OBJECTIVES: Sex differences permeate many aspects of dementia with Lewy bodies (DLB), including epidemiology, pathogenesis, disease progression, and symptom manifestation. However, less is known about potential sex differences in patterns of neurodegeneration in DLB. Here, we test whether grey matter networks also differ between female and male DLB patients. To assess the specificity of these sex differences to DLB, we additionally investigate sex differences in healthy controls (HCs). METHODS: A total of 119 (68.7 ± 8.4 years) male and 45 female (69.9 ± 9.1 years) DLB patients from three European centres and the Mayo Clinic were included in this study. Additionally, we included 119 male and 45 female age-matched HCs from the Mayo Clinic. Grey matter volumes of 58 cortical, subcortical, cerebellar, and pontine brain regions derived from structural magnetic resonance images were corrected for age, intracranial volume, and centre. Sex-specific grey matter networks for DLB patients and HCs were constructed by correlating each pair of brain regions. Network properties of the correlation matrices were compared between sexes and groups. Additional analyses were conducted on W-scored data to identify DLB-specific findings. RESULTS: Networks of male HCs and male DLB patients were characterised by a lower nodal strength compared to their respective female counterparts. In comparison to female HCs, the grey matter networks of male HCs showed a higher global efficiency, modularity, and a lower number of modules. None of the global and nodal network measures showed significant sex differences in DLB. CONCLUSIONS: The disappearance of sex differences in the structural grey matter networks of DLB patients compared to HCs may indicate a sex-dependent network vulnerability to the alpha-synuclein pathology in DLB. Future studies might investigate whether the differences in structural network measures are associated with differences in cognitive scores and clinical symptoms between the sexes.

Center for Age Related Medicine Stavanger University Hospital Stavanger Norway

Day Hospital of Geriatrics Memory Resource and Research Centre of Strasbourg Department of Geriatrics Hopitaux Universitaires de Strasbourg Strasbourg France

Department of Neurology and Alzheimer Center VU University Medical Center Amsterdam Netherlands

Department of Neurology Mayo Clinic Rochester USA

Department of Old Age Psychiatry Institute of Psychiatry Psychology and Neuroscience King's College London London UK

Department of Radiology Mayo Clinic Rochester USA

Division of Clinical Geriatrics Center for Alzheimer Research Department of Neurobiology Care Sciences and Society Karolinska Institutet Stockholm Sweden

Medical Psychology Unit Department of Medicine Institute of Neurosciences University of Barcelona Barcelona Spain

Motol University Hospital Prague Czech Republic

Quantitative Health Sciences Mayo Clinic Rochester MN US

University Hospital of Psychiatry and Psychotherapy Bern University of Bern Bern Switzerland

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Abdelnour Carla, Ferreira Daniel, Oppedal Ketil, Cavallin Lena, Bousiges Olivier, Wahlund Lars Olof, Hort Jakub, et al. 2020. ‘The Combined Effect of Amyloid-β and Tau Biomarkers on Brain Atrophy in Dementia with Lewy Bodies’. NeuroImage: Clinical 27 (January): 102333. 10.1016/j.nicl.2020.102333. PubMed DOI PMC

Avants B. B., Epstein C. L., Grossman M., and Gee J. C.. 2008. ‘Symmetric Diffeomorphic Image Registration with Cross-Correlation: Evaluating Automated Labeling of Elderly and Neurodegenerative Brain’. Medical Image Analysis, Special Issue on The Third International Workshop on Biomedical Image Registration – WBIR 2006, 12 (1): 26–41. 10.1016/j.media.2007.06.004. PubMed DOI PMC

Ballmaier Martina, O’Brien John T., Burton Emma J., Thompson Paul M., Rex David E., Narr Katherine L., McKeith Ian G., DeLuca Heather, and Toga Arthur W.. 2004. ‘Comparing Gray Matter Loss Profiles between Dementia with Lewy Bodies and Alzheimer’s Disease Using Cortical Pattern Matching: Diagnosis and Gender Effects’. NeuroImage 23 (1): 325–35. 10.1016/j.neuroimage.2004.04.026. PubMed DOI

