Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy

Chia-Feng Lu, Po-Shan Wang, Yuan-Lin Lao, Hsiu-Mei Wu, Bing-Wen Soong, Yu-Te Wu

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

The cerebellum involves diverse functions from motor coordination to higher cognitive functions. Impairment of the cerebellum can cause ataxia and cerebellar cognitive affective syndrome. Multiple system atrophy of the cerebellar type (MSA-C) is a neurodegenerative disorder with atrophy of medullo-ponto-cerebellar (MPC) white matter (WM). To understand the role of the cerebellum from the perspective of the local structure to the global function in the presence of MPC WM degeneration, we acquired T1-weighted and diffusion tensor images for 17 patients with MSA-C and 19 normal controls. We concurrently used the measures of local morphology, including MPC WM volume and inner surface area, and properties of global network organization based on graph theory for the MSA-C and control groups. The results showed that MPC WM degeneration caused the destruction of cerebello-ponto-cerebral loops, resulting in reduced communication efficiency between regions in the whole-brain network. In addition, the sulcal area of the inner cortical surface in the cerebellum decreased linearly with the MPC WM volume, and the inferoposterior lobe exhibited a steeper atrophy rate than that of vermis regions. We concluded that the integrity of MPC WM is critical in sustaining the local morphology and the global functions of the whole-brain fiber network. © 2013 Springer-Verlag.
Original languageEnglish
Pages (from-to)947-958
Number of pages12
JournalBrain Structure and Function
Volume219
Issue number3
DOIs
Publication statusPublished - 2014
Externally publishedYes

Fingerprint

Multiple System Atrophy
Cerebellum
Brain
Atrophy
Cerebellar Ataxia
Surface Properties
Neurodegenerative Diseases
Cognition
White Matter
Communication
Control Groups

Keywords

  • Diffusion tensor imaging
  • Graph theory
  • Multiple system atrophy
  • Shape index
  • Surface morphology
  • White matter degeneration
  • adult
  • article
  • ataxia
  • brain atrophy
  • brain size
  • cerebellum
  • cerebellum atrophy
  • cerebellum vermis
  • clinical article
  • controlled study
  • female
  • human
  • interpersonal communication
  • male
  • middle aged
  • motor coordination
  • nerve degeneration
  • priority journal
  • Shy Drager syndrome
  • white matter
  • aged
  • brain mapping
  • image processing
  • nerve cell network
  • nuclear magnetic resonance imaging
  • pathology
  • procedures
  • Adult
  • Aged
  • Brain Mapping
  • Cerebellum
  • Female
  • Humans
  • Image Processing, Computer-Assisted
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Multiple System Atrophy
  • Nerve Net
  • White Matter

Cite this

Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy. / Lu, Chia-Feng; Wang, Po-Shan; Lao, Yuan-Lin; Wu, Hsiu-Mei; Soong, Bing-Wen; Wu, Yu-Te.

In: Brain Structure and Function, Vol. 219, No. 3, 2014, p. 947-958.

