A preliminary study on the influence of rehabilitation on the brain network by the graph theoretic analysis for patients with incomplete spinal cord injury_West China Medical Journal

Authors：

FENG Yutong ¹ , GE Yunxiang ² , DOU Weibei ² , WU Qiong ¹ ,  PAN Yu ¹

1. Department of Rehabilitation Medicine, Tsinghua University Affiliated Beijing Tsinghua Changgung Hospital, Beijing 102218,P. R. China;
2. Department of Electronic Engineering, Tsinghua University, Beijing 100084, P. R. China;

Corresponding author：

PAN Yu, Email: py10335@163.com

Keywords：

Spinal cord injury; Brain network; Graph theoretic analysis

DOI：

10.7507/1002-0179.202104015

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Objective To explore the effect mechanism of rehabilitation therapy post incomplete spinal cord injury (ISCI) in the view of graph theoretic analysis of the whole brain regions by the means of resting state functional magnetic resonance imaging (rs-fMRI).Methods Patients with ISCI admitted to the Department of Rehabilitation Medicine of Tsinghua University Affiliated Beijing Tsinghua Changgung Hospital from January 2017 to June 2020 were selected and healthy subjects recruited in the same period were also selected. The patients were given comprehensive rehabilitation treatment for 2 weeks, including physical therapy, functional electrical stimulation treadwheel, walking training, etc. Healthy subjects and patients before and after treatment course were examined by rs-fMRI. While patients were assessed using the motor and sensory scores of American Spinal Injury Association (ASIA), muscle tone assessment, pain assessment, Walking Index for spinal cord injury (WISCI) as well as the Spinal Cord Independence Measure (SCIM).Results A total of 23 ISCI patients and 22 healthy subjects were included. After 2 weeks of treatment, ASIA lower limb motor function scores (P<0.001), ASIA sensory scores (P=0.005), Visual Analogue Scale (VAS) (P=0.027), WISCI (P=0.005) and SCIM (P<0.001) scores of the patients were significantly improved compared with before treatment. Before treatment, compared with healthy subjects, ISCI patients had lower betweenness centrality (BC) in the brain regions of R38, lower local efficiency (LE) in L21, L22, L39, L41, L42, L44, L48, R22, R39 and lower weighted degree (WD) in L22, L39, L41, L44, L48, R22, R39. After treatment, compared with the healthy subjects, the BC of R5, R6, R7, AR111 and AL112 of ISCI patients increased and in R6 and AR94, the clustering coefficient increased. The LE and WD of L21 and R21 in ISCI patients after treatment were higher than those before treatment.Conclusions The functional analysis of the whole brain network based on graph analysis can sensitively reflect the changes of brain network remodeling in patients with ISCI. Spinal cord injury can cause the decline of graph theoretical attributes of the auditory center-related brain regions. After rehabilitation treatment, the sensorimotor cortex, auditory center and extravertebral brain regions information transmitting ability in the whole brain network are improved, suggesting that rehabilitation training may participate in brain function remodeling by activating the sensorimotor center and non-motor center-related brain regions.

Citation： FENG Yutong, GE Yunxiang, DOU Weibei, WU Qiong, PAN Yu. A preliminary study on the influence of rehabilitation on the brain network by the graph theoretic analysis for patients with incomplete spinal cord injury. West China Medical Journal, 2021, 36(7): 882-888. doi: 10.7507/1002-0179.202104015 Copy

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2.	Biswal B, Yetkin FZ, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med, 1995, 34(4): 537-541.
3.	Zhu L, Wu G, Zhou X, et al. Altered spontaneous brain activity in patients with acute spinal cord injury revealed by resting-state functional MRI. PLoS One, 2015, 10(3): e0118816.
4.	Pan Y, Dou WB, Wang YH, et al. Non-concomitant cortical structural and functional alterations in sensorimotor areas following incomplete spinal cord injury. Neural Regen Res, 2017, 12(12): 2059-2066.
5.	王方永, 李建军. 脊髓损伤神经学分类国际标准(ASIA 2011版)最新修订及标准解读. 中国康复理论与实践, 2012, 18(8): 797-800.
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11.	Honey CJ, Thivierge JP, Sporns O. Can structure predict function in the human brain?. Neuroimage, 2010, 52(3): 766-776.
12.	Wang J, Zuo X, He Y. Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci, 2010, 4: 16.
13.	De Vico Fallani F, Astolfi L, Cincotti F, et al. Cortical functional connectivity networks in normal and spinal cord injured patients: Evaluation by graph analysis. Hum Brain Mapp, 2007, 28(12): 1334-1346.
14.	Min YS, Chang Y, Park JW, et al. Change of brain functional connectivity in patients with spinal cord injury: graph theory based approach. Ann Rehabil Med, 2015, 39(3): 374-383.
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16.	Sang L, Qin W, Liu Y, et al. Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. Neuroimage, 2012, 61(4): 1213-1225.
17.	Chen Q, Zheng W, Chen X, et al. Reorganization of the somatosensory pathway after subacute incomplete cervical cord injury. Neuroimage Clin, 2019, 21: 101674.
18.	Filipp ME, Travis BJ, Henry SS, et al. Differences in neuroplasticity after spinal cord injury in varying animal models and humans. Neural Regen Res, 2019, 14(1): 7-19.
19.	Xu K, Liu H, Li H, et al. Amplitude of low-frequency fluctuations in bipolar disorder: a resting state fMRI study. J Affect Disord, 2014, 152-154: 237-242.
20.	Dien J, Brian ES, Molfese DL, et al. Combined ERP/fMRI evidence for early word recognition effects in the posterior inferior temporal gyrus. Cortex, 2013, 49(9): 2307-2321.
21.	Wegner C, Filippi M, Korteweg T, et al. Relating functional changes during hand movement to clinical parameters in patients with multiple sclerosis in a multi-centre fMRI study. Eur J Neurol, 2008, 15(2): 113-122.

