Skip to main content

Advertisement

SpringerLink
Log in

Impaired topological architecture of brain structural networks in idiopathic Parkinson’s disease: a DTI study

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Parkinson’s disease (PD) is considered as a neurodegenerative disorder of the brain central nervous system. But, to date, few studies adopted the network model to reveal topological changes in brain structural networks in PD patients. Additionally, although the concept of rich club organization has been widely used to study brain networks in various brain disorders, there is no study to report the changed rich club organization of brain networks in PD patients. Thus, we collected diffusion tensor imaging (DTI) data from 35 PD patients and 26 healthy controls and adopted deterministic tractography to construct brain structural networks. During the network analysis, we calculated their topological properties, and built the rich club organization of brain structural networks for both subject groups. By comparing the between-group differences in topological properties and rich club organizations, we found that the connectivity strength of the feeder and local connections are lower in PD patients compared to those of the healthy controls. Furthermore, using a network-based statistic (NBS) approach, we identified uniformly significantly decreased connections in two modules, the limbic/paralimbic/subcortical module and the cognitive control/attention module, in patients compared to controls. In addition, for the topological properties of brain network topology in the PD patients, we found statistically increased shortest path length and decreased global efficiency. Statistical comparisons of nodal properties were also widespread in the frontal and parietal regions for the PD patients. These findings may provide useful information to better understand the abnormalities of brain structural networks in PD patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agosta, F., Canu, E., Stefanova, E., Sarro, L., Tomic, A., Spica, V., Comi, G., Kostic, V. S., & Filippi, M. (2014). Mild cognitive impairment in Parkinson’s disease is associated with a distributed pattern of brain white matter damage. Human Brain Mapping, 35(5), 1921–1929.

    Article  PubMed  Google Scholar 

  • Alexander, A. L., Hasan, K. M., Lazar, M., Tsuruda, J. S., & Parker, D. L. (2001). Analysis of partial volume effects in diffusion-tensor MRI. Magnetic Resonance Imaging, 45(5), 770–780.

    CAS  Google Scholar 

  • Auning, E., Kjærvik, V. K., Selnes, P., Aarsland, D., Haram, A., Bjørnerud, A., Hessen, E., Esnaashari, A., & Fladby, T. (2014). White matter integrity and cognition in Parkinson’s disease: a cross-sectional study. BMJ open, 4(1), e003976.

  • Ball, G., Aljabar, P., Zebari, S., Tusor, N., Arichi, T., Merchant, N., Robinson, E. C., Ogundipe, E., Rueckert, D., Edwards, A. D., & Counsell, S. J. (2014). Rich-club organization of the newborn human brain. PNAS, 111(20), 7456–7461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrens, T., Woolrich, M., Jenkinson, M., Johansen-Berg, H., Nunes, R., Clare, S., Matthews, P., Brady, J., & Smith, S. (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine, 50(5), 1077–1088.

    Article  CAS  PubMed  Google Scholar 

  • Behrens, T., Berg, H. J., Jbabdi, S., Rushworth, M., & Woolrich, M. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage, 34(1), 144–155.

    Article  CAS  PubMed  Google Scholar 

  • Buckner, R. L., Sepulcre, J., Talukdar, T., Krienen, F. M., Liu, H., Hedden, T., Andrews-Hanna, J. R., Sperling, R. A., & Johnson, K. A. (2009). Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. Journal of Neuroscience, 29(6), 1860–1873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, Q., Shu, N., An, L., Wang, P., Sun, L., Xia, M. R., Wang, J. H., Gong, G. L., Zang, Y. F., Wang, Y. F., & He, Y. (2013). Probabilistic diffusion tractography and graph theory analysis reveal abnormal white matter structural connectivity networks in drug-naive boys with attention deficit/hyperactivity disorder. Journal of Neuroscience, 33(26), 10676–10687.

    Article  CAS  PubMed  Google Scholar 

  • Carlesimo, G. A., Piras, F., Assogna, F., Pontieri, F. E., Caltagirone, C., & Spalletta, G. (2012). Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology, 78(24), 1939–1945.

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri, K., Healy, D. G., & Schapira, A. H. (2006). Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurology, 5(3), 235–245.

    Article  PubMed  Google Scholar 

  • Cheng, H., Wang, Y., Sheng, J., Kronenberger, W. G., Mathews, V. P., Hummer, T. A., & Saykin, A. J. (2012). Characteristics and variability of structural networks derived from diffusion tensor imaging. NeuroImage, 61(4), 1153–1164.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cole, M. W., Repovs, G., & Anticevic, A. (2014). The frontoparietal control system: a central role in mental health. The Neuroscientist, 20(6), 652–664.