Barnes Lisa L., Lamar Melissa, and Schneider Julie A.. 2019. ‘Sex Differences in Mixed Neuropathologies in Community-Dwelling Older Adults’. Brain Research 1719 (September): 11–16. 10.1016/j.brainres.2019.05.028. PubMed DOI PMC

Bates B. T., Zhang S., Dufek J. S., and Chen F. C.. 1996. ‘The Effects of Sample Size and Variability on the Correlation Coefficient’. Medicine and Science in Sports and Exercise 28 (3): 386–91. 10.1097/00005768-199603000-00015. PubMed DOI

Bayram Ece, Coughlin David G., Banks Sarah J., and Litvan Irene. 2021. ‘Sex Differences for Phenotype in Pathologically Defined Dementia with Lewy Bodies’. Journal of Neurology Neurosurgery and Psychiatry 92 (7): 745–50. 10.1136/jnnp-2020-325668. PubMed DOI PMC

Beach Thomas G., Adler Charles H., Lue LihFen, Sue Lucia I., Bachalakuri Jyothi, Henry-Watson Jonette, Sasse Jeanne, et al. 2009. ‘Unified Staging System for Lewy Body Disorders: Correlation with Nigrostriatal Degeneration, Cognitive Impairment and Motor Dysfunction’. Acta Neuropathologica 117 (6): 613. 10.1007/s00401-009-0538-8. PubMed DOI PMC

van de Beek M., Babapour Mofrad R., van Steenoven I., Vanderstichele H., Scheltens P., Teunissen C. E., Lemstra A. W., and van der Flier W. M.. 2020. ‘Sex-Specific Associations with Cerebrospinal Fluid Biomarkers in Dementia with Lewy Bodies’. Alzheimer’s Research & Therapy 12 (1): 44. 10.1186/s13195-020-00610-9. PubMed DOI PMC

Beheshti Iman, Nugent Scott, Potvin Olivier, and Duchesne Simon. 2021. ‘Disappearing Metabolic Youthfulness in the Cognitively Impaired Female Brain’. Neurobiology of Aging 101 (May): 224–29. 10.1016/j.neurobiolaging.2021.01.026. PubMed DOI

Bustamante-Barrientos Felipe A., Méndez-Ruette Maxs, Ortloff Alexander, Luz-Crawford Patricia, Rivera Francisco J., Figueroa Carlos D., Molina Luis, and Bátiz Luis Federico. 2021. ‘The Impact of Estrogen and Estrogen-Like Molecules in Neurogenesis and Neurodegeneration: Beneficial or Harmful?’ Frontiers in Cellular Neuroscience 15. https://www.frontiersin.org/articles/10.3389/fncel.2021.636176. PubMed DOI PMC

Canales-Rodríguez Erick Jorge, Alonso-Lana Silvia, Verdolini Norma, Sarró Salvador, Feria Isabel, Montoro Irene, Garcia-Ruiz Beatriz, et al. 2021. ‘Age- and Gender-Related Differences in Brain Tissue Microstructure Revealed by Multi-Component T2 Relaxometry’. Neurobiology of Aging 106 (October): 68–79. 10.1016/j.neurobiolaging.2021.06.002. PubMed DOI

Chiu Pai-Yi, Teng Po-Ren, Wei Cheng-Yu, Wang Chein-Wei, and Tsai Chun-Tang. 2018. ‘Gender Difference in the Association and Presentation of Visual Hallucinations in Dementia with Lewy Bodies: A Cross-Sectional Study’. International Journal of Geriatric Psychiatry 33 (1): 193–99. 10.1002/gps.4706. PubMed DOI

Dauwan Meenakshi, van Dellen Edwin, van Boxtel Lotte, van Straaten Elisabeth C. W., de Waal Hanneke, Lemstra Afina W., Gouw Alida A., et al. 2016. ‘EEG-Directed Connectivity from Posterior Brain Regions Is Decreased in Dementia with Lewy Bodies: A Comparison with Alzheimer’s Disease and Controls’. Neurobiology of Aging 41 (May): 122–29. 10.1016/j.neurobiolaging.2016.02.017. PubMed DOI

