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Reorganization of the brain in spinal cord injury: a meta-analysis of functional MRI studies

  • Functional Neuroradiology
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Abstract

Purpose

Reorganization of the brain is considered the key mechanism of functional recovery in patients after spinal cord injury (SCI). This meta-analysis assessed abnormal brain activation in SCI patients to understand the pattern of reorganization in the brain after SCI.

Methods

Functional magnetic resonance imaging (fMRI) studies that compared SCI patients with controls and were published before August 30, 2018, were extracted from the PubMed, Web of Science, and EMBASE databases. Voxel-wise whole-brain meta-analysis and region-of-interest meta-analysis of group differences were separately performed. Then, meta-regression analysis was conducted with several clinical characteristics as regressors.

Results

Sixteen studies that met the inclusion criteria were identified. Compared with control individuals, SCI patients showed increased activation in the sensorimotor cortex in both whole-brain and region-of-interest (ROI) analyses. In addition, whole-brain meta-analysis revealed increased activation in the cerebellum, and this increase was positively correlated with lesion level and injury severity.

Conclusion

Our results demonstrated that reorganization occurred mainly in the sensorimotor system of the brain after SCI, implying that brain functions involved in sensorimotor demands can still be preserved in this condition. These findings provide opportunities for future studies in terms of therapeutic strategies and prognosis assessment.

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References

  1. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J (2011) Functional regeneration of respiratory pathways after spinal cord injury. Nature 475(7355):196–200. https://doi.org/10.1038/nature10199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Jain NB, Ayers GD, Peterson EN, Harris MB, Morse L, O’Connor KC, Garshick E (2015) Traumatic spinal cord injury in the United States, 1993-2012. JAMA 313(22):2236–2243. https://doi.org/10.1001/jama.2015.6250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Cristante AF, Barros Filho TE, Marcon RM, Letaif OB, Rocha ID (2012) Therapeutic approaches for spinal cord injury. Clinics 67(10):1219–1224

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bayona NA, Bitensky J, Teasell R (2005) Plasticity and reorganization of the uninjured brain. Top Stroke Rehabil 12(3):1–10. https://doi.org/10.1310/a422-g91u-q4hb-86xc

    Article  PubMed  Google Scholar 

  5. Weiller C, May A, Sach M, Buhmann C, Rijntjes M (2006) Role of functional imaging in neurological disorders. J Magn Reson Imaging 23(6):840–850. https://doi.org/10.1002/jmri.20591

    Article  PubMed  Google Scholar 

  6. Bisby MA (1981) Axonal transport in the central axon of sensory neurons during regeneration of their peripheral axon. Neurosci Lett 21(1):7–11

    Article  CAS  PubMed  Google Scholar 

  7. Hains BC, Black JA, Waxman SG (2003) Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury. J Comp Neurol 462(3):328–341. https://doi.org/10.1002/cne.10733

    Article  PubMed  Google Scholar 

  8. Kim BG, Dai HN, McAtee M, Vicini S, Bregman BS (2006) Remodeling of synaptic structures in the motor cortex following spinal cord injury. Exp Neurol 198(2):401–415. https://doi.org/10.1016/j.expneurol.2005.12.010

    Article  PubMed  Google Scholar 

  9. Ogawa S, Lee TM (1990) Magnetic resonance imaging of blood vessels at high fields: in vivo and in vitro measurements and image simulation. Magn Reson Med 16(1):9–18

    Article  CAS  PubMed  Google Scholar 

  10. Curt A, Alkadhi H Fau - Crelier GR, Crelier Gr Fau - Boendermaker SH, Boendermaker Sh Fau - Hepp-Reymond M-C, Hepp-Reymond Mc Fau - Kollias SS, Kollias SS (2002) Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. (0006-8950 (Print))

  11. Jutzeler CR, Freund P, Huber E, Curt A, Kramer JLK (2015) Neuropathic pain and functional reorganization in the primary sensorimotor cortex after spinal cord injury. J Pain 16(12):1256–1267. https://doi.org/10.1016/j.jpain.2015.08.008