    Article  PubMed  PubMed Central  Google Scholar 

  • Collin, G., Kahn, R. S., de Reus, M. A., Cahn, W., & van den Heuvel, M. P. (2014a). Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophrenia Bulletin, 40(2), 438–448.

    Article  PubMed  Google Scholar 

  • Collin, G., Sporns, O., Mandl, R. C., & van den Heuvel, M. P. (2014b). Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cerebral Cortex, 24(9), 2258–2267.

    Article  PubMed  Google Scholar 

  • Cools, R., Rogers, R., Barker, R. A., & Robbins, T. W. (2010). Top-down attentional control in Parkinson’s disease: salient considerations. Journal Cognitive Neuroscience, 22(5), 848–859.

    Article  Google Scholar 

  • Crossley, N. A., Mechelli, A., Scott, J., Carletti, F., Fox, P. T., McGuire, P., & Bullmore, E. T. (2014). The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain, 137(Pt 8), 2382–2395.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daianu, M., Jahanshad, N., Nir, T. M., Jack, C. R., Jr., Weiner, M. W., Bernstein, M. A., Thompson, P. M., & I Alzheimer’s Disease Neuroimaging. (2015). Rich club analysis in the Alzheimer’s disease connectome reveals a relatively undisturbed structural core network. Human Brain Mapping, 36(8), 3087–3103.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daniel, S. E., & Lees, A. J. (1993). Parkinson’s disease society brain bank, London: overview and research. Journal of Neural Transmission Supplementum, 39, 165–172.

    CAS  PubMed  Google Scholar 

  • Dauer, W., & Przedborski, S. (2003). Parkinson’s disease: mechanisms and models. Neuron, 39(6), 889–909.

    Article  CAS  PubMed  Google Scholar 

  • Diederich, N. J., Fenelon, G., Stebbins, G., & Goetz, C. G. (2009). Hallucinations in Parkinson disease. Nature Reviews Neurology, 5(6), 331–342.

    Article  CAS  PubMed  Google Scholar 

  • Drui, G., Carnicella, S., Carcenac, C., Favier, M., Bertrand, A., Boulet, S., & Savasta, M. (2014). Loss of dopaminergic nigrostriatal neurons accounts for the motivational and affective deficits in Parkinson’s disease. Molecular Psychiatry, 19(3), 358–367.

    Article  CAS  PubMed  Google Scholar 

  • Gattellaro, G., Minati, L., Grisoli, M., Mariani, C., Carella, F., Osio, M., Ciceri, E., Albanese, A., & Bruzzone, M. G. (2009). White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. American Journal of Neuroradiology, 30(6), 1222–1226.

  • Gong, G., He, Y., Concha, L., Lebel, C., Gross, D. W., Evans, A. C., & Beaulieu, C. (2009). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex, 19, 524–536.

    Article  PubMed  Google Scholar 

  • Gottlich, M., Munte, T. F., Heldmann, M., Kasten, M., Hagenah, J., & Kramer, U. M. (2013). Altered resting state brain networks in Parkinson’s disease. PloS One, 8(10), e77336.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagmann, P., Kurant, M., Gigandet, X., Thiran, P., Wedeen, V. J., Meuli, R., & Thiran, J. P. (2007). Mapping human whole-brain structural networks with diffusion MRI. PloS One, 2(7), e597.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrington, D. L., Rubinov, M., Durgerian, S., Mourany, L., Reece, C., Koenig, K., Bullmore, E., Long, J. D., Paulsen, J. S., P-HiotHS Group, & Rao, S. M. (2015). Network topology and functional connectivity disturbances precede the onset of Huntington’s disease. Brain, 138(Pt 8), 2332–2346.

    Article  PubMed  PubMed Central  Google Scholar 

  • He, Y., Wang, J. H., Wang, L., Chen, Z. J., Yan, C., Yang, H., Tang, H., Zhu, C., Gong, Q., Zang, Y., & Evans, A. C. (2009). Uncovering intrinsic modular organization of spontaneous brain activity in humans. PloS One, 4(4), e5226.

    Article  PubMed  PubMed Central  Google Scholar 

  • Helmich, R. C., Derikx, L. C., Bakker, M., Scheeringa, R., Bloem, B. R., & Toni, I. (2010). Spatial remapping of cortico-striatal connectivity in Parkinson’s disease. Cerebral Cortex, 20(5), 1175–1186.