Dicks Ellen, Tijms Betty M., Kate Mara Ten, Gouw Alida A., Benedictus Marije R., Teunissen Charlotte E., Barkhof Frederik, Scheltens Philip, and van der Flier Wiesje M.. 2018. ‘Gray Matter Network Measures Are Associated with Cognitive Decline in Mild Cognitive Impairment’. Neurobiology of Aging 61 (January): 198–206. 10.1016/j.neurobiolaging.2017.09.029. PubMed DOI

Diez-Cirarda Maria, Gabilondo Iñigo, Ibarretxe-Bilbao Naroa, Gómez-Esteban Juan Carlos, Kim Jinhee, Lucas-Jiménez Olaia, Del Pino Rocio, et al. 2021. ‘Contributions of Sex, Depression, and Cognition on Brain Connectivity Dynamics in Parkinson’s Disease’. Npj Parkinson’s Disease 7 (1): 1–10. 10.1038/s41531-021-00257-9. PubMed DOI PMC

Fereshtehnejad Seyed-Mohammad, Religa Dorota, Westman Eric, Aarsland Dag, Lökk Johan, and Eriksdotter Maria. 2013. ‘Demography, Diagnostics, and Medication in Dementia with Lewy Bodies and Parkinson’s Disease with Dementia: Data from the Swedish Dementia Quality Registry (SveDem)’. Neuropsychiatric Disease and Treatment 9: 927–35. 10.2147/NDT.S45840. PubMed DOI PMC

Ferreira Daniel, Przybelski Scott A., Lesnick Timothy G., Lemstra Afina W., Londos Elisabet, Blanc Frederic, Nedelska Zuzana, et al. 2020. ‘β-Amyloid and Tau Biomarkers and Clinical Phenotype in Dementia with Lewy Bodies’. Neurology 95 (24): e3257–68. 10.1212/WNL.0000000000010943. PubMed DOI PMC

Fujimi Kouhei, Sasaki Kensuke, Noda Kazuhito, Wakisaka Yoshinobu, Tanizaki Yumihiro, Matsui Yukiko, Sekita Atsuko, et al. 2008. ‘Clinicopathological Outline of Dementia with Lewy Bodies Applying the Revised Criteria: The Hisayama Study’. Brain Pathology 18 (3): 317–25. 10.1111/j.17503639.2008.00169.x. PubMed DOI PMC

Gan Jinghuan, Chen Zhichao, Shi Zhihong, Li Xudong, Liu Shuai, Liu Yiming, Zhu Hongcan, et al. 2022. ‘Sex Differences in Clinical Cognitive Impairment with Lewy Bodies: A Chinese Multicenter Study’. Biology of Sex Differences 13 (1): 55. 10.1186/s13293-022-00464-w. PubMed DOI PMC

He Yong, Chen Zhang, and Evans Alan. 2008. ‘Structural Insights into Aberrant Topological Patterns of Large-Scale Cortical Networks in Alzheimer’s Disease’. Journal of Neuroscience 28 (18): 4756–66. 10.1523/JNEUROSCI.0141-08.2008. PubMed DOI PMC

Hua Xue, Hibar Derrek P., Lee Suh, Toga Arthur W., Jack Clifford R., Weiner Michael W., Thompson Paul M., and Alzheimer’s Disease Neuroimaging Initiative. 2010. ‘Sex and Age Differences in Atrophic Rates: An ADNI Study with N=1368 MRI Scans’. Neurobiology of Aging 31 (8): 1463–80. 10.1016/j.neurobiolaging.2010.04.033. PubMed DOI PMC

Jones S. A. Vann, and O’Brien J. T.. 2014. ‘The Prevalence and Incidence of Dementia with Lewy Bodies: A Systematic Review of Population and Clinical Studies’. Psychological Medicine 44 (4): 673–83. 10.1017/S0033291713000494. PubMed DOI

