脊髓型颈椎病患者解压术前后丘脑-皮质功能改变的静息态fMRI研究
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摘要
目的通过纵向观察脊髓型颈椎病(CSM)患者减压术前后静息态丘脑-皮质功能连接(FC)的变化,探讨脑皮层重塑参与临床功能恢复的相关机制。方法对43例减压术前CSM患者、21例术后3个月随访的CSM患者和43例年龄和性别匹配的健康对照者(HC)进行脑功能磁共振成像扫描。数据经静息态f MRI数据处理助手(DPARSF)预处理后,分别选取左、右侧丘脑作为种子区,将该种子区与大脑其他区域每一个体素的f MRI信号进行分析,得到FC系数并构建功能连接图,运用双独立样本t检验比较CSM患者组减压术前后与对照组之间的功能连接差异,配对t检验比较患者手术前、术后3个月组间大脑功能连接差异。采用日本骨科协会(JOA)评分及颈椎功能障碍指数(NDI)问卷评价患者临床功能。用Pearson相关性分析功能连接差异和临床功能评估之间的相关性。结果与HC组相比,术前CSM患者左侧丘脑与双侧舌回/楔叶(视联合皮质/初级视皮层)/右侧小脑后叶间FC值增加(Voxel P <0. 01,Cluster P <0. 05,GRF校正);术后3个月CSM患者右侧丘脑与双侧中央旁小叶/中央前回之间的FC值减低但是与桥脑/颞上回间FC值明显升高。与术前CSM患者相比,术后CSM患者丘脑与双侧中央旁小叶/中央前回之间的FC值减低但是与后扣带回、角回、内侧前额叶之间的FC值增加(Voxel P <0. 01,Cluster P <0. 05,GRF校正)。术前CSM患者左侧丘脑与双侧舌回/楔叶/右侧小脑后叶FC值与感觉JOA评分存在明显相关性(r=0. 568,P=0. 000)。术后CSM患者丘脑与中央旁小叶/中央前回FC值与上肢运动JOA评分存在明显相关性(r=0. 448,P=0. 042)。结论减压术前后CSM患者存在丘脑-皮质功能连接异常。视觉或感觉运动联合功能网络重塑参与适应、代偿脊髓损伤和减压后中枢系统功能改变,辅助患者临床功能恢复。
Objective The purpose of this study was to characterize the changes of thalamo-cortex longitudinally in resting-state functional connectivity before and after decompression,and to explore how the possible mechanism of cortical remodeling adapts to the recovery of clinical function. Methods 43 pre-decompression CSM patients,21 CSM patients in follow-up 3 months after surgery,and 43 age-and sex-well-matched healthy controls underwent brain rs-fMRI scans. After the data was pretreated by the resting state f MRI data processing assistant( DPARSF),the left and right thalamus were selected as the seed regions,and the f MRI signals of each voxel in the seed region and other regions of the brain were analyzed to obtain the FC coefficients and constructed. Functional connectivity maps were used to compare the differences in functional connectivity between the CSM patients before and after surgery and the control group by paired independent ttest. Paired t-test was used to compare differences in brain functional connectivity between the patients before and 3 months after surgery. The Japanese Orthopaedic Association Scores( JOA) score and the Neck Disability Index Scores( NDI)questionnaire were used to evaluate the clinical function of the patients. Pearson correlation analysis was used to link the association between differences and clinical function assessments. Results Compared with HC,left thalamus in pre-decompression CSM patients exhibited increased FC values with bilateral lingual gyrus/cuneus( Visual Association Cortex/Primary Visual Cortex)/right cerebellum posterior lobe( Voxel P value < 0. 01,Cluster P value < 0. 05,GRF). Three months post-decompression CSM patients manifested reduced FC between right thalamus and bilateral paracentral lobule/precentral gyrus but significantly decreased functional connectivity in the thalamo-pons/-superior temporal gyrus compared with HC.In comparison with pre-decompression CSM patients,the post-decompression CSM patients showed increased FC in the thalamo-posterior cingulate,-angular convolution,-medial prefrontal cortex but significantly decreased functional connectivity in the paracentral lobule/precentral gyrus. There was a significant correlation between the left thalamus and bilateral lingual gyrus/cuneus/right cerebellum posterior lobe in pre-decompression CSM patients with sensory JOA scores( r =0. 568,P = 0. 000). And there was a significant correlation between the thalamus and the paracentral lobule/precentral gyrusin post-decompression CSM patients with Upper limb movement,JOA scores( r = 0. 448,P = 0. 042( P < 0. 05)). Conclusion There is abnormal thalamic-cortical connection in CSM patients before and after decompression. The combined functional network of visual or sensorimotor remodeling participates in adaptation,compensates for spinal cord injury,and changes central nervous system function after decompression,and assists in the recovery of clinical function
