Skip to main content
SpringerLink
Log in

Investigating the overlapping associations of prior concussion, default mode connectivity, and executive function-based symptoms

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Growing evidence suggests that younger athletes with greater concussion history are more likely to endorse greater subjective cognitive (e.g., executive function) symptoms, but not perform worse on objective cognitive testing. We sought to identify biological correlates of elevated cognitive symptoms in 100 healthy, collegiate-aged athletes with varying degrees of concussion history. Associations between concussion history with subjectively-rated executive function were assessed with generalized linear models. Using resting state fMRI, we examined associations between concussion history and between-and within-network connectivity across three networks integral to executive function; default mode network (DMN), frontoparietal network (FPN), and ventral attention network (VAN). Relationships of between-and within-network connectivity with subjective executive function were assessed. Although the large majority of participants did not report clinically relevant levels of executive difficulties, there was a significant association between concussion history and higher behavioral regulation-related symptoms; B = .04[.01, .07], p = .011. A significant elevation in total within-network connectivity was observed among those with a greater concussion history, B = .02[.002, .03], p = .028, which was primarily driven by a positive association between concussion history and within DMN connectivity, B = .02[.004, .04], p = .014. Higher behavioral regulation-related symptoms were associated with greater total within-network connectivity, B = 0.57[0.18, 0.96], p = .005, and increased within-network connectivity for the DMN, B = .49[.12, .86], p = .010). The current study identified a distinct biological correlate, increased within-DMN connectivity, which was associated with both a greater history of concussion and greater behavioral regulation symptoms. Future studies are required to determine the degree to which these changes associated with concussion history may evolve toward objective cognitive decline over the lifespan.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The data utilized as part of this study that support the reported findings are available from the corresponding author, upon reasonable request.

References

  • Bonnelle, V., Ham, T. E., Leech, R., Kinnunen, K. M., Mehta, M. A., Greenwood, R. J., & Sharp, D. J. (2012). Salience network integrity predicts default mode network function after traumatic brain injury. Proceedings of the National Academy of Sciences of the United States of America, 109(12), 4690–4695. https://doi.org/10.1073/pnas.1113455109.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brett, B. L., Huber, D. L., Wild, A., Nelson, L. D., & McCrea, M. A. (2019). Age of first exposure to American football and behavioral, cognitive, psychological, and physical outcomes in high school and collegiate football players. Sports Health, 1941738119849076.https://doi.org/10.1177/1941738119849076

  • Caccese, J. B., Iverson, G. L., Hunzinger, K. J., Asken, B. M., Clugston, J. R., Cameron, K. L., … Investigators, C. C. (2021). Factors associated with symptom reporting in U.S. Service Academy Cadets and NCAA student athletes without concussion: Findings from the CARE consortium. Sports Medicine. https://doi.org/10.1007/s40279-020-01415-4

  • Chen, H., Sheng, X., Luo, C., Qin, R., Ye, Q., Zhao, H., … Alzheimer's Disease Neuroimaging, I. (2020). The compensatory phenomenon of the functional connectome related to pathological biomarkers in individuals with subjective cognitive decline. Translation Neurodegeneration, 9(1), 21.https://doi.org/10.1186/s40035-020-00201-6

  • Churchill, N., Hutchison, M. G., Leung, G., Graham, S., & Schweizer, T. A. (2017). Changes in functional connectivity of the brain associated with a history of sport concussion: A preliminary investigation. Brain Injury, 31(1), 39–48. https://doi.org/10.1080/02699052.2016.1221135

    Article  PubMed  Google Scholar 

  • Churchill, N. W., Hutchison, M. G., Graham, S. J., & Schweizer, T. A. (2021). Concussion risk and resilience: Relationships with Pre-Injury Salience Network Connectivity. Journal of Neurotrauma, 38(22), 3097–3106. https://doi.org/10.1089/neu.2021.0123

    Article  PubMed  Google Scholar 

  • D'Souza, M. M., Kumar, M., Choudhary, A., Kaur, P., Kumar, P., Rana, P., … Singh, A. K. (2020). Alterations of connectivity patterns in functional brain networks in patients with mild traumatic brain injury: A longitudinal resting-state functional magnetic resonance imaging study. The Neuroradiology Journal, 33(2), 186–197.https://doi.org/10.1177/1971400920901706

  • Dillen, K. N. H., Jacobs, H. I. L., Kukolja, J., von Reutern, B., Richter, N., Onur, O. A., … Fink, G. R. (2016). Aberrant functional connectivity differentiates retrosplenial cortex from posterior cingulate cortex in prodromal Alzheimer’s disease. Neurobiology of Aging, 44, 114–126.https://doi.org/10.1016/j.neurobiolaging.2016.04.010

