Age-related functional reorganization, structural changes, and preserved cognition

Neurobiology of Aging

Volumn 35, Issue 1, 2014, Pages 42-54

  Meunier, David ^a   Stamatakis, Emmanuel A ^a,b   Tyler, Lorraine K ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Aging; Complex networks; Functional MRI; Sentence processing

Indexed keywords

ADULT; AGED; AGING; ARTICLE; AUDITORY STIMULATION; COGNITION; COMPREHENSION; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HEAD MOVEMENT; HUMAN; HUMAN EXPERIMENT; LANGUAGE ABILITY; LANGUAGE PROCESSING; LEFT HEMISPHERE; MALE; MENTAL DETERIORATION; MINI MENTAL STATE EXAMINATION; NORMAL HUMAN; PRETEST POSTTEST DESIGN; PRIORITY JOURNAL; RIGHT HEMISPHERE; STIMULUS RESPONSE; TASK PERFORMANCE;

AGING; COMPLEX NETWORKS; FUNCTIONAL MRI; SENTENCE PROCESSING;

ADOLESCENT; ADULT; AGED; AGING; COGNITION; FEMALE; FRONTAL LOBE; HUMANS; LANGUAGE TESTS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; YOUNG ADULT;

EID: 84885180493     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.07.003     Document Type: Article

References (84)