    Article  PubMed  Google Scholar 

  • Huang, C., Tang, C., Feigin, A., Lesser, M., Ma, Y., Pourfar, M., Dhawan, V., & Eidelberg, D. (2007). Changes in network activity with the progression of Parkinson’s disease. Brain, 130(Pt 7), 1834–1846.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jahanshahi, M., Jones, C. R., Zijlmans, J., Katzenschlager, R., Lee, L., Quinn, N., Frith, C. D., & Lees, A. J. (2010). Dopaminergic modulation of striato-frontal connectivity during motor timing in Parkinson’s disease. Brain, 133(Pt 3), 727–745.

    Article  PubMed  Google Scholar 

  • Jankovic, J. (2008). Parkinson’s disease: clinical features and diagnosis. Journal of Neurology, Neurosurgery, and Psychiatry, 79(4), 368–376.

    Article  CAS  PubMed  Google Scholar 

  • Kamagata, K., Motoi, Y., Abe, O., Shimoji, K., Hori, M., Nakanishi, A., Sano, T., Kuwatsuru, R., Aoki, S., & Hattori, N. (2012). White matter alteration of the cingulum in Parkinson disease with and without dementia: evaluation by diffusion tensor tract–specific analysis. American Journal of Neuroradiology, 33(5), 890–895.

    Article  CAS  PubMed  Google Scholar 

  • Karagulle, K. A. T., Lehericy, S., Luciana, M., Ugurbil, K., & Tuite, P. (2008). Altered diffusion in the frontal lobe in Parkinson disease. American Journal of Neuroradiology, 29(3), 501–505.

    Article  Google Scholar 

  • Kendi, A. K., Lehericy, S., Luciana, M., Ugurbil, K., & Tuite, P. (2008). Altered diffusion in the frontal lobe in Parkinson disease. American Journal of Neuroradiology, 29(3), 501–505.

  • Kim, J. H., Auerbach, J. M., Rodriguez-Gomez, J. A., Velasco, I., Gavin, D., Lumelsky, N., Lee, S. H., Nguyen, J., Sanchez-Pernaute, R., Bankiewicz, K., & McKay, R. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease. Nature, 418(6893), 50–56.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H. J., Kim, S. J., Kim, H. S., Choi, C. G., Kim, N., Han, S., Jang, E. H., Chung, S. J., & Lee, C. S. (2013). Alterations of mean diffusivity in brain white matter and deep gray matter in Parkinson’s disease. Neuroscience letters, 550, 64–68.

  • Kocher, M., Gleichgerrcht, E., Nesland, T., Rorden, E., Fridriksson, J., Spampinato, M. V. & Bonilha, L. (2015). Individual variability in the anatomical distribution of nodes participating in rich club structural networks. Frontiers in Neural Circuits, 916.

  • Latora, V., & Marchiori, M. (2001). Efficient behavior of small-world networks. Physical review letters, 87(19), 198701.

  • Le Bihan, D., & Johansen-Berg, H. (2012). Diffusion MRI at 25: exploring brain tissue structure and function. NeuroImage, 61(2), 324–341.

    Article  PubMed  Google Scholar 

  • Lees, A. J., Hardy, J., & Revesz, T. (2009). Parkinson’s disease. Lancet, 373(9680), 2055–2066.

    Article  CAS  PubMed  Google Scholar 

  • Lewis, S. J., Dove, A., Robbins, T. W., Barker, R. A., & Owen, A. M. (2003). Cognitive impairments in early Parkinson’s disease are accompanied by reductions in activity in frontostriatal neural circuitry. Journal of Neuroscience, 23(15), 6351–6356.

    CAS  PubMed  Google Scholar 

  • Lo, C. Y., Wang, P. N., Chou, K. H., Wang, J., He, Y., & Lin, C. P. (2010). Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer’s disease. Journal of Neuroscience, 30(50), 16876–16885.

    Article  CAS  PubMed  Google Scholar 

  • Melzer, T. R., Watts, R., MacAskill, M. R., Pitcher, T. L., Livingston, L., Keenan, R. J., Dalrymple-Alford, J. C., & Anderson, T. J. (2012). Grey matter atrophy in cognitively impaired Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 83(2), 188–194.

    Article  PubMed  Google Scholar 

  • Melzer, T. R., Watts, R., MacAskill, M. R., Pitcher, T. L., Livingston, L., Keenan, R. J., Dalrymple-Alford, J. C., & Anderson, T. J. (2013). White matter microstructure deteriorates across cognitive stages in Parkinson disease. Neurology, 80(20), 1841–1849.