Kane Joseph P. M., Surendranathan Ajenthan, Bentley Allison, Barker Sally A. H., Taylor John-Paul, Thomas Alan J., Allan Louise M., et al. 2018. ‘Clinical Prevalence of Lewy Body Dementia’. Alzheimer’s Research & Therapy 10 (1): 19. 10.1186/s13195-018-0350-6. PubMed DOI PMC

Kantarci Kejal, Lowe Val J., Boeve Bradley F., Senjem Matthew L., Tosakulwong Nikki, Lesnick Timothy G., Spychalla Anthony J., et al. 2017. ‘AV-1451 Tau and β-Amyloid Positron Emission Tomography Imaging in Dementia with Lewy Bodies’. Annals of Neurology 81 (1): 58–67. 10.1002/ana.24825. PubMed DOI PMC

ten Kate Mara, Visser Pieter Jelle, Bakardjian Hovagim, Barkhof Frederik, Sikkes Sietske A. M., van der Flier Wiesje M., Scheltens Philip, et al. 2018. ‘Gray Matter Network Disruptions and Regional Amyloid Beta in Cognitively Normal Adults’. Frontiers in Aging Neuroscience 10. https://www.frontiersin.org/articles/10.3389/fnagi.2018.00067. PubMed DOI PMC

Lemaitre H, Goldman AL, Sambataro F, Verchinski BA, Meyer-Lindenberg A, Weinberger DR, and Mattay VS. 2012. ‘Normal Age-Related Brain Morphometric Changes: Nonuniformity across Cortical Thickness, Surface Area and Grey Matter Volume?’ Neurobiology of Aging 33 (3): 617.e1–617.e9. 10.1016/j.neurobiolaging.2010.07.013. PubMed DOI PMC

Mårtensson Gustav, Pereira Joana B., Mecocci Patrizia, Vellas Bruno, Tsolaki Magda, Kłoszewska Iwona, Soininen Hilkka, et al. 2018. ‘Stability of Graph Theoretical Measures in Structural Brain Networks in Alzheimer’s Disease’. Scientific Reports 8 (1): 11592. 10.1038/s41598-018-29927-0. PubMed DOI PMC

Masuda-Suzukake Masami, Nonaka Takashi, Hosokawa Masato, Oikawa Takayuki, Arai Tetsuaki, Akiyama Haruhiko, Mann David M. A., and Hasegawa Masato. 2013. ‘Prion-like Spreading of Pathological α-Synuclein in Brain’. Brain 136 (4): 1128–38. 10.1093/brain/awt037. PubMed DOI PMC

McKeith I. G., Dickson D. W., Lowe J., Emre M., O’Brien J. T., Feldman H., Cummings J., et al. 2005. ‘Diagnosis and Management of Dementia with Lewy Bodies: Third Report of the DLB Consortium’. Neurology 65 (12): 1863–72. 10.1212/01.wnl.0000187889.17253.b1. PubMed DOI

Mosconi Lisa, Berti Valentina, Dyke Jonathan, Schelbaum Eva, Jett Steven, Loughlin Lacey, Jang Grace, et al. 2021. ‘Menopause Impacts Human Brain Structure, Connectivity, Energy Metabolism, and Amyloid-Beta Deposition’. Scientific Reports 11 (1): 10867. 10.1038/s41598-021-90084-y. PubMed DOI PMC

Mouton A., Blanc F., Gros A., Manera V., Fabre R., Sauleau E., Gomez-Luporsi I., et al. 2018. ‘Sex Ratio in Dementia with Lewy Bodies Balanced between Alzheimer’s Disease and Parkinson’s Disease Dementia: A Cross-Sectional Study’. Alzheimer’s Research & Therapy 10 (September): 92. 10.1186/s13195-018-0417-4. PubMed DOI PMC

