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Homotopic region connectivity during concussion recovery: A longitudinal fMRI study


Autoři: Catherine D. Chong aff001;  Lujia Wang aff002;  Kun Wang aff002;  Stephen Traub aff001;  Jing Li aff002
Působiště autorů: Mayo Clinic Arizona, Phoenix, AZ, United States of America aff001;  School of Computing, Informatics and Decision Systems Engineering, Arizona State University, Tempe, AZ, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221892

Souhrn

Objectives

To (i) investigate alterations in homotopic functional connectivity (hfc) in concussed patients relative to healthy controls (HC) and to (ii) interrogate whether hfc in concussed patients normalized during the recovery process. The relationship between symptom recovery and change in hfc was assessed using post-hoc analyses.

Methods

This study included 15 concussed patients (mean age = 39.1, SD = 10.1; sex: 13 females, 2 males) and 15 HC (mean age = 39.1, SD = 11.7; sex: 13 females, 2 males). Hfc patterns were interrogated using resting-state magnetic resonance imaging (rs-MRI) for 29 a priori selected pain-processing regions. Concussed patients underwent imaging at two time-points; at 1-month post-concussion (mean time following concussion: 28 days, SD = 9.5) and again at 5-months post-concussion (mean time following concussion: 121 days, SD = 13). At both time-points, symptoms associated with concussion were assessed using the Sports Concussion Assessment Tool (SCAT-3).

Results

Concussed patients had significantly weaker hfc in the following six regions 1-month post-concussion compared to HC: middle cingulate, posterior insula, middle occipital, spinal trigeminal nucleus, precentral and the pulvinar. There were no regions of significantly stronger hfc in concussed patients relative to HC. Longitudinally, patients showed significant symptom recovery 5-months post-concussion and had significant strengthening of hfc patterns in seven homotopic ROIs: middle cingulate, posterior insula, middle occipital, secondary somatosensory area, spinal trigeminal nucleus, precentral, and the pulvinar. Post-hoc analyses indicated a significant negative correlation between somatosensory functional connectivity strengthening and symptom severity.

Conclusion

At 1-month post-concussion, patients had significantly weaker hfc in a number of pain-processing regions relative to HC. However, over a period of 5-months, region-pair connectivity showed significant recovery and normalization. Those patients with more successful symptom recovery at 5-months post-concussion had more functional somatosensory strengthening, suggesting an association between functional strengthening and post-concussion symptom recovery.

Klíčová slova:

Prefrontal cortex – Emotions – Neuroimaging – Left hemisphere – Right hemisphere – Magnetic resonance imaging – Migraine – Neurological signaling


Zdroje

1. Faul M, Xu L, Wald M, Coronado V. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths, 2002–2006. Atlanta: Centers for Disease Control and Prevention2010.

2. Sigurdardottir S, Andelic N, Roe C, Jerstad T, Schanke AK. Post-concussion symptoms after traumatic brain injury at 3 and 12 months post-injury: a prospective study. Brain injury: [BI]. 2009;23(6):489–97. Epub 2009/06/02. doi: 10.1080/02699050902926309 19484622.

3. Kurca E, Sivak S, Kucera P. Impaired cognitive functions in mild traumatic brain injury patients with normal and pathologic magnetic resonance imaging. Neuroradiology. 2006;48(9):661–9. Epub 2006/06/21. doi: 10.1007/s00234-006-0109-9 16786351.

4. Munivenkatappa A, Deepika A, Prathyusha V, Devi I, Shukla D. Can an abnormal CT scan be predicted from common symptoms after mild head injury in children? Journal of pediatric neurosciences. 2013;8(3):183–7. Epub 2014/01/29. doi: 10.4103/1817-1745.123659 24470808; PubMed Central PMCID: PMC3888031.

5. Borich M, Babul AN, Huang PH, Boyd L, Virji-Babul N. Alterations in resting state brain networks in concussed adolescent athletes. Journal of neurotrauma. 2014. Epub 2014/07/11. doi: 10.1089/neu.2013.3269 25010041.

6. Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA. Functional connectivity in mild traumatic brain injury. Human brain mapping. 2011;32(11):1825–35. Epub 2011/01/25. doi: 10.1002/hbm.21151 21259381; PubMed Central PMCID: PMC3204375.

7. Johnson B, Zhang K, Gay M, Horovitz S, Hallett M, Sebastianelli W, et al. Alteration of Brain Default Network in Subacute Phase of Injury in Concussed Individuals: Resting-state fMRI study. NeuroImage. 2012;59(1):511–8. doi: 10.1016/j.neuroimage.2011.07.081 21846504; PubMed Central PMCID: PMC3196274.

8. Sours C, Zhuo J, Janowich J, Aarabi B, Shanmuganathan K, Gullapalli RP. Default mode network interference in mild traumatic brain injury—a pilot resting state study. Brain research. 2013;1537:201–15. Epub 2013/09/03. doi: 10.1016/j.brainres.2013.08.034 23994210; PubMed Central PMCID: PMC3835746.

