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Multimodal MRI Study of Human Brain Connectivity: Cognitive Networks

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Multimodal MRI Study of Human Brain Connectivity: Cognitive Networks Multimodal MRI Study of Human Brain Connectivity: Cognitive Networks Roser Sala Llonch Aquesta tesi doctoral està subjecta a la llicència Reconeixement- NoComercial – Sen seObraDerivada 3.0. Espanya de Creative Commons . Esta tesis doctoral está sujeta a la licencia Reconoc imiento - NoComercial – SinObr aDerivada 3.0. Esp aña de Creative Commons. This doctoral thesis is licensed under the Cre ative Commons Attribution- NonCommercial- NoDeriv s 3.0. Spa in License . Multimodal MRI Study of Human Brain Connectivity: Cognitive Networks Thesis presented by: Roser Sala Llonch to obtain the degree of doctor from the University of Barcelona in accordance with the requirements of the international PhD diploma Supervised by: Dr. Carme Junque´ Plaja, and Dr. David Bartres´ Faz Department of Psychiatry and Clinical Psychobiology Medicine Doctoral Program University of Barcelona 2014 A les meves `avies Barcelona, 13 November 2014 Dr. Carme Junque´ Plaja and Dr. David Bartres´ Faz, Professors at the University of Barcelona, CERTIFY that they have guided and supervised the doctoral thesis entitled ’ Multimodal MRI Study of Human Brain Connectivity: Cog- nitive Networks’ presented by Roser Sala Llonch. They hereby assert that this thesis fulfils the requirements to present her defense to be awarded the title of doctor. Signatures, Dr Carme Junque´ Plaja Dr. David Bartres´ Faz This thesis has been undertaken in the Neuropsychology Group of the Department of Psychiatry and Clinical Psychobiology, Faculty of Medicine, University of Barcelona. The group is a consolidated re- search group by the Generalitat de Catalunya ( grants 2009 SGR941 and 2014 SGR98) and it is part of the Institut d’Investigacions Biom`ediques August Pi i Sunyer (IDIBAPS). The present work has been financially supported by a PhD trainning scholarship of the National Research Program, conferred by the Span- ish Government to the PhD candidate (BES-2011-047053). In addi- tion financial support for the studies was also recieved by the Span- ish Ministerio de Ciencia e Innovaci´on (grants SAF20090748, PSI2010- 16174, and PSI2013-41393), the Instituto Carlos III (grants FIS080036 and FIS1200013), and the Instituto de Mayores y Servicios Sociales (IM- SERSO, grant 2011/200). Contents Foreword v Related academic work vii Glossary of abbreviations xiii Glossary of neuroimaging definitions xv 1 Introduction 1 1.1 MRI and brain connectivity . .1 1.1.1 Diffusion MRI . .3 1.1.2 Functional MRI . .4 Seed-based correlation . .5 Independent Component Analysis (ICA) . .6 Whole-brain connectivity approaches using graph-theory . .6 1.2 Network-based organization of healthy brains . .6 1.3 FMRI during cognitive states . 11 1.3.1 Working memory networks . 12 1.3.2 Episodic memory networks . 12 1.4 FMRI in healthy aging . 15 1.4.1 Compensation vs Dedifferentiation . 16 Compensation . 16 Dedifferentiation . 17 1.4.2 Cognitive Models in aging . 17 The HAROLD model . 17 The CRUNCH model . 18 i The PASA model . 18 1.4.3 Connectivity-related changes in Aging . 18 1.5 Alzheimer’s Disease . 23 1.5.1 Alzheimer’s disease and task-fMRI . 23 1.5.2 Alzheimer’s disease and large-scale networks . 