  • Esopenko, C., Chow, T. W., Tartaglia, M. C., Bacopulos, A., Kumar, P., Binns, M. A., … Levine, B. (2017). Cognitive and psychosocial function in retired professional hockey players. Journal of Neurology, Neurosurgery and Psychiatry, 88(6), 512–519.https://doi.org/10.1136/jnnp-2016-315260

  • Hafkemeijer, A., Altmann-Schneider, I., Oleksik, A. M., van de Wiel, L., Middelkoop, H. A., van Buchem, M. A., … Rombouts, S. A. (2013). Increased functional connectivity and brain atrophy in elderly with subjective memory complaints. Brain Connect, 3(4), 353–362.https://doi.org/10.1089/brain.2013.0144

  • Hampshire, A., MacDonald, A., & Owen, A. M. (2013). Hypoconnectivity and hyperfrontality in retired American football players. Science and Reports, 3, 2972. https://doi.org/10.1038/srep02972

    Article  Google Scholar 

  • Hillary, F. G., & Grafman, J. H. (2017). Injured brains and adaptive networks: The benefits and costs of hyperconnectivity. Trends in Cognitive Sciences, 21(5), 385–401. https://doi.org/10.1016/j.tics.2017.03.003

    Article  PubMed  PubMed Central  Google Scholar 

  • Iyer, K. K., Zalesky, A., Barlow, K. M., & Cocchi, L. (2019). Default mode network anatomy and function is linked to pediatric concussion recovery. Annals of Clinical Translational Neurology, 6(12), 2544–2554. https://doi.org/10.1002/acn3.50951

    Article  PubMed  PubMed Central  Google Scholar 

  • Jilka, S. R., Scott, G., Ham, T., Pickering, A., Bonnelle, V., Braga, R. M., … Sharp, D. J. (2014). Damage to the salience network and interactions with the default mode network. Journal of Neuroscience, 34(33), 10798–10807.https://doi.org/10.1523/JNEUROSCI.0518-14.2014

  • Jo, H. J., Saad, Z. S., Simmons, W. K., Milbury, L. A., & Cox, R. W. (2010). Mapping sources of correlation in resting state FMRI, with artifact detection and removal. NeuroImage, 52(2), 571–582. https://doi.org/10.1016/j.neuroimage.2010.04.246

    Article  PubMed  Google Scholar 

  • Johnson, B., Zhang, K., Gay, M., Horovitz, S., Hallett, M., Sebastianelli, W., & Slobounov, S. (2012). Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. NeuroImage, 59(1), 511–518. https://doi.org/10.1016/j.neuroimage.2011.07.081

    Article  PubMed  Google Scholar 

  • Jones, D. T., Knopman, D. S., Gunter, J. L., Graff-Radford, J., Vemuri, P., Boeve, B. F., … Alzheimer's Disease Neuroimaging, I. (2016). Cascading network failure across the Alzheimer's disease spectrum. Brain, 139(Pt 2), 547–562.https://doi.org/10.1093/brain/awv338

  • Jorm, A. F., Christensen, H., Korten, A. E., Henderson, A. S., Jacomb, P. A., & Mackinnon, A. (1997). Do cognitive complaints either predict future cognitive decline or reflect past cognitive decline? A longitudinal study of an elderly community sample. Psychological Medicine, 27(1), 91–98. https://doi.org/10.1017/s0033291796003923

    Article  CAS  PubMed  Google Scholar 

  • Kay, T., Harrington, D. E., Adams, R., Anderson, T., Berrol, S., Cicerone, K., … Malec, J. (1993). Definition of mild traumatic brain injury. The Journal of Head Trauma Rehabilitation, 8(3), 86-87

  • Mannix, R., Iverson, G. L., Maxwell, B., Atkins, J. E., Zafonte, R., & Berkner, P. D. (2014). Multiple prior concussions are associated with symptoms in high school athletes. Annals of Clinical Translational Neurology, 1(6), 433–438. https://doi.org/10.1002/acn3.70

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier, T. B., Bellgowan, P. S. F., & Mayer, A. R. (2017a). Longitudinal assessment of local and global functional connectivity following sports-related concussion. Brain Imaging and Behavior, 11(1), 129–140. https://doi.org/10.1007/s11682-016-9520-y

    Article  PubMed  Google Scholar 

  • Meier, T. B., Lancaster, M. A., Mayer, A. R., Teague, T. K., & Savitz, J. (2017b). Abnormalities in functional connectivity in collegiate football athletes with and without a concussion history: Implications and role of neuroactive kynurenine pathway metabolites. Journal of Neurotrauma, 34(4), 824–837. https://doi.org/10.1089/neu.2016.4599