Nelson Peter T., Schmitt Frederick A., Jicha Gregory A., Kryscio Richard J., Abner Erin L., Smith Charles D., Van Eldik Linda J., and Markesbery William R.. 2010. ‘Association between Male Gender and Cortical Lewy Body Pathology in Large Autopsy Series’. Journal of Neurology 257 (11): 1875–81. 10.1007/s00415-010-5630-4. PubMed DOI PMC

Newman M. E. J. 2004. ‘Fast Algorithm for Detecting Community Structure in Networks’. Physical Review E 69 (6): 066133. 10.1103/PhysRevE.69.066133. PubMed DOI

Nicastro Nicolas, Mak Elijah, Surendranathan Ajenthan, Rittman Timothy, Rowe James B., and O’Brien John T.. 2021. ‘Altered Structural Connectivity Networks in Dementia with Lewy Bodies’. Brain Imaging and Behavior, January. 10.1007/s11682-020-00444-x. PubMed DOI PMC

Oppedal Ketil, Borda Miguel G, Ferreira Daniel, Westman Eric, and Aarsland Dag. 2019. ‘European DLB Consortium: Diagnostic and Prognostic Biomarkers in Dementia with Lewy Bodies, a Multicenter International Initiative’. Neurodegenerative Disease Management 9 (5): 247–50. 10.2217/nmt-2019-0016. PubMed DOI

Pelkmans Wiesje, Vromen Ellen M., Dicks Ellen, Scheltens Philip, Teunissen Charlotte E., Barkhof Frederik, van der Flier Wiesje M., Tijms Betty M., and Alzheimer’s Disease Neuroimaging Initiative. 2022. ‘Grey Matter Network Markers Identify Individuals with Prodromal Alzheimer’s Disease Who Will Show Rapid Clinical Decline’. Brain Communications 4 (2): fcac026. 10.1093/braincomms/fcac026. PubMed DOI PMC

Peraza Luis R., Kaiser Marcus, Firbank Michael, Graziadio Sara, Bonanni Laura, Onofrj Marco, Colloby Sean J., Blamire Andrew, O’Brien John, and Taylor John-Paul. 2014. ‘FMRI Resting State Networks and Their Association with Cognitive Fluctuations in Dementia with Lewy Bodies’. NeuroImage: Clinical 4 (January): 558–65. 10.1016/j.nicl.2014.03.013. PubMed DOI PMC

Peraza Luis R., Taylor John-Paul, and Kaiser Marcus. 2015. ‘Divergent Brain Functional Network Alterations in Dementia with Lewy Bodies and Alzheimer’s Disease’. Neurobiology of Aging 36 (9): 2458–67. 10.1016/j.neurobiolaging.2015.05.015. PubMed DOI PMC

Pereira Joana B., Mijalkov Mite, Kakaei Ehsan, Mecocci Patricia, Vellas Bruno, Tsolaki Magda, Kłoszewska Iwona, et al. 2016. ‘Disrupted Network Topology in Patients with Stable and Progressive Mild Cognitive Impairment and Alzheimer’s Disease’. Cerebral Cortex (New York, NY) 26 (8): 3476–93. 10.1093/cercor/bhw128. PubMed DOI PMC

Perez F., Helmer C., Dartigues J. F., Auriacombe S., and Tison F.. 2010. ‘A 15-Year Population-Based Cohort Study of the Incidence of Parkinson’s Disease and Dementia with Lewy Bodies in an Elderly French Cohort’. Journal of Neurology, Neurosurgery & Psychiatry 81 (7): 742–46. 10.1136/jnnp.2009.189142. PubMed DOI

Qi Shouliang, Meesters Stephan, Nicolay Klaas, Ter Haar Romeny Bart M., and Ossenblok Pauly. 2015. ‘The Influence of Construction Methodology on Structural Brain Network Measures: A Review’. Journal of Neuroscience Methods 253 (September): 170–82. 10.1016/j.jneumeth.2015.06.016. PubMed DOI