9. Shen K, Misic B, Cipollini BN, Bezgin G, Buschkuehl M, Hutchison RM, et al. Stable long-range interhemispheric coordination is supported by direct anatomical projections. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(20):6473–8. Epub 2015/05/06. doi: 10.1073/pnas.1503436112 25941372; PubMed Central PMCID: PMC4443345.

10. Wei P, Zhang Z, Lv Z, Jing B. Strong Functional Connectivity among Homotopic Brain Areas Is Vital for Motor Control in Unilateral Limb Movement. Frontiers in Human Neuroscience. 2017;11:366. Epub 2017/07/28. doi: 10.3389/fnhum.2017.00366 28747880; PubMed Central PMCID: PMC5506200.

11. Zhu Y, Song X, Xu M, Hu X, Li E, Liu J, et al. Impaired interhemispheric synchrony in Parkinson's disease with depression. Scientific reports. 2016;6:27477. Epub 2016/06/07. doi: 10.1038/srep27477 27265427; PubMed Central PMCID: PMC4893739.

12. Tang C, Zhao Z, Chen C, Zheng X, Sun F, Zhang X, et al. Decreased Functional Connectivity of Homotopic Brain Regions in Chronic Stroke Patients: A Resting State fMRI Study. PloS one. 2016;11(4):e0152875. Epub 2016/04/14. doi: 10.1371/journal.pone.0152875 27074031; PubMed Central PMCID: PMC4830618.

13. Qi R, Liu C, Weng Y, Xu Q, Chen L, Wang F, et al. Disturbed Interhemispheric Functional Connectivity Rather than Structural Connectivity in Irritable Bowel Syndrome. Frontiers in molecular neuroscience. 2016;9:141. Epub 2016/12/22. doi: 10.3389/fnmol.2016.00141 27999530; PubMed Central PMCID: PMC5138208.

14. Lang X, Wang L, Zhuo CJ, Jia F, Wang LN, Wang CL. Reduction of Interhemispheric Functional Connectivity in Sensorimotor and Visual Information Processing Pathways in Schizophrenia. Chinese medical journal. 2016;129(20):2422–6. Epub 2016/10/18. doi: 10.4103/0366-6999.191758 27748333; PubMed Central PMCID: PMC5072253.

15. Zhou F, Zhao Y, Huang M, Zeng X, Wang B, Gong H. Disrupted interhemispheric functional connectivity in chronic insomnia disorder: a resting-state fMRI study. Neuropsychiatric disease and treatment. 2018;14:1229–40. Epub 2018/05/26. doi: 10.2147/NDT.S162325 29795981; PubMed Central PMCID: PMC5957476.

16. Sours C, Rosenberg J, Kane R, Roys S, Zhuo J, Shanmuganathan K, et al. Associations between interhemispheric functional connectivity and the Automated Neuropsychological Assessment Metrics (ANAM) in civilian mild TBI. Brain imaging and behavior. 2015;9(2):190–203. Epub 2014/02/22. doi: 10.1007/s11682-014-9295-y 24557591; PubMed Central PMCID: PMC4141037.

17. Corrigan JD, Bogner J. Initial reliability and validity of the Ohio State University TBI Identification Method. The Journal of head trauma rehabilitation. 2007;22(6):318–29. Epub 2007/11/21. doi: 10.1097/01.HTR.0000300227.67748.77 18025964.

18. Beck AT, Steer RA, Ball R, Ranieri W. Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. Journal of personality assessment. 1996;67(3):588–97. Epub 1996/12/01. doi: 10.1207/s15327752jpa6703_13 8991972.

19. Chin EY, Nelson LD, Barr WB, McCrory P, McCrea MA. Reliability and Validity of the Sport Concussion Assessment Tool-3 (SCAT3) in High School and Collegiate Athletes. The American Journal of Sports Medicine. 2016;44(9):2276–85. Epub 2016/06/10. doi: 10.1177/0363546516648141 27281276.

20. Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics. 2016;14(3):339–51. Epub 2016/04/15. doi: 10.1007/s12021-016-9299-4 27075850.

21. Ashburner J, Friston KJ. Nonlinear spatial normalization using basis functions. Human brain mapping. 1999;7(4):254–66. Epub 1999/07/17. 10408769.

22. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, et al. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR American journal of neuroradiology. 2001;22(7):1326–33. Epub 2001/08/11. 11498421.

23. Chang C, Metzger CD, Glover GH, Duyn JH, Heinze HJ, Walter M. Association between heart rate variability and fluctuations in resting-state functional connectivity. NeuroImage. 2013;68:93–104. Epub 2012/12/19. doi: 10.1016/j.neuroimage.2012.11.038 23246859; PubMed Central PMCID: PMC3746190.

24. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage. 2014;84:320–41. Epub 2013/09/03. doi: 10.1016/j.neuroimage.2013.08.048 23994314; PubMed Central PMCID: PMC3849338.

25. Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. The New England journal of medicine. 2013;368(15):1388–97. Epub 2013/04/12. doi: 10.1056/NEJMoa1204471 23574118; PubMed Central PMCID: PMC3691100.

26. Chong CD, Gaw N, Fu Y, Li J, Wu T, Schwedt TJ. Migraine classification using magnetic resonance imaging resting-state functional connectivity data. Cephalalgia: an international journal of headache. 2016. Epub 2016/06/17. doi: 10.1177/0333102416652091 27306407.

27. Duerden EG, Albanese MC. Localization of pain-related brain activation: a meta-analysis of neuroimaging data. Human brain mapping. 2013;34(1):109–49. Epub 2011/12/02. doi: 10.1002/hbm.21416 22131304.

28. Peyron R, Laurent B, Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiologie clinique = Clinical neurophysiology. 2000;30(5):263–88. Epub 2000/12/29. 11126640.

29. Huang S, Li J, Chen K, Wu T, Ye J, Wu X, et al. A Transfer Learning Approach for Network Modeling. IIE transactions: industrial engineering research & development. 2012;44(11):915–31. Epub 2012/11/01. doi: 10.1080/0740817x.2011.649390 24526804; PubMed Central PMCID: PMC3920601.

30. Friedman J, Hastie T, Tibshirani R. Sparse inverse covariance estimation with the graphical lasso. Biostatistics (Oxford, England). 2008;9(3):432–41. Epub 2007/12/15. doi: 10.1093/biostatistics/kxm045 18079126; PubMed Central PMCID: PMC3019769.

31. Hu LS, Ning S, Eschbacher JM, Baxter LC, Gaw N, Ranjbar S, et al. Radiogenomics to characterize regional genetic heterogeneity in glioblastoma. Neuro-Oncology. 2017;19(1):128–37. doi: 10.1093/neuonc/now135 27502248; PubMed Central PMCID: PMC5193022.

32. Ikpotokin O, Edokpa IW. Correlation Analysis: The Bootstrap Approach. International Journal of Scientific & Engineering Research. 2013;4(5):1695–702.

33. Robinson GK. That BLUP is a Good Thing: The Estimation of Random Effects.

34. SCAT3. British journal of sports medicine. 2013;47(5):259. Epub 2013/03/13. 23479480.

35. Borsook D, Veggeberg R, Erpelding N, Borra R, Linnman C, Burstein R, et al.

36. Zhang J, Su J, Wang M, Zhao Y, Zhang QT, Yao Q, et al. The Posterior Insula Shows Disrupted Brain Functional Connectivity in Female Migraineurs Without Aura Based on Brainnetome Atlas. 2017;7(1):16868. doi: 10.1038/s41598-017-17069-8 29203874.

37. Maleki N, Barmettler G, Moulton EA, Scrivani S, Veggeberg R, Spierings EL, et al. Female migraineurs show lack of insular thinning with age. Pain. 2015;156(7):1232–9. Epub 2015/03/17. doi: 10.1097/j.pain.0000000000000159 25775358; PubMed Central PMCID: PMC4474740.

38. Churchill NW, Hutchison MG, Graham SJ, Schweizer TA.

39. Heine J, Pruss H, Kopp UA, Wegner F, Then Bergh F, Munte T, et al. Beyond the limbic system: disruption and functional compensation of large-scale brain networks in patients with anti-LGI1 encephalitis. 2018;89(11):1191–9. doi: 10.1136/jnnp-2017-317780 29886429.

40. Timmermann L, Ploner M, Haucke K, Schmitz F, Baltissen R, Schnitzler A. Differential coding of pain intensity in the human primary and secondary somatosensory cortex. Journal of neurophysiology. 2001;86(3):1499–503. Epub 2001/09/06. doi: 10.1152/jn.2001.86.3.1499 11535693.

41. Torquati K, Pizzella V, Della Penna S, Franciotti R, Babiloni C, Rossini PM, et al. Comparison between SI and SII responses as a function of stimulus intensity. Neuroreport. 2002;13(6):813–9. Epub 2002/05/09. doi: 10.1097/00001756-200205070-00016 11997693.

42. Vakhtin AA, Calhoun VD, Jung RE, Prestopnik JL, Taylor PA, Ford CC. Changes in intrinsic functional brain networks following blast-induced mild traumatic brain injury. Brain injury: [BI]. 2013;27(11):1304–10. Epub 2013/09/12. doi: 10.3109/02699052.2013.823561 24020442.

43. Youssef AM, Ludwick A, Wilcox SL, Lebel A, Peng K, Colon E, et al. In child and adult migraineurs the somatosensory cortex stands out … again: An arterial spin labeling investigation. Human brain mapping. 2017;38(8):4078–87. Epub 2017/06/01. doi: 10.1002/hbm.23649 28560777; PubMed Central PMCID: PMC5509164.


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