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Cerebello-cerebral Functional Connectivity Networks in Major Depressive Disorder: a CAN-BIND-1 Study Report

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Abstract

Neuroimaging studies have demonstrated aberrant structure and function of the “cognitive-affective cerebellum” in major depressive disorder (MDD), although the specific role of the cerebello-cerebral circuitry in this population remains largely uninvestigated. The objective of this study was to delineate the role of cerebellar functional networks in depression. A total of 308 unmedicated participants completed resting-state functional magnetic resonance imaging scans, of which 247 (148 MDD; 99 healthy controls, HC) were suitable for this study. Seed-based resting-state functional connectivity (RsFc) analysis was performed using three cerebellar regions of interest (ROIs): ROI1 corresponded to default mode network (DMN)/inattentive processing; ROI2 corresponded to attentional networks, including frontoparietal, dorsal attention, and ventral attention; ROI3 corresponded to motor processing. These ROIs were delineated based on prior functional gradient analyses of the cerebellum. A general linear model was used to perform within-group and between-group comparisons. In comparison to HC, participants with MDD displayed increased RsFc within the cerebello-cerebral DMN (ROI1) and significantly elevated RsFc between the cerebellar ROI1 and bilateral angular gyrus at a voxel threshold (p < 0.001, two-tailed) and at a cluster level (p < 0.05, FDR-corrected). Group differences were non-significant for ROI2 and ROI3. These results contribute to the development of a systems neuroscience approach to the diagnosis and treatment of MDD. Specifically, our findings confirm previously reported associations between MDD, DMN, and cerebellum, and highlight the promising role of these functional and anatomical locations for the development of novel imaging-based biomarkers and targets for neuromodulation therapies. ClinicalTrials.gov TRN: NCT01655706; Date of Registration: August 2nd, 2012.

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Acknowledgements

The authors would like to acknowledge the contributions of Mojdeh Zamyadi and Jacqueline Harris for data quality control, Andrew Davis and Geoffrey Hall for sequence assessment and standardization, Yuelee Khoo for statistical analysis of the demographics data, and Alice Rueda for analysis of the neuroimaging data.

Funding

Canadian Biomarker Integration Network in Depression (CAN-BIND) is an Integrated Discovery Program carried out in partnership with, and financial support from, the Ontario Brain Institute, an independent non-profit corporation, funded partially by the Ontario government. The opinions, results, and conclusions are those of the authors and no endorsement by the Ontario Brain Institute is intended or should be inferred. Additional funding was provided by Canadian Institutes of Health Research, Lundbeck, Bristol Myers Squibb, and Servier. Funding and/or in-kind support was also provided by the investigators’ academic institutions.

Author information

Authors and Affiliations

  1. Department of Psychology, Northeastern University, Boston, MA, USA

    Sheeba Arnold Anteraper, Yoon Ji Lee, Jovicarole Raya & Susan Whitfield-Gabrieli

  2. Carle Foundation Hospital, Urbana, IL, USA

    Sheeba Arnold Anteraper

  3. Alan and Lorraine Bressler Clinical and Research Program for Autism Spectrum Disorder, Massachusetts General Hospital, Boston, MA, USA

    Sheeba Arnold Anteraper

  4. Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA

    Xavier Guell

  5. Interventional Psychiatry Program, St. Michael’s Hospital, 193 Yonge Street 6-013, Toronto, ON, M5B 1M8, Canada

    Ilya Demchenko, Sidney H. Kennedy & Venkat Bhat

  6. Keenan Research Centre for Biomedical Science, St. Michael’s Hospital, Toronto, ON, Canada

    Nathan W. Churchill & Tom A. Schweizer

  7. Neuroscience Research Program, St. Michael’s Hospital, Toronto, ON, Canada

    Nathan W. Churchill, Tom A. Schweizer, Sidney H. Kennedy & Venkat Bhat

  8. Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ON, Canada

    Benicio N. Frey

  9. Mood Disorders Program and Women’s Health Concerns Clinic, St. Joseph’s Healthcare Hamilton, Hamilton, ON, Canada

    Benicio N. Frey

  10. Department of Psychiatry and the Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada

    Stefanie Hassel & Glenda M. MacQueen

  11. Department of Psychiatry, University of British Columbia, Vancouver, BC, Canada

    Raymond W. Lam

  12. Departments of Psychiatry and Psychology, Queen’s University, Kingston, ON, Canada

    Roumen Milev

  13. Providence Care, Kingston, ON, Canada

    Roumen Milev

  14. Rotman Research Institute, Baycrest Health Sciences, Toronto, ON, Canada

    Stephen C. Strother

  15. Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada

    Stephen C. Strother

  16. Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, USA

    Susan Whitfield-Gabrieli

  17. Institute of Medical Science, University of Toronto, Toronto, ON, Canada

    Sidney H. Kennedy & Venkat Bhat

  18. Department of Psychiatry, University of Toronto, Toronto, ON, Canada

    Sidney H. Kennedy & Venkat Bhat

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  1. Sheeba Arnold Anteraper
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  2. Xavier Guell
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  3. Yoon Ji Lee
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CAN-BIND Investigator Team

