Neuroanatomical and functional alterations of insula in mild traumatic brain injury patients at the acute stage
- 8 Downloads
Cognitive impairment is a major cause of disability and decline in quality of life in mild traumatic brain injury (mTBI) survivors, but the underlying pathophysiology is still poorly understood. The insula has extensive connections to other cortex and is believed to responsible for integrating external and internal processes and controlling cognitive functions. To explore this hypothesis, we investigated early alterations in the gray matter volume (GMV) and brain functional connectivity (FC) of insula in mTBI patients within 7 days after injury and any possible correlations with cognitive function. A total of 58 mTBI patients at the acute stage and 32 matched healthy controls were recruited and underwentT1-weighted magnetic resonance imaging (MRI)andresting-state functional MRI scans within 7 days of injury. FC was characterized using seed-based region of interest analysis method. The patients’ cognitive function was evaluated with Montreal Cognitive Assessment (MoCA) score. The resulting of GMV and FC of insula were correlated with cognitive alterations. We found that the GMV was significantly reduced only in the right insula in mTBI patients and no significant GMV increase was observed in either hemisphere. mTBI patients demonstrated decreased FC in the right parahippocampal gyrus and increased FC in the right supramargianl gyrus. In addition, compared to the healthy controls, the mTBI patients in the acute stage presented a decline in the visuospatial/executive (p = 0.013) and attention (p = 0.038) subcategories. In the mTBI group, the changes in GMV in the right insula were positively correlated with poor attention performance (r = 0.316, p = 0.016). Our data demonstrated alterations of the GMV and resting-stateFC of the right insula in mTBI patients at the acute stage. These early changes in GMV and resting-state FC perhaps serve as a potential biomarker for improving the understanding of cognitive decline for mTBI in the acute setting.
KeywordsMild traumatic brain injury Gray matter volume Functional connectivity Cognitive function MRI
This work was supported by the National Natural Science Foundation of China (No.81870563), Jiangsu Provincial Special Program of Medical Science (BE2017614), Youth Medical Talents of Jiangsu Province (No. QNRC2016062), 14th “Six Talent Peaks” Project of Jiangsu Province (No. YY-079), and the Nanjing Medical University grant (No. 2017NJMU123).
Compliance with ethical standards
Conflict of interests
The authors declare that there is no potential conflict of interests regarding the publication of this paper.
The current study was approved by the Research Ethics Committee of the Nanjing Medical University.
Informed consent was obtained from all individual participants included in the study.
- 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, 4690–4695.CrossRefGoogle Scholar
- Carlozzi, N. E., Kirsch, N. L., Kisala, P. A., & Tulsky, D. S. (2015). An examination of the Wechsler adult intelligence scales, fourth edition (WAIS-IV) in individuals with complicated mild, moderate and severe traumatic brain injury (TBI). The Clinical Neuropsychologist, 29, 21–37.CrossRefGoogle Scholar
- Chao-Gan, Y., & Yu-Feng, Z. (2010). DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 4, 13.Google Scholar
- Dall'Acqua, P., Johannes, S., Mica, L., Simmen, H. P., Glaab, R., Fandino, J., Schwendinger, M., Meier, C., Ulbrich, E. J., Muller, A., Jancke, L., & Hanggi, J. (2016). Connectomic and surface-based morphometric correlates of acute mild traumatic brain injury. Frontiers in Human Neuroscience, 10, 127.CrossRefGoogle Scholar
- Dall'Acqua, P., Johannes, S., Mica, L., Simmen, H. P., Glaab, R., Fandino, J., Schwendinger, M., Meier, C., Ulbrich, E. J., Muller, A., Jancke, L., & Hanggi, J. (2017). Prefrontal cortical thickening after mild traumatic brain injury: A one-year magnetic resonance imaging study. Journal of Neurotrauma, 34, 3270–3279.CrossRefGoogle Scholar
- Hasan, K. M., Wilde, E. A., Miller, E. R., Kumar Patel, V., Staewen, T. D., Frisby, M. L., Garza, H. M., McCarthy, J. J., Hunter, J. V., Levin, H. S., Robertson, C. S., & Narayana, P. A. (2014). Serial atlas-based diffusion tensor imaging study of uncomplicated mild traumatic brain injury in adults. Journal of Neurotrauma, 31, 466–475.CrossRefGoogle Scholar