    Article  PubMed  Google Scholar 

  12. Freund P, Weiskopf N, Ward NS, Hutton C, Gall A, Ciccarelli O, Craggs M, Friston K, Thompson AJ (2011) Disability, atrophy and cortical reorganization following spinal cord injury. Brain J Neurol 134(Pt 6):1610–1622. https://doi.org/10.1093/brain/awr093

    Article  Google Scholar 

  13. Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N, Surguladze S (2012) A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry 27(8):605–611. https://doi.org/10.1016/j.eurpsy.2011.04.001

    Article  CAS  PubMed  Google Scholar 

  14. Nardone R, Holler Y, Sebastianelli L, Versace V, Saltuari L, Brigo F, Lochner P, Trinka E (2018) Cortical morphometric changes after spinal cord injury. Brain Res Bull 137:107–119. https://doi.org/10.1016/j.brainresbull.2017.11.013

    Article  PubMed  Google Scholar 

  15. Kokotilo KJ, Eng JJ, Curt A (2009) Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J Neurotrauma 26(11):2113–2126. https://doi.org/10.1089/neu.2008.0688

    Article  PubMed  Google Scholar 

  16. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6(7):e1000100. https://doi.org/10.1371/journal.pmed.1000100

    Article  PubMed  PubMed Central  Google Scholar 

  17. Radua J, Mataix-Cols D (2012) Meta-analytic methods for neuroimaging data explained. Biol Mood Anxiety Disord 2:6. https://doi.org/10.1186/2045-5380-2-6

    Article  PubMed  PubMed Central  Google Scholar 

  18. Radua J, Rubia K, Canales E, Pomarol-Clotet E, Fusar-Poli P, Mataix-Cols D (2014) Anisotropic kernels for coordinate-based meta-analyses of neuroimaging studies. Front Psych 5:13. https://doi.org/10.3389/fpsyt.2014.00013

    Article  Google Scholar 

  19. Radua J, Mataix-Cols D (2009) Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry J Ment Sci 195(5):393–402. https://doi.org/10.1192/bjp.bp.108.055046

    Article  Google Scholar 

  20. Shoham S, Halgren E, Maynard EM, Normann RA (2001) Motor-cortical activity in tetraplegics. Nature 413(6858):793. https://doi.org/10.1038/35101651

    Article  CAS  PubMed  Google Scholar 

  21. Turner JA, Lee JS, Martinez O, Medlin AL, Schandler SL, Cohen MJ (2001) Somatotopy of the motor cortex after long-term spinal cord injury or amputation. IEEE Trans Neural Syst Rehabil Eng 9(2):154–160. https://doi.org/10.1109/7333.928575

    Article  CAS  PubMed  Google Scholar 

  22. Mikulis DJ, Jurkiewicz MT, McIlroy WE, Staines WR, Rickards L, Kalsi-Ryan S, Crawley AP, Fehlings MG, Verrier MC (2002) Adaptation in the motor cortex following cervical spinal cord injury. Neurology 58(5):794–801

    Article  CAS  PubMed  Google Scholar 

  23. Sabbah P, de SS, Leveque C, Gay S, Pfefer F, Nioche C, Sarrazin JL, Barouti H, Tadie M, Cordoliani YS (2002) Sensorimotor cortical activity in patients with complete spinal cord injury: a functional magnetic resonance imaging study. J Neurotrauma 19(1):53–60. https://doi.org/10.1089/089771502753460231

    Article  CAS  PubMed  Google Scholar 

  24. Turner JA, Lee JS, Schandler SL, Cohen MJ (2003) An fMRI investigation of hand representation in paraplegic humans. Neurorehabil Neural Repair 17(1):37–47. https://doi.org/10.1177/0888439002250443

    Article  PubMed  Google Scholar 

  25. Alkadhi H, Brugger P, Boendermaker SH, Crelier G, Curt A, Hepp-Reymond MC, Kollias SS (2005) What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb Cortex 15(2):131–140. https://doi.org/10.1093/cercor/bhh116

