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01-10-2018 | Research Article

Small-world indices via network efficiency for brain networks from diffusion MRI

Authors: Lan Lin, Zhenrong Fu, Cong Jin, Miao Tian, Shuicai Wu

Published in: Experimental Brain Research | Issue 10/2018

Abstract

The small-world architecture has gained considerable attention in anatomical brain connectivity studies. However, how to adequately quantify small-worldness in diffusion networks has remained a problem. We addressed the limits of small-world measures and defined new metric indices: the small-world efficiency (SWE) and the small-world angle (SWA), both based on the tradeoff between high global and local efficiency. To confirm the validity of the new indices, we examined the behavior of SWE and SWA of networks based on the Watts–Strogatz model as well as the diffusion tensor imaging (DTI) data from 75 healthy old subjects (aged 50–70). We found that SWE could classify the subjects into different age groups, and was correlated with individual performance on the WAIS-IV test. Moreover, to evaluate the sensitivity of the proposed measures to network, two network attack strategies were applied. Our results indicate that the new indices outperform their predecessors in the analysis of DTI data.

Akil H, Martone ME, Van Essen DC (2011) Challenges and opportunities in mining neuroscience data. Science 331(6018):708CrossRefPubMedPubMedCentral

Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56(5):924–935CrossRefPubMedPubMedCentral

Ashburner J (2009) Computational anatomy with the SPM software. Magn Reson Imaging 27(8):1163–1174CrossRefPubMed

Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26(3):839–851CrossRefPubMed

Bai F, Shu N, Yuan Y, Shi Y, Yu H, Wu D et al (2012) Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J Neurosci 32(12):4307–4318CrossRefPubMed

Bartzokis G, Sultzer D, Lu PH, Nuechterlein KH, Mintz J, Cummings JL (2004) Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical “disconnection” in aging and Alzheimer’s disease. Neurobiol Aging 25(7):843–851CrossRefPubMed

Bassett DS, Bullmore ED (2006) Small-world brain networks. Neurosci 12(6):512–523

Bellec P, Benhajali Y, Carbonell F, Dansereau C, Albouy G, Pelland M, Orban P (2015) Impact of the resolution of brain parcels on connectome-wide association studies in fMRI. Neuroimage 123:212–228CrossRefPubMed

Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang DU (2006) Complex networks: Structure and dynamics. Phys Rep 424(4):175–308CrossRef

Bortoletto M, Veniero D, Thut G, Miniussi C (2015) The contribution of TMS–EEG coregistration in the exploration of the human cortical connectome. Neurosci Biobehav Rev 49:114–124CrossRefPubMed

Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186CrossRefPubMed

Chen VCH, Shen CY, Liang SHY, Li ZH, Tyan YS, Liao YT et al (2016) Assessment of abnormal brain structures and networks in major depressive disorder using morphometric and connectome analyses. J Affect Disord 205:103–111CrossRefPubMed

Chhabra A, Thakkar RS, Andreisek G, Chalian M, Belzberg AJ, Blakeley J et al (2013) Anatomic MR imaging and functional diffusion tensor imaging of peripheral nerve tumors and tumor like conditions. Am J Neuroradiol 34(4):802–807CrossRefPubMed

Cui Z, Zhong S, Xu P, He Y, Gong G (2013) Panda: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci 7(42):42PubMedPubMedCentral

de Reus MA, Van den Heuvel MP (2013) The parcellation-based connectome: limitations and extensions. Neuroimage 80:397–404CrossRefPubMed

Delbeuck X, Van der Linden M, Collette F (2003) Alzheimer’disease as a disconnection syndrome? Neuropsychol Rev 13(2):79–92CrossRefPubMed

Gigandet X, Griffa A, Kober T, Daducci A, Gilbert G, Connelly A et al (2013) A connectome-based comparison of diffusion MRI schemes. PloS one 8(9):e75061CrossRefPubMedPubMedCentral

Hagmann P, Kurant M, Gigandet X, Thiran P, Wedeen VJ, Meuli R, Thiran JP (2007) Mapping human whole-brain structural networks with diffusion MRI. PloS one 2(7):e597CrossRefPubMedPubMedCentral

Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ,et al (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci 107(44):19067–19072CrossRefPubMed

Humphries MD, Gurney K, Prescott TJ (2006) The brainstem reticular formation is a small-world, not scale-free, network. Proc R Soc Lond B Biol Sci 273(1585):503–511CrossRef

Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62(2):782–790CrossRefPubMed

Johansenberg H, Rushworth MF (2009) Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32(1):75CrossRef