  • Meppelink, A. M., de Jong, B. M., Renken, R., Leenders, K. L., Cornelissen, F. W., & van Laar, T. (2009). Impaired visual processing preceding image recognition in Parkinson’s disease patients with visual hallucinations. Brain, 132(11), 2980–2993.

    Article  PubMed  Google Scholar 

  • Mori, S., & van Zijl, P. C. (2002). Fiber tracking: principles and strategies - a technical review. NMR in Biomedicine, 15(7–8), 468–480.

    Article  PubMed  Google Scholar 

  • Nagano-Saito, A., Washimi, Y., Arahata, Y., Kachi, T., Lerch, J. P., Evans, A. C., Dagher, A., & Ito, K. (2005). Cerebral atrophy and its relation to cognitive impairment in Parkinson disease. Neurology, 64(2), 224–229.

    Article  CAS  PubMed  Google Scholar 

  • Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping, 15(1), 1–25.

    Article  PubMed  Google Scholar 

  • Olde, D. K. T., Hillebrand, A., Stoffers, D., Deijen, J. B., Twisk, J. W., Stam, C. J., & Berendse, H. W. (2014). Disrupted brain network topology in Parkinson’s disease: a longitudinal magnetoencephalography study. Brain, 137(Pt 1), 197–207.

    Article  Google Scholar 

  • Onnela, J. P., Saramäki, J., Kertész, J., & Kaski, K. (2005). Intensity and coherence of motifs in weighted complex networks. Physical Review E, 71(6), 065103.

  • Owen, A. M. (2004). Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry. The Neuroscientist, 10(6), 525–537.

    Article  PubMed  Google Scholar 

  • Parikh, P. T., Sandhu, G. S., Blackham, K. A., Coffey, M. D., Hsu, D., Liu, K., Jesberger, J., Griswold, M., & Sunshine, J. L. (2011). Evaluation of image quality of a 32-channel versus a 12-channel head coil at 1.5 T for MR imaging of the brain. American Journal of Neuroradiology, 32(2), 365–373.

    Article  CAS  PubMed  Google Scholar 

  • Peterson, D. S., Pickett, K. A., Duncan, R., Perlmutter, J., & Earhart, G. M. (2014). Gait-related brain activity in people with Parkinson disease with freezing of gait. PloS One, 9(3), e90634.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rolheiser, T. M., Fulton, H. G., Good, K. P., Fisk, J. D., McKelvey, J. R., Scherfler, C., Khan, N. M., Leslie, R. A., & Robertson, H. A. (2011). Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson’s disease. Journal of Neurology, 258(7), 1254–1260.

    Article  PubMed  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. NeuroImage, 52(3), 1059–1069.

    Article  PubMed  Google Scholar 

  • Salomon, R., Darulova, J., Narsude, M., & van der Zwaag, W. (2014). Comparison of an 8-channel and a 32-channel coil for high-resolution fMRI at 7 T. Brain Topography, 27(2), 209–212.

    Article  PubMed  Google Scholar 

  • Scolari, M., Seidl-Rathkopf, K. N, & Kastner, S. (2015). Functions of the human frontoparietal attention network: evidence from neuroimaging. Current Opinion in Behavioral Sciences, 132–39.

  • Shin, D. H., Han, B. S., Kim, H. S., & Lee, P. H. (2008). Diffusion tensor imaging in patients with essential tremor. American Journal of Neuroradiology, 29(1), 151–153.

  • Shine, J. M., Matar, E., Ward, P. B., Frank, M. J., Moustafa, A. A., Pearson, M., Naismith, S. L., & Lewis, S. J. (2013a). Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain, 136(Pt 12), 3671–3681.

    Article  PubMed  Google Scholar 

  • Shine, J. M., Moustafa, A. A., Matar, E., Frank, M. J., & Lewis, S. J. (2013). The role of frontostriatal impairment in freezing of gait in Parkinson’s disease. Frontiers in Systems Neuroscience, 761.

  • Shu, N., Liu, Y., Li, K., Duan, Y., Wang, J., Yu, C., Dong, H., Ye, J., & He, Y. (2011). Diffusion tensor tractography reveals disrupted topological efficiency in white matter structural networks in multiple sclerosis. Cerebral Cortex, 21(11), 2565–2577.