    Article  PubMed  Google Scholar 

  26. Cramer SC, Lastra L, Lacourse MG, Cohen MJ (2005) Brain motor system function after chronic, complete spinal cord injury. Brain J Neurol 128(Pt 12):2941–2950. https://doi.org/10.1093/brain/awh648

    Article  Google Scholar 

  27. Lotze M, Laubis-Herrmann U, Topka H (2006) Combination of TMS and fMRI reveals a specific pattern of reorganization in M1 in patients after complete spinal cord injury. Restor Neurol Neurosci 24(2):97–107

    CAS  PubMed  Google Scholar 

  28. Cramer SC, Orr EL, Cohen MJ, Lacourse MG (2007) Effects of motor imagery training after chronic, complete spinal cord injury. Exp Brain Res 177(2):233–242. https://doi.org/10.1007/s00221-006-0662-9

    Article  PubMed  Google Scholar 

  29. Wrigley PJ, Press Sr Fau - Gustin SM, Gustin Sm Fau - Macefield VG, Macefield Vg Fau - Gandevia SC, Gandevia Sc Fau - Cousins MJ, Cousins Mj Fau - Middleton JW, Middleton Jw Fau - Henderson LA, Henderson La Fau - Siddall PJ, Siddall PJ (2009) Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. (1872-6623 (Electronic))

  30. Gustin SM, Wrigley PJ, Henderson LA, Siddall PJ (2010) Brain circuitry underlying pain in response to imagined movement in people with spinal cord injury. Pain 148(3):438–445. https://doi.org/10.1016/j.pain.2009.12.001

    Article  PubMed  Google Scholar 

  31. Lundell H, Christensen MS, Barthelemy D, Willerslev-Olsen M, Biering-Sorensen F, Nielsen JB (2011) Cerebral activation is correlated to regional atrophy of the spinal cord and functional motor disability in spinal cord injured individuals. NeuroImage 54(2):1254–1261. https://doi.org/10.1016/j.neuroimage.2010.09.009

    Article  CAS  PubMed  Google Scholar 

  32. Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta TA, Raza S, Doddapaneni HV, Metcalf GA, Muzny DM, Gibbs RA, Petrosino JF, Shulman RJ, Versalovic J (2015) Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome 3:36. https://doi.org/10.1186/s40168-015-0101-x

    Article  PubMed  PubMed Central  Google Scholar 

  33. Donoghue JP, Suner S, Sanes JN (1990) Dynamic organization of primary motor cortex output to target muscles in adult rats. II. Rapid reorganization following motor nerve lesions. Exp Brain Res 79(3):492–503

    Article  CAS  PubMed  Google Scholar 

  34. Qi HX, Stepniewska I, Kaas JH (2000) Reorganization of primary motor cortex in adult macaque monkeys with long-standing amputations. J Neurophysiol 84(4):2133–2147. https://doi.org/10.1152/jn.2000.84.4.2133

    Article  CAS  PubMed  Google Scholar 

  35. Ramu J, Bockhorst KH, Mogatadakala KV, Narayana PA (2006) Functional magnetic resonance imaging in rodents: methodology and application to spinal cord injury. J Neurosci Res 84(6):1235–1244. https://doi.org/10.1002/jnr.21030

    Article  CAS  PubMed  Google Scholar 

  36. Dunlop SA (2008) Activity-dependent plasticity: implications for recovery after spinal cord injury. Trends Neurosci 31(8):410–418. https://doi.org/10.1016/j.tins.2008.05.004

    Article  CAS  PubMed  Google Scholar 

  37. Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW (1999) Cortical motor reorganization after paraplegia: an EEG study. Neurology 53(4):736–743

    Article  CAS  PubMed  Google Scholar 

  38. Walker HK (1990) The cerebellum. In: rd, Walker HK, Hall WD, Hurst JW (eds) Clinical methods: the history, physical, and laboratory examinations. Butterworths Butterworth Publishers, a division of Reed Publishing, Boston