Jones DK (2010) Challenges and limitations of quantifying brain connectivity in vivo with diffusion MRI. Imaging Med 2(3):341CrossRef

Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701CrossRefPubMed

Lin L, Jin C, Fu Z, Zhang B, Bin G, Wu S (2016) Predicting healthy older adult’s brain age based on structural connectivity networks using artificial neural networks. Comput Methods Progr Biomed 125:8–17CrossRef

Liu Y, Duan Y, He Y, Wang J, Xia M, Yu C et al (2012) Altered topological organization of white matter structural networks in patients with neuromyelitis optica. PloS one 7(11):e48846CrossRefPubMedPubMedCentral

Lo CY, Wang PN, Chou KH, Wang J, He Y, Lin CP (2010) Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer’s disease. J Neurosci 30(50):16876–16885CrossRefPubMed

Long Z, Duan X, Wang Y, Liu F, Zeng L, Zhao JP, Chen H (2015) Disrupted structural connectivity network in treatment-naive depression. Prog Neuropsychopharmacol Biol Psychiatry 56:18–26CrossRefPubMed

Mori S, van Zijl P (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15(7–8):468–480CrossRefPubMed

O’Sullivan M, Jones DK, Summers PE, Morris RG, Williams SCR, Markus HS (2001) Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology 57(4):632–638CrossRefPubMed

Odish OF, Caeyenberghs K, Hosseini H, Van Den Bogaard SJ, Roos RA, Leemans A (2015) Dynamics of the connectome in Huntington’s disease: a longitudinal diffusion MRI study. NeuroImage Clinl 9:32–43CrossRef

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

Shu N, Liu Y, Li J, Li Y, Yu C, Jiang T (2009) Altered anatomical network in early blindness revealed by diffusion tensor tractography. PloS one, 4(9):e7228CrossRefPubMedPubMedCentral

Simard D, Nadeau L, Kröger H (2004) Fastest learning in small-world neural networks. Phys Lett A 336(1):8–15CrossRef

Sporns O (2012) From simple graphs to the connectome: networks in neuroimaging. Neuroimage 62(2):881–886CrossRefPubMed

Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1(4):e42CrossRefPubMedPubMedCentral

Strogatz SH (2001) Exploring complex networks. Nature 410(6825):268CrossRefPubMed

Telesford QK, Joyce KE, Hayasaka S, Burdette JH, Laurienti PJ (2011) The ubiquity of small-world networks. Brain Connect 1(5):367CrossRefPubMedPubMedCentral

Teng X, Yong H (2012) Mapping the Alzheimer’s brain with connectomics. Front Psychiatry 2:77

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

Vaessen MJ, Hofman PAM, Tijssen HN, Aldenkamp AP, Jansen JF, Backes WH (2010) The effect and reproducibility of different clinical DTI gradient sets on small world brain connectivity measures. Neuroimage 51(3):1106–1116CrossRefPubMed

van den Heuvel MP, Mandl RC, Stam CJ, Kahn RS, Pol HEH (2010) Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J Neurosci 30(47):15915–15926CrossRefPubMed

Wang B, Fan Y, Lu M, Li S, Song Z, Peng X et al (2013) Brain anatomical networks in world class gymnasts: a DTI tractography study. NeuroImage 65:476–487CrossRefPubMed

Wang T, Shi F, Jin Y, Yap PT, Wee CY, Zhang J et al (2016) Multilevel deficiency of white matter connectivity networks in alzheimer’s disease: a diffusion mri study with dti and hardi models. Neural Plast 2016(2):2947136PubMedPubMedCentral

Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393(6684):440CrossRef

Weiss LG, Saklofske DH, Coalson DL, Raiford SE (2010) WAIS-IV clinical use and interpretation. Academic Press, San Diego

Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50(3):970–983CrossRefPubMed

Zhao T, Cao M, Niu H, Zuo XN, Evans A, He Y et al (2015) Age-related changes in the topological organization of the white matter structural connectome across the human lifespan. Hum Brain Mapp 36(10):3777–3792CrossRefPubMed

Title: Small-world indices via network efficiency for brain networks from diffusion MRI
Authors: Lan Lin
Zhenrong Fu
Cong Jin
Miao Tian
Shuicai Wu
Publication date: 01-10-2018
Publisher: Springer Berlin Heidelberg
Published in: Experimental Brain Research / Issue 10/2018
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-018-5326-z

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Springer Medicine

Small-world indices via network efficiency for brain networks from diffusion MRI

Abstract

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Springer Medicine

Abstract

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