24 2 Hypotheses and Objectives 27 3 Methods 29 3.1 Study Sample . 29 3.1.1 Subjects included in each study . 29 3.2 Acquisition and paradigms . 31 3.2.1 MRI sequences . 31 Structural T1 . 31 Diffusion MRI . 31 Functional MRI . 31 3.2.2 Functional Paradigms . 31 Working memory task . 31 Episodic memory task . 34 3.2.3 Subjects’ selection and clinical/neuropsychological assessment . 34 3.3 Analysis of structural MRI . 34 3.4 Analysis of Diffusion MRI . 35 3.4.1 The DTI approach . 35 3.4.2 Tract Based Spatial Statistics . 36 3.4.3 Tractography . 37 3.5 Analysis of fMRI . 37 3.5.1 Data preprocessing for fMRI data . 37 3.5.2 Image Registration . 38 3.5.3 Model-driven analysis . 39 FEAT for task-fmri . 39 Seed-based correlation for resting fmri . 39 3.5.4 Data-driven analysis . 40 Tensor-ICA for task-fMRI . 41 Temporal Concatenation ICA and dual-regression for resting-fMRI . 42 3.6 Advanced fMRI analysis: whole-brain connectivity . 43 3.6.1 Graph Theory . 43 3.6.2 Other approaches: FSLNets . 47 4 Results 49 5 General Discussion 117 ii 6 Conclusions 127 A Methodological issues in Graph Theory 129 A.1 Introduction and motivation of the study . 129 A.2 Methods . 130 A.2.1 Evaluation of different brain parcellations strategies . 130 A.2.2 Evaluation of networks at different threshold levels . 132 A.3 Results . 132 A.3.1 Network metrics . 134 A.3.2 Correlations with age . 134 B Resum en catal`a 135 Acknowledgments 145 Agra¨ıments 147 Abstract 149 References 153 iii iv FOREWORD This thesis, presented for the degree of Doctor by the University of Barcelona, is the result of different studies carried out over a four-year period at the Depart- ment of Psychiatry and Clinical Psychobiology of the University of Barcelona. During this period, I have obtained the degree of Master in Neuroscience, which is linked to the Doctorate in Medicine Program (Quality Mention MCD2008- 00023; Mention to Excellence MEE2011-0316) at the University of Barcelona. This thesis follows the published papers format, and it includes four published peer-reviewed papers, one paper that is under review process and one unpub- lished study. The 6 studies are presented in the following order: 1. Sala-Llonch, R., Pena˜ Gomez,´ C., Arenaza-Urquijo, E. M., Vidal-Pineiro,˜ D., Bar- gallo,´ N., Junque,´ C., and Bartres-Faz,´ D. (2012b). Brain connectivity during resting state and subsequent working memory task predicts behavioural performance. Cor- tex, 48(9):1187–96 2. Sala-Llonch, R., Palacios, E.M., Junque,´ C., Bargallo,´ N., and Vendrell, P. Functional and structural connectivity of visuospatial and visuoperceptual working memory, Submitted, under revision. 3. Sala-Llonch, R., Arenaza-Urquijo, E. M., Valls-Pedret, C., Vidal-Pineiro,˜ D., Bargallo,´ N., Junque,´ C., and Bartres-Faz,´ D. (2012a). Dynamic functional reorganizations and relationship with working memory performance in healthy aging. Frontiers in human neuroscience, 6(June):152 4. Sala-Llonch, R., Junque,´ C., Arenaza-Urquijo, E. M., Vidal-Pineiro,˜ D., Valls-Pedret, C., Palacios, E. M., Domenech,` S., Salva,` A., Bargallo,´ N., and Bartres-Faz,´ D. (2014). Changes in whole-brain functional networks and memory performance in aging. Neurobiology of aging, 35(10):2193–202 5. Sala-Llonch et al. Whole-brain network interactions and aging. Relationship with cognition. in preparation 6. Sala-Llonch, R., Fortea, J., Bartres-Faz,´ D., Bosch, B., Llado,´ A., Pena˜ Gomez,´ C., Antonell, A., Castellanos-Pinedo, F., Bargallo,´ N., Molinuevo, J. L., and Sanchez-´ Valle, R. (2013). Evolving brain functional abnormalities in PSEN1 mutation carri- ers: a resting and visual encoding fMRI study. Journal of Alzheimer’s disease : JAD, 36(1):165–75 v vi Related Academic Work List of additional publications of the candidate that are not included in the thesis. These papers are the result of collaborative work with other projects during the time of the thesis: 2014 Baggio, H.-C., Segura, B., Sala-Llonch, R., Marti, M.-J., Valldeoriola, F., Compta, Y., Tolosa, E., and Junque,´ C. (2014b). Cognitive impairment and resting-state network connectivity in Parkinson’s disease. Human brain mapping. 2014 Vidal-Pineiro,˜ D., Valls-Pedret, C., Fernandez-Cabello, S., Arenaza-Urquijo, E. M., Sala- Llonch, R., Solana, E., Bargallo, N., Junque, C., Ros, E., and Bartres-Faz,´ D. (2014b). De- creased Default Mode Network connectivity correlates with age-associated structural and cognitive changes. Frontiers in Aging Neuroscience, 6(256). 2014 Baggio, H.-C., Sala-Llonch, R., Segura, B., Marti, M.-J., Valldeoriola, F., Compta, Y., Tolosa, E., and Junque,´ C. (2014a). Functional brain networks and cognitive deficits in Parkin- son’s disease. Human brain mapping, 35(9):4620–34. 2014 Vidal-Pineiro,˜ D., Martin-Trias, P., Arenaza-Urquijo, E. M., Sala-Llonch, R., Clemente, I. C., Mena-Sanchez,´ I., Bargallo,´ N., Falcon,´ C., Pascual-Leone, A., and Bartres-Faz,´ D. (2014a). Task-dependent activity and connectivity predict episodic memory network- based responses to brain stimulation in healthy aging. Brain stimulation, 7(2):287–96. 2013 Arenaza-Urquijo, E. M., Molinuevo, J.-L., Sala-Llonch, R., Sole-Padull´ es,´ C., Balasa, M., Bosch, B., Olives, J., Antonell, A., Llado,´ A., Sanchez-Valle,´ R., Rami, L., and Bartres-Faz,´ D. (2013). Cognitive reserve proxies relate to gray matter loss in cognitively healthy el- derly with abnormal cerebrospinal fluid amyloid-β levels. Journal of Alzheimer’s disease : JAD, 35(4):715–26. 2013 Garc´ıa-Garc´ıa, I., Jurado, M. A., Garolera, M., Segura, B., Sala-Llonch, R., Marques-Iturria,´ I., Pueyo, R., Sender-Palacios, M. J., Vernet-Vernet, M., Narberhaus, A., Ariza, M., and Junque,´ C. (2013). Alterations of the salience network in obesity: a resting-state fMRI study. Human brain mapping, 34(11):2786–97. 2013 Jovicich, J., Marizzoni, M., Sala-Llonch, R., Bosch, B., Bartres-Faz,´ D., Arnold, J., Benninghoff, J., Wiltfang, J., Roccatagliata, L., Nobili, F., Hensch, T., Trankner,¨ A., Schonknecht,¨ P., Leroy, M., Lopes, R., Bordet, R., Chanoine, V., Ranjeva, J.-P., Didic, M., Gros-Dagnac, H., Payoux, P., Zoccatelli, G., Alessandrini, F., Beltramello, A., Bargallo,´ N., Blin, O., and Frisoni, G. B. (2013). Brain morphometry reproducibility in multi-center 3T MRI studies: a comparison of cross-sectional and longitudinal segmentations. NeuroIm- age, 83:472–84. 2013 Moreno*, F., Sala-Llonch*, R., Barandiaran, M., Sanchez-Valle,´ R., Estanga, A., Bartres-´ Faz, D., Sistiaga, A., Alzualde, A., Fernandez,´ E., Mart´ı Masso,´ J. F., Lopez´ de Munain, A., and Indakoetxea, B. n. (2013). Distinctive age-related temporal cortical thinning in asymptomatic granulin gene mutation carriers. Neurobiology of aging, 34(5):1462–8. * (equal contribution) vii viii 2013 Palacios*, E.
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