    Article  PubMed  Google Scholar 

  • Meier, T. B., Giraldo-Chica, M., Espana, L. Y., Mayer, A. R., Harezlak, J., Nencka, A. S., … McCrea, M. A. (2020). Resting-state fMRI metrics in acute sport-related concussion and their association with clinical recovery: A study from the NCAA-DOD CARE consortium. Journal of Neurotrauma, 37(1), 152–162.https://doi.org/10.1089/neu.2019.6471

  • Meier, T., Espana, L., Kirk, A., Nader, A. M., Powell, J., Nelson, L. D., … Brett, B. L. (2021). Association of prior concussion with hippocampal volume and symptoms in collegiate-aged athletes. Journal of Neurotrauma.https://doi.org/10.1089/neu.2020.7143

  • Mez, J., Daneshvar, D. H., Kiernan, P. T., Abdolmohammadi, B., Alvarez, V. E., Huber, B. R., … McKee, A. C. (2017). Clinicopathological Evaluation of Chronic Traumatic Encephalopathy in Players of American Football. JAMA, 318(4), 360-370.https://doi.org/10.1001/jama.2017.8334

  • Montenigro, P. H., Alosco, M. L., Martin, B. M., Daneshvar, D. H., Mez, J., Chaisson, C. E., … Tripodis, Y. (2017). Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players. Journal of Neurotrauma, 34(2), 328–340.https://doi.org/10.1089/neu.2016.4413

  • Numbers, K., Crawford, J. D., Kochan, N. A., Draper, B., Sachdev, P. S., & Brodaty, H. (2020). Participant and informant memory-specific cognitive complaints predict future decline and incident dementia: Findings from the Sydney Memory and Ageing Study. PLoS ONE, 15(5), e0232961. https://doi.org/10.1371/journal.pone.0232961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orr, C. A., Albaugh, M. D., Watts, R., Garavan, H., Andrews, T., Nickerson, J. P., … Hudziak, J. J. (2016). Neuroimaging biomarkers of a history of concussion observed in asymptomatic young athletes. Journal of Neurotrauma, 33(9), 803–810.https://doi.org/10.1089/neu.2014.3721

  • Rabin, L. A., Wang, C., Mogle, J. A., Lipton, R. B., Derby, C. A., & Katz, M. J. (2020). An approach to classifying subjective cognitive decline in community-dwelling elders. Alzheimers Dement (Amst), 12(1), e12103. https://doi.org/10.1002/dad2.12103

    Article  Google Scholar 

  • Schaefer, A., Kong, R., Gordon, E. M., Laumann, T. O., Zuo, X. N., Holmes, A. J., … Yeo, B. T. T. (2018). Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cerebral Cortex, 28(9), 3095–3114.https://doi.org/10.1093/cercor/bhx179

  • Seichepine, D. R., Stamm, J. M., Daneshvar, D. H., Riley, D. O., Baugh, C. M., Gavett, B. E., … Stern, R. A. (2013). Profile of self-reported problems with executive functioning in college and professional football players. Journal of Neurotrauma, 30(14), 1299–1304.https://doi.org/10.1089/neu.2012.2690

  • Sridharan, D., Levitin, D. J., & Menon, V. (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences of the United States of America, 105(34), 12569–12574. https://doi.org/10.1073/pnas.0800005105.

    Article  PubMed  PubMed Central  Google Scholar 

  • Terpstra, A. R., Vasquez, B. P., Colella, B., Tartaglia, M. C., Tator, C. H., Mikulis, D., … Green, R. E. A. (2019). Comprehensive Neuropsychiatric and Cognitive Characterization of Former Professional Football Players: Implications for Neurorehabilitation. Frontiers in Neurology, 10, 712.https://doi.org/10.3389/fneur.2019.00712

  • Tooley, U. A., Mackey, A. P., Ciric, R., Ruparel, K., Moore, T. M., Gur, R. C., … Bassett, D. S. (2020). Associations between neighborhood SES and functional brain network development. Cerebral Cortex, 30(1), 1–19.https://doi.org/10.1093/cercor/bhz066

  • Verfaillie, S. C. J., Pichet Binette, A., Vachon-Presseau, E., Tabrizi, S., Savard, M., Bellec, P., … Group, P.-A. R. (2018). Subjective cognitive decline is associated with altered default mode network connectivity in individuals with a family history of Alzheimer's disease. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(5), 463–472.https://doi.org/10.1016/j.bpsc.2017.11.012

  • Viviano, R. P., & Damoiseaux, J. S. (2020). Functional neuroimaging in subjective cognitive decline: Current status and a research path forward. Alzheimers Res Ther, 12(1), 23. https://doi.org/10.1186/s13195-020-00591-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Risacher, S. L., West, J. D., McDonald, B. C., Magee, T. R., Farlow, M. R., … Saykin, A. J. (2013). Altered default mode network connectivity in older adults with cognitive complaints and amnestic mild cognitive impairment. Journal of Alzheimers Disease, 35(4), 751–760.https://doi.org/10.3233/JAD-130080