1. Abe O., Aoki S., Hayashi N., Yamada H., Kunimatsu A., Mori H., Yoshikawa T., Okubo T., Ohtomo K. Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol. Aging 2002, 23:433-441.
2. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3:e17.
3. Anderton B.H. Ageing of the brain. Mech Ageing Dev. 2002, 123:811-817.
4. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
5. Bassett D.S., Wymbs N.F., Porter M.A., Mucha P.J., Carlson J.M., Grafton S.T. Dynamic reconfiguration of human brain networks during learning. Proc. Natl. Acad. Sci. U.S.A 2011, 108:7641-7646.
6. Bozic M., Tyler L.K., Ives D.T., Randall B., Marslen-Wilson W.D. Bihemispheric foundations for human speech comprehension. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17439-17444.
7. Bright P., Moss H.E., Stamatakis E.A., Tyler L.K. Longitudinal studies of semantic dementia: the relationship between structural and functional changes over time. Neuropsychologia 2008, 46:2177-2188.
8. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J.Neurosci. 2009, 29:1860-1873.
9. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 2009, 10:186-198.
10. Burke D.M., Shafto M.A. Language and aging. The Handbook of Aging and Cognition 2008, 373-443. Psychology Press, New York and Hove. F.I. Craik, T.A. Salthouse (Eds.).
11. Burock M.A., Buckner R.L., Woldorff M.G., Rosen B.R., Dale A.M. Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI. Neuroreport 1998, 9:3735-3739.
12. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD Model. Psychol. Aging 2002, 17:85-100.
13. Cabeza R., Anderson N.D., Locantore J.K., McIntosh A.R. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 2002, 17:1394-1402.
14. Caplan D. Activating brain systems for syntax and semantics. Neuron 1999, 24:292-293.
15. Craik F.I., Salthouse T.A. The Handbook of Aging and Cognition 2000, Lawrence Erlbaum Associates, Hillsdale, NJ.
16. Crinion J.T., Lambon-Ralph M.A., Warburton E.A., Howard D., Wise R.J. Temporal lobe regions engaged during normal speech comprehension. Brain 2003, 126:1193-1201.
17. Davis S.W., Dennis N.A., Buchler N.G., White L.E., Madden D.J., Cabeza R. Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 2009, 46:530-541.
18. Davis S.W., Dennis N.A., Daselaar S.M., Fleck M.S., Cabaza R. Que PASA? The posterior-anterior shift in aging. Cereb. Cortex 2008, 18:1201-1209.
19. Davis S.W., Kragel J.E., Madden D.J., Cabeza R. The architecture of cross-hemispheric communication in the aging brain: linking behavior to functional and structural connectivity. Cereb. Cortex 2012, 22:232-242.
20. de Frias C.M., Lovden M., Lindenberger U., Nilsson L.G. Revisiting the dedifferentiation hypothesis with longitudinal multi-cohort data. Intelligence 2007, 35:381-392.
21. Dodel S., Golestani N., Pallier C., ElKouby V., Le Bihan D., Poline J.B. Condition-dependent functional connectivity: syntax networks in bilinguals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:921-935.
22. Dronkers N.F., Wilkins D.P., Van Valin R.D., Redfern B.B., Jaeger J.J. Lesion analysis of the brain areas involved in language comprehension. Cognition 2004, 92:145-177.
23. Eguiluz V.M., Chialvo D.R., Cecchi G.A., Baliki M., Apkarian A.V. Scale-free brain functional networks. Phys. Rev. Lett. 2005, 94:018102.
24. Ferreira L.K., Busatto G.F. Resting-state functional connectivity in normal brain aging. Neurosci. Biobehav. Rev. 2013, 37:384-400.
25. Fornito A., Zalesky A., Bullmore E.T. Network scaling effects in graph analytic studies of human resting-state fMRI data. Front. Sys. Neurosci. 2010, 4:22.
26. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997, 6:218-229.
27. Ghisletta P., Lindenberger U. Age-based structural dynamics between perceptual speed and knowledge in the Berlin Aging Study: direct evidence for ability dedifferentiation in old age. Psychol. Aging 2003, 18:696-713.
28. Ginestet C.E., Nichols T.E., Bullmore E.T., Simmons A. Brain network analysis: separating cost from topology using cost-integration. PLoS One 2011, 6:e21570.
29. Ginestet C.E., Simmons A. Statistical parametric network analysis of functional connectivity dynamics during a working memory task. Neuroimage 2011, 55:688-704.
30. Gong G., Rosa-Neto P., Carbonell F., Chen Z.J., He Y., Evans A.C. Age- and gender-related differences in the cortical anatomical network. J.Neurosci. 2009, 29:15684-15693.
31. Gong N.J., Wong C.S., Chan C.C., Leung L.M., Chu Y.C. Correlations between microstructural alterations and severity of cognitive deficiency in Alzheimer's disease and mild cognitive impairment: a diffusional kurtosis imaging study. Magn. Reson. Imaging 2013, 31:688-694.
32. Good C.D., Johnsrude I., Ashburner J., Henson R.N.A., Friston K.J., Frackowiak R.S. Avoxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
33. Grady C.L., McIntosh A.R., Rajah M.N., Beig S., Craik F.I. The effects of age on the neural correlates of episodic encoding. Cereb. Cortex 1999, 9:805-814.
34. Griffiths J.D., Marslen-Wilson W.D., Stamatakis E.A., Tyler L.K. Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax. Cereb. Cortex 2013, 23:139-147.
35. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., Sporns O. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6:e159.
36. Hagoort P. How the brain solves the binding problem for language: a neurocomputational model of syntactic processing. Neuroimage 2003, 20(suppl 1):S18-S29.
37. He Y., Evans A. Graph theoretical modeling of brain connectivity. Curr. Opin. Neurol. 2010, 23:341-350.
38. 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.
39. Hochberg Y. Asharper Bonferroni procedure for multiple tests of significance. Biometrika 1988, 75:800-802.
40. Indefrey P., Cutler A. Pre-lexical and lexical processing in listening. The Cognitive Neurosciences 2004, 759-774. MIT Press, Cambridge, MA. M.S. Gazzaniga (Ed.).
41. Josephs O., Henson R.N. Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos. Trans. Roy. Soc. Lond. B Biol. Sci. 1999, 354:1215-1228.
42. Kalpouzos G., Persson J., Nyberg L. Local brain atrophy accounts for functional activity differences in normal aging. Neurobiol. Aging 2012, 33:623. e1-623.e13.
43. Kramer A.F., Erickson K.I. Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn. Sci. 2007, 11:342-348.
