Altered limbic functional connectivity in individuals with subjective cognitive decline: Converging and diverging findings across Chinese and German cohorts

Author:

Jiang Xueyan123ORCID,Hu Xiaochen4ORCID,Daamen Marcel2ORCID,Wang Xiaoqi1,Fan Chunqiu1,Meiberth Dix24,Spottke Annika25,Roeske Sandra2,Fliessbach Klaus26,Spruth Eike Jakob78,Altenstein Slawek78,Lohse Andrea8,Hansen Niels9,Glanz Wenzel10,Incesoy Enise I.101112ORCID,Dobisch Laura10,Janowitz Daniel13,Rauchmann Boris‐Stephan14ORCID,Ramirez Alfredo26151617ORCID,Kilimann Ingo1819ORCID,Munk Matthias H.2021ORCID,Wang Xiao22,Schneider Luisa‐Sophie22ORCID,Gabelin Tatjana22,Roy Nina2,Wolfsgruber Steffen26,Kleineidam Luca26,Hetzer Stefan23ORCID,Dechent Peter24,Ewers Michael25ORCID,Scheffler Klaus26ORCID,Amthauer Holger27ORCID,Buchert Ralph2728ORCID,Essler Markus29,Drzezga Alexander23031ORCID,Rominger Axel3233ORCID,Krause Bernd J.34ORCID,Reimold Matthias35,Priller Josef783637ORCID,Schneider Anja26ORCID,Wiltfang Jens93839ORCID,Buerger Katharina1325,Perneczky Robert14254041ORCID,Teipel Stefan1819,Laske Christoph2042,Peters Oliver722ORCID,Düzel Emrah1011ORCID,Wagner Michael26ORCID,Jiang Jiehui43ORCID,Jessen Frank2415ORCID,Boecker Henning244ORCID,Han Ying134546ORCID

Affiliation:

1. Department of Neurology Xuanwu Hospital of Capital Medical University Beijing China

2. German Center for Neurodegenerative Diseases (DZNE) Bonn Germany

3. Key Laboratory of Biomedical Engineering of Hainan Province School of Biomedical Engineering Hainan University Haikou China

4. Department of Psychiatry, University of Cologne Medical Faculty Cologne Germany

5. Department of Neurology University of Bonn Bonn Germany

6. University of Bonn Medical Center Department of Neurodegenerative Disease and Geriatric Psychiatry/Psychiatry Bonn Germany

7. German Center for Neurodegenerative Diseases (DZNE) Berlin Germany

8. Department of Psychiatry and Psychotherapy Charité Berlin Germany

9. Department of Psychiatry and Psychotherapy University Medical Center Goettingen University of Goettingen Goettingen Germany

10. German Center for Neurodegenerative Diseases (DZNE) Magdeburg Germany

11. Institute of Cognitive Neurology and Dementia Research (IKND) Otto‐von‐Guericke University Magdeburg Germany

12. Department for Psychiatry and Psychotherapy University Clinic Magdeburg Magdeburg Germany

13. Institute for Stroke and Dementia Research (ISD) University Hospital LMU Munich Munich Germany

14. Department of Psychiatry and Psychotherapy University Hospital LMU Munich Munich Germany

15. Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD) University of Cologne Cologne Germany

16. Division of Neurogenetics and Molecular Psychiatry Department of Psychiatry and Psychotherapy Faculty of Medicine and University Hospital University of Cologne Cologne Germany

17. Department of Psychiatry & Glenn Biggs Institute for Alzheimer's and Neurodegenerative Diseases San Antonio Texas USA

18. German Center for Neurodegenerative Diseases (DZNE) Rostock Germany

19. Department of Psychosomatic Medicine Rostock University Medical Center Rostock Germany

20. German Center for Neurodegenerative Diseases (DZNE) Tuebingen Germany

21. Department of Psychiatry and Psychotherapy University of Tuebingen Tuebingen Germany

22. Charité – Universitätsmedizin Berlin Corporate Member of Freie Universität Berlin and Humboldt‐Universität zu Berlin‐Institute of Psychiatry and Psychotherapy Berlin Germany