    Article  PubMed  Google Scholar 

  • Skidmore, F., Korenkevych, D., Liu, Y., He, G., Bullmore, E., & Pardalos, P. M. (2011). Connectivity brain networks based on wavelet correlation analysis in Parkinson fMRI data. Neuroscience Letters, 499(1), 47–51.

    Article  CAS  PubMed  Google Scholar 

  • Surdhar, I., Gee, M., Bouchard, T., Coupland, N., Malykhin, N., & Camicioli, R. (2012). Intact limbic-prefrontal connections and reduced amygdala volumes in Parkinson’s disease with mild depressive symptoms. Parkinsonism & Related Disorders, 18(7), 809–813.

    Article  Google Scholar 

  • Tessitore, A., Amboni, M., Esposito, F., Russo, A., Picillo, M., Marcuccio, L., Pellecchia, M. T., Vitale, C., Cirillo, M., Tedeschi, G., & Barone, P. (2012). Resting-state brain connectivity in patients with Parkinson’s disease and freezing of gait. Parkinsonism & Related Disorders, 18(6), 781–787.

    Article  Google Scholar 

  • Tewarie, P., Steenwijk, M. D., Tijms, B. M., Daams, M., Balk, L. J., Stam, C. J., Uitdehaag, B. M., Polman, C. H., Geurts, J. J., Barkhof, F., Pouwels, P. J., Vrenken, H., & Hillebrand, A. (2014). Disruption of structural and functional networks in long-standing multiple sclerosis. Human Brain Mapping, 35(12), 5946–5961.

    Article  PubMed  Google Scholar 

  • Tian, L., Wang, J., Yan, C., & He, Y. (2011). Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. NeuroImage, 54(1), 191–202.

    Article  PubMed  Google Scholar 

  • Tinaz, S., Courtney, M. G., & Stern, C. E. (2011). Focal cortical and subcortical atrophy in early Parkinson’s disease. Movement Disorders, 26(3), 436–441.

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.

    Article  CAS  PubMed  Google Scholar 

  • van den Heuvel, M. P., & Sporns, O. (2011). Rich-club organization of the human connectome. Journal of Neuroscience, 31(44), 15775–15786.

    Article  PubMed  Google Scholar 

  • van den Heuvel, M. P., Kahn, R. S., Goni, J., & Sporns, O. (2012). High-cost, high-capacity backbone for global brain communication. PNAS, 109(28), 11372–11377.

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Heuvel, M. P., Sporns, O., Collin, G., Scheewe, T., Mandl, R. C., Cahn, W., Goni, J., Hulshoff Pol, H. E., & Kahn, R. S. (2013). Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry, 70(8), 783–792.

    Article  PubMed  Google Scholar 

  • van Mierlo, T. J., Chung, C., Foncke, E. M., Berendse, H. W., & van den Heuvel, O. A. (2015). Depressive symptoms in Parkinson’s disease are related to decreased hippocampus and amygdala volume. Movement Disorders, 30(2), 245–252.

    Article  PubMed  Google Scholar 

  • Vercruysse, S., Leunissen, I., Vervoort, G., Vandenberghe, W., Swinnen, S., & Nieuwboer, A. (2015). Microstructural changes in white matter associated with freezing of gait in Parkinson’s disease. Movement Disorders, 30(4), 567–576.

    Article  PubMed  Google Scholar 

  • Vincent, J. L., Kahn, I., Snyder, A. Z., Raichle, M. E., & Buckner, R. L. (2008). Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100(6), 3328–3342.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Wang, L., Zang, Y., Yang, H., Tang, H., Gong, Q., Chen, Z., Zhu, C., & He, Y. (2009). Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Human Brain Mapping, 30(5), 1511–1523.

    Article  PubMed  Google Scholar 

  • Wang, J., Zuo, X., Dai, Z., Xia, M., Zhao, Z., Zhao, X., Jia, J., Han, Y., & He, Y. (2013). Disrupted functional brain connectome in individuals at risk for Alzheimer’s disease. Biological Psychiatry, 73(5), 472–481.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Wang, X., Xia, M., Liao, X., Evans, A., & He, Y. (2015). GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Frontiers in Human Neuroscience, 9386.

  • Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of ‘small-world’ networks. Nature, 393(6684), 440–442.

    Article  CAS  PubMed  Google Scholar 

  • Wedeen, V. J., Rosene, D. L., Wang, R., Dai, G., Mortazavi, F., Hagmann, P., Kaas, J. H., & Tseng, W.-Y. I. (2012). The geometric structure of the brain fiber pathways. Science, 335(6076), 1628–1634.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams-Gray, C. H., Hampshire, A., Robbins, T. W., Owen, A. M., & Barker, R. A. (2007). Catechol O-methyltransferase Val158Met genotype influences frontoparietal activity during planning in patients with Parkinson’s disease. Journal of Neuroscience, 27(18), 4832–4838.

