Differential age-dependent associations of gray matter volume and white matter integrity with processing speed in healthy older adults

NeuroImage

Volumn 123, Issue , 2015, Pages 42-50

  Hong, Zhaoping ^a   Ng, Kwun Kei ^a   Sim, Sam K Y ^a   Ngeow, Mei Yi ^a   Zheng, Hui ^a   Lo, June C ^a   Chee, Michael W L ^a   Zhou, Juan ^a,b  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE DISTRIBUTION; AGED; AGING; ARTICLE; BRAIN FUNCTION; BRAIN SIZE; CAPSULA INTERNA; EXTERNAL CAPSULE; FEMALE; FRACTIONAL ANISOTROPY; GRAY MATTER; HAN CHINESE; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; MIDDLE OCCIPITAL GYRUS; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PUTAMEN; VERY ELDERLY; VOXEL BASED MORPHOMETRY; WHITE MATTER; ANATOMY AND HISTOLOGY; BRAIN; MIDDLE AGED;

AGED; AGED, 80 AND OVER; AGING; BRAIN; FEMALE; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; WHITE MATTER;

EID: 84941127602     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.08.034     Document Type: Article

References (83)

1. Abe O., Yamasue H., Aoki S., Suga M., Yamada H., Kasai K., Masutani Y., Kato N., Kato N., Ohtomo K. Aging in the CNS: comparison of gray/white matter volume and diffusion tensor data. Neurobiol. Aging 2008, 29:102-116.
2. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986, 9:357-381.
3. Andersson J.L.R., Jenkinson M., Smith S.M. Non-linear registration, aka spatial normalisation. FMRIB technical report TR07JA2 2007.
4. 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.
5. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007, 38:95-113.
6. Batista S., Zivadinov R., Hoogs M., Bergsland N., Heininen-Brown M., Dwyer M.G., Weinstock-Guttman B., Benedict R.H. Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J. Neurol. 2012, 259:139-146.
7. Bendlin B.B., Fitzgerald M.E., Ries M.L., Xu G., Kastman E.K., Thiel B.W., Rowley H.A., Lazar M., Alexander A.L., Johnson S.C. White matter in aging and cognition: a cross-sectional study of microstructure in adults aged eighteen to eighty-three. Dev. Neuropsychol. 2010, 35:257-277.
8. Bennett I.J., Madden D.J. Disconnected aging: cerebral white matter integrity and age-related differences in cognition. Neuroscience 2014, 276:187-205.
9. Bennett I.J., Motes M.A., Rao N.K., Rypma B. White matter tract integrity predicts visual search performance in young and older adults. Neurobiol. Aging 2012, 33:433.
10. Borghesani P.R., Madhyastha T.M., Aylward E.H., Reiter M.A., Swarny B.R., Schaie K.W., Willis S.L. The association between higher order abilities, processing speed, and age are variably mediated by white matter integrity during typical aging. Neuropsychologia 2013, 51:1435-1444.
11. Bucur B., Madden D.J., Spaniol J., Provenzale J.M., Cabeza R., White L.E., Huettel S.A. Age-related slowing of memory retrieval: contributions of perceptual speed and cerebral white matter integrity. Neurobiol. Aging 2008, 29:1070-1079.
12. Cerella J., Hale S. The rise and fall in information-processing rates over the life span. Acta Psychol. 1994, 86:109-197.
13. Charlton R., Barrick T., McIntyre D., Shen Y., O'Sullivan M., Howe F., Clark C., Morris R., Markus H. White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology 2006, 66:217-222.
14. Chee M.W., Chen K.H., Zheng H., Chan K.P., Isaac V., Sim S.K., Chuah L.Y., Schuchinsky M., Fischl B., Ng T.P. Cognitive function and brain structure correlations in healthy elderly East Asians. NeuroImage 2009, 46:257-269.
15. Cortese S., Imperati D., Zhou J., Proal E., Klein R.G., Mannuzza S., Ramos-Olazagasti M.A., Milham M.P., Kelly C., Castellanos F.X. White matter alterations at 33-Year follow-up in adults with childhood attention-deficit/hyperactivity disorder. Biol. Psychiatry 2013, 74:591-598.
