Rich club analysis in the Alzheimer's disease connectome reveals a relatively undisturbed structural core network

Human Brain Mapping

Volumn 36, Issue 8, 2015, Pages 3087-3103

  Daianu, Madelaine ^a   Jahanshad, Neda ^a   Nir, Talia M ^a   Jack, Clifford R ^b   Weiner, Michael W ^c,d   Bernstein, Matt A ^b   Thompson, Paul M ^a,e  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; DWI; graph theory; mild cognitive impairment; MRI; rich club

Indexed keywords

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; BRAIN SIZE; CONNECTOME; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NERVE CELL NETWORK; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RICH CLUB NETWORK; TRACTOGRAPHY; AGING; BRAIN; CLINICAL TRIAL; COGNITIVE DEFECT; MENTAL HEALTH; MULTICENTER STUDY; NERVE TRACT; PATHOLOGY; PROCEDURES;

AGED; AGING; ALZHEIMER DISEASE; BRAIN; COGNITIVE DYSFUNCTION; CONNECTOME; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; MENTAL STATUS SCHEDULE; NEURAL PATHWAYS;

EID: 84930387060     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22830     Document Type: Article

References (59)

1. Alzheimer's Association Colorado. 2014 Fact Sheet Alzheimer's Disease. Available at: http://www.alz.org/downloads/Facts_Figures_2014.pdf. Accessed on October 15, 2014.
2. Aganj I. Lenglet C, Sapiro G, Yacoub E, Ugurbil K, Harel N (2010): Reconstruction of the orientation distribution function in single and multiple shell q-ball imaging within constant solid angle. Magn Reson Med 64:554−466.
3. Aganj I. Lenglet C, Jahanshad N, Yacoub E, Harel N, Thompson PM, Sapiro G (2011): A Hough transform global probabilistic approach to multiple-subject diffusion MRI tractography. Med Image Anal 15:414−425.
4. Alvarez-Hamelin JI, Dall'Asta L, Barrat A, Vespignani A (2006): Large scale networks fingerprinting and visualization using k-core decomposition. In: Weiss Y, Scholkopf B, Platt J, editors. Cambridge (Massachusetts): MIT Press. pp 44–55.
5. Axer M, Amunts K, Grässel D, Palm C, Dammers J, Axer H, Pietrzyk U, Zilles K (2010): A novel approach to the human connectome: Ultra-high resolution mapping of fiber tracts in the brain. Neuroimage 54:1091–1101.
6. Basser PJ, Jones DK (2002): Diffusion-tensor MRI: Theory, experimental design and data analysis–a technical review. NMR Biomed 15:456–467.
7. Braak H, Braak E (1996): Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. ActaNeuropathol 67:677–685.
8. Braskie MN, Jahanshad N, Stein JL, Barysheva M, McMahon KL, de Zubicaray GI, Martin NG, Wright KL, Ringman JM, Toga AW, Thompson PM (2012): Common Alzheimer's Disease risk variant within the CLU gene affect white matter microstructure in young adults. J Neurosci 31:6764–6770.
9. Brown JA, Terashima KH, Burggren AC, Ercoli LM, Miller KJ, Small GW, Bookheimer SY (2011): Brain network local interconnectivity loss in aging APOE-4 allele carriers. PNAS 108:20760–20765.
10. Bruner E, Jacobs HI (2013): Alzheimer's disease: The downside of a highly evolved parietal lobe? J Alzheimers Dis 35:227–240.
11. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009): Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29:1860–1873.
12. Clerx L, Visser PJ, Verhey F, Aalten P (2012): New MRI markers for Alzheimer's disease: A meta-analysis of diffusion tensor imaging and a comparison with medial temporal lobe measurements. J Alzheimer's Dis 29:405–429.
13. Coleman M (2005): Axon degeneration mechanisms: Commonality amid diversity. Nat Rev Neurosci 6:889–898.
14. Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014): The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 37(Pt 8):2382–2395.
15. Daianu M, Jahanshad N, Nir TM, Dennis E, Toga AW, Jack CR Jr., Weiner MW, Thompson PM, and the Alzheimer's Disease Neuroimaging Initiative (2012): Analyzing the structural k-core of brain connectivity networks in normal aging and Alzheimer's disease. In NIBAD’12 MICCAI Workshop on Novel Imaging Biomarkers for Alzheimer's Disease and Related Disorders, Nice, France, pp 52–62.
16. Daianu M, Jahanshad N, Nir TM, Toga AW, Jack CR Jr., Weiner MW, Thompson PM and the Alzheimer's Disease Neuroimaging Initiative (2013): Breakdown of brain connectivity between normal aging and Alzheimer's disease: A structural k-core network analysis. Brain Connectivity 3:407–422.
