Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy

Chia-Feng Lu, Bing-Wen Soong, Hsiu-Mei Wu, Shin Teng, Po-Shan Wang, Yu-Te Wu

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Multiple system atrophy of the cerebellar type is a sporadic neurodegenerative disorder of the central nervous system. We hypothesized that the white matter degeneration of the cerebellum and pons in this disease may cause a breakdown of cerebellar structural networks and further reduce the network efficiency of cerebellar-connected cerebral regions. Diffusion tensor tractography was used to construct the structural networks of 19 cerebellar-type multiple system atrophy patients, who were compared with 19 age- and sex-matched controls. Graph theory was used to assess the small-world properties and topological organization of structure networks in both the control and patient groups. Our results showed that the cerebellar-type multiple system atrophy patients exhibited altered small-world architecture with significantly increased characteristic shortest path lengths and decreased clustering coefficients. We also found that white matter degeneration in the cerebellum was characterized by reductions in network strength (number and integrity of fiber connections) of the cerebellar regions, which further induced extensively decreased network efficiency for numerous cerebral regions. Finally, we found that the reductions in nodal efficiency of the cerebellar lobules and bilateral sensorimotor, prefrontal, and basal ganglia regions negatively correlated with the severity of ataxia for the cerebellar-type multiple system atrophy patients. This study demonstrates for the first time that the brains of cerebellar-type multiple system atrophy patients exhibit disrupted topological organization of white matter structural networks. Thus, this study provides structural evidence of the relationship between abnormalities of white matter integrity and network efficiency that occurs in cerebellar-type multiple system atrophy. © 2013 Movement Disorder Society.
Original languageEnglish
Pages (from-to)362-369
Number of pages8
JournalMovement Disorders
Volume28
Issue number3
DOIs
Publication statusPublished - 2013
Externally publishedYes

Fingerprint

Multiple System Atrophy
Brain
Cerebellum
Cerebellar Ataxia
Diffusion Tensor Imaging
Pons
Basal Ganglia
Neurodegenerative Diseases
Cluster Analysis
Central Nervous System
Control Groups
White Matter

Keywords

  • Diffusion tensor imaging
  • Graph theory
  • Multiple system atrophy
  • Network efficiency
  • Small world
  • adult
  • article
  • ataxia
  • basal ganglion
  • cerebellum
  • cerebellum degeneration
  • clinical article
  • controlled study
  • diffusion tensor imaging
  • disease severity
  • female
  • human
  • male
  • nerve cell network
  • nuclear magnetic resonance scanner
  • pons
  • prefrontal cortex
  • priority journal
  • sensorimotor cortex
  • Shy Drager syndrome
  • white matter
  • white matter lesion
  • Adult
  • Brain
  • Brain Mapping
  • Case-Control Studies
  • Cerebellum
  • Diffusion Magnetic Resonance Imaging
  • Female
  • Humans
  • Image Processing, Computer-Assisted
  • Male
  • Middle Aged
  • Multiple System Atrophy
  • Nerve Net
  • Neural Pathways
  • Severity of Illness Index

Cite this

Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy. / Lu, Chia-Feng; Soong, Bing-Wen; Wu, Hsiu-Mei; Teng, Shin; Wang, Po-Shan; Wu, Yu-Te.

In: Movement Disorders, Vol. 28, No. 3, 2013, p. 362-369.