16. Daye Z.J., Xie J., Li H. A sparse structured shrinkage estimator for nonparametric varying-coefficient model with an application in genomics. J. Comput. Graph. Stat. 2012, 21:110-133.
17. DeLong M., Alexander G., Georgopoulos A., Crutcher M., Mitchell S., Richardson R. Role of basal ganglia in limb movements. Hum. Neurobiol. 1984, 2:235.
18. Eckert M.A., Keren N.I., Roberts D.R., Calhoun V.D., Harris K.C. Age-related changes in processing speed: unique contributions of cerebellar and prefrontal cortex. Front. Hum. Neurosci. 2010, 4:1-14.
19. Ell S.W., Helie S., Hutchinson S. Contributions of the putamen to cognitive function. Horizon in Neuroscience 2011, Nova Publishers. A. Costa, E. Villalba (Eds.).
20. Fjell A.M., Walhovd K.B. Structural brain changes in aging: courses, causes and cognitive consequences. Rev. Neurosci. 2010, 21:187-221.
21. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12:189-198.
22. Giorgio A., Santelli L., Tomassini V., Bosnell R., Smith S., De Stefano N., Johansen-Berg H. Age-related changes in grey and white matter structure throughout adulthood. NeuroImage 2010, 51:943-951.
23. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 2001, 14:21-36.
24. Haasz J., Westlye E.T., Fjaer S., Espeseth T., Lundervold A., Lundervold A.J. General fluid-type intelligence is related to indices of white matter structure in middle-aged and old adults. NeuroImage 2013, 83:372-383.
25. Haber S.N. Integrative networks across basal ganglia circuits. Handbook of Basal Ganglia Structure and Function 2010, Elsevier, Oxford. H. Steiner, K.Y. Tseng (Eds.).
26. Hayasaka S., Nichols T.E. Combining voxel intensity and cluster extent with permutation test framework. NeuroImage 2004, 23:54-63.
27. Hayes A.F. Beyond Baron and Kenny: statistical mediation analysis in the new millennium. Commun. Monogr. 2009, 76:408-420.
28. Imperati D., Colcombe S., Kelly C., Di Martino A., Zhou J., Castellanos F.X., Milham M.P. Differential development of human brain white matter tracts. PLoS One 2011, 6.
29. Jacobs H.I., Leritz E.C., Williams V.J., Van Boxtel M.P., Elst W., Jolles J., Verhey F.R., McGlinchey R.E., Milberg W.P., Salat D.H. Association between white matter microstructure, executive functions, and processing speed in older adults: the impact of vascular health. Hum. Brain Mapp. 2013, 34:77-95.
30. Jernigan T.L., Archibald S.L., Fennema-Notestine C., Gamst A.C., Stout J.C., Bonner J., Hesselink J.R. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 2001, 22:581-594.
31. Kalpouzos G., Chetelat G., Baron J.C., Landeau B., Mevel K., Godeau C., Barre L., Constans J.M., Viader F., Eustache F., Desgranges B. Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging. Neurobiol. Aging 2009, 30:112-124.
32. Kennedy K.M., Raz N. Aging white matter and cognition: differential effects of regional variations in diffusion properties on memory, executive functions, and speed. Neuropsychologia 2009, 47:916-927.
33. Kennedy K.M., Raz N. Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk. Brain Res. 2009, 1297:41-56.
34. Kennedy K.M., Erickson K.I., Rodrigue K.M., Voss M.W., Colcombe S.J., Kramer A.F., Acker J.D., Raz N. Age-related differences in regional brain volumes: a comparison of optimized voxel-based morphometry to manual volumetry. Neurobiol. Aging 2009, 30:1657-1676.
35. Kerchner G.A., Racine C.A., Hale S., Wilheim R., Laluz V., Miller B.L., Kramer J.H. Cognitive processing speed in older adults: relationship with white matter integrity. PLoS One 2012, 7.
36. Kochunov P., Glahn D.C., Lancaster J., Thompson P.M., Kochunov V., Rogers B., Fox P., Blangero J., Williamson D.E. Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan. NeuroImage 2011, 58:41-49.
