Skip to main content

Advertisement

SpringerLink
Log in

Aberrant brain functional hubs convergence in the acute severe traumatic brain injury patients with rapidly recovering

  • Functional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

We aimed to identify the aberrant functional hubs in patients with acute severe traumatic brain injury (sTBI) and investigate whether they could help inform prognosis.

Methods

Twenty-eight sTBI patients and health controls underwent imaging scanning. The graph-theoretical measure of degree centrality (DC) was applied to identify the abnormal brain functional hubs and conjoined with regions of interest-based analysis to investigate their interaction and impact on whole-brain. We further split sTBI patients into two subgroups according to their recovery to explore whether the fractional amplitude of low-frequency fluctuation (fALFF) roles in functional connectivity (FC) differential areas to help inform the patients’ long-term prognosis.

Results

We identified the part of prefrontal cortex (PFC), precentral and postcentral gyrus (Pre-/Post-CG), cingulate gyrus (CgG), posterior medial cortex (PMC), and brainstem that could be core hubs whose DC was significantly increased in patients with acute sTBI. The interaction strength of the paired hubs could be enhanced (CG-PFC, CgG-PFC, CG-brainstem, CgG-brainstem, PMC-brainstem, and PFC-brainstem) and weakened (CG-CgG, CG-PMC, CgG-PMC, and PMC-PFC), compared with healthy controls. We also found abnormal FC in 5 hubs to whole-brain. The spontaneous brain activities in the FC differential regions [e.g., the fALFF and mean fALFF value] were valid to predict outcome at 6-month in patients with sTBI.

Conclusion

We demonstrated a compensatory mechanism that part of brain regions will converge into abnormal functional hubs in patients with acute sTBI, which provides a potential approach to objectively predicting patients’ long-term outcome.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data could be available from corresponding author.

References

  1. Yang C, Ma Y, Xie L et al (2022) Intracranial pressure monitoring in the intensive care unit for patients with severe traumatic brain injury: analysis of the CENTER-TBI China Registry. Neurocrit Care 37(1):160–171

    Article  Google Scholar 

  2. Stocchetti NC, Carbonara M, Citerio G et al (2017) Severe traumatic brain injury: targeted management in the intensive care unit. Lancet Neurol 16:452–464

    Article  Google Scholar 

  3. Kondziella D, Fisher PM, Larsen VA et al (2017) Functional MRI for assessment of the default mode network in acute brain injury. Neurocrit Care 27:401–406

    Article  Google Scholar 

  4. Damoiseaux JS, Rombouts SA, Barkhof F et al (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853

    Article  Google Scholar 

  5. Cheibel RS, Newsome MR, Steinberg JL et al (2007) Altered brain activation during cognitive control in patients with moderate to severe traumatic brain injury. Neurorehabil Neural Repair 21:36–45

    Article  Google Scholar 

  6. Mallas EJ, De Simoni S, Scott G et al (2021) Abnormal dorsal attention network activation in memory impairment after traumatic brain injury. Brain 144:114–127

    Article  Google Scholar 

  7. Bonnelle V, Ham TE, Leech R et al (2012) Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci USA 109:4690–4695

    Article  Google Scholar 

  8. Medaglia JD (2017) Functional neuroimaging in traumatic brain injury: from nodes to networks. Front Neurol 8:407

    Article  Google Scholar 

  9. Claassen J, Doyle K, Matory A et al (2019) Detection of Brain activation in unresponsive patients with acute brain injury. N Engl J Med 380:2497–2505

    Article  Google Scholar 

  10. Glasser MF, Smith SM, Marcus DS et al (2016) The human connectome project’s neuroimaging approach. Nat Neurosci 19:1175–1187

    Article  Google Scholar 

  11. Caeyenberghs K, Verhelst H, Clemente A et al (2017) Mapping the functional connectome in traumatic brain injury: What can graph metrics tell us? Neuroimage 160:113–123

    Article  Google Scholar 

  12. Qin P, Wu X, Wu C et al (2021) Higher-order sensorimotor circuit of the brain’s global network supports human consciousness. Neuroimage 231:117850

    Article  Google Scholar 

  13. Zou QH, Zhu CZ, Yang Y et al (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172:137–141

    Article  Google Scholar 

  14. Guo H, Liu R, Sun Z et al (2019) Evaluation of prognosis in patients with severe traumatic brain injury using resting-state functional magnetic resonance imaging. World Neurosurg 121:e630–e639

    Article  Google Scholar 

  15. Zhang J, Zhang E, Yuan C et al (2022) Abnormal default mode network could be a potential prognostic marker in patients with disorders of consciousness. Clin Neurol Neurosurg 218:107294