Research output: Contribution to journalArticle

Lu, C-F, Soong, B-W, Wu, H-M, Teng, S, Wang, P-S & Wu, Y-T 2013, 'Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy', Movement Disorders, vol. 28, no. 3, pp. 362-369. https://doi.org/10.1002/mds.25314
Lu, Chia-Feng ; Soong, Bing-Wen ; Wu, Hsiu-Mei ; Teng, Shin ; Wang, Po-Shan ; Wu, Yu-Te. / Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy. In: Movement Disorders. 2013 ; Vol. 28, No. 3. pp. 362-369.
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title = "Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy",
abstract = "Multiple system atrophy of the cerebellar type is a sporadic neurodegenerative disorder of the central nervous system. We hypothesized that the white matter degeneration of the cerebellum and pons in this disease may cause a breakdown of cerebellar structural networks and further reduce the network efficiency of cerebellar-connected cerebral regions. Diffusion tensor tractography was used to construct the structural networks of 19 cerebellar-type multiple system atrophy patients, who were compared with 19 age- and sex-matched controls. Graph theory was used to assess the small-world properties and topological organization of structure networks in both the control and patient groups. Our results showed that the cerebellar-type multiple system atrophy patients exhibited altered small-world architecture with significantly increased characteristic shortest path lengths and decreased clustering coefficients. We also found that white matter degeneration in the cerebellum was characterized by reductions in network strength (number and integrity of fiber connections) of the cerebellar regions, which further induced extensively decreased network efficiency for numerous cerebral regions. Finally, we found that the reductions in nodal efficiency of the cerebellar lobules and bilateral sensorimotor, prefrontal, and basal ganglia regions negatively correlated with the severity of ataxia for the cerebellar-type multiple system atrophy patients. This study demonstrates for the first time that the brains of cerebellar-type multiple system atrophy patients exhibit disrupted topological organization of white matter structural networks. Thus, this study provides structural evidence of the relationship between abnormalities of white matter integrity and network efficiency that occurs in cerebellar-type multiple system atrophy. {\circledC} 2013 Movement Disorder Society.",
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author = "Chia-Feng Lu and Bing-Wen Soong and Hsiu-Mei Wu and Shin Teng and Po-Shan Wang and Yu-Te Wu",
note = "被引用次數:7 Export Date: 31 March 2016 CODEN: MOVDE 通訊地址: Wang, P.-S.; Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, No. 155, Li-Nong Street, Section 2, Pei-Tou, Taipei, 112, Taiwan; 電子郵件: ytwu@ym.edu.tw 商標: SIGNA EXCITE, Medical System, United States 製造商: Medical System, United States 參考文獻: Gilman, S., Wenning, G.K., Low, P.A., Second consensus statement on the diagnosis of multiple system atrophy (2008) Neurology., 71, pp. 670-676; Quinn, N., Multiple system atrophy-the nature of the beast (1989) J Neurol Neurosurg Psychiatry., 52 (SUPPL.), pp. 78-89; Wenning, G.K., Colosimo, C., Geser, F., Poewe, W., Multiple system atrophy (2004) Lancet Neurol., 3, pp. 93-103; Miyatake, S., Mochizuki, H., Naka, T., Brain volume analyses and somatosensory evoked potentials in multiple system atrophy (2010) JNeurol., 257, pp. 419-425; Stefanova, N., B{\"u}cke, P., Duerr, S., Wenning, G.K., Multiple system atrophy: an update (2009) Lancet Neurol., 8, pp. 1172-1178; Ito, M., Watanabe, H., Kawai, Y., Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy (2007) J Neurol Neurosurg Psychiatry., 78, pp. 722-728; Kanazawa, M., Shimohata, T., Terajima, K., Quantitative evaluation of brainstem involvement in multiple system atrophy by diffusion-weighted MR imaging (2004) J Neurol., 251, pp. 1121-1124; Shiga, K., Yamada, K., Yoshikawa, K., Mizuno, T., Nishimura, T., Nakagawa, M., Local tissue anisotropy decreases in cerebellopetal fibers and pyramidal tract in multiple system atrophy (2005) J Neurol., 252, pp. 589-596; Ramnani, N., The primate cortico-cerebellar system: anatomy and function (2006) Nat Rev Neurosci., 7, pp. 511-522; Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems (2009) Nat Rev Neurosci., 10, pp. 186-198; Lee, Y.-C., Liao, Y.-C., Wang, P.-S., Lee, I.H., Lin, K.-P., Soong, B.