37. Lebel C., Gee M., Camicioli R., Wieler M., Martin W., Beaulieu C. Diffusion tensor imaging of white matter tract evolution over the lifespan. NeuroImage 2012, 60:340-352.
38. Lindenberger U., von Oertzen T., Ghisletta P., Hertzog C. Cross-sectional age variance extraction: what's change got to do with it?. Psychol. Aging 2011, 26:34-47.
39. Lovden M., Kohncke Y., Laukka E.J., Kalpouzos G., Salami A., Li T.Q., Fratiglioni L., Backman L. Changes in perceptual speed and white matter microstructure in the corticospinal tract are associated in very old age. NeuroImage 2014, 102(Pt 2):520-530.
40. Lu P.H., Lee G.J., Raven E.P., Tingus K., Khoo T., Thompson P.M., Bartzokis G. Age-related slowing in cognitive processing speed is associated with myelin integrity in a very healthy elderly sample. J. Clin. Exp. Neuropsychol. 2011, 33:1059-1068.
41. 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.
42. Madden D.J., Bennett I.J., Song A.W. Cerebral white matter integrity and cognitive aging: contributions from diffusion tensor imaging. Neuropsychol. Rev. 2009, 19:415-435.
43. Madden D.J., Bennett I.J., Burzynska A., Potter G.G., Chen N.K., Song A.W. Diffusion tensor imaging of cerebral white matter integrity in cognitive aging. Biochim. Biophys. Acta 2012, 1822:386-400.
44. Marchand W.R., Lee J.N., Thatcher J.W., Hsu E.W., Rashkin E., Suchy Y., Chelune G., Starr J., Barbera S.S. Putamen coactivation during motor task execution. Neuroreport 2008, 19:957-960.
45. Maxwell S.E., Cole D.A. Bias in cross-sectional analyses of longitudinal mediation. Psychol. Methods 2007, 12:23-44.
46. Mori S., Wakana S., Van Zijl P.C.M., Nagae-Poetscher L.M. MRI atlas of human white matter 2005, Elsevier, Amsterdam, The Netherlands.
47. O'Sullivan M., Jones D., Summers P., Morris R., Williams S., Markus H. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 2001, 57:632-638.
48. Ostby Y., Tamnes C.K., Fjell A.M., Westlye L.T., Due-Tonnessen P., Walhovd K.B. Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30years. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:11772-11782.
49. 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.
50. Pfefferbaum A., Adalsteinsson E., Sullivan E.V. Frontal circuitry degradation marks healthy adult aging: evidence from diffusion tensor imaging. NeuroImage 2005, 26:891.
51. Rao S.M., Mayer A.R., Harrington D.L. The evolution of brain activation during temporal processing. Nat. Neurosci. 2001, 4:317-323.
52. Reitan R.M., Wolfson D. The Halstead-Reitan Neuropsychological Test Battery 1985, Neuropsychology Press, Tucson, Ariz.
53. Righart R., Duering M., Gonik M., Jouvent E., Reyes S., Hervé D., Chabriat H., Dichgans M. Impact of regional cortical and subcortical changes on processing speed in cerebral small vessel disease. NeuroImage 2013, 2:854-861.
54. Salami A., Eriksson J., Nilsson L.G., Nyberg L. Age-related white matter microstructural differences partly mediate age-related decline in processing speed but not cognition. Biochim. Biophys. Acta 2012, 1822:408-415.
55. Salthouse T.A. Processing capacity and its role on the relations between age and memory. Memory performance and competencies: Issues in growth and development 1995, 111-126.
56. Salthouse T.A. Aging and measures of processing speed. Biol. Psychol. 2000, 54:35-54.
57. Salthouse T.A. When does age-related cognitive decline begin?. Neurobiol. Aging 2009, 30:507-514.
58. Salthouse T.A. Selective review of cognitive aging. J. Int. Neuropsychol. Soc. 2010, 16:754-760.
59. Salthouse T.A. Neuroanatomical substrates of age-related cognitive decline. Psychol. Bull. 2011, 137:753-784.
60. Salthouse T.A., Ferrer-Caja E. What needs to be explained to account for age-related effects on multiple cognitive variables?. Psychol. Aging 2003, 18:91-110.