Roberts Rosebud O., Geda Yonas E., Knopman David S., Cha Ruth H., Pankratz V. Shane, Boeve Bradley F., Ivnik Robert J., Tangalos Eric G., Petersen Ronald C., and Rocca Walter A.. 2008. ‘The Mayo Clinic Study of Aging: Design and Sampling, Participation, Baseline Measures and Sample Characteristics’. Neuroepidemiology 30 (1): 58–69. 10.1159/000115751. PubMed DOI PMC

Rubinov Mikail, and Sporns Olaf. 2010. ‘Complex Network Measures of Brain Connectivity: Uses and Interpretations’. NeuroImage, Computational Models of the Brain, 52 (3): 1059–69. 10.1016/j.neuroimage.2009.10.003. PubMed DOI

Sanabria-Diaz Gretel, Melie-García Lester, Iturria-Medina Yasser, Alemán-Gómez Yasser, Hernández-González Gertrudis, Valdés-Urrutia Lourdes, Galán Lídice, and Valdés-Sosa Pedro. 2010. ‘Surface Area and Cortical Thickness Descriptors Reveal Different Attributes of the Structural Human Brain Networks’. NeuroImage 50 (4): 1497–1510. 10.1016/j.neuroimage.2010.01.028. PubMed DOI

Sang Feng, Chen Yaojing, Chen Kewei, Dang Mingxi, Gao Shudan, and Zhang Zhanjun. 2021. ‘Sex Differences in Cortical Morphometry and White Matter Microstructure During Brain Aging and Their Relationships to Cognition’. Cerebral Cortex (New York, N.Y.: 1991) 31 (11): 5253–62. 10.1093/cercor/bhab155. PubMed DOI

Savica Rodolfo, Grossardt Brandon R., Bower James H., Boeve Bradley F., Ahlskog J. Eric, and Rocca Walter A.. 2013. ‘Incidence of Dementia with Lewy Bodies and Parkinson’s Disease Dementia’. JAMA Neurology 70 (11): 1396–1402. 10.1001/jamaneurol.2013.3579. PubMed DOI PMC

Schönbrodt Felix D., and Perugini Marco. 2013. ‘At What Sample Size Do Correlations Stabilize?’ Journal of Research in Personality 47 (5): 609–12. 10.1016/j.jrp.2013.05.009. DOI

Simon Christopher, Soga Tomoko, Okano Hirotaka James, and Parhar Ishwar. 2021. ‘α-Synuclein-Mediated Neurodegeneration in Dementia with Lewy Bodies: The Pathobiology of a Paradox’. Cell & Bioscience 11 (1): 196. 10.1186/s13578-021-00709-y. PubMed DOI PMC

Stam C. J. 2010. ‘Characterization of Anatomical and Functional Connectivity in the Brain: A Complex Networks Perspective’. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology 77 (3): 186–94. 10.1016/j.ijpsycho.2010.06.024. PubMed DOI

Statsenko Yauhen, Habuza Tetiana, Smetanina Darya, Simiyu Gillian Lylian, Uzianbaeva Liaisan, Gorkom Klaus Neidl-Van, Zaki Nazar, et al. 2022. ‘Brain Morphometry and Cognitive Performance in Normal Brain Aging: Age- and Sex-Related Structural and Functional Changes’. Frontiers in Aging Neuroscience 13. https://www.frontiersin.org/article/10.3389/fnagi.2021.713680. PubMed DOI PMC

Strogatz Steven H. 2001. ‘Exploring Complex Networks’. Nature 410 (6825): 268–76. 10.1038/35065725. PubMed DOI

Tijms Betty M., Kate Mara ten, Gouw Alida A., Borta Andreas, Verfaillie Sander, Teunissen Charlotte E., Scheltens Philip, Barkhof Frederik, and van der Flier Wiesje M.. 2018. ‘Gray Matter Networks and Clinical Progression in Subjects with Predementia Alzheimer’s Disease’. Neurobiology of Aging 61 (January): 75–81. 10.1016/j.neurobiolaging.2017.09.011. PubMed DOI