  • Yasuno, F., Kazui, H., Yamamoto, A., Morita, N., Kajimoto, K., Ihara, M., … Kishimoto, T. (2015). Resting-state synchrony between the retrosplenial cortex and anterior medial cortical structures relates to memory complaints in subjective cognitive impairment. Neurobiology of Aging, 36(6), 2145–2152.https://doi.org/10.1016/j.neurobiolaging.2015.03.006

  • Zanchi, D., Montandon, M. L., Sinanaj, I., Rodriguez, C., Depoorter, A., Herrmann, F. R., … Haller, S. (2017). Decreased fronto-parietal and increased default mode network activation is associated with subtle cognitive deficits in elderly controls. Neurosignals, 25(1), 127–138.https://doi.org/10.1159/000486152

  • Zanto, T. P., & Gazzaley, A. (2013). Fronto-parietal network: Flexible hub of cognitive control. Trends in Cognitive Sciences, 17(12), 602–603. https://doi.org/10.1016/j.tics.2013.10.001

    Article  PubMed  Google Scholar 

  • Zhang, L., Yang, K. H., & King, A. I. (2004). A proposed injury threshold for mild traumatic brain injury. Journal of Biomechanical Engineering, 126(2), 226–236. https://doi.org/10.1115/1.1691446

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Luisa Bohorquez-Montoya, Jennifer Powell, Alexander Kirk, Amy Nader, and Dan Huber at the Medical College of Wisconsin for data collection, quality assurance, and data management; and Andrew S. Nencka, Brad Swearingen, and the MRI technicians at the Center for Imaging Research at the Medical College of Wisconsin for assistance in MRI data collection.

Funding

Research reported in this publication was supported by the National Institute Of Neurological Disorders And Stroke of the National Institutes of Health under Award Number R01NS102225. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The REDCap electronic database and the Adult Translational Research Unit used for this project were supported by the National Center for Advancing Translational Sciences, National Institutes of Health, Award Number UL1TR001436. BLB acknowledges support from the National Institute of Neurological Disorders and Stroke (Award Number L30NS113158) and National Institute on Aging (Award Number K23 AG073528).This research was completed in part with computational resources and technical support provided by the Research Computing Center at the Medical College of Wisconsin.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Medical College of Wisconsin, 8701 West Watertown Plank Road, Milwaukee, WI, 53226, USA

    Benjamin L. Brett, Lezlie Y. España & Timothy B. Meier

  2. Department of Neurology, Medical College of Wisconsin, Milwaukee, WI, USA

    Benjamin L. Brett & Andrew M. Bryant

  3. The Mind Research Network/Lovelace Biomedical and Environmental Research Institute, Neurology and Psychiatry Departments, University of New Mexico School of Medicine, Department of Psychology, University of New Mexico, Albuquerque, NM, USA

    Andrew R. Mayer

  4. Department of Biomedical Engineering, Medical College of Wisconsin, Milwaukee, WI, USA

    Timothy B. Meier

  5. Department of Cell Biology, Neurobiology and Anatomy, Medical College of Wisconsin, Milwaukee, WI, USA

    Timothy B. Meier

Authors
  1. Benjamin L. Brett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew M. Bryant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lezlie Y. España
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrew R. Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Timothy B. Meier
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

B.L. Brett, PhD- Designed and conceptualized study; major role in acquisition of the data; analyzed data; drafted and revised the manuscript for intellectual content.

A.M. Bryant, PhD- drafted and revised the manuscript for intellectual content.

L.Y. España, BA- Major role in acquisition of the data; analyzed data; revised the manuscript for intellectual content.

A.R. Mayer, PhD- Designed and conceptualized study; revised the manuscript for intellectual content.

T.B. Meier, PhD- Designed and conceptualized study; major role in acquisition of the data; analyzed data; drafted and revised the manuscript for intellectual content.

Corresponding author

Correspondence to Timothy B. Meier.

Ethics declarations

Ethical approval

The study was approved by the Institutional Review Board at the Medical College of Wisconsin.

Consent to participate

All participants provided written informed consent as part of study enrollment.

Consent to publish

The authors have the right to publish the data.

Competing interests

The Authors declare that there is no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 39 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brett, B.L., Bryant, A.M., España, L.Y. et al. Investigating the overlapping associations of prior concussion, default mode connectivity, and executive function-based symptoms. Brain Imaging and Behavior 16, 1275–1283 (2022). https://doi.org/10.1007/s11682-021-00617-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-021-00617-2

Keywords

Search

Navigation