Contributions

Study conceptualization: Sheeba Arnold Anteraper, Venkat Bhat; methodology development: Sheeba Arnold Anteraper, Nathan. W. Churchill, Venkat Bhat; formal analysis and investigation: Nathan W. Churchill, Tom A. Schweizer, Venkat Bhat; writing — original draft preparation: Sheeba Arnold Anteraper, Xavier Guell, Ilya Demchenko, Venkat Bhat; writing — review and editing: Sheeba Arnold Anteraper, Xavier Guell, Yoon Ji Lee, Jovicarole Raya, Ilya Demchenko, Nathan W. Churchill, Benicio N. Frey, Stefanie Hassel, Raymond W. Lam, Glenda M. MacQueen, Roumen Milev, Tom A. Schweizer, Stephen C. Strother, Susan Whitfield-Gabrieli, Sidney H. Kennedy, Venkat Bhat. All authors read and approved the final version of the manuscript. The data acquisition was supported by the CAN-BIND Investigator Team. There were no separate resources for this project.

Corresponding author

Correspondence to Venkat Bhat.

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Ethics Approval

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. All study procedures were approved by the Institutional Ethics Board at University Health Network, Toronto, Ontario, Canada; Centre for Addiction and Mental Health, Toronto, Ontario, Canada; St. Joseph’s Healthcare, Hamilton, Ontario, Canada; Providence Care Hospital, Kingston, Ontario, Canada; Djavad Mowafaghian Centre for Brain Health, Vancouver, British Columbia, Canada; and Hotchkiss Brain Institute, Calgary, Alberta, Canada.

Consent to Participate and Publish

All participants provided written, informed consent to participate in the study and have their data published.

Conflict of Interest

SAA, XG, YJL, JR, ID, NWC, BNF, SH, GMM, TAS, and SWG have no conflicts of interest to declare. RWL has received honoraria or research funds from Allergan, Asia–Pacific Economic Cooperation, BC Leading Edge Foundation, Canadian Institutes of Health Research, Canadian Network for Mood and Anxiety Treatments, Canadian Psychiatric Association, Hansoh, Healthy Minds Canada, Janssen, Lundbeck, Lundbeck Institute, Mitacs, Myriad Neuroscience, Ontario Brain Institute, Otsuka, Pfizer, St. Jude Medical, University Health Network Foundation, and VGH-UBC Hospital Foundation. RM has received consulting and speaking honoraria from AbbVie, Allergan, Eisai, Janssen, KYE, Lallemand, Lundbeck, Otsuka, and Sunovion, and research grants from CAN-BIND, Canadian Institutes of Health Research, Janssen, Lallemand, Lundbeck, Nubiyota, Ontario Brain Institute, and Ontario Mental Health Foundation. SCS reports partial support from Canadian Biomarker Integration Network in Depression and Canadian Institutes of Health Research (MOP 137097) grants during the conduct of the study, and grants from Ontario Brain Institute, Canadian Foundation for Innovation and Brain Canada, outside the submitted work. He is also a senior scientific advisor for the neuroimaging data analysis company ADMdx, Inc. ( www. admdx.com), which specializes in brain image analysis to enable diagnosis, prognosis, and drug effect detection for Alzheimer disease and various other forms of dementia. SHK has received honoraria or research funds from Abbott, Alkermes, Allergan, Boehringer Ingelheim, Brain Canada, Canadian Institutes of Health Research, Janssen, Lundbeck, Lundbeck Institute, Ontario Brain Institute, Ontario Research Fund, Otsuka, Pfizer, Servier, Sunovion, Sun Pharmaceuticals, and holds stock in Field Trip Health. VB is supported by an Academic Scholar Award from the University of Toronto Department of Psychiatry, and has received research support from Canadian Institutes of Health Research, Brain & Behavior Foundation, Ministry of Health Innovation Funds, Royal College of Physicians and Surgeons of Canada, Department of Defense, Canada, New Frontiers in Research Fund, and an investigator-initiated trial from Roche Canada.

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Anteraper, S.A., Guell, X., Lee, Y.J. et al. Cerebello-cerebral Functional Connectivity Networks in Major Depressive Disorder: a CAN-BIND-1 Study Report. Cerebellum 22, 26–36 (2023). https://doi.org/10.1007/s12311-021-01353-5

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