Changing topological patterns in normal aging using large-scale structural networks

Neurobiology of Aging

Volumn 33, Issue 5, 2012, Pages 899-913

  Zhu, Wanlin ^a,b   Wen, Wei ^a,b   He, Yong ^c   Xia, Aihua ^d   Anstey, Kaarin J ^e   Sachdev, Perminder ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b PRINCE OF WALES HOSPITAL   (Australia)

^c BEIJING NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Connectivity; Grey matter volume; Magnetic resonance imaging; Morphometry; Normal aging; Small world

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BRAIN ASYMMETRY; BRAIN REGION; BRAIN SIZE; CLUSTER ANALYSIS; COHORT ANALYSIS; GRAPH THEORY; GRAY MATTER; HESCHL GYRUS; HIPPOCAMPUS; HUMAN; INSULA; MATHEMATICAL PHENOMENA; NERVE CELL NETWORK; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL;

ADULT; AGED; AGING; BRAIN MAPPING; COGNITION; COHORT STUDIES; HUMANS; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; MODELS, NEUROLOGICAL; YOUNG ADULT;

EID: 84858335107     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.06.022     Document Type: Article

References (70)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol 2007, 3:e17.
2. Achard S., Salvador R., Whitcher B., Suckling J., Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci 2006, 26:63-72.
3. Andrews-Hanna J.R., Snyder A.Z., Vincent J.L., Lustig C., Head D., Raichle M.E., Buckner R.L. Disruption of large-scale brain systems in advanced aging. Neuron 2007, 56:924-935.
4. Anstey K.J., Low L.-F., Christensen H., Sachdev P. Level of cognitive performance as a correlate and predictor of health behaviors that protect against cognitive decline in late life: The path through life study. Intelligence 2008, 37:600-606.
5. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
6. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
7. Bassett D.S., Bullmore E., Verchinski B.A., Mattay V.S., Weinberger D.R., Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci 2008, 28:9239-9248.
8. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci 2008, 1124:1-38.
9. Buckner R.L., Snyder A.Z., Shannon B.J., LaRossa G., Sachs R., Fotenos A.F., Sheline Y.I., Klunk W.E., Mathis C.A., Morris J.C., Mintun M.A. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci 2005, 25:7709-7717.
10. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci 2009, 10:186-198.
11. Bullmore E.T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M.J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging 1999, 18:32-42.
12. Buzsaki G., Geisler C., Henze D.A., Wang X.J. Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci 2004, 27:186-193.
13. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 2002, 17:85-100.
14. Chen Z.J., He Y., Rosa-Neto P., Germann J., Evans A.C. Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb. Cortex 2008, 18:2374-2381.
15. Chklovskii D.B., Schikorski T., Stevens C.F. Wiring optimization in cortical circuits. Neuron 2002, 34:341-347.
16. Damoiseaux J.S., Beckmann C.F., Arigita E.J., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Rombouts S.A. Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18:1856-1864.
17. Daselaar S.M., Veltman D.J., Rombouts S.A., Raaijmakers J.G., Jonker C. Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. Brain 2003, 126:43-56.
18. Dickson D.W., Crystal H.A., Mattiace L.A., Masur D.M., Blau A.D., Davies P., Yen S.H., Aronson M.K. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging 1992, 13:179-189.
19. Duan H., Wearne S.L., Rocher A.B., Macedo A., Morrison J.H., Hof P.R. Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb. Cortex 2003, 13:950-961.
20. Evans A.C., Collins D.L., Mills S.R., Brown E.D., Kelly R.L., Peters T.M. 3D statistical neuroanatomical models from 305 MRI volumes. IEEE Nuclear Science Symposium and Medical Imaging Conference 1994, 1813-1817.