Objective The purpose of this study was to characterize the changes of thalamo-cortex longitudinally in resting-state functional connectivity before and after decompression,and to explore how the possible mechanism of cortical remodeling adapts to the recovery of clinical function. Methods 43 pre-decompression CSM patients,21 CSM patients in follow-up 3 months after surgery,and 43 age-and sex-well-matched healthy controls underwent brain rs-fMRI scans. After the data was pretreated by the resting state f MRI data processing assistant( DPARSF),the left and right thalamus were selected as the seed regions,and the f MRI signals of each voxel in the seed region and other regions of the brain were analyzed to obtain the FC coefficients and constructed. Functional connectivity maps were used to compare the differences in functional connectivity between the CSM patients before and after surgery and the control group by paired independent ttest. Paired t-test was used to compare differences in brain functional connectivity between the patients before and 3 months after surgery. The Japanese Orthopaedic Association Scores( JOA) score and the Neck Disability Index Scores( NDI)questionnaire were used to evaluate the clinical function of the patients. Pearson correlation analysis was used to link the association between differences and clinical function assessments. Results Compared with HC,left thalamus in pre-decompression CSM patients exhibited increased FC values with bilateral lingual gyrus/cuneus( Visual Association Cortex/Primary Visual Cortex)/right cerebellum posterior lobe( Voxel P value < 0. 01,Cluster P value < 0. 05,GRF). Three months post-decompression CSM patients manifested reduced FC between right thalamus and bilateral paracentral lobule/precentral gyrus but significantly decreased functional connectivity in the thalamo-pons/-superior temporal gyrus compared with HC.In comparison with pre-decompression CSM patients,the post-decompression CSM patients showed increased FC in the thalamo-posterior cingulate,-angular convolution,-medial prefrontal cortex but significantly decreased functional connectivity in the paracentral lobule/precentral gyrus. There was a significant correlation between the left thalamus and bilateral lingual gyrus/cuneus/right cerebellum posterior lobe in pre-decompression CSM patients with sensory JOA scores( r =0. 568,P = 0. 000). And there was a significant correlation between the thalamus and the paracentral lobule/precentral gyrusin post-decompression CSM patients with Upper limb movement,JOA scores( r = 0. 448,P = 0. 042( P < 0. 05)). Conclusion There is abnormal thalamic-cortical connection in CSM patients before and after decompression. The combined functional network of visual or sensorimotor remodeling participates in adaptation,compensates for spinal cord injury,and changes central nervous system function after decompression,and assists in the recovery of clinical function
引文
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11 Cordes D,Haughton VM,Arfanakis K,et al. Mapping functionally related regions of brain with functional connectivity MR imaging[J].American Journal of Neuroradiology,2000,21:1636-1644.
12 Cordes D,Haughton VM,Arfanakis K,et al. Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state”data[J]. AJNR,2001,22:1326-1333.
13 Tomasi D,Volkow ND. Association between functional connectivity hubs and brain networks[J]. Cereb Cortex,2011,21:2003-2013.
14 谭永明,周福庆,刘志礼,等.脊髓型颈椎病患者减压术后感觉运动皮层局部一致性改变的静息态功能MRI研究[J].中华放射学杂志,2016,50:495-499.
15 BC H,JA B,SG W,Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury[J]. The Journal of Comparative Neurology,2003,462:328-341.