44. Latora V., Marchiori M. Efficient behavior of small-world networks. Phys. Rev. Lett. 2001, 87:198701.
45. Latora V., Marchiori M. Economic small-world behavior in weighted networks. Eur. Phys. J. B 2003, 32:249-263.
46. Madden D.J., Whiting W.L., Huettel S.A., White L.E., MacFall J.R., Provenzale J.M. Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 2004, 21:1174-1181.
47. Meier T.B., Desphande A.S., Vergun S., Nair V.A., Song J., Biswal B.B., Meyerand M.E., Birn R.M., Prabhakaran V. Support vector machine classification and characterization of age-related reorganization of functional brain networks. Neuroimage 2012, 60:601-613.
48. Meng X.L., Rosenthal R., Rubin D.B. Comparing correlated correlation coefficients. Psychol. Bull. 1992, 111:172-175.
49. Meunier D., Achard S., Morcom A., Bullmore E. Age-related changes in modular organization of human brain functional networks. Neuroimage 2009, 44:715-723.
50. Newman M.E. The structure and function of complex networks. SIAM Rev. 2003, 45:167-256.
51. Papoutsi M., Stamatakis E.A., Griffiths J.D., Marslen-Wilson W.D., Tyler L.K. Is left fronto-temporal connectivity essential for syntax? Effective connectivity, tractography and performance in left-hemisphere damaged patients. Neuroimage 2011, 58:656-664.
52. Park D.C., Polk T.A., Park R., Minear M., Savage A., Smith M.R. Aging reduces neural specialisation in ventral visual cortex. Proc. Natl. Acad. Sci. U.S.A 2004, 101:13091-13095.
53. Park D.C., Reuter-Lorenz P.A. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 2009, 60:173-196.
54. Persson J., Nyberg L., Lind J., Larsson A., Nilsson L.G., Ingvar M., Buckner R.L. Structure-function correlates of cognitive decline in aging. Cereb. Cortex 2006, 16:907-915.
55. Pfefferbaum A., Sullivan E.V., Hedehus M., Lim K.O., Adalsteinsson E., Moseley M. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn. Reson. Med. 2000, 44:259-268.
56. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
57. Price C.J. Areview and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 2012, 62:816-847.
58. Rabbitt P., Ibrahim S., Lunn M., Scott M., Thacker N., Hutchinson C., Horan M., Pendleton N., Jackson A. Age-associated losses of brain volume predictlongitudinal cognitive declines over 8 to 20 years. Neuropsychology 2008, 22:3-9.
59. Raven J.C. Colored Progressive Matrices 1995, Oxford Psychologists Press Ltd., Oxford.
60. 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.
61. Rovio S., Spulber G., Nieminen L.J., Niskanen E., Winblad B., Tuomilehto J., Nissinen A., Soininen H., Kivipelto M. The effect of midlife physical activity on structural brain changes in the elderly. Neurobiol. Aging 2010, 31:1927-1936.
62. Salami A., Eriksson J., Nyberg L. Opposing effects of aging on large-scale brain systems for memory encoding and cognitive control. J.Neurosci. 2012, 32:10749-10757.
63. 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.
64. Salthouse T.A. Theoretical Perspectives on Cognitive Aging 1991, Lawrence Erlbaum Associates, Hillsdale, NJ.
65. Scott S.K., Blank C.C., Rosen S., Wise R.J. Identification of a pathway for intelligible speech in the left temporal lobe. Brain 2000, 123:2400-2406.
66. Shinkareva S.V., Mason R.A., Malave V.L., Wang W., Mitchell T.M., Just M.A. Using fMRI brain activation to identify cognitive states associated with perception of tools and dwellings. PLoS One 2008, 3:e1394.
67. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003, 6:309-315.
68. Stamatakis E.A., Shafto M.A., Williams G., Tam P., Tyler L.K. White matter changes and word finding failures with increasing age. PLoS One 2011, 6:e14496.
69. Steiger J.H. Tests for comparing elements of a correlation matrix. Psychol. Bull. 1980, 87:245-251.
70. Taylor K.I., Stamatakis E.A., Tyler L.K. Crossmodal integration of object features: voxel-based correlations in brain-damaged patients. Brain 2009, 132:671-683.
71. Thomas A.G., Dennis A., Bandettini P.A., Johansen-Berg H. The effects of aerobic activity on brain structure. Front. Psychol. 2012, 3:86.
72. Tomasi D., Volkow N.D. Aging and functional brain networks. Mol. Psychiatry 2012, 17. 471, 549-558.
73. Tyler L.K., Marslen-Wilson W.D. Fronto-temporal brain systems supporting spoken language comprehension. Philos. Trans. Roy. Soc. Lond. B. Biol. Sci. 2008, 363:1037-1054.
74. Tyler L.K., Marslen-Wilson W.D., Randall B., Wright P., Devereux B.J., Zhuang J., Papoutsi M., Stamatakis E.A. Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage. Brain 2011, 134:415-431.
75. Tyler L.K., Marslen-Wilson W.D., Stamatakis E.A. Dissociating neuro-cognitive component processes: voxel-based correlational methodology. Neuropsychologia 2005, 43:771-778.
76. Tyler L.K., Shafto M.A., Randall B., Wright P., Marslen-Wilson W.D., Stamatakis E.A. Preserving syntactic processing across the adult life span: the modulation of the frontotemporal language system in the context of age-related atrophy. Cereb. Cortex 2010, 20:352-364.
77. 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.
78. van den Heuvel M.P., Stam C.J., Kahn R.S., Hulshoff H.E. Efficiency of functional brain networks and intellectural performance. J.Neurosci. 2009, 29:7619-7624.
79. van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
80. Vannest J.J., Karunanayaka P.R., Altaye M., Schmithorst V.J., Plante E.M., Eaton K.J., Rasmussen J.M., Holland S.K. Comparison of fMRI data from passive listening and active-response story processing tasks in children. J.Magn. Reson. Imaging 2009, 29:971-976.
81. Wang J., Zuo X., He Y. Graph-based network analysis of resting-state functional MRI. Front. Syst. Neurosci. 2010, 4:16.
82. Wang L., Li Y., Metzak P., He Y., Woodward T.S. Age-related changes in topological patterns of large-scale brain functional networks during memory encoding and recognition. Neuroimage 2012, 50:862-872.
83. Yang Y., Liang P., Lu S., Li K., Zhong N. The role of the DLPFC in inductive reasoning of MCI patients and normal agings: an fMRI study. Sci. China C Life Sci. 2009, 52:789-795.
84. Zalesky A., Fornito A., Harding I.H., Cocchi L., Yucel M., Pantelis C., Bullmore E.T. Whole-brain anatomical networks: does the choice of nodes matter?. Neuroimage 2010, 50:970-983.