61. Schubotz R.I., Friederici A.D., von Cramon D.Y. Time perception and motor timing: a common cortical and subcortical basis revealed by fMRI. NeuroImage 2000, 11:1-12.
62. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., Giedd J.N., Wise S.P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. Off. J. Soc. Neurosci. 2008, 28:3586-3594.
63. Sheikh J.I., Yesavage J.A. Geriatric Depression Scale (GDS): recent evidence and development of a shorter version. Clin. Gerontol. 1986, 5:165-173.
64. Shenkin S.D., Bastin M.E., Macgillivray T.J., Deary I.J., Starr J.M., Rivers C.S., Wardlaw J.M. Cognitive correlates of cerebral white matter lesions and water diffusion tensor parameters in community-dwelling older people. Cerebrovasc. Dis. 2005, 20:310-318.
65. Smith A. Symbol Digit Modalities Test 1991, Western Psychological Services, Los Angeles, C.A.
66. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44:83-98.
67. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31:1487-1505.
68. 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.
69. Sullivan E.V., Pfefferbaum A. Diffusion tensor imaging and aging. Neurosci. Biobehav. Rev. 2006, 30:749-761.
70. Sullivan E.V., Rohlfing T., Pfefferbaum A. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiol. Aging 2010, 31:464-481.
71. Tibshirani R. Regression shrinkage and selection via the lasso. J. R. Stat. Soc. Ser. B Methodol. 1996, 267-288.
72. Turner R.S., Desmurget M., Grethe J., Crutcher M.D., Grafton S.T. Motor subcircuits mediating the control of movement extent and speed. J. Neurophysiol. 2003, 90:3958-3966.
73. Vernooij M.W., Ikram M.A., Vrooman H.A., Wielopolski P.A., Krestin G.P., Hofman A., Niessen W.J., Van der Lugt A., Breteler M. White matter microstructural integrity and cognitive function in a general elderly population. Arch. Gen. Psychiatry 2009, 66:545.
74. Voineskos A.N., Rajji T.K., Lobaugh N.J., Miranda D., Shenton M.E., Kennedy J.L., Pollock B.G., Mulsant B.H. Age-related decline in white matter tract integrity and cognitive performance: a DTI tractography and structural equation modeling study. Neurobiol. Aging 2012, 33:21-34.
75. Wakana S., Jiang H., Nagae-Poetscher L.M., Van Zijl P.C., Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004, 230:77-87.
76. Walhovd K.B., Fjell A.M., Reinvang I., Lundervold A., Dale A.M., Eilertsen D.E., Quinn B.T., Salat D., Makris N., Fischl B. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol. Aging 2005, 26:1261-1270. (discussion 1275-1268).
77. Walhovd K.B., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Fjell A.M. Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol. Aging 2011, 32:916-932.
78. Wechsler D. WMS-III Administration and Scoring Manual 1997, The Psychological Corporation, San Antonio, Tex.
79. Westlye L.T., Walhovd K.B., Dale A.M., Bjornerud A., Due-Tonnessen P., Engvig A., Grydeland H., Tamnes C.K., Ostby Y., Fjell A.M. Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cereb. Cortex 2010, 20:2055-2068.
80. Ystad M., Hodneland E., Adolfsdottir S., Haasz J., Lundervold A.J., Eichele T., Lundervold A. Cortico-striatal connectivity and cognition in normal aging: a combined DTI and resting state fMRI study. NeuroImage 2011, 55:24-31.
81. Zahr N.M., Rohlfing T., Pfefferbaum A., Sullivan E.V. Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. NeuroImage 2009, 44:1050-1062.
82. Zhang H., Sachdev P.S., Wen W., Kochan N.A., Zhu W., Crawford J.D., Brodaty H., Slavin M.J., Reppermund S., Kang K. Neuroanatomical correlates of cognitive performance in late life. Dement. Geriatr. Cogn. Disord. 2011, 32:216-226.
83. Zhou J., Greicius M.D., Gennatas E.D., Growdon M.E., Jang J.Y., Rabinovici G.D., Kramer J.H., Weiner M., Miller B.L., Seeley W.W. Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 2010, 133:1352-1367.