cognitive impairment APOE Apolipoprotein E MD Mean diffusivity BNT Boston Naming Test MDS Movement Disorders Society BPP Bistable Perceptual Paradigm Met Methionine CDIC Centre de Diagnòstic per la Imatge Clínic MMSE Mini-Mental State Examination CDR Clinical Dementia Rating scale MoCA Montreal Cognitive Assessment COMT Catechol-O-methyltransferase MRI Magnetic resonance imaging CSF Cerebrospinal fluid PCT Pentagon Copying Test DAT Dopamine transporter PD Parkinson’s disease DLB Dementia with Lewy bodies PDD Parkinson’s disease dementia DSM Diagnostic and Stastistical Manual of Mental Disorders PD-MCI Parkinson’s disease mild cognitive impairment DTI Diffusion tensor imaging RAVLT Rey Auditory Verbal Learning Test DWI Diffusion weighted imaging RD Radial diffusivity EEG Electroencephalography RBD REM-sleep behavior disorder FA Fractional anisotropy REM Rapid eye movement FDG-PET Fludeoxyglucose Positron Emission Tomography ROFC Rey-Osterrieth Figure Copy FLAIR Fluid-Attenuated Inversion Recovery ROI Region of interest fMRI Functional Magnetic Resonance Imaging SDMT Symbol Digit Modalities Test FRT Facial Recognition Test SPECT Single-photon emission computed tomography FWE Family wise error TBSS Tract-based Spatial Statistics GBA Glucosylceramidase TMT Trail Making Test H&Y Hoehn & Yahr scale UPDRS Unified Parkinson’s disease Rating Scale ICV Intracranial volume Val Valine JHU John Hopkins University atlas VBM Voxel-based morphometry JLOT Judgment of Line Orientation Test VFDT Visual Form Discrimination Test LGN Lateral geniculate nucleus VVT Vienna Visuo-constructional Test MAO Monoamine oxidase WAIS Wechsler Adult Intelligence Scale V CHAPTER 1. GENERAL INTRODUCTION A GENERAL VIEW OF PARKINSON’S DISEASE Parkinson’s disease (PD) is the most common neurodegenerative disorder after Alzheimer’s disease (AD) and its incidence is expected to only rise as worldwide populations age, especially in developing Eastern nations (Dorsey et al., 2007). The prevalence of PD in industrialized countries is estimated at approximately 1% at 60 years of age or older (Nussbaum & Ellis, 2003), and it is rarely seen
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