1. Kokotilo KJ, Eng JJ, Curt A. Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J Neurotrauma, 2009, 26(11): 2113-2126.
2. Biswal B, Yetkin FZ, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med, 1995, 34(4): 537-541.
3. Zhu L, Wu G, Zhou X, et al. Altered spontaneous brain activity in patients with acute spinal cord injury revealed by resting-state functional MRI. PLoS One, 2015, 10(3): e0118816.
4. Pan Y, Dou WB, Wang YH, et al. Non-concomitant cortical structural and functional alterations in sensorimotor areas following incomplete spinal cord injury. Neural Regen Res, 2017, 12(12): 2059-2066.
5. 王方永, 李建军. 脊髓损伤神经学分类国际标准(ASIA 2011版)最新修订及标准解读. 中国康复理论与实践, 2012, 18(8): 797-800.
6. Zheng W, Ge Y, Ren S, et al. Abnormal static and dynamic functional connectivity of resting-state fMRI in multiple system atrophy. Aging (Albany NY), 2020, 12(16): 16341-16356.
7. Liu Y, Xiong H, Li X, et al. Abnormal baseline brain activity in neuromyelitis optica patients without brain lesion detected by resting-state functional magnetic resonance imaging. Neuropsychiatr Dis Treat, 2020, 16: 71-79.
8. Bullmore Ed, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci, 2009, 10(3): 186-198.
9. Sporns O, Chialvo DR, Kaiser M, et al. Organization, development and function of complex brain networks. Trends Cogn Sci, 2004, 8(9): 418-425.
10. Micheloyannis S, Vourkas M, Tsirka V, et al. The influence of ageing on complex brain networks: a graph theoretical analysis. Hum Brain Mapp, 2009, 30(1): 200-208.
11. Honey CJ, Thivierge JP, Sporns O. Can structure predict function in the human brain?. Neuroimage, 2010, 52(3): 766-776.
12. Wang J, Zuo X, He Y. Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci, 2010, 4: 16.
13. De Vico Fallani F, Astolfi L, Cincotti F, et al. Cortical functional connectivity networks in normal and spinal cord injured patients: Evaluation by graph analysis. Hum Brain Mapp, 2007, 28(12): 1334-1346.
14. Min YS, Chang Y, Park JW, et al. Change of brain functional connectivity in patients with spinal cord injury: graph theory based approach. Ann Rehabil Med, 2015, 39(3): 374-383.
15. Nishimura Y, Onoe H, Onoe K, et al. Neural substrates for the motivational regulation of motor recovery after spinal-cord injury. PLoS One, 2011, 6(9): e24854.
16. Sang L, Qin W, Liu Y, et al. Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. Neuroimage, 2012, 61(4): 1213-1225.
17. Chen Q, Zheng W, Chen X, et al. Reorganization of the somatosensory pathway after subacute incomplete cervical cord injury. Neuroimage Clin, 2019, 21: 101674.
18. Filipp ME, Travis BJ, Henry SS, et al. Differences in neuroplasticity after spinal cord injury in varying animal models and humans. Neural Regen Res, 2019, 14(1): 7-19.
19. Xu K, Liu H, Li H, et al. Amplitude of low-frequency fluctuations in bipolar disorder: a resting state fMRI study. J Affect Disord, 2014, 152-154: 237-242.
20. Dien J, Brian ES, Molfese DL, et al. Combined ERP/fMRI evidence for early word recognition effects in the posterior inferior temporal gyrus. Cortex, 2013, 49(9): 2307-2321.
21. Wegner C, Filippi M, Korteweg T, et al. Relating functional changes during hand movement to clinical parameters in patients with multiple sclerosis in a multi-centre fMRI study. Eur J Neurol, 2008, 15(2): 113-122.

West China Medical Journal

A preliminary study on the influence of rehabilitation on the brain network by the graph theoretic analysis for patients with incomplete spinal cord injury

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