17. Daianu M, Dennis EL, Jahanshad N, Nir TM, Toga AW, Jack CR Jr., Weiner MW, Thompson PM (2014a): Disrupted brain connectivity in Alzheimer's disease: Effects of network thresholding. In: Schultz T et al., editor. Computational Diffusion MRI and Brain Connectivity, Mathematics and Visualization, Springer International Publishing, pp 199–207.
18. Daianu M, Jahanshad N, Villalon-Reina JE, Mendez MF, Bartzokis G, Jimenez EE, Joshi A, Barsuglia J, Thompson PM (2014b): Rich club network analysis shows distinct patterns of disruption in frontotemporal dementia and Alzheimer's disease. MICCAI’14 Computational Diffusion MRI (CDMRI) Workshop, Boston, MA, pp 13–22.
19. Daianu M, Jahanshad N, Nir TM, Leonardo CD, Jack CR Jr., Weiner MW, Bernstein M, Thompson PM (2014c): Algebraic connectivity of brain networks shows patterns of segregation leading to reduced network robustness in Alzheimer's disease. MICCAI’14 Computational Diffusion MRI (CDMRI) Workshop, Boston, MA, pp 55–64.
20. Daianu M, Jahanshad N, Mendez MF, Bartzokis G, Jimenez EE, Thompson PM (2015a): Communication of brain network core connections altered in behavioral variant frontotemporal dementia but possibly preserved in early-onset Alzheimer's disease. SPIE Medical Imaging, 9413. pii:941322.
21. Daianu M, Mezher A, Jahanshad N, Hibar DP, Nir TM, Jack CR, Weiner M, Bernstein M, Thompson PM (2015b): Spectral graph theory and graph energy metrics show evidence for the Alzheimer's disease disconnection syndrome in APOE-4 risk gene carriers. Proc IEEE Int Symp Biomed Imaging, In Press.
22. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006): An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980.
23. Engel J Jr., Thompson PM, Stern JM, Staba RJ, Bragin A, Mody I (2013): Connectomics and epilepsy. Curr Opin Neurol 26:186–194.
24. Ewers M, Insel P, Jagust WJ, Shaw L, Trojanowski JQ, Aisen P, Petersen RC, Schuff N, Weiner MW, Alzheimer's Disease Neuroimaging Initiative (ADNI) (2012): CSF biomarker and PIB-PET-derived beta-amyloid signature predicts metabolic, gray matter, and cognitive changes in nondemented subjects. Cereb Cortex 22:1993–2004.
25. Filippi M, Agosta F, Barkhof F, Dubois B, Fox NC, Frisoni GB, Jack CR, Johannsen P, Miller BL, Nestor PJ, Scheltens P, Sorbi S, Teipel S, Thompson PM, Wahlund LO (2012): EFNS (European Federation of Neurological Societies) Task Force: The use of neuroimaging in the diagnosis and management of dementia. Eur J Neurol 19:1487–1501.
26. Fischl B, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B (2004): Automatically parcellating the human cerebral cortex. Cerebral Cortex 14:11–22.
27. Hagmann P (2008): Mapping the Structural Core of Human Cerebral Cortex. PLOS Biology 6:1479–1493.
28. Ingalhalikar M, Smith A, Parker D, Satterthwaite TD, Elliott MA, Ruparel K, Hakonarson H, Gur RE, Gur RC, Verma R (2013): Sex differences in the structural connectome of the human brain. PNAS 111:823–828.
29. Jack CR, Bernstein MA, Borowski BJ, Gunter JL, Fox NC, Thompson PM, Schuff N, Krueger G, Killiany RJ, DeCarli CS, Dale AM, Carmichael OW, Tosun D, Weiner MW (2010): Update on the magnetic resonance imaging core of the Alzheimer's disease neuroimaging initiative. Alzheimers Dement 6:212–220.
30. Jahanshad N, Zhan L, Bernstein MA, Borowski B, Jack CR, Toga AW, Thompson PM (2010): Diffusion tensor imaging in seven minutes: Determining trade-offs between spatial and directional resolution. Proc IEEE Int Symp Biomed Imaging 1161–1164.
31. Jahanshad N, Aganj I, Lenglet C, Joshi A, Jin Y, Barysheva M, McMahon KL, de Zubicaray GI, Martin NG, Wright MJ, Toga AW, Sapiro G, Thompson PM (2011): Sex differences in the human connectome: 4-Tesla high angular resolution diffusion imaging (HARDI) tractography in 234 young adult twins. Proc IEEE Int Symp Biomed Imaging 939–943.
32. Jahanshad N, Valcour VG, Nir TM, Kohannim O, Busovaca E, Nicolas K, Thompson PM (2012): Disrupted brain networks in the aging HIV+ population. Brain Connectivity 2:335–344.
33. Jin Y, Shi Y, Zhan L, de Zubicaray GI, McMahon KL, Martin NG, Wright MJ, Thompson PM (2013): Labeling white matter tracts in Hardi by fusing multiple tract atlases with applications to genetics. Proc IEEE Int Symp Biomed Imaging 2013:512–515.
34. Jin Y, Shi Y, Zhan L, Gutman BA, de Zubicaray GI, McMahon KL, Wright MJ, Toga AW, Thompson PM (2014): Automatic clustering of white matter fibers in brain diffusion MRI with an application to genetics. Neuroimage 100:75–90.
35. Jin Y, Shi Y, Zhan L, Thompson PM (2015): Automated multi-atlas labeling of the fornix and its integrity in Alzheimer's disease. Proc IEEE Int Symp Biomed Imaging 140–143.