    Article  Google Scholar 

  16. Carney N, Totten AM, O’Reilly C et al (2017) Guidelines for the management of severe traumatic brain injury Fourth Edition. Neurosurgery 80:6–15

    Article  Google Scholar 

  17. Satterthwaite TD, Elliott MA, Gerraty RT et al (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240–256

    Article  Google Scholar 

  18. Palacios EM, Sala-Llonch R, Junque C et al (2013) Resting-state functional magnetic resonance imaging activity and connectivity and cognitive outcome in traumatic brain injury. JAMA Neurol 70:845–851

    Article  Google Scholar 

  19. Warthen KG, Boyse-Peacor A, Jones KG et al (2020) Sex differences in the human reward system: convergent behavioral, autonomic and neural evidence. Soc Cogn Affect Neurosci 15(7):789–801

    Article  Google Scholar 

  20. Zuo XN, Ehmke R, Mennes M et al (2012) Network centrality in the human functional connectome. Cereb Cortex 22:1862–1875

    Article  Google Scholar 

  21. Liu X, Zheng J, Liu B et al (2018) Altered connection properties of important network hubs may be neural risk factors for individuals with primary insomnia. Sci Rep 8:5891

    Article  Google Scholar 

  22. van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17:683–696

    Article  Google Scholar 

  23. Caeyenberghs K, Leemans A, De Decker C et al (2012) Brain connectivity and postural control in young traumatic brain injury patients: A diffusion MRI based network analysis. Neuroimage Clin 1:106–115

    Article  Google Scholar 

  24. Jin H, Fishman ZH, Ye M et al (2021) Top-down control of sweet and bitter taste in the mammalian brain. Cell 184(257–271):e216

    Google Scholar 

  25. Beissner F, Schumann A, Brunn F et al (2014) Advances in functional magnetic resonance imaging of the human brainstem. Neuroimage 86:91–98

    Article  Google Scholar 

  26. Leon-Carrion J, Leon-Dominguez U, Pollonini L et al (2012) Synchronization between the anterior and posterior cortex determines consciousness level in patients with traumatic brain injury (TBI). Brain Res 1476:22–30

    Article  Google Scholar 

  27. Zhang H, Dai R, Qin P et al (2017) Posterior cingulate cross-hemispheric functional connectivity predicts the level of consciousness in traumatic brain injury. Sci Rep 7:387

    Article  Google Scholar 

  28. Sharp DJ, Scott G, Leech R (2014) Network dysfunction after traumatic brain injury. Nat Rev Neurol 10:156–166

    Article  Google Scholar 

  29. Venkatesan UM, Dennis NA, Hillary FG (2015) Chronology and chronicity of altered resting-state functional connectivity after traumatic brain injury. J Neurotrauma 32:252–264

    Article  Google Scholar 

  30. Snider SB, Bodien YG, Frau-Pascual A et al (2020) Ascending arousal network connectivity during recovery from traumatic coma. Neuroimage Clin 28:102503

    Article  Google Scholar 

Download references

Acknowledgements

We thank the department of radiology for supplying image scanning platform.

Funding

Hospital Level Support Projects (Fcjs202050).

Author information

Author notes

  1. Jun Zhang and Hongying Zhang contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Clinical Medical College of Yangzhou University, Yangzhou, 225000, China

    Jun Zhang, Hengzhu Zhang, Fuli Yan, Enpeng Zhang, Yunlong Pei, Min Wei, Xingdong Wang, Xiaodong Wang & Lun Dong

  2. Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, 200040, China

    Jun Zhang

  3. Department of Radiology, Clinical Medical College of Yangzhou University, Yangzhou, 225000, China

    Hongying Zhang

Authors
  1. Jun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hengzhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fuli Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Enpeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yunlong Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Min Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xingdong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaodong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lun Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception and design (LD, JZ, XDW), data collection (JZ, LD, HYZ), data analysis (JZ), drafting (JZ), helping with drafting (HZZ, FLY, EPZ), draft revision(YLP, MW, XDW, XDW).

Corresponding authors

Correspondence to Xiaodong Wang or Lun Dong.

Ethics declarations

Ethics approval

This study was approved by the Medical Ethics Committee (2020KY-179). All procedures performed were in accordance with the ethical standards of the institutional committee.

Consent to participate

Informed consent, and assent if indicated, was obtained from all participants.

Consent for publication

All authors approved the final manuscript for publication.

Competing interests

The authors report no conflicts of interest in this work.

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 (DOC 27 KB)

Supplementary file2 (DOC 81 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Zhang, H., Zhang, H. et al. Aberrant brain functional hubs convergence in the acute severe traumatic brain injury patients with rapidly recovering. Neuroradiology 65, 145–155 (2023). https://doi.org/10.1007/s00234-022-03048-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-022-03048-y

Keywords

Search

Navigation