16 Kaas JH,Qi H-X,Burish MJ,et al. Cortical and subcortical plasticity in the brains of humans,primates,and rats after damage to sensory afferents in the dorsal columns of the spinal cord[J]. Exp Neurol,2008,209:407-416.
17 Henderson LA,Siddall PJ,Wrigley PJ,et al. Functional reorganization of the brain in humans following spinal cord injury:evidence for underlying changes in cortical anatomy[J]. J Neurosci,2011,31:2630-2637.
18 PC F,CD F,PM G. Brain systems for encoding and retrieval of auditory-verbal memory:an in vivo study in humans[J]. Brain,1995,118:401-416.
19 Molnar-Szakacs I,Uddin LQ. Self-processing and the default mode network:interactions with the mirror neuron system[J]. Front Hum Neurosci,2013,7:571.
20 Lakatos P,Chen CM,O’connell MN,et al. Neuronal oscillations and multisensory interaction in primary auditory cortex[J]. Neuron,2007,53:279-292.
21 Driver J,Noesselt T. Multisensory interplay reveals crossmodal influences on'sensory-specific'brain regions,neural responses,and judgments[J]. Neuron,2008,57:11-23.
22 Macaluso E,Driver J. Multisensory spatial interactions:a window onto functional integration in the human brain[J]. Trends Neurosci,2005,28:264-271.
23 Cappe C,Barone P. Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey[J].Eur J Neurosci,2005,22:2886-2902.
24 Menon V,Uddin LQ. Saliency,switching,attention and control:a network model of insula function[J]. Brain Struct Funct,2010,214:655-667.
25 Zhu L,Wu G,Zhu X,et al. Altered spontaneous brain activity in patients with acute spinal cord injury revealed by resting-state functional MRI[J]. PLo S One,2015,10:e0118816.
26 Moxon KA,Oliviero A,Aguilar J,et al. Cortical reorganization after spinal cord injury:always for good?[J]. Neuroscience,2014,283:78-94.
27 Wen CY,Cui JL,Mak KC,et al. Diffusion tensor imaging of somatosensory tract in cervical spondylotic myelopathy and its link with electrophysiological evaluation[J]. Spine J,2014,14:1493-1500.
28 Fouad K,Krajacic A,Tetzlaff W. Spinal cord injury and plasticity:opportunities and challenges[J]. Brain Res Bull,2011,84:337-342.
29 Lee J,Satkunendrarajah K,Fehlings MG. Development and characterization of a novel rat model of cervical spondylotic myelopathy:the impact of chronic cord compression on clinical,neuroanatomical,and neurophysiological outcomes[J]. J Neurotrauma,2012,29:1012-1027.
30 Frigon A,Barrière Grégory,Leblond Hugues,et al. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat[J]. J Neurophysiol,2009,102:2667-2680.
2 Yarbrough CK,Murphy RKJ,Ray WZ,et al. The natural history and clinical presentation of cervical spondylotic myelopathy[J]. Adv Orthop,2012,2012:480643.
3 Nardone R,H9ller Y,Brigo F,et al. Functional brain reorganization after spinal cord injury:systematic review of animal and human studies[J]. Brain Res,2013,1504:58-73.
4 Yukawa Y,Kato F,Ito K,et al. Postoperative changes in spinal cord signal intensity in patients with cervical compression myelopathy:comparison between preoperative and postoperative magnetic resonance images[J]. J Neurosurg Spine,2008,8:524-528.
5 Jurkiewicz MT,Mikulis DJ,Fehlings MG. Sensorimotor cortical activation in patients with cervical spinal cord injury with persisting paralysis[J]. Neurorehabil Neural Repair,2010,24:136-140.
6 Nishimura Y,Hirotaka O,Kayo O,et al. Neural substrates for the motivational regulation of motor recovery after spinal-cord injury[J].PLo S One,2011,6:e24854.
7 Goncalves S,Stevens TK,Doyle-Pettypiece P,et al. N-acetylaspartate in the motor and sensory cortices following functional recovery after surgery for cervical spondylotic myelopathy[J]. J Neurosurg Spine,2016,25:436-443.
8 Moussellard HP,Meyer A,Biot D,et al. Early neurological recovery course after surgical treatment of cervical spondylotic myelopathy:a prospective study with 2-year follow-up using three different functional assessment tests[J]. Eur Spine J,2014,23:1508-1514.
