Strategic white matter microstructure damage can lead to cognitive impairment in cerebral small vessel disease: disconnection syndrome

doi:10.11817/j.issn.1673-9248.2020.06.003

Abstract

Abstract:

Cerebral small vessel disease (CSVD) is the most common vascular cause of cognitive impairment in the elderly. The lesion-symptom mapping studies found that the damage of strategically located white matter microstructure may be the potential pathogenesis of CSVD-related cognitive impairment, namely cortical-cortical or cortical-subcortical disconnection syndrome. Diffusion tensor imaging (DTI) provides a non-invasive fiber tracking method for the study of white matter microstructure damage. Therefore, this article reviews the study of disconnection syndrome in CSVD-related cognitive impairment and the correlation between fiber microstructure damage and different cognitive domain dysfunction in DTI studies.

Key words: Cerebral small vessel disease, Cognitive impairment, Disconnection syndrome, Microstructure damage, Diffusion tensor imaging

Lili Huang, Yun Xu. Strategic white matter microstructure damage can lead to cognitive impairment in cerebral small vessel disease: disconnection syndrome[J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2020, 14(06): 327-332.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhnxgbzz.cma-cmc.com.cn/EN/10.11817/j.issn.1673-9248.2020.06.003

https://zhnxgbzz.cma-cmc.com.cn/EN/Y2020/V14/I06/327

Figures/Tables 1

References 54

1	Wardlaw JM, Smith C, Dichgans M. Small vessel disease: mechanisms and clinical implications [J]. Lancet Neurol, 2019, 18(7): 684-696.
2	刘品一, 黄丽丽, 徐运. 脑小血管病和脑微循环研究进展 [J]. 中国卒中杂志, 2017, 12(2): 132-142.
3	Dey AK, Stamenova V, Turner G, et al. Pathoconnectomics of cognitive impairment in small vessel disease: a systematic review [J]. Alzheimers Dement, 2016, 12(7): 831-845.
4	Vermeer SE, Longstreth WT, Koudstaal PJ. Silent brain infarcts: a systematic review [J]. Lancet Neurol, 2007, 6(7): 611-619. URL
5	TerTelgte A, van Leijsen EMC, Wiegertjes K, et al. Cerebral small vessel disease: from a focal to a global perspective [J]. Nat Rev Neurol, 2018, 14(7): 387-398.
6	METACOHORTS for the study of vascular disease and its contribution to cognitive decline and neurodegeneration: an initiative of the Joint Programme for Neurodegenerative Disease Research [J]. Alzheimers Dement, 2016, 12(12): 1235-1249.
7	顾雨铖, 徐运. 脑小血管病与血管性认知损害:关注神经影像学 [J]. 国际脑血管病杂志, 2017, 25(3): 244-250.
8	Pasi M, van Uden IW, Tuladhar AM, et al. White matter microstructural damage on diffusion tensor imaging in cerebral small vessel disease: clinical consequences [J]. Stroke, 2016, 47(6): 1679-1684.
9	Williams OA, Zeestraten EA, Benjamin P, et al. Predicting dementia in cerebral small vessel disease using an automatic diffusion tensor image segmentation technique [J]. Stroke, 2019, 50(10): 2775-2782.
10	Prins ND, van Dijk EJ, den Heijer T, et al. Cerebral small-vessel disease and decline in information processing speed, executive function and memory [J]. Brain, 2005, 128(Pt 9): 2034-2041.
11	顾雨铖, 刘任远, 秦若梦,等. 总MRI脑小血管病评分与认知功能的相关性 [J]. 国际脑血管病杂志, 2018, 26(7): 521-527.
12	Muñoz Maniega S, Meijboom R, Chappell FM, et al. Spatial gradient of microstructural changes in normal-appearing white matter in tracts affected by white matter hyperintensities in older age [J]. Front Neurol, 2019, 10: 784.
13	Geschwind N. Disconnexion syndromes in animals and man: part Ⅰ [J]. Brain, 1965, 88(2): 237-294.
14	Catani M, ffytche DH. The rises and falls of disconnection syndromes [J]. Brain, 2005, 128: 2224-2239.
15	Biesbroek JM, Weaver NA, Biessels GJ. Lesion location and cognitive impact of cerebral small vessel disease [J]. Clin Sci, 2017, 131(8): 715-728.
16	Bullmore E, Sporns O. The economy of brain network organization [J]. Nat Rev Neurosci, 2012, 13(5): 336-349. URL
17	Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging [J]. Lancet Neurol, 2013, 12(5): 483-497. URL
18	Ye Q, Bai F. Contribution of diffusion, perfusion and functional MRI to the disconnection hypothesis in subcortical vascular cognitive impairment [J]. Stroke Vasc Neurol, 2018, 3(3): 131-139.
19	Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges [J]. Lancet Neurol, 2010, 9(7): 689-701. URL
20	Wang S, Jiaerken Y, Yu X, et al. Understanding the association between psychomotor processing speed and white matter hyperintensity: A comprehensive multi-modality MR imaging study [J]. Hum Brain Mapp, 2020, 41(3): 605-616.
21	Nir TM, Jahanshad N, Villalon-Reina JE, et al. Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging [J]. Neuroimage Clin, 2013, 3: 180-195.
22	Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review [J]. NMR Biomed, 2002, 15: 435-455.
23	Schmahmann JD, Smith EE, Eichler FS, et al. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates [J]. Ann N Y Acad Sci, 2008, 1142: 266-309.
24	Bhadelia RA, Price LL, Tedesco KL, et al. Diffusion tensor imaging, white matter lesions, the corpus callosum, and gait in the elderly [J]. Stroke, 2009, 40(12): 3816-3820.