Research output: Contribution to journalArticle

Lu, Chia-Feng ; Wang, Po-Shan ; Lao, Yuan-Lin ; Wu, Hsiu-Mei ; Soong, Bing-Wen ; Wu, Yu-Te. / Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy. In: Brain Structure and Function. 2014 ; Vol. 219, No. 3. pp. 947-958.
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title = "Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy",
abstract = "The cerebellum involves diverse functions from motor coordination to higher cognitive functions. Impairment of the cerebellum can cause ataxia and cerebellar cognitive affective syndrome. Multiple system atrophy of the cerebellar type (MSA-C) is a neurodegenerative disorder with atrophy of medullo-ponto-cerebellar (MPC) white matter (WM). To understand the role of the cerebellum from the perspective of the local structure to the global function in the presence of MPC WM degeneration, we acquired T1-weighted and diffusion tensor images for 17 patients with MSA-C and 19 normal controls. We concurrently used the measures of local morphology, including MPC WM volume and inner surface area, and properties of global network organization based on graph theory for the MSA-C and control groups. The results showed that MPC WM degeneration caused the destruction of cerebello-ponto-cerebral loops, resulting in reduced communication efficiency between regions in the whole-brain network. In addition, the sulcal area of the inner cortical surface in the cerebellum decreased linearly with the MPC WM volume, and the inferoposterior lobe exhibited a steeper atrophy rate than that of vermis regions. We concluded that the integrity of MPC WM is critical in sustaining the local morphology and the global functions of the whole-brain fiber network. {\circledC} 2013 Springer-Verlag.",
keywords = "Diffusion tensor imaging, Graph theory, Multiple system atrophy, Shape index, Surface morphology, White matter degeneration, adult, article, ataxia, brain atrophy, brain size, cerebellum, cerebellum atrophy, cerebellum vermis, clinical article, controlled study, female, human, interpersonal communication, male, middle aged, motor coordination, nerve degeneration, priority journal, Shy Drager syndrome, white matter, aged, brain mapping, image processing, nerve cell network, nuclear magnetic resonance imaging, pathology, procedures, Adult, Aged, Brain Mapping, Cerebellum, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Multiple System Atrophy, Nerve Net, White Matter",
author = "Chia-Feng Lu and Po-Shan Wang and Yuan-Lin Lao and Hsiu-Mei Wu and Bing-Wen Soong and Yu-Te Wu",
note = "被引用次數:2 Export Date: 31 March 2016 通訊地址: Soong, B.-W.; Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, No. 155, Li-Nong Street, Pei-Tou, Taipei 112, Taiwan; 電子郵件: bwsoong@gmail.com 參考文獻: Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks (2007) PLoS Comput Biol, 3, pp. e17; Armstrong, R.A., Cairns, N.J., Lantos, P.L., A quantitative study of the pathological changes in white matter in multiple system atrophy (2007) Neuropathology, 27 (3), pp. 221-227. , DOI 10.1111/j.1440-1789.2007.00759.x; Beg, M.F., Miller, M.I., Trouv{\'e}, A., Younes, L., Computing large deformation metric mappings via geodesic flows of diffeomorphisms (2005) Int J Comput Vision, 61, pp. 139-157; Brenneis, C., Boesch, S.M., Egger, K.E., Seppi, K., Scherfler, C., Schocke, M., Wenning, G.K., Poewe, W., Cortical atrophy in the cerebellar variant of multiple system atrophy: A voxel-based morphometry study (2006) Mov Disord, 21, pp. 159-165; Bullmore, E., Sporns, O., Complex brain networks: Graph theoretical analysis of structural and functional systems (2009) Nat Rev Neurosci, 10, pp. 186-198; Chen, H., Zhang, T., Guo, L., Li, K., Yu, X., Li, L., Hu, X., Liu, T., Coevolution of gyral folding and structural connection patterns in primate brains (2012) Cereb Cortex, , doi:10.1093/cercor/bhs113; Gilman, S., Wenning, G.K., Low, P.A., Brooks, D.J., Mathias, C.J., Trojanowski, J.Q., Wood, N.W., Vidailhet, M., Second consensus statement on the diagnosis of multiple system atrophy (2008) Neurology, 71, pp. 670-676; Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C.F., Menon, V., Greicius, M.D., Distinct cerebellar contributions to intrinsic connectivity networks (2009) J Neurosci, 29, pp. 8586-8594; Habas, P.A., Scott, J.A., Roosta, A., Rajagopalan, V., Kim, K., Rousseau, F., Barkovich, A.J., Studholme, C., Early folding patterns and asymmetries of the normal human brain detected from in utero MRI (2012) Cereb Cortex, 22, pp. 13-25; Harris, A.D., Pereira, R.S., Mitchell, J.R., Hill, M.D., Sevick, R.J., Frayne, R., A comparison of images generated from diffusion-weighted and diffusion-tensor imaging data in hyper-acute stroke (2004) Journal of Magnetic Resonance Imaging, 20 (2), pp. 193-200. , DOI 10.1002/jmri.20116; Hauser, T.-K., Luft, A., Skalej, M., Nagele, T., Kircher, T.T.J., Leube, D.T., Schulz, J.B., Visualization and quantification of disease progression in multiple system atrophy (2006) Movement Disorders, 21 (10), pp. 1674-1681. , DOI 10.1002/mds.21032; Hilgetag, C.C., Barbas, H., Role of mechanical factors in the morphology of the primate cerebral cortex (2006) PLoS Comput Biol, 2, pp. e22; Holmes, G., The cerebellum of man (1939) Brain, 62, pp. 1-30; Hu, H.-H., Guo, W.-Y., Chen, H.-Y., Wang, P.-S., Hung, C.-I., Hsieh, J.-C., Wu, Y.-T., Morphological regionalization using fetal magnetic resonance images of normal developing brains (2009) Eur J Neurosci, 29, pp. 1560-1567; Hu, H.-H., Chen, H.-Y., Hung, C.-I., Guo, W.-Y., Wu, Y.-T., Shape and curvedness analysis of brain morphology using human fetal magnetic resonance images in utero (2013) Brain Struct Funct, , doi:10.1007/s00429-012-0469-3; 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year = "2014",
doi = "10.1007/s00429-013-0545-3",
language = "English",
volume = "219",
pages = "947--958",
journal = "Anatomy and Embryology",
issn = "0177-5154",
publisher = "Springer Verlag",
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}

