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Cingulo-opercular and frontoparietal control network connectivity and executive functioning in older adults

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Abstract

Executive function is a cognitive domain that typically declines in non-pathological aging. Two cognitive control networks that are vulnerable to aging—the cingulo-opercular (CON) and fronto-parietal control (FPCN) networks—play a role in various aspects of executive functioning. However, it is unclear how communication within these networks at rest relates to executive function subcomponents in older adults. This study examines the associations between CON and FPCN connectivity and executive function performance in 274 older adults across working memory, inhibition, and set-shifting tasks. Average CON connectivity was associated with better working memory, inhibition, and set-shifting performance, while average FPCN connectivity was associated solely with working memory. CON region of interest analyses revealed significant connections with classical hub regions (i.e., anterior cingulate and anterior insula) for each task, language regions for verbal working memory, right hemisphere dominance for inhibitory control, and widespread network connections for set-shifting. FPCN region of interest analyses revealed largely right hemisphere fronto-parietal connections important for working memory and a few temporal lobe connections for set-shifting. These findings characterize differential brain-behavior relationships between cognitive control networks and executive function in aging. Future research should target these networks for intervention to potentially attenuate executive function decline in older adults.

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Data availability

Data are managed under the data sharing agreement established with NIA and the parent R01 clinical trial Data Safety and Monitoring Board in the context of an ongoing Phase III clinical trial (ACT study, R01AG054077). All trial data will be made publicly available 2 years after completion of the parent clinical trial, per NIA and DSMB agreement. Requests for baseline data can be submitted to the ACT Publication and Presentation (P&P) Committee and will require submission of a data use, authorship, and analytic plan for review by the P&P committee (ajwoods@phhp.ufl.edu).

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Funding

This work was supported by the National Institute on Aging [NIA R01AG054077, NIA K01AG050707, NIA P30AG072980, T32AG020499], the State of Arizona and Arizona Department of Health Services (ADHS), the University of Florida Center for Cognitive Aging and Memory Clinical Translational Research, the McKnight Brain Research Foundation, and National Heart, Lung, and Blood Institute [T32HL134621].

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  1. Center for Cognitive Aging and Memory, McKnight Brain Institute, University of Florida, Gainesville, FL, USA

    Hanna K. Hausman, Cheshire Hardcastle, Alejandro Albizu, Jessica N. Kraft, Nicole D. Evangelista, Emanuel M. Boutzoukas, Kailey Langer, Andrew O’Shea, Eric Porges, Steven T. DeKosky, Michael Marsiske, Ronald Cohen & Adam J. Woods

  2. Department of Clinical and Health Psychology, College of Public Health and Health Professions, University of Florida, Gainesville, FL, USA

    Hanna K. Hausman, Cheshire Hardcastle, Nicole D. Evangelista, Emanuel M. Boutzoukas, Kailey Langer, Andrew O’Shea, Eric Porges, Michael Marsiske, Ronald Cohen & Adam J. Woods

  3. Department of Neuroscience, College of Medicine, University of Florida, Gainesville, FL, USA

    Alejandro Albizu & Jessica N. Kraft

  4. Brain Imaging, Behavior and Aging Laboratory, Department of Psychology and Evelyn F. McKnight Brain Institute, University of Arizona, Tucson, AZ, USA

    Emily J. Van Etten, Pradyumna K. Bharadwaj, Hyun Song, Samantha G. Smith & Gene E. Alexander

  5. Department of Neurology, College of Medicine, University of Florida, Gainesville, FL, USA

    Steven T. DeKosky

  6. Department of Psychiatry, Neuroscience and Physiological Sciences Graduate Interdisciplinary Programs, and BIO5 Institute, University of Arizona and Arizona Alzheimer’s Disease Consortium, Tucson, AZ, USA

    Georg A. Hishaw & Gene E. Alexander

  7. Department of Biostatistics, College of Public Health and Health Professions, College of Medicine, University of Florida, Gainesville, FL, USA

    Samuel Wu

Authors
  1. Hanna K. Hausman
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  2. Cheshire Hardcastle
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  3. Alejandro Albizu
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  4. Jessica N. Kraft
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  5. Nicole D. Evangelista
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  6. Emanuel M. Boutzoukas
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  7. Kailey Langer
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  8. Andrew O’Shea
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  9. Emily J. Van Etten
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  10. Pradyumna K. Bharadwaj
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  11. Hyun Song
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  12. Samantha G. Smith
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  13. Eric Porges
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  14. Steven T. DeKosky
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  15. Georg A. Hishaw
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  16. Samuel Wu
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  17. Michael Marsiske
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  18. Ronald Cohen
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  19. Gene E. Alexander
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  20. Adam J. Woods
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Contributions

HH and AW contributed to the conception and design of this specific study. HH extracted the data, performed the statistical analyses, and wrote the first draft of the manuscript. CH wrote various sections of the discussion. EP, GH, SW, SD, GA, MM, RC, and AW were involved in project administration. All authors contributed to manuscript revision, read, and approved the submitted version.

Corresponding author

Correspondence to Adam J. Woods.

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The authors declare no competing interests.

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Hausman, H.K., Hardcastle, C., Albizu, A. et al. Cingulo-opercular and frontoparietal control network connectivity and executive functioning in older adults. GeroScience 44, 847–866 (2022). https://doi.org/10.1007/s11357-021-00503-1

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  • DOI: https://doi.org/10.1007/s11357-021-00503-1

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