21. Ferrarini L., Veer I.M., Baerends E., van Tol M.J., Renken R.J., van der Wee N.J., Veltman D.J., Aleman A., Zitman F.G., Penninx B.W., van Buchem M.A., Reiber J.H., Rombouts S.A., Milles J. Hierarchical functional modularity in the resting-state human brain. Hum. Brain Mapp 2008.
22. Fisher R.A. Frequency distribution of the values of the correlation coefficient in samples of an indefinitely large population. Biometrika 1915, 10:507-521.
23. Fjell A.M., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Walhovd K.B. High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 2009, 19:2001-2012.
24. Freeman L. A set of measures of centrality based upon betweenness. Sociometry 1977, 40:35-41.
25. Friston K.J., Glaser D.E., Henson R.N., Kiebel S., Phillips C., Ashburner J. Classical and Bayesian inference in neuroimaging: applications. Neuroimage 2002, 16:484-512.
26. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
27. Grady C.L. Functional brain imaging and age-related changes in cognition. Biol. Psychol 2000, 54:259-281.
28. Grady C.L., McIntosh A.R., Bookstein F., Horwitz B., Rapoport S.I., Haxby J.V. Age-related changes in regional cerebral blood flow during working memory for faces. Neuroimage 1998, 8:409-425.
29. Gutchess A.H., Welsh R.C., Hedden T., Bangert A., Minear M., Liu L.L., Park D.C. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity. J. Cogn. Neurosci 2005, 17:84-96.
30. Hagmann P., Kurant M., Gigandet X., Thiran P., Wedeen V.J., Meuli R., Thiran J.P. Mapping human whole-brain structural networks with diffusion MRI. PLoS ONE 2007, 2:e597.
31. He Y., Chen Z., Evans A. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J. Neurosci 2008, 28:4756-4766.
32. He Y., Chen Z.J., Evans A.C. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb. Cortex 2007, 17:2407-2419.
33. Head D., Buckner R.L., Shimony J.S., Williams L.E., Akbudak E., Conturo T.E., McAvoy M., Morris J.C., Snyder A.Z. Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb. Cortex 2004, 14:410-423.
34. Hedden T., Gabrieli J.D. Insights into the ageing mind: a view from cognitive neuroscience. Nat. Rev. Neurosci 2004, 5:87-96.
35. Horwitz B., Grady C.L., Schlageter N.L., Duara R., Rapoport S.I. Intercorrelations of regional cerebral glucose metabolic rates in Alzheimer's disease. Brain Res 1987, 407:294-306.
36. Kaiser M., Hilgetag C.C. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput. Biol 2006, 2:e95.
37. Kemper T.L. Neuroanatomical and neuropathological changes during aging and dementia. Clinical Neurology of Aging 1994, Oxford University Press, New York, NY. M.L. Albert, J.E. Knoefel (Eds.).
38. Latora V., Marchiori M. Efficient Behavior of Small-World Networks. Phys Rev Lett 2001, 87:198701.
39. Lerch J.P., Worsley K., Shaw W.P., Greenstein D.K., Lenroot R.K., Giedd J., Evans A.C. Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI. Neuroimage 2006, 31:993-1003.
40. Liu Y., Liang M., Zhou Y., He Y., Hao Y., Song M., Yu C., Liu H., Liu Z., Jiang T. Disrupted small-world networks in schizophrenia. Brain 2008, 131:945-961.
41. Madden D.J., Turkington T.G., Provenzale J.M., Denny L.L., Hawk T.C., Gottlob L.R., Coleman R.E. Adult age differences in the functional neuroanatomy of verbal recognition memory. Hum. Brain Mapp 1999, 7:115-135.
42. Maslov S., Sneppen K. Specificity and stability in topology of protein networks. Science 2002, 296:910-913.
43. Mesulam M. Defining neurocognitive networks in the BOLD new world of computed connectivity. Neuron 2009, 62:1-3.
44. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., Alon U. Network motifs: simple building blocks of complex networks. Science 2002, 298:824-827.
45. Mitchell K.J., Johnson M.K., Raye C.L., D'Esposito M. fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Brain Res. Cogn. Brain Res 2000, 10:197-206.
46. Muller-Linow M., Hilgetag C.C., Hutt M.T. Organization of excitable dynamics in hierarchical biological networks. PLoS Comput. Biol 2008, 4:e1000190.
47. Newman M.E.J. The Structure and Function of Complex Networks. SIAM. ReView 2003, 45:167-256.