Tremblay Christina, Rahayel Shady, Vo Andrew, Morys Filip, Shafiei Golia, Abbasi Nooshin, Markello Ross D, Gan-Or Ziv, Misic Bratislav, and Dagher Alain. 2021. ‘Brain Atrophy Progression in Parkinson’s Disease Is Shaped by Connectivity and Local Vulnerability’. Brain Communications 3 (4): fcab269. 10.1093/braincomms/fcab269. PubMed DOI PMC

Tsunoda Naoko, Hashimoto Mamoru, Ishikawa Tomohisa, Fukuhara Ryuji, Yuki Seiji, Tanaka Hibiki, Hatada Yutaka, Miyagawa Yusuke, and Ikeda Manabu. 2018. ‘Clinical Features of Auditory Hallucinations in Patients With Dementia With Lewy Bodies: A Soundtrack of Visual Hallucinations’. The Journal of Clinical Psychiatry 79 (3): 1673. 10.4088/JCP.17m11623. PubMed DOI

Utsumi Kumiko, Fukatsu Ryo, and Hara Yuko. 2021. ‘Gender Differences in Initial Symptoms and Symptoms at Diagnosis in Dementia with Lewy Bodies’. Psychogeriatrics 21 (1): 144–45. 10.1111/psyg.12642. PubMed DOI

Verfaillie Sander C. J., Slot Rosalinde E. R., Dicks Ellen, Prins Niels D., Overbeek Jozefien M., Teunissen Charlotte E., Scheltens Philip, Barkhof Frederik, van der Flier Wiesje M., and Tijms Betty M.. 2018. ‘A More Randomly Organized Grey Matter Network Is Associated with Deteriorating Language and Global Cognition in Individuals with Subjective Cognitive Decline’. Human Brain Mapping 39 (8): 3143–51. 10.1002/hbm.24065. PubMed DOI PMC

Voevodskaya Olga, Pereira Joana B., Volpe Giovanni, Lindberg Olof, Stomrud Erik, van Westen Danielle, Westman Eric, and Hansson Oskar. 2018. ‘Altered Structural Network Organization in Cognitively Normal Individuals with Amyloid Pathology’. Neurobiology of Aging 64 (April): 15–24. 10.1016/j.neurobiolaging.2017.11.014. PubMed DOI

Wakabayashi Koichi. 2020. ‘Where and How Alpha-Synuclein Pathology Spreads in Parkinson’s Disease:’ Neuropathology 40 (5): 415–25. 10.1111/neup.12691. PubMed DOI

Warren Jason D., Rohrer Jonathan D., Schott Jonathan M., Fox Nick C., Hardy John, and Rossor Martin N.. 2013. ‘Molecular Nexopathies: A New Paradigm of Neurodegenerative Disease’. Trends in Neurosciences 36 (10): 561–69. 10.1016/j.tins.2013.06.007. PubMed DOI PMC

Yau Y., Zeighami Y., Baker T. E., Larcher K., Vainik U., Dadar M., Fonov V. S., et al. 2018. ‘Network Connectivity Determines Cortical Thinning in Early Parkinson’s Disease Progression’. Nature Communications 9 (1): 12. 10.1038/s41467-017-02416-0. PubMed DOI PMC

Zalesky Andrew, Fornito Alex, Harding Ian H., Cocchi Luca, Yücel Murat, Pantelis Christos, and Bullmore Edward T.. 2010. ‘Whole-Brain Anatomical Networks: Does the Choice of Nodes Matter?’ NeuroImage 50 (3): 970–83. 10.1016/j.neuroimage.2009.12.027. PubMed DOI

Zeighami Yashar, Ulla Miguel, Iturria-Medina Yasser, Dadar Mahsa, Zhang Yu, Larcher Kevin Michel-Herve, Fonov Vladimir, Evans Alan C, Collins D Louis, and Dagher Alain. 2015. ‘Network Structure of Brain Atrophy in de Novo Parkinson’s Disease’. Edited by Van Essen David C. ELife 4 (September): e08440. 10.7554/eLife.08440. PubMed DOI PMC