36. Li J, Jin Y, Shi Y, Dinov ID, Wang DJ, Toga AW, Thompson PM (2013): Voxelwise spectral diffusional connectivity and its applications to Alzheimer's disease and intelligence prediction. Med Image Comput Comput Assist Interv 16:655–662.
37. Mori S, van Zijl PC (2002): Fiber tracking: Principles and strategies–A technical review. NMR Biomed 15:468–480.
38. Nir TM, Jahanshad N, Jack CR, Weiner MW, Toga AW, Thompson PM, and the Alzheimer's Disease Neuroimaging Initiative (2012a): Small world network measures predict white matter degeneration in patients with early-stage mild cognitive impairment. In: Proc IEEE Int Symp Biomed Imaging, pp 1405–1408.
39. Nir TM, Jahanshad N, Toga AW, Bernstein MA, Jack CR, Weiner MW, Thompson PM (2012b): ADNI connectivity network breakdown predicts imminent volumetric atrophy in early mild cognitive impairment. MBIA Lect Notes Comput Sci 7509:41–50.
40. Nir TM, Jahanshad N, Villalon-Reina JE, Toga AW, Jack CR, Weiner MW, Thompson PM (2013): Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging. NeuroImage: Clinical 3:80–195.
41. Prasad G, Nir TM, Toga AW, Thompson PM (2013a): Tractography density and network measures in Alzheimer's Disease. In: Proc IEEE Int Symp Biomed Imaging (ISBI), pp 692–695.
42. Prasad G, Burkart J, Joshi SH, Nir TM, Toga AW, Thompson PM (2013b): A dynamical clustering model of brain connectivity inspired by the N-body problem. Multimodal Brain Image Analysis, Lecture Notes in Computer Science: Springer, 8159:129–137.
43. Reijmer YD, Leemans A, Caeyenberghs K, Heringa SM, Koek HL, Biessels GJ (2013): Disruption of cerebral networks and cognitive impairment in Alzheimer disease. Neurology 80:1370–1377.
44. Rowley J, Fonov V, Wu O, Eskildsen SF, Schoemaker D, Wu L, Mohades S, Shin M, Sziklas V, Cheewakriengkrai L, Shmuel A, Dagher A, Gauthier S, Rosa-Neto P, Alzheimer's Disease Neuroimaging Initiative (2013): White matter abnormalities and structural hippocampal disconnections in amnestic mild cognitive impairment and Alzheimer's disease. PLoS ONE 8:e74776.
45. Rubinov M, Sporns O (2010): Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 52:1059–1069.
46. Sporns O (2011): Networks of the Brain. Cambridge, MA. pp 5–31.
47. Sporns O, Honey CJ, Kötter R (2007): Identification and classification of hubs in brain networks. PLoS ONE 2:e1049.
48. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens Ph (2007): Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex 17:92–99.
49. Thompson PM, Hayashi KM, de Zubicaray G, Janke AL, Rose SE, Semple J, Herman D, Hong MS, Dittmer SS, Doddrell DM, Toga AW (2003): Dynamics of gray matter loss in Alzheimer's disease. J Neurosci 23:994–1005.
50. Toga AW, Thompson PM (2013): Connectomics sheds new light on Alzheimer's disease. Biol Psychiatry 73:390–392.
51. van den Heuvel MP, Sporns O (2011): Rich-club organization of the human connectome. J Neurosci 31:15775–15786.
52. van den Heuvel MP, Kahn RS, Goñi J, Sporns O (2012): High-cost, high-capacity backbone for global brain communication. PNAS 109:11372–11377.
53. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goñi J, Hulshoff Pol HE, Kahn RS (2013): Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70:783–792.
54. Wang J, Zuo X, Dai Z, Xia M, Zhao Z, Zhao X, Jia J, Han Y, He Y (2012): Disrupted functional brain connectome in individuals at risk for Alzheimer's disease. Biol Psychiatry 73:472–481.
55. Watts DJ, Strogatz SH (1998): Collective dynamics of “small-world” networks. Nature 393: 440–442.
56. Zamora-López G, Zhou C, Kurths J (2010): Cortical hubs form a module for multisensory integration on top of the hierarchy of cortical networks. Front Neuroinform 4:1.
57. Zhan L, Jahanshad N, Jin Y, Lenglet C, Mueller BA, Sapiro G, Ugurbil K, Harel N, Toga AW, Lim KO, Thompson PM (2013): Magnetic resonance field strength effects on diffusion measures and brain connectivity networks. Brain Connectivity 3:72–86.
58. Zhan L, Bernstein MA, Borowski B, Jack CR Jr., Thompson PM (2014a): Evaluation of diffusion imaging protocols for the Alzheimer's disease neuroimaging initiative. In: Proc IEEE Int Symp Biomed Imaging, pp 710–713.
59. Zhan L, Jahanshad N, Jin Y, Nir TM, Leonardo C, Bernstein M, Borowski B, Jack CR Jr., Thompson PM (2014b): Understanding scanner upgrade effects on brain integrity and connectivity measures. In: Proc IEEE Int Symp Biomed Imaging, pp 234–237.