TY - JOUR

T1 - Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy

AU - Lu, Chia-Feng

AU - Wang, Po-Shan

AU - Lao, Yuan-Lin

AU - Wu, Hsiu-Mei

AU - Soong, Bing-Wen

AU - Wu, Yu-Te

N1 - 被引用次數:2 Export Date: 31 March 2016 通訊地址: Soong, B.-W.; Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, No. 155, Li-Nong Street, Pei-Tou, Taipei 112, Taiwan; 電子郵件: bwsoong@gmail.com 參考文獻: Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks (2007) PLoS Comput Biol, 3, pp. e17; Armstrong, R.A., Cairns, N.J., Lantos, P.L., A quantitative study of the pathological changes in white matter in multiple system atrophy (2007) Neuropathology, 27 (3), pp. 221-227. , DOI 10.1111/j.1440-1789.2007.00759.x; Beg, M.F., Miller, M.I., Trouvé, A., Younes, L., Computing large deformation metric mappings via geodesic flows of diffeomorphisms (2005) Int J Comput Vision, 61, pp. 139-157; Brenneis, C., Boesch, S.M., Egger, K.E., Seppi, K., Scherfler, C., Schocke, M., Wenning, G.K., Poewe, W., Cortical atrophy in the cerebellar variant of multiple system atrophy: A voxel-based morphometry study (2006) Mov Disord, 21, pp. 159-165; Bullmore, E., Sporns, O., Complex brain networks: Graph theoretical analysis of structural and functional systems (2009) Nat Rev Neurosci, 10, pp. 186-198; Chen, H., Zhang, T., Guo, L., Li, K., Yu, X., Li, L., Hu, X., Liu, T., Coevolution of gyral folding and structural connection patterns in primate brains (2012) Cereb Cortex, , doi:10.1093/cercor/bhs113; Gilman, S., Wenning, G.K., Low, P.A., Brooks, D.J., Mathias, C.J., Trojanowski, J.Q., Wood, N.W., Vidailhet, M., Second consensus statement on the diagnosis of multiple system atrophy (2008) Neurology, 71, pp. 670-676; Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C.F., Menon, V., Greicius, M.D., Distinct cerebellar contributions to intrinsic connectivity networks (2009) J Neurosci, 29, pp. 8586-8594; Habas, P.A., Scott, J.A., Roosta, A., Rajagopalan, V., Kim, K., Rousseau, F., Barkovich, A.J., Studholme, C., Early folding patterns and asymmetries of the normal human brain detected from in utero MRI (2012) Cereb Cortex, 22, pp. 13-25; Harris, A.D., Pereira, R.S., Mitchell, J.R., Hill, M.D., Sevick, R.J., Frayne, R., A comparison of images generated from diffusion-weighted and diffusion-tensor imaging data in hyper-acute stroke (2004) Journal of Magnetic Resonance Imaging, 20 (2), pp. 193-200. , DOI 10.1002/jmri.20116; Hauser, T.-K., Luft, A., Skalej, M., Nagele, T., Kircher, T.T.J., Leube, D.T., Schulz, J.B., Visualization and quantification of disease progression in multiple system atrophy (2006) Movement Disorders, 21 (10), pp. 1674-1681. , DOI 10.1002/mds.21032; Hilgetag, C.C., Barbas, H., Role of mechanical factors in the morphology of the primate cerebral cortex (2006) PLoS Comput Biol, 2, pp. e22; Holmes, G., The cerebellum of man (1939) Brain, 62, pp. 1-30; Hu, H.-H., Guo, W.-Y., Chen, H.-Y., Wang, P.-S., Hung, C.-I., Hsieh, J.-C., Wu, Y.-T., Morphological regionalization using fetal magnetic resonance images of normal developing brains (2009) Eur J Neurosci, 29, pp. 1560-1567; Hu, H.-H., Chen, H.-Y., Hung, C.-I., Guo, W.-Y., Wu, Y.-T., Shape and curvedness analysis of brain morphology using human fetal magnetic resonance images in utero (2013) Brain Struct Funct, , doi:10.1007/s00429-012-0469-3; Ito, M., Watanabe, H., Kawai, Y., Atsuta, N., Tanaka, F., Naganawa, S., Fukatsu, H., Sobue, G., Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy (2007) Journal of Neurology, Neurosurgery and Psychiatry, 78 (7), pp. 722-728. , DOI 10.1136/jnnp.2006.104075; Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Gamst, A.C., Stout, J.C., Bonner, J., Hesselink, J.R., Effects of age on tissues and regions of the cerebrum and cerebellum (2001) Neurobiology of Aging, 22 (4), pp. 581-594. , DOI 10.1016/S0197-4580(01)00217-2, PII S0197458001002172; Kanazawa, M., Shimohata, T., Terajima, K., Onodera, O., Tanaka, K., Tsuji, S., Okamoto, K., Nishizawa, M., Quantitative evaluation of brainstem involvement in multiple system atrophy by diffusion-weighted MR imaging (2004) Journal of Neurology, 251 (9), pp. 1121-1124. , DOI 10.1007/s00415-004-0494-0; Kawai, Y., Suenaga, M., Takeda, A., Ito, M., Watanabe, H., Tanaka, F., Kato, K., Sobue, G., Cognitive impairments in multiple system atrophy: MSA-C vs MSA-P (2008) Neurology, 70 (16 PART 2), pp. 1390-1396. , DOI 10.1212/01.wnl.0000310413.04462.6a, PII 0000611420080415100005; 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PY - 2014