25	Duering M, Zieren N, Herve D, et al. Strategic role of frontal white matter tracts in vascular cognitive impairment: a voxel-based lesion-symptom mapping study in CADASIL [J]. Brain, 2011, 134: 2366-2375. URL
26	Smith EE, Salat DH, Jeng J, et al. Correlations between MRI white matter lesion location and executive function and episodic memory [J]. Neurology, 2011, 76(17): 1492-1499.
27	de Laat KF, Tuladhar AM, van Norden AG, et al. Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease [J]. Brain, 2011, 134: 73-83. URL
28	Kantarci K, Senjem ML, Avula R, et al. Diffusion tensor imaging and cognitive function in older adults with no dementia [J]. Neurology, 2011, 77(1): 26-34.
29	Kerchner GA, Racine CA, Hale S, et al. Cognitive processing speed in older adults: relationship with white matter integrity [J]. PLoS One, 2012, 7(11): e50425.
30	Biesbroek JM, Kuijf HJ, van der Graaf Y, et al. Association between subcortical vascular lesion location and cognition: a voxel-based and tract-based lesion-symptom mapping study. The SMART-MR study [J]. PLoS One, 2013, 8(4): e60541.
31	Duering M, Gonik M, Malik R, et al. Identification of a strategic brain network underlying processing speed deficits in vascular cognitive impairment [J]. Neuroimage, 2013, 66: 177-183. URL
32	Duering M, Gesierich B, Seiler S, et al. Strategic white matter tracts for processing speed deficits in age-related small vessel disease [J]. Neurology, 2014, 82(22): 1946-1950. URL
33	Tuladhar AM, van Norden AG, de Laat KF, et al. White matter integrity in small vessel disease is related to cognition [J]. Neuroimage Clin, 2015, 7: 518-524.
34	Biesbroek JM, Weaver NA, Hilal S, et al. Impact of strategically located white matter hyperintensities on cognition in memory clinic patients with small vessel disease [J]. PloS One, 2016, 11(11): e0166261.
35	O'Sullivan M, Barrick TR, Morris RG, et al. Damage within a network of white matter regions underlies executive dysfunction in CADASIL [J]. Neurology, 2005, 65(10): 1584-1590.
36	van der Holst HM, Tuladhar AM, Zerbi V, et al. White matter changes and gait decline in cerebral small vessel disease [J]. Neuroimage Clin, 2018, 17: 731-738.
37	Ghanavati T, Smitt MS, Lord SR, et al. Deep white matter hyperintensities, microstructural integrity and dual task walking in older people [J]. Brain Imaging Behav, 2018, 12(5): 1488-1496.
38	Poole VN, Wooten T, Iloputaife I, et al. Compromised prefrontal structure and function are associated with slower walking in older adults [J]. Neuroimage Clin, 2018, 20: 620-626.
39	Chen HF, Huang LL, Li HY, et al. Microstructural disruption of the right inferior fronto-occipital and inferior longitudinal fasciculus contributes to WMH-related cognitive impairment [J]. CNS Neurosci Ther, 2020, 26(5): 576-588.
40	Mamiya PC, Richards TL, Kuhl PK. Right forceps minor and anterior thalamic radiation predict executive function skills in young bilingual adults [J]. Front Psychol, 2018, 9: 118.
41	Sasson E, Doniger GM, Pasternak O, et al. Structural correlates of cognitive domains in normal aging with diffusion tensor imaging [J]. Brain Struct Funct, 2012, 217(2): 503-515. URL
42	Perry ME, McDonald CR, Hagler DJ, et al. White matter tracts associated with set-shifting in healthy aging [J]. Neuropsychologia, 2009, 47(13): 2835-2842. URL
43	Wen W, Zhu W, He Y, et al. Discrete neuroanatomical networks are associated with specific cognitive abilities in old age [J]. J Neurosci, 2011, 31(4): 1204-1212.
44	Penke L, Munoz Maniega S, Murray C, et al. A general factor of brain white matter integrity predicts information processing speed in healthy older people [J]. J Neurosci, 2010, 30(22): 7569-7574.
45	O'Sullivan M, Jones DK, Summers PE, et al. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline [J]. Neurology, 2001, 57(4): 632-638.
46	Johnson NF, Gold BT, Brown CA, et al. Endothelial function is associated with white matter microstructure and executive function in older adults [J]. Front Aging Neurosci, 2017, 9: 255.
47	Cummings JL. Frontal-subcortical circuits and human behavior [J]. Arch Neurol, 1993, 50(8): 873-880.
48	Makris N, Kennedy DN, McInerney S, et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study [J]. Cereb Cortex, 2005, 15(6): 854-869.
49	Barbey AK, Colom R, Solomon J, et al. An integrative architecture for general intelligence and executive function revealed by lesion mapping [J]. Brain, 2012, 135: 1154-1164. URL
50	Rizvi B, Narkhede A, Last BS, et al. The effect of white matter hyperintensities on cognition is mediated by cortical atrophy [J]. Neurobiol Aging, 2018, 64: 25-32.
51	Chen X, Huang L, Ye Q, et al. Disrupted functional and structural connectivity within default mode network contribute to WMH-related cognitive impairment [J]. Neuroimage Clin, 2019, 24: 102088.
52	Tekin S, Cummings JL. Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update [J]. J Psychosom Res, 2002, 53(2): 647-654.
53	Dichgans M, Markus HS, Salloway S, et al. Donepezil in patients with subcortical vascular cognitive impairment: a randomised double-blind trial in CADASIL [J]. Lancet Neurol, 2008, 7(4): 310-318. URL
54	黄丽丽, 杨丹, 徐运. 前列腺素及其类似物治疗和预防脑小血管病的可能性 [J]. 国际脑血管病杂志, 2019(1): 37-43.