    Article  CAS  PubMed  Google Scholar 

  • Zalesky, A., Fornito, A., & Bullmore, E. T. (2010a). Network-based statistic: identifying differences in brain networks. NeuroImage, 53(4), 1197–1207.

    Article  PubMed  Google Scholar 

  • Zalesky, A., Fornito, A., Harding, I. H., Cocchi, L., Yücel, M., Pantelis, C., & Bullmore, E. T. (2010b). Whole-brain anatomical networks: does the choice of nodes matter? NeuroImage, 50(3), 970–983.

    Article  PubMed  Google Scholar 

  • Zalesky, A., Fornito, A., Seal, M. L., Cocchi, L., Westin, C. F., Bullmore, E. T., Egan, G. F., & Pantelis, C. (2011). Disrupted axonal fiber connectivity in schizophrenia. Biological Psychiatry, 69(1), 80–89.

    Article  PubMed  Google Scholar 

  • Zhan, W., Kang, G. A., Glass, G. A., Zhang, Y., Shirley, C., Millin, R., Possin, K. L., Nezamzadeh, M., Weiner, M. W., Marks Jr, W. J., & Schuff, N. (2012). Regional alterations of brain microstructure in Parkinson’s disease using diffusion tensor imaging. Movement disorders, 27(1), 90–97.

  • Zhang, K., Yu, C., Zhang, Y., Wu, X., Zhu, C., Chan, P., & Li, K. (2011). Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson’s disease. European Journal of Radiology, 77(2), 269–273.

    Article  PubMed  Google Scholar 

  • Zhang, R., Wei, Q., Kang, Z., Zalesky, A., Li, M., Xu, Y., Li, L., Wang, J., Zheng, L., Wang, B., Zhao, J., Zhang, J., & Huang, R. (2015). Disrupted brain anatomical connectivity in medication-naive patients with first-episode schizophrenia. Brain Structure and Function, 220(2), 1145–1159.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, Z., Shemmassian, S., Wijekoon, C., Kim, W., Bookheimer, S. Y., & Pouratian, N. (2014). DTI correlates of distinct cognitive impairments in Parkinson’s disease. Human Brain Mapping, 35(4), 1325–1333.

    Article  PubMed  Google Scholar 

  • Zhong, S., He, Y., & Gong, G. (2015). Convergence and divergence across construction methods for human brain white matter networks: an assessment based on individual differences. Human Brain Mapping, 36(5), 1995–2013.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We appreciate English editing assistance of Drs. Rhoda E. and Edmund F. Perozzi.

Author information

Authors and Affiliations

  1. Center for the Study of Applied Psychology, Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, School of Psychology, Brain Study Institute, South China Normal University, Guangzhou, 510631, China

    Changhong Li, Ruibin Zhang, Qing Ma, Qin Xu, Liqing Liu & Ruiwang Huang

  2. Department of Radiology, Guangdong Academy of Medical Sciences, Guangdong General Hospital, Guangzhou, China

    Biao Huang, Wanqun Yang & Jieying Feng

  3. Department of Neurology, Guangdong Academy of Medical Sciences, Guangdong General Hospital, Guangzhou, China

    Lijuan Wang, Limin Wang & Yuhu Zhang

Authors
  1. Changhong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Biao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruibin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qing Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wanqun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lijuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Limin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jieying Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Liqing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yuhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ruiwang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Biao Huang or Ruiwang Huang.

Ethics declarations

Funding

This work was supported by the funding from the National Natural Science Foundation of China (Grant numbers: 81271548, 81271560, 81371535, 81428013, and 81471654).

Conflict of interest

The authors declare that they have no competing financial interests. We declare that our work described here has not been submitted elsewhere for publication, neither in whole or in part, and all the authors listed have approved the manuscript that is enclosed. All authors of this research paper have directly participated in the planning, execution, or analysis of this study. All authors of this paper have also read and approved the final submitted version.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Changhong Li and Biao Huang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 903 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, C., Huang, B., Zhang, R. et al. Impaired topological architecture of brain structural networks in idiopathic Parkinson’s disease: a DTI study. Brain Imaging and Behavior 11, 113–128 (2017). https://doi.org/10.1007/s11682-015-9501-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-015-9501-6

Keywords

Search

Navigation