-W., Comparison of cerebellar ataxias: A three-year prospective longitudinal assessment (2011) Mov Disord., 26, pp. 2081-2087; Schmitz-H{\"u}bsch, T., du Montcel, S.T., Baliko, L., Scale for the assessment and rating of ataxia (2006) Neurology., 66, pp. 1717-1720; Woods, R.P., Grafton, S.T., Holmes, C.J., Cherry, S.R., Mazziotta, J.C., Automated image registration: i. general methods and intrasubject, intramodality validation (1998) J Comput Assist Tomogr., 22, pp. 139-152; 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 Vis., 61, pp. 139-157; Basser, P.J., Mattiello, J., LeBihan, D., Estimation of the effective self-diffusion tensor from the NMR spin echo (1994) J Magn Reson B., 103, pp. 247-254; Mori, S., Crain, B.J., Chacko, V.P., Van Zijl, P.C.M., Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging (1999) Ann Neurol., 45, pp. 265-269; Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain (2002) Neuroimage., 15, pp. 273-289; Rubinov, M., Sporns, O., Complex network measures of brain connectivity: Uses and interpretations (2010) Neuroimage., 52, pp. 1059-1069; Watts, D.J., Strogatz, S.H., Collective dynamics of 'small-world' networks (1998) Nature., 393, pp. 440-442; Humphries, M.D., Gurney, K., Network 'Small-world-ness': a quantitative method for determining canonical network equivalence (2008) PLoS One., 3, pp. e0002051; Latora, V., Marchiori, M., Efficient behavior of small-world networks (2001) Phys Rev Lett., 87, p. 198701; Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks (2007) PLoS Comput Biol., 3 (2), pp. e17; Liu, Y., Liang, M., Zhou, Y., Disrupted small-world networks in schizophrenia (2008) Brain., 131, pp. 945-961; Shapiro, S.S., Wilk, M.B., An analysis of variance test for normality (complete samples) (1965) Biometrika., 52, pp. 591-611; Mann, H.B., Whitney, D.R., On a test of whether one of two random variables is stochastically larger than the other (1947) Ann Math Stat., 18, pp. 50-60; Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing (1995) J R Stat Soc Series B Stat Methodol., 57, pp. 289-300; 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, pp. 221-227; Papp, M.I., Kahn, J.E., Lantos, P.L., Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome) (1989) JNeurol Sci., 94, pp. 79-100; Tu, P.-H., Galvin, J.E., Baba, M., Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble α-synuclein (1998) Ann Neurol., 44, pp. 415-422; Inoue, M., Yagishita, S., Ryo, M., Hasegawa, K., Amano, N., Matsushita, M., The distribution and dynamic density of oligodendroglial cytoplasmic inclusions (GCIs) in multiple system atrophy: a correlation between the density of GCIs and the degree of involvement of striatonigral and olivopontocerebellar systems (1997) Acta Neuropathol., 93, pp. 585-591; Ozawa, T., Paviour, D., Quinn, N.P., The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations (2004) Brain., 127, pp. 2657-2671; Matsuo, A., Akiguchi, I., Lee, G.C., McGeer, E.G., McGeer, P.L., Kimura, J., Myelin degeneration in multiple system atrophy detected by unique antibodies (1998) Am J Pathol., 153, pp. 735-744; Probst-Cousin, S., Rickert, C.H., Schmid, K.W., Gullotta, F., Cell death mechanisms in multiple system atrophy (1998) J Neuropathol Exp Neurol., 57, pp. 814-821; Wakabayashi, K., Mori, F., Nishie, M., An autopsy case of early ({"}minimal change{"}) olivopontocerebellar atrophy (multiple system atrophy-cerebellar) (2005) Acta Neuropathol., 110, pp. 185-190; Brooks, D.J., Seppi, K., Proposed neuroimaging criteria for the diagnosis of multiple system atrophy (2009) Mov Disord., 24, pp. 949-964; Gong, G., He, Y., Concha, L., Mapping anatomical connectivity patterns of human cerebral cortex. Using in vivo diffusion tensor imaging tractography (2009) Cereb Cortex., 19, pp. 524-536; Li, Y., Liu, Y., Li, J., Brain anatomical network and intelligence (2009) PLoS Comput Biol., 5, pp. e1000395; Wakabayashi, K., Takahashi, H., Cellular pathology in multiple system atrophy (2006) Neuropathology., 26, pp. 338-345; Habas, C., Kamdar, N., Nguyen, D., Distinct cerebellar contributions to intrinsic connectivity networks (2009) J Neurosci., 29, pp. 8586-8594; O'Reilly, J.X., Beckmann, C.F., Tomassini, V., Ramnani, N., Johansen-Berg, H., Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity (2010) Cereb Cortex., 20, pp. 953-965; Ramnani, N., Behrens, T.E.J., Johansen-Berg, H., The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans (2006) Cereb Cortex., 16, pp. 811-818; Kawai, Y., Suenaga, M., Takeda, A., Cognitive impairments in multiple system atrophy (2008) Neurology., 70, pp. 1390-1396; Taniwaki, T., Nakagawa, M., Yamada, T., Cerebral metabolic changes in early multiple system atrophy: a PET study (2002) J Neurol Sci., 200, pp. 79-84; Trouillas, P., Takayanagi, T., Hallett, M., International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome (1997) J Neurol Sci., 145, pp. 205-211; Yan, C., Gong, G., Wang, J., Sex- and brain size-related small-world structural cortical networks in young adults: a DTI tractography study (2011) Cereb Cortex., 21, pp. 449-458; Wedeen, V.J., Wang, R.P., Schmahmann, J.D., Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers (2008) Neuroimage., 41, pp. 1267-1277",
year = "2013",
doi = "10.1002/mds.25314",
language = "English",
volume = "28",
pages = "362--369",
journal = "Movement Disorders",
issn = "0885-3185",
publisher = "John Wiley and Sons Inc.",
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}