23. Berlin Center for Advanced Neuroimaging Charité – Universitätsmedizin Berlin Berlin Germany

24. MR‐Research in Neurosciences, Department of Cognitive Neurology Georg‐August‐University Goettingen Goettingen Germany

25. German Center for Neurodegenerative Diseases (DZNE) Munich Germany

26. Department for Biomedical Magnetic Resonance University of Tuebingen Tuebingen Germany

27. Department of Nuclear Medicine, Charité ‐ Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt‐Universität zu Berlin and Berlin Institute of Health Berlin Germany

28. Department of Diagnostic and Interventional Radiology and Nuclear Medicine University Medical Center Hamburg‐Eppendorf Hamburg Germany

29. Department of Nuclear Medicine University Hospital Bonn Bonn Germany

30. Department of Nuclear Medicine, Faculty of Medicine and University Hospital Cologne University of Cologne Germany

31. Institute of Neuroscience and Medicine (INM‐2), Molecular Organization of the Brain Forschungszentrum Jülich Germany

32. Department of Nuclear Medicine Ludwig‐Maximilian‐University Munich Munich Germany

33. Department of Nuclear Medicine, Inselspital, Bern University Hospital University of Bern Switzerland

34. Department of Nuclear Medicine Rostock University Medical Centre Rostock, Germany

35. Department of Nuclear Medicine and Clinical Molecular Imaging Eberhard‐Karls‐University Tuebingen Germany

36. School of Medicine, Technical University of Munich Department of Psychiatry and Psychotherapy Munich Germany

37. University of Edinburgh and UK DRI Edinburgh UK

38. German Center for Neurodegenerative Diseases (DZNE) Goettingen Germany

39. Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), Department of Medical Sciences University of Aveiro Aveiro Portugal

40. Munich Cluster for Systems Neurology (SyNergy) Munich Munich Germany

41. Ageing Epidemiology Research Unit (AGE), School of Public Health Imperial College London London UK

42. Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy University of Tuebingen Tuebingen Germany

43. Institute of Biomedical Engineering Shanghai University Shanghai China

44. Clinical Functional Imaging Group  Department of Diagnostic and Interventional Radiology University Hospital Bonn Bonn Germany

45. Center of Alzheimer's Disease Beijing Institute for Brain Disorders Beijing China

46. National Clinical Research Center for Geriatric Disorders Beijing China

Abstract

AbstractINTRODUCTIONIt remains unclear whether functional brain networks are consistently altered in individuals with subjective cognitive decline (SCD) of diverse ethnic and cultural backgrounds and whether the network alterations are associated with an amyloid burden.METHODSCross‐sectional resting‐state functional magnetic resonance imaging connectivity (FC) and amyloid‐positron emission tomography (PET) data from the Chinese Sino Longitudinal Study on Cognitive Decline and German DZNE Longitudinal Cognitive Impairment and Dementia cohorts were analyzed.RESULTSLimbic FC, particularly hippocampal connectivity with right insula, was consistently higher in SCD than in controls, and correlated with SCD‐plus features. Smaller SCD subcohorts with PET showed inconsistent amyloid positivity rates and FC–amyloid associations across cohorts.DISCUSSIONOur results suggest an early adaptation of the limbic network in SCD, which may reflect increased awareness of cognitive decline, irrespective of amyloid pathology. Different amyloid positivity rates may indicate a heterogeneous underlying etiology in Eastern and Western SCD cohorts when applying current research criteria. Future studies should identify culture‐specific features to enrich preclinical Alzheimer's disease in non‐Western populations.Highlights Common limbic hyperconnectivity across Chinese and German subjective cognitive decline (SCD) cohorts was observed. Limbic hyperconnectivity may reflect awareness of cognition, irrespective of amyloid load. Further cross‐cultural harmonization of SCD regarding Alzheimer's disease pathology is required.

Funder

National Natural Science Foundation of China

Chinesisch-Deutsche Zentrum für Wissenschaftsförderung

Deutsches Zentrum für Neurodegenerative Erkrankungen

Publisher

Wiley

Subject

Psychiatry and Mental health,Cellular and Molecular Neuroscience,Geriatrics and Gerontology,Neurology (clinical),Developmental Neuroscience,Health Policy,Epidemiology

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