Y1 - 2014

N2 - The cerebellum involves diverse functions from motor coordination to higher cognitive functions. Impairment of the cerebellum can cause ataxia and cerebellar cognitive affective syndrome. Multiple system atrophy of the cerebellar type (MSA-C) is a neurodegenerative disorder with atrophy of medullo-ponto-cerebellar (MPC) white matter (WM). To understand the role of the cerebellum from the perspective of the local structure to the global function in the presence of MPC WM degeneration, we acquired T1-weighted and diffusion tensor images for 17 patients with MSA-C and 19 normal controls. We concurrently used the measures of local morphology, including MPC WM volume and inner surface area, and properties of global network organization based on graph theory for the MSA-C and control groups. The results showed that MPC WM degeneration caused the destruction of cerebello-ponto-cerebral loops, resulting in reduced communication efficiency between regions in the whole-brain network. In addition, the sulcal area of the inner cortical surface in the cerebellum decreased linearly with the MPC WM volume, and the inferoposterior lobe exhibited a steeper atrophy rate than that of vermis regions. We concluded that the integrity of MPC WM is critical in sustaining the local morphology and the global functions of the whole-brain fiber network. © 2013 Springer-Verlag.

AB - The cerebellum involves diverse functions from motor coordination to higher cognitive functions. Impairment of the cerebellum can cause ataxia and cerebellar cognitive affective syndrome. Multiple system atrophy of the cerebellar type (MSA-C) is a neurodegenerative disorder with atrophy of medullo-ponto-cerebellar (MPC) white matter (WM). To understand the role of the cerebellum from the perspective of the local structure to the global function in the presence of MPC WM degeneration, we acquired T1-weighted and diffusion tensor images for 17 patients with MSA-C and 19 normal controls. We concurrently used the measures of local morphology, including MPC WM volume and inner surface area, and properties of global network organization based on graph theory for the MSA-C and control groups. The results showed that MPC WM degeneration caused the destruction of cerebello-ponto-cerebral loops, resulting in reduced communication efficiency between regions in the whole-brain network. In addition, the sulcal area of the inner cortical surface in the cerebellum decreased linearly with the MPC WM volume, and the inferoposterior lobe exhibited a steeper atrophy rate than that of vermis regions. We concluded that the integrity of MPC WM is critical in sustaining the local morphology and the global functions of the whole-brain fiber network. © 2013 Springer-Verlag.

KW - Diffusion tensor imaging

KW - Graph theory

KW - Multiple system atrophy

KW - Shape index

KW - Surface morphology

KW - White matter degeneration

KW - adult

KW - article

KW - ataxia

KW - brain atrophy

KW - brain size

KW - cerebellum

KW - cerebellum atrophy

KW - cerebellum vermis

KW - clinical article

KW - controlled study

KW - female

KW - human

KW - interpersonal communication

KW - male

KW - middle aged

KW - motor coordination

KW - nerve degeneration

KW - priority journal

KW - Shy Drager syndrome

KW - white matter

KW - aged

KW - brain mapping

KW - image processing

KW - nerve cell network

KW - nuclear magnetic resonance imaging

KW - pathology

KW - procedures

KW - Adult

KW - Aged

KW - Brain Mapping

KW - Cerebellum

KW - Female

KW - Humans

KW - Image Processing, Computer-Assisted

KW - Magnetic Resonance Imaging

KW - Male

KW - Middle Aged

KW - Multiple System Atrophy

KW - Nerve Net

KW - White Matter

UR - http://www.scopus.com/inward/record.url?eid=2-s2.0-84902361634&partnerID=40&md5=6e319302d8a621cad1c6361091619629

UR - https://www.scopus.com/results/citedbyresults.uri?sort=plf-f&cite=2-s2.0-84902361634&src=s&imp=t&sid=708b0b4c92da525322f38f573e36fba3&sot=cite&sdt=a&sl=0&origin=recordpage&editSaveSearch=&txGid=a75da27cefb70b3ac6ffe65f8040a899

U2 - 10.1007/s00429-013-0545-3

DO - 10.1007/s00429-013-0545-3

M3 - Article

VL - 219

SP - 947

EP - 958

JO - Anatomy and Embryology

JF - Anatomy and Embryology

SN - 0177-5154

IS - 3

ER -