TY - JOUR

T1 - Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy

AU - Lu, Chia-Feng

AU - Soong, Bing-Wen

AU - Wu, Hsiu-Mei

AU - Teng, Shin

AU - Wang, Po-Shan

AU - Wu, Yu-Te

N1 - 被引用次數:7 Export Date: 31 March 2016 CODEN: MOVDE 通訊地址: Wang, P.-S.; Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, No. 155, Li-Nong Street, Section 2, Pei-Tou, Taipei, 112, Taiwan; 電子郵件: ytwu@ym.edu.tw 商標: SIGNA EXCITE, Medical System, United States 製造商: Medical System, United States 參考文獻: Gilman, S., Wenning, G.K., Low, P.A., Second consensus statement on the diagnosis of multiple system atrophy (2008) Neurology., 71, pp. 670-676; Quinn, N., Multiple system atrophy-the nature of the beast (1989) J Neurol Neurosurg Psychiatry., 52 (SUPPL.), pp. 78-89; Wenning, G.K., Colosimo, C., Geser, F., Poewe, W., Multiple system atrophy (2004) Lancet Neurol., 3, pp. 93-103; Miyatake, S., Mochizuki, H., Naka, T., Brain volume analyses and somatosensory evoked potentials in multiple system atrophy (2010) JNeurol., 257, pp. 419-425; Stefanova, N., Bücke, P., Duerr, S., Wenning, G.K., Multiple system atrophy: an update (2009) Lancet Neurol., 8, pp. 1172-1178; Ito, M., Watanabe, H., Kawai, Y., Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy (2007) J Neurol Neurosurg Psychiatry., 78, pp. 722-728; Kanazawa, M., Shimohata, T., Terajima, K., Quantitative evaluation of brainstem involvement in multiple system atrophy by diffusion-weighted MR imaging (2004) J Neurol., 251, pp. 1121-1124; Shiga, K., Yamada, K., Yoshikawa, K., Mizuno, T., Nishimura, T., Nakagawa, M., Local tissue anisotropy decreases in cerebellopetal fibers and pyramidal tract in multiple system atrophy (2005) J Neurol., 252, pp. 589-596; Ramnani, N., The primate cortico-cerebellar system: anatomy and function (2006) Nat Rev Neurosci., 7, pp. 511-522; Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems (2009) Nat Rev Neurosci., 10, pp. 186-198; Lee, Y.-C., Liao, Y.-C., Wang, P.-S., Lee, I.H., Lin, K.-P., Soong, B.-W., Comparison of cerebellar ataxias: A three-year prospective longitudinal assessment (2011) Mov Disord., 26, pp. 2081-2087; Schmitz-Hübsch, T., du Montcel, S.T., Baliko, L., Scale for the assessment and rating of ataxia (2006) Neurology., 66, pp. 1717-1720; Woods, R.P., Grafton, S.T., Holmes, C.J., Cherry, S.R., Mazziotta, J.C., Automated image registration: i. general methods and intrasubject, intramodality validation (1998) J Comput Assist Tomogr., 22, pp. 139-152; Beg, M.F., Miller, M.I., Trouvé, A., Younes, L., Computing large deformation metric mappings via geodesic flows of diffeomorphisms (2005) Int J Comput Vis., 61, pp. 139-157; Basser, P.J., Mattiello, J., LeBihan, D., Estimation of the effective self-diffusion tensor from the NMR spin echo (1994) J Magn Reson B., 103, pp. 247-254; Mori, S., Crain, B.J., Chacko, V.P., Van Zijl, P.C.M., Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging (1999) Ann Neurol., 45, pp. 265-269; Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain (2002) Neuroimage., 15, pp. 273-289; Rubinov, M., Sporns, O., Complex network measures of brain connectivity: Uses and interpretations (2010) Neuroimage., 52, pp. 1059-1069; Watts, D.J., Strogatz, S.H., Collective dynamics of 'small-world' networks (1998) Nature., 393, pp. 440-442; Humphries, M.D., Gurney, K., Network 'Small-world-ness': a quantitative method for determining canonical network equivalence (2008) PLoS One., 3, pp. e0002051; Latora, V., Marchiori, M., Efficient behavior of small-world networks (2001) Phys Rev Lett., 87, p. 198701; Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks (2007) PLoS Comput Biol., 3 (2), pp. e17; Liu, Y., Liang, M., Zhou, Y., Disrupted small-world networks in schizophrenia (2008) Brain., 131, pp. 945-961; Shapiro, S.S., Wilk, M.B., An analysis of variance test for normality (complete samples) (1965) Biometrika., 52, pp. 591-611; Mann, H.B., Whitney, D.R., On a test of whether one of two random variables is stochastically larger than the other (1947) Ann Math Stat., 18, pp. 50-60; Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing (1995) J R Stat Soc Series B Stat Methodol., 57, pp. 289-300; 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, pp. 221-227; Papp, M.I., Kahn, J.E., Lantos, P.L., Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome) (1989) JNeurol Sci., 94, pp. 79-100; Tu, P.-H., Galvin, J.E., Baba, M., Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble α-synuclein (1998) Ann Neurol., 44, pp. 415-422; Inoue, M., Yagishita, S., Ryo, M., Hasegawa, K., Amano, N., Matsushita, M., The distribution and dynamic density of oligodendroglial cytoplasmic inclusions (GCIs) in multiple system atrophy: a correlation between the density of GCIs and the degree of involvement of striatonigral and olivopontocerebellar systems (1997) Acta Neuropathol., 93, pp. 585-591; Ozawa, T., Paviour, D., Quinn, N.P., The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations (2004) Brain., 127, pp. 2657-2671; Matsuo, A., Akiguchi, I., Lee, G.C., McGeer, E.G., McGeer, P.L., Kimura, J., Myelin degeneration in multiple system atrophy detected by unique antibodies (1998) Am J Pathol., 153, pp. 735-744; Probst-Cousin, S., Rickert, C.H., Schmid, K.W., Gullotta, F., Cell death mechanisms in multiple system atrophy (1998) J Neuropathol Exp Neurol., 57, pp. 814-821; Wakabayashi, K., Mori, F., Nishie, M., An autopsy case of early ("minimal change") olivopontocerebellar atrophy (multiple system atrophy-cerebellar) (2005) Acta Neuropathol., 110, pp. 185-190; Brooks, D.J., Seppi, K., Proposed neuroimaging criteria for the diagnosis of multiple system atrophy (2009) Mov Disord., 24, pp. 949-964; Gong, G., He, Y., Concha, L., Mapping anatomical connectivity patterns of human cerebral cortex. Using in vivo diffusion tensor imaging tractography (2009) Cereb Cortex., 19, pp. 524-536; Li, Y., Liu, Y., Li, J., Brain anatomical network and intelligence (2009) PLoS Comput Biol., 5, pp. e1000395; Wakabayashi, K., Takahashi, H., Cellular pathology in multiple system atrophy (2006) Neuropathology., 26, pp. 338-345; Habas, C., Kamdar, N., Nguyen, D., Distinct cerebellar contributions to intrinsic connectivity networks (2009) J Neurosci., 29, pp. 8586-8594; O'Reilly, J.X., Beckmann, C.F., Tomassini, V., Ramnani, N., Johansen-Berg, H., Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity (2010) Cereb Cortex., 20, pp. 953-965; Ramnani, N., Behrens, T.E.J., Johansen-Berg, H., The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans (2006) Cereb Cortex., 16, pp. 811-818; Kawai, Y., Suenaga, M., Takeda, A., Cognitive impairments in multiple system atrophy (2008) Neurology., 70, pp. 1390-1396; Taniwaki, T., Nakagawa, M., Yamada, T., Cerebral metabolic changes in early multiple system atrophy: a PET study (2002) J Neurol Sci., 200, pp. 79-84; Trouillas, P., Takayanagi, T., Hallett, M., International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome (1997) J Neurol Sci., 145, pp. 205-211; Yan, C., Gong, G., Wang, J., Sex- and brain size-related small-world structural cortical networks in young adults: a DTI tractography study (2011) Cereb Cortex., 21, pp. 449-458; Wedeen, V.J., Wang, R.P., Schmahmann, J.D., Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers (2008) Neuroimage., 41, pp. 1267-1277