9 Al-Tamimi YZ,Guilfoyle M,Seeley H,et al. Measurement of longterm outcome in patients with cervical spondylotic myelopathy treated surgically[J]. Eur Spine J,2013,22:2552-2557.
10 van den Heuvel MP,HE HP. Exploring the brain network:a review on resting-state f MRI functional connectivity[J]. Eur Neuropsychopharmacol,2010,20:519-534.
11 Cordes D,Haughton VM,Arfanakis K,et al. Mapping functionally related regions of brain with functional connectivity MR imaging[J].American Journal of Neuroradiology,2000,21:1636-1644.
12 Cordes D,Haughton VM,Arfanakis K,et al. Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state”data[J]. AJNR,2001,22:1326-1333.
13 Tomasi D,Volkow ND. Association between functional connectivity hubs and brain networks[J]. Cereb Cortex,2011,21:2003-2013.
14 谭永明,周福庆,刘志礼,等.脊髓型颈椎病患者减压术后感觉运动皮层局部一致性改变的静息态功能MRI研究[J].中华放射学杂志,2016,50:495-499.
15 BC H,JA B,SG W,Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury[J]. The Journal of Comparative Neurology,2003,462:328-341.
16 Kaas JH,Qi H-X,Burish MJ,et al. Cortical and subcortical plasticity in the brains of humans,primates,and rats after damage to sensory afferents in the dorsal columns of the spinal cord[J]. Exp Neurol,2008,209:407-416.
17 Henderson LA,Siddall PJ,Wrigley PJ,et al. Functional reorganization of the brain in humans following spinal cord injury:evidence for underlying changes in cortical anatomy[J]. J Neurosci,2011,31:2630-2637.
18 PC F,CD F,PM G. Brain systems for encoding and retrieval of auditory-verbal memory:an in vivo study in humans[J]. Brain,1995,118:401-416.
19 Molnar-Szakacs I,Uddin LQ. Self-processing and the default mode network:interactions with the mirror neuron system[J]. Front Hum Neurosci,2013,7:571.
20 Lakatos P,Chen CM,O’connell MN,et al. Neuronal oscillations and multisensory interaction in primary auditory cortex[J]. Neuron,2007,53:279-292.
21 Driver J,Noesselt T. Multisensory interplay reveals crossmodal influences on'sensory-specific'brain regions,neural responses,and judgments[J]. Neuron,2008,57:11-23.
22 Macaluso E,Driver J. Multisensory spatial interactions:a window onto functional integration in the human brain[J]. Trends Neurosci,2005,28:264-271.
23 Cappe C,Barone P. Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey[J].Eur J Neurosci,2005,22:2886-2902.
24 Menon V,Uddin LQ. Saliency,switching,attention and control:a network model of insula function[J]. Brain Struct Funct,2010,214:655-667.
25 Zhu L,Wu G,Zhu X,et al. Altered spontaneous brain activity in patients with acute spinal cord injury revealed by resting-state functional MRI[J]. PLo S One,2015,10:e0118816.
26 Moxon KA,Oliviero A,Aguilar J,et al. Cortical reorganization after spinal cord injury:always for good?[J]. Neuroscience,2014,283:78-94.
27 Wen CY,Cui JL,Mak KC,et al. Diffusion tensor imaging of somatosensory tract in cervical spondylotic myelopathy and its link with electrophysiological evaluation[J]. Spine J,2014,14:1493-1500.
28 Fouad K,Krajacic A,Tetzlaff W. Spinal cord injury and plasticity:opportunities and challenges[J]. Brain Res Bull,2011,84:337-342.
29 Lee J,Satkunendrarajah K,Fehlings MG. Development and characterization of a novel rat model of cervical spondylotic myelopathy:the impact of chronic cord compression on clinical,neuroanatomical,and neurophysiological outcomes[J]. J Neurotrauma,2012,29:1012-1027.
30 Frigon A,Barrière Grégory,Leblond Hugues,et al. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat[J]. J Neurophysiol,2009,102:2667-2680.