  39. Desmurget M, Sirigu A (2012) Conscious motor intention emerges in the inferior parietal lobule. Curr Opin Neurobiol 22(6):1004–1011. https://doi.org/10.1016/j.conb.2012.06.006

    Article  CAS  PubMed  Google Scholar 

  40. Callahan A, Anderson KD, Beattie MS, Bixby JL, Ferguson AR, Fouad K, Jakeman LB, Nielson JL, Popovich PG, Schwab JM, Lemmon VP (2017) Developing a data sharing community for spinal cord injury research. Exp Neurol 295:135–143. https://doi.org/10.1016/j.expneurol.2017.05.012

    Article  PubMed  PubMed Central  Google Scholar 

  41. Urbin MA, Royston DA, Weber DJ, Boninger ML, Collinger JL (2018) What is the functional relevance of reorganization in primary motor cortex after spinal cord injury? Neurobiol Dis 121:286–295. https://doi.org/10.1016/j.nbd.2018.09.009

    Article  PubMed  Google Scholar 

  42. Zhu L, Wu G, Zhou X, Li J, Wen Z, Lin F (2015) Altered spontaneous brain activity in patients with acute spinal cord injury revealed by resting-state functional MRI. PLoS One 10(3):e0118816. https://doi.org/10.1371/journal.pone.0118816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chen Q, Zheng W, Chen X, Li X, Wang L, Qin W, Li K, Chen N (2018) Whether visual-related structural and functional changes occur in brain of patients with acute incomplete cervical cord injury: a multimodal based MRI study. Neuroscience 393:284–294. https://doi.org/10.1016/j.neuroscience.2018.10.014

    Article  CAS  PubMed  Google Scholar 

  44. Hawasli AH, Rutlin J, Roland JL, Murphy RKJ, Song SK, Leuthardt EC, Shimony JS, Ray WZ (2018) Spinal cord injury disrupts resting-state networks in the human brain. J Neurotrauma 35(6):864–873. https://doi.org/10.1089/neu.2017.5212

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

Grant support was provided by the National Natural Science Fund of China (No. 81771346;81874002), the Chinese Postdoctoral Science Foundation (No. 2015T80725), the Technology Research and Development Program of Jinan City (No. 201704133), the Natural Science Funds of Shandong Province (No.ZR2016HP41), Shandong Medical and Health Science and Technology Development Programs (No.2016WS0618), and Science and Technology Development Program of Taian City (No.201640576).

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Author notes

  1. WW and WX contributed equally to this work.

Authors and Affiliations

  1. Department of Orthopedics, Shandong First Medical University/ West China Hospital, Sichuan University, Chengdu, Shandong/Sichuan, China

    Wenzhao Wang, Wei Xie, Lei Liu, Song Zhou, Jixue Shi & Bin Ning

  2. Department Spinal Surgery, Jinan Central Hospital Affiliated to Shandong University, Jinan, Shandong, China

    Wenzhao Wang, Wei Xie, Lei Liu, Jian Liu, Song Zhou, Jixue Shi, Jianan Chen & Bin Ning

  3. Department Obstetrics and Gynecology, The Second Affiliated Hospital of Shandong First Medical University, Taian, Shandong, China

    Qianqian Zhang

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  1. Wenzhao Wang
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  2. Wei Xie
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  3. Qianqian Zhang
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Correspondence to Bin Ning.

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All procedures performed in the studies involving human participants were in accordance with the ethical standards of Shandong University research committee and with the 1964 Helsinki Declaration and its later amendments.

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Wang, W., Xie, W., Zhang, Q. et al. Reorganization of the brain in spinal cord injury: a meta-analysis of functional MRI studies. Neuroradiology 61, 1309–1318 (2019). https://doi.org/10.1007/s00234-019-02272-3

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  • DOI: https://doi.org/10.1007/s00234-019-02272-3

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