第一作者	发表年份	研究对象	数量	年龄（岁）	病变	分析方法	信息处理速度	执行功能	记忆	步态
Bhadelia RA^[24]	2009	社区老年人	173	72.83±7.72	WMH	ROI	-	-	-	胼胝体膝部
Duering M^[25]	2011	CADASIL	215	47.9±10.7	WMH，腔隙	ROI	双侧ATR，胼胝体压部，胼胝体膝部，左侧CST	-	胼胝体压部	-
Smith EE^[26]	2011	社区人群（对照组40人，MCI 94人，AD 11人）	145	71.2±4.74；72.9±5.5；74.1±6.9	WMH	VLSM	-	双侧额下白质、双侧颞枕、右顶叶脑室周围白质，双侧内囊前肢。	颞枕叶白质、右侧顶叶白质和左侧内囊	-
de Laat KF^[27]	2011	CSVD	429	65.2（8.9）	WMH，LI	VBA， TBSS	-	-	-	胼胝体膝部
Kantarci K^[28]	2011	非痴呆老年人	220	79（52，95）	-	VBA	-	后扣带和前扣带	下纵束，后扣带回，前扣带回	-
Kerchner GA^[29]	2012	老年人	174	69.6±5.9	-	TBSS	胼胝体膝部，胼胝体压部	-	-	-
Biesbroek JM^[30]	2013	明显动脉病变患者	516	56.7±9.4	WMH，腔隙	ROI	-	ATR，上纵束	-	-
Duering M^[31]	2013	CADASIL	235	48（15.5）	WMH，腔隙	ROI	左侧ATR，左侧CS T，胼胝体膝部，扣带回皮质扣带束，扣带海马	-	-	-
Duering M^[32]	2014	社区老年人	584	67.4±9.2	-	VLSM	双侧ATR，胼胝体膝部	-	-	-
Tuladhar AM^[33]	2015	CSVD	444	65.3±8.9	WMH、腔隙	TBSS	-	胼胝体膝部，胼胝体压部	-	-
Biesbroek JM^[34]	2016	记忆门诊中CSVD患者	167	72.8±9.1	WMH	VLSM	ATR，胼胝体膝部	ATR，胼胝体膝部	胼胝体膝部	-
O'Sullivan M^[35]	2016	CADASIL	18	46.3±11.1	WMH	VBA	-	左侧扣带回皮质扣带束	-	-
van der Holst HM^[36]	2017	CSVD	275	62.9±8.2	WMH，腔隙	TBSS	-	-	-	胼胝体和放射冠
Ghanavati T^[37]	2018	老年人	62	80.0±4.2	WMH	TBSS	-	-	-	胼胝体膝部，胼胝体压部
Poole VN^[38]	2018	老年人	68	84.3±4.4	WMH	TBSS	-	ATR，上纵束	-	ATR，上纵束
Chen HF^[39]	2020	对照23人， WMH不伴CI 19人， WMH伴CI 22人	41	62.3±1.50； 67.1±1.66； 65.1±1.54	WMH	AFQ	-	双侧ATR，左下额枕束，右下纵束，右上纵束	-	-