48. Nielson K.A., Langenecker S.A., Garavan H. Differences in the functional neuroanatomy of inhibitory control across the adult life span. Psychol. Aging 2002, 17:56-71.
49. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol 2009, 60:173-196.
50. Park D.C., Welsh R.C., Marshuetz C., Gutchess A.H., Mikels J., Polk T.A., Noll D.C., Taylor S.F. Working memory for complex scenes: age differences in frontal and hippocampal activations. J. Cogn. Neurosci 2003, 15:1122-1134.
51. Peters A., Moss M.B., Sethares C. Effects of aging on myelinated nerve fibers in monkey primary visual cortex. J. Comp. Neurol 2000, 419:364-376.
52. Raz N. Aging of the brain and its impact on cognitive performance: integration of structural and functional findings. The Handbook of Aging and Cognition 2000, Erlbaum, Hillsdale, NJ. F.I.M. Craik, T.A. Salthouse (Eds.).
53. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., Dahle C., Gerstorf D., Acker J.D. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 2005, 15:1676-1689.
54. Raz N., Rodrigue K.M., Head D., Kennedy K.M., Acker J.D. Differential aging of the medial temporal lobe: a study of a five-year change. Neurology 2004, 62:433-438.
55. Resnick S.M., Pham D.L., Kraut M.A., Zonderman A.B., Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J. Neurosci 2003, 23:3295-3301.
56. Reuter-Lorenz P.A., Jonides J., Smith E.E., Hartley A., Miller A., Marshuetz C., Koeppe R.A. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J. Cogn. Neurosci 2000, 12:174-187.
57. Rosen A.C., Prull M.W., Gabrieli J.D., Stoub T., O'Hara R., Friedman L., Yesavage J.A., deToledo-Morrell L. Differential associations between entorhinal and hippocampal volumes and memory performance in older adults. Behav. Neurosci 2003, 117:1150-1160.
58. Rubinov M., Knock S.A., Stam C.J., Micheloyannis S., Harris A.W., Williams L.M., Breakspear M. Small-world properties of nonlinear brain activity in schizophrenia. Hum. Brain Mapp 2007, 30:403-416.
59. Rubinov M., McIntosh A.R., Valenzuela M.J., Breakspear M. Simulation of Neuronal Death and Network Recovery in a Computational Model of Distributed Cortical Activity. Am. J. Geriatr. Psychiatry 2008, 17:210-217.
60. Sachdev P.S., Anstey K.J., Parslow R.A., Wen W., Maller J., Kumar R., Christensen H., Jorm A.F. Pulmonary function, cognitive impairment and brain atrophy in a middle-aged community sample. Dement. Geriatr. Cogn. Disord 2006, 21:300-308.
61. Salat D.H., Tuch D.S., Greve D.N., van der Kouwe A.J., Hevelone N.D., Zaleta A.K., Rosen B.R., Fischl B., Corkin S., Rosas H.D., Dale A.M. Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol. Aging 2005, 26:1215-1227.
62. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., Greicius M.D. Neurodegenerative diseases target large-scale human brain networks. Neuron 2009, 62:42-52.
63. Sporns O., Tononi G., Kotter R. The human connectome: A structural description of the human brain. PLoS Comput. Biol 2005, 1:e42.
64. Stam C.J. Functional connectivity patterns of human magnetoencephalographic recordings: a "small-world" network?. Neurosci. Lett 2004, 355:25-28.
65. Stebbins G.T., Carrillo M.C., Dorfman J., Dirksen C., Desmond J.E., Turner D.A., Bennett D.A., Wilson R.S., Glover G., Gabrieli J.D. Aging effects on memory encoding in the frontal lobes. Psychol. Aging 2002, 17:44-55.
66. Tootell R.B., Tsao D., Vanduffel W. Neuroimaging weighs in: Humans meet macaques in "primate" visual cortex. J. Neurosci 2003, 23:3981-3989.
67. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
68. Watts D.J., Strogatz S.H. Collective dynamics of "small-world" networks. Nature 1998, 393:440-442.
69. Wen W., Sachdev P. The topography of white matter hyperintensities on brain MRI in healthy 60 to 64-year-old individuals. Neuroimage 2004, 22:144-154.
70. Whittaker J. Graphical Models in Applied Multivariate Statistics 1990, John Wiley & Sons, New York.