PY - 2013

Y1 - 2013

N2 - Multiple system atrophy of the cerebellar type is a sporadic neurodegenerative disorder of the central nervous system. We hypothesized that the white matter degeneration of the cerebellum and pons in this disease may cause a breakdown of cerebellar structural networks and further reduce the network efficiency of cerebellar-connected cerebral regions. Diffusion tensor tractography was used to construct the structural networks of 19 cerebellar-type multiple system atrophy patients, who were compared with 19 age- and sex-matched controls. Graph theory was used to assess the small-world properties and topological organization of structure networks in both the control and patient groups. Our results showed that the cerebellar-type multiple system atrophy patients exhibited altered small-world architecture with significantly increased characteristic shortest path lengths and decreased clustering coefficients. We also found that white matter degeneration in the cerebellum was characterized by reductions in network strength (number and integrity of fiber connections) of the cerebellar regions, which further induced extensively decreased network efficiency for numerous cerebral regions. Finally, we found that the reductions in nodal efficiency of the cerebellar lobules and bilateral sensorimotor, prefrontal, and basal ganglia regions negatively correlated with the severity of ataxia for the cerebellar-type multiple system atrophy patients. This study demonstrates for the first time that the brains of cerebellar-type multiple system atrophy patients exhibit disrupted topological organization of white matter structural networks. Thus, this study provides structural evidence of the relationship between abnormalities of white matter integrity and network efficiency that occurs in cerebellar-type multiple system atrophy. © 2013 Movement Disorder Society.

AB - Multiple system atrophy of the cerebellar type is a sporadic neurodegenerative disorder of the central nervous system. We hypothesized that the white matter degeneration of the cerebellum and pons in this disease may cause a breakdown of cerebellar structural networks and further reduce the network efficiency of cerebellar-connected cerebral regions. Diffusion tensor tractography was used to construct the structural networks of 19 cerebellar-type multiple system atrophy patients, who were compared with 19 age- and sex-matched controls. Graph theory was used to assess the small-world properties and topological organization of structure networks in both the control and patient groups. Our results showed that the cerebellar-type multiple system atrophy patients exhibited altered small-world architecture with significantly increased characteristic shortest path lengths and decreased clustering coefficients. We also found that white matter degeneration in the cerebellum was characterized by reductions in network strength (number and integrity of fiber connections) of the cerebellar regions, which further induced extensively decreased network efficiency for numerous cerebral regions. Finally, we found that the reductions in nodal efficiency of the cerebellar lobules and bilateral sensorimotor, prefrontal, and basal ganglia regions negatively correlated with the severity of ataxia for the cerebellar-type multiple system atrophy patients. This study demonstrates for the first time that the brains of cerebellar-type multiple system atrophy patients exhibit disrupted topological organization of white matter structural networks. Thus, this study provides structural evidence of the relationship between abnormalities of white matter integrity and network efficiency that occurs in cerebellar-type multiple system atrophy. © 2013 Movement Disorder Society.

KW - Diffusion tensor imaging

KW - Graph theory

KW - Multiple system atrophy

KW - Network efficiency

KW - Small world

KW - adult

KW - article

KW - ataxia

KW - basal ganglion

KW - cerebellum

KW - cerebellum degeneration

KW - clinical article

KW - controlled study

KW - diffusion tensor imaging

KW - disease severity

KW - female

KW - human

KW - male

KW - nerve cell network

KW - nuclear magnetic resonance scanner

KW - pons

KW - prefrontal cortex

KW - priority journal

KW - sensorimotor cortex

KW - Shy Drager syndrome

KW - white matter

KW - white matter lesion

KW - Adult

KW - Brain

KW - Brain Mapping

KW - Case-Control Studies

KW - Cerebellum

KW - Diffusion Magnetic Resonance Imaging

KW - Female

KW - Humans

KW - Image Processing, Computer-Assisted

KW - Male

KW - Middle Aged

KW - Multiple System Atrophy

KW - Nerve Net

KW - Neural Pathways

KW - Severity of Illness Index

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