第一作者	发表年份	研究对象	数量	年龄（岁）	病变	分析方法	信息处理速度	执行功能	记忆	步态
Bhadelia RA^[24]	2009	社区老年人	173	72.83±7.72	WMH	ROI	-	-	-	胼胝体膝部
Duering M^[25]	2011	CADASIL	215	47.9±10.7	WMH，腔隙	ROI	双侧ATR，胼胝体压部，胼胝体膝部，左侧CST	-	胼胝体压部	-
Smith EE^[26]	2011	社区人群（对照组40人，MCI 94人，AD 11人）	145	71.2±4.74；72.9±5.5；74.1±6.9	WMH	VLSM	-	双侧额下白质、双侧颞枕、右顶叶脑室周围白质，双侧内囊前肢。	颞枕叶白质、右侧顶叶白质和左侧内囊	-
de Laat KF^[27]	2011	CSVD	429	65.2（8.9）	WMH，LI	VBA， TBSS	-	-	-	胼胝体膝部
Kantarci K^[28]	2011	非痴呆老年人	220	79（52，95）	-	VBA	-	后扣带和前扣带	下纵束，后扣带回，前扣带回	-
Kerchner GA^[29]	2012	老年人	174	69.6±5.9	-	TBSS	胼胝体膝部，胼胝体压部	-	-	-
Biesbroek JM^[30]	2013	明显动脉病变患者	516	56.7±9.4	WMH，腔隙	ROI	-	ATR，上纵束	-	-
Duering M^[31]	2013	CADASIL	235	48（15.5）	WMH，腔隙	ROI	左侧ATR，左侧CS T，胼胝体膝部，扣带回皮质扣带束，扣带海马	-	-	-
Duering M^[32]	2014	社区老年人	584	67.4±9.2	-	VLSM	双侧ATR，胼胝体膝部	-	-	-
Tuladhar AM^[33]	2015	CSVD	444	65.3±8.9	WMH、腔隙	TBSS	-	胼胝体膝部，胼胝体压部	-	-
Biesbroek JM^[34]	2016	记忆门诊中CSVD患者	167	72.8±9.1	WMH	VLSM	ATR，胼胝体膝部	ATR，胼胝体膝部	胼胝体膝部	-
O'Sullivan M^[35]	2016	CADASIL	18	46.3±11.1	WMH	VBA	-	左侧扣带回皮质扣带束	-	-
van der Holst HM^[36]	2017	CSVD	275	62.9±8.2	WMH，腔隙	TBSS	-	-	-	胼胝体和放射冠
Ghanavati T^[37]	2018	老年人	62	80.0±4.2	WMH	TBSS	-	-	-	胼胝体膝部，胼胝体压部
Poole VN^[38]	2018	老年人	68	84.3±4.4	WMH	TBSS	-	ATR，上纵束	-	ATR，上纵束
Chen HF^[39]	2020	对照23人， WMH不伴CI 19人， WMH伴CI 22人	41	62.3±1.50； 67.1±1.66； 65.1±1.54	WMH	AFQ	-	双侧ATR，左下额枕束，右下纵束，右上纵束	-	-