- Hillary, F. G., Slocomb, J., Hills, E. C., Fitzpatrick, N. M., Medaglia, J. D., Wang, J., Good, D. C., & Wylie, G. R. (2011). Changes in resting connectivity during recovery from severe traumatic brain injury. International journal of psychophysiology : official journal of the International Organization of Psychophysiology, 82, 115–123.CrossRefGoogle Scholar
- Iraji, A., Benson, R. R., Welch, R. D., O'Neil, B. J., Woodard, J. L., Ayaz, S. I., Kulek, A., Mika, V., Medado, P., Soltanian-Zadeh, H., Liu, T., Haacke, E. M., & Kou, Z. (2015). Resting state functional connectivity in mild traumatic brain injury at the acute stage: Independent component and seed-based analyses. Journal of Neurotrauma, 32, 1031–1045.CrossRefGoogle Scholar
- Jagoda, A. S., Bazarian, J. J., Bruns, J. J., Jr., Cantrill, S. V., Gean, A. D., Howard, P. K., Ghajar, J., Riggio, S., Wright, D. W., Wears, R. L., Bakshy, A., Burgess, P., Wald, M. M., & Whitson, R. R. (2008). Clinical policy: Neuroimaging and decisionmaking in adult mild traumatic brain injury in the acute setting. Annals of Emergency Medicine, 52, 714–748.CrossRefGoogle Scholar
- Jarrett, M., Tam, R., Hernandez-Torres, E., Martin, N., Perera, W., Zhao, Y., Shahinfard, E., Dadachanji, S., Taunton, J., Li, D. K., & Rauscher, A. (2016). A prospective pilot investigation of brain volume, white matter Hyperintensities, and hemorrhagic lesions after mild traumatic brain injury. Frontiers in Neurology, 7, 11.CrossRefGoogle Scholar
- Lange, R. T., Brickell, T. A., French, L. M., Merritt, V. C., Bhagwat, A., Pancholi, S., & Iverson, G. L. (2012). Neuropsychological outcome from uncomplicated mild, complicated mild, and moderate traumatic brain injury in US military personnel. Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists, 27, 480–494.CrossRefGoogle Scholar
- Len, T. K., & Neary, J. P. (2011). Cerebrovascular pathophysiology following mild traumatic brain injury. Clinical Physiology and Functional Imaging, 31, 85–93.Google Scholar
- Lipton, M. L., Gulko, E., Zimmerman, M. E., Friedman, B. W., Kim, M., Gellella, E., Gold, T., Shifteh, K., Ardekani, B. A., & Branch, C. A. (2009). Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology, 252, 816–824.CrossRefGoogle Scholar
- Marquez de la Plata, C. D., Garces, J., Shokri Kojori, E., Grinnan, J., Krishnan, K., Pidikiti, R., Spence, J., Devous, M. D., Sr., Moore, C., McColl, R., Madden, C., & Diaz-Arrastia, R. (2011). Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. Archives of Neurology, 68, 74–84.CrossRefGoogle Scholar
- McCrory, P., Meeuwisse, W., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R., Engebretsen, L., Johnston, K., Kutcher, J., Raftery, M., Sills, A., Benson, B., Davis, G., Ellenbogen, R., Guskiewicz, K., Herring, S. A., Iverson, G., Jordan, B., Kissick, J., McCrea, M., McIntosh, A., Maddocks, D., Makdissi, M., Purcell, L., Putukian, M., Schneider, K., Tator, C., & Turner, M. (2013). Consensus statement on concussion in sport - the 4th international conference on concussion in sport held in Zurich, November 2012. Physical therapy in sport : official journal of the Association of Chartered Physiotherapists in Sports Medicine, 14, e1–e13.CrossRefGoogle Scholar
- Nasreddine, Z. S., Phillips, N. A., Bedirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J. L., & Chertkow, H. (2005). The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53, 695–699.CrossRefGoogle Scholar
- Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., & Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of neuroscience : the official journal of the Society for Neuroscience, 27, 2349–2356.CrossRefGoogle Scholar
- Tu, Y., Yu, T., Wei, Y., Sun, K., Zhao, W., & Yu, B. (2016). Structural brain alterations in hemifacial spasm: A voxel-based morphometry and diffusion tensor imaging study. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology, 127, 1470–1474.CrossRefGoogle Scholar
- Zhu, D. C., Covassin, T., Nogle, S., Doyle, S., Russell, D., Pearson, R. L., Monroe, J., Liszewski, C. M., DeMarco, J. K., & Kaufman, D. I. (2015). A potential biomarker in sports-related concussion: Brain functional connectivity alteration of the default-mode network measured with longitudinal resting-state fMRI over thirty days. Journal of Neurotrauma, 32, 327–341.CrossRefGoogle Scholar