[1]	Shiyuan Wang, Aihua Zhang. Progress of research on the mechanism of chronic kidney disease-related cognitive impairment [J]. Chinese Journal of Kidney Disease Investigation(Electronic Edition), 2023, 12(03): 163-167.
[2]	Wenxuan Chang, Ting Wang, Wei Liu, Tianqi Lan, Jing Peng, Shiyao Wang, Xiaopeng Zhang, Chen Feng, Xuemei Gong, Min Zhu. Research progress of executive dysfunction caused by cerebral small vessel disease [J]. Chinese Journal of Digestion and Medical Imageology(Electronic Edition), 2023, 13(03): 179-182.
[3]	Jinyi Zhao, Zhengying Sun, Hongyi Li, Mingcheng Hu, Xiaoshen Wang, Xiaohang Shi, Yuning Wang, Weiyang Sun, Jian Xing. Imaging study of assessment of gray matter atrophy in patients with subcortical ischemic cerebrovascular disease with cognitive impairment based on structural magnetic resonance imaging [J]. Chinese Journal of Digestion and Medical Imageology(Electronic Edition), 2023, 13(01): 10-14.
[4]	Lei Geng, Zhaoting Zhang, Lei Xu, Hai Huang, Yi Sun, Fumeng Yang, Kai Xu, Chunfeng Hu. Application of diffusion tensor imaging of the basal ganglia circuit in patients with prodromal Parkinson's disease [J]. Chinese Journal of Clinicians(Electronic Edition), 2023, 17(9): 995-1003.
[5]	Ying Zhu, Axiang Zhou, Sen Li, Xu Wang, Guanghui Qi, Ce Yang. The diagnostic basis of long COVID and its effects on the operational efficiency for helicopter pilots [J]. Chinese Journal of Diagnostics(Electronic Edition), 2023, 11(03): 145-152.
[6]	Zhenzhen Yao, Angang Chen, Yanan Zhou, Gaofeng Zhao, Shenshuai Zhang, Jinguo Zhai, Min Chen. Research progress on the characteristics, mechanism and intervention of cognitive impairment in schizophrenia [J]. Chinese Journal of Diagnostics(Electronic Edition), 2023, 11(01): 28-32.
[7]	Wenhua Ding, Yuwei Wang, Jingjing Qiu, Qiong Yang, Yurong Geng. Research progress on imaging biomarkers and motor dysfunction in cerebral small vessel disease [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(05): 429-434.
[8]	Ganzhe Liu, Fen Ai. MiRNA-210 improved vascular cognitive impairment in rats by inhibiting HIF-1α expression [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(05): 489-494.
[9]	Chang Sun, Shigang Zhao, Wenting Bai. The relationship between the cognitive impairment after stroke and the hormone levels [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(05): 471-476.
[10]	Meijuan Yan, Lihui Shao. Correlation between lipoprotein (a) and arteriosclerotic cerebral small vessel disease in elderly population without diabetes, hyperlipidemia and hypertension [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(05): 458-463.
[11]	Lin Liu, Qishan Zhang, Manqian Liao, Yurong Chen, Bei Li, Yucheng He, Shengtao Tang. HTRA1-related autosomal dominant cerebral small vessel disease: a family report and literature review [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(04): 379-385.
[12]	Daohe Wang, Yuanyuan Shi. Value of 8-iso-PGF2α and P selectin in evaluating cognitive function of patients with cerebral small vessel disease [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(04): 364-368.
[13]	Yu Zhang, Yujie Cai, Riqing Lin, Qinjie Qiu, Lili Cui, Dong Zheng, Haihong Zhou. Effect of TNS1 on cognitive function in mice with radiation-induced brain injury [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(03): 244-253.
[14]	Hongmei Hu, Wenli Hu. Research progress in total burden assessment scale for cerebral small vessel disease [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(02): 145-149.
[15]	Zhuoran Li, Wenli Hu. Association of biomarkers of endothelial function, inflammation, and neurodegenerative diseases with arteriosclerotic cerebral small vessel disease [J]. Chinese Journal of Cerebrovascular Diseases(Electronic Edition), 2023, 17(01): 57-60.

Please choose a citation manager

Content to export