Network-specific effects of age and in-scanner subject motion: A resting-state fMRI study of 238 healthy adults

NeuroImage

Volumn 63, Issue 3, 2012, Pages 1364-1373

  Mowinckel, Athanasia M ^a   Espeseth, Thomas ^b,c   Westlye, Lars T ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b CENTRE FOR ADVANCED STUDY   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Aging; Dual regression; Functional connectivity; ICA; Resting state FMRI; Subject motion

Indexed keywords

ADULT; AGED; AGING; ARTICLE; COGNITION; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; INDEPENDENT COMPONENT ANALYSIS; MALE; MOTION; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RESTING STATE FUNCTIONAL CONNECTIVITY; RESTING STATE NETWORK; TASK PERFORMANCE;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; ARTIFACTS; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTION; NEURAL PATHWAYS; REST; YOUNG ADULT;

EID: 84866182896     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.08.004     Document Type: Article

References (68)

1. Agosta F., Pievani M., Geroldi C., Copetti M., Frisoni G.B., Filippi M. Resting state fMRI in Alzheimer's disease: beyond the default mode network. Neurobiol. Aging 2012, 33:1564-1578.
2. Allen E.A., Erhardt E.B., Damaraju E., Gruner W., Segall J.M., Silva R.F., Havlicek M., Rachakonda S., Fries J., Kalyanam R., Michael A.M., Caprihan A., Turner J.A., Eichele T., Adelsheim S., Bryan A.D., Bustillo J., Clark V.P., Feldstein Ewing S.W., Filbey F., Ford C.C., Hutchison K., Jung R.E., Kiehl K.A., Kodituwakku P., Komesu Y.M., Mayer A.R., Pearlson G.D., Phillips J.P., Sadek J.R., Stevens M., Teuscher U., Thoma R.J., Calhoun V.D. A baseline for the multivariate comparison of resting-state networks. Front. Syst. Neurosci. 2011, 5:2.
3. Andrews-Hanna J.R., Snyder A.Z., Vincent J.L., Lustig C., Head D., Raichle Marcus E., Buckner R.L. Disruption of large-scale brain systems in advanced aging. Neuron 2007, 56:924-935.
4. Bäckman L., Almkvist O., Andersson J., Nordberg A., Winblad B., Reineck R., Långström B. Brain activation in young and older adults during implicit and explicit retrieval. J. Cogn. Neurosci. 1997, 9:378-391.
5. Beck A.T., Steer R.A., Ball R., Ranieri W.F. Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J. Pers. Assess. 1996, 67:588-597.
6. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:1001-1013.
7. Beckmann C.F., Mackay C.E., Filippini N., Smith S.M. Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. Neuroimage 2009, 47(Suppl. 1):S148. 10.1016/S1053-8119(09)71511-3.
8. Binnewijzend M.A., Schoonheim M.M., Sanz-Arigita E., Wink A.M., van der Flier W.M., Tolboom N., Adriaanse S.M., Damoiseaux J.S., Scheltens P., van Berckel B.N., Barkhof F. Resting-state fMRI changes in Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2012, 33(9):2018-2028.
9. Biswal B.B., Mennes M., Zuo X.-N., Gohel S., Kelly C., Smith S.M., Beckmann C.F., Adelstein J.S., Buckner R.L., Colcombe S., Dogonowski A.-M., Ernst M., Fair D., Hampson M., Hoptman M.J., Hyde J.S., Kiviniemi V.J., Kötter R., Li S.-J., Lin C.-P., Lowe M.J., Mackay C., Madden D.J., Madsen K.H., Margulies D.S., Mayberg H.S., McMahon K., Monk C.S., Mostofsky S.H., Nagel B.J., Pekar J.J., Peltier S.J., Petersen S.E., Riedl V., Rombouts S.A.R.B., Rypma B., Schlaggar B.L., Schmidt S., Seidler R.D., Siegle G.J., Sorg C., Teng G.-J., Veijola J., Villringer A., Walter M., Wang L., Weng X.-C., Whitfield-Gabrieli S., Williamson P., Windischberger C., Zang Y.-F., Zhang H.-Y., Castellanos F.X., Milham M.P. Toward discovery science of human brain function. Proc. Natl. Acad. Sci. 2010, 107:4734-4739.
10. Bluhm R., Osuch E., Lanius R., Boksman K., Neufeld R., Theberge J., Williamson P. Default mode network connectivity: effects of age, sex, and analytic approach. Neuroreport 2008, 19:4.
11. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
12. Cabeza R. Cognitive neuroscience of aging: contributions of functional neuroimaging. Scand. J. Psychol. 2001, 42:277-286.
13. Cabeza R., Anderson N.D., Houle S., Mangels J.A., Nyberg L. Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J. Cogn. Neurosci. 2000, 12:197-206.
14. 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.
15. Cabeza R., Daselaar S.M., Dolcos F., Prince S.E., Budde M., Nyberg L. Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 2004, 14:364-375.
16. Cole D.M., Smith S.M., Beckmann C.F. Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front. Syst. Neurosci. 2010, 5:12.
17. Damoiseaux J.S., Beckmann C.F., Arigita E.J.S., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Rombouts S.A.R.B. Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18:1856-1864.
18. Delis D., Kramer J., Kaplan E., Ober B. California Verbal Learning Test-Second Edition 2000, The Psychological Corporation, San Antonio, TX.
19. Dennis N.A., Cabeza R. Neuroimaging of healthy cognitive aging. The Handbook of Aging and Cognition 2008, Psychology Press, NY, USA. F.I.M. Craik, T.A. Salthouse (Eds.).
20. Espeseth T., Christoforou A., Lundervold A.J., Steen V.M., Le Hellard S., Reinvang I. Imaging and cognitive genetics: The Norwegian Cognitive NeuroGenetics Sample. Twin Res. Hum. Genet. 2012, 15:442-452.
21. Filippini N., MacIntosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of brain activity in young carriers of the APOE-ε4 allele. Proc. Natl. Acad. Sci. 2009, 106:7209-7214.
22. Filippini N., Nickerson L.D., Beckmann C.F., Ebmeier K.P., Frisoni G.B., Matthews P.M., Smith S.M., Mackay C.E. Age-related adaptations of brain function during a memory task are also present at rest. Neuroimage 2012, 59:3821-3828.
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. 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, 12:9.
25. Grady C.L., Maisog J.M., Horwitz B., Ungerleider L.G., Mentis M.J., Salerno J.A., Pietrini P., Wagner E., Haxby J.V. Age-related changes in cortical blood flow activation during visual processing of faces and location. J. Neurosci. 1994, 14:1450-1462.
26. Grady C.L., Bernstein L.J., Beig S., Siegenthaler A.L. The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. Psychol. Aging 2002, 17:7-23.
27. Grady C.L., Springer M.V., Hongwanishkul D., McIntosh A.R., Winocur G. Age-related changes in brain activity across the adult lifespan. J. Cogn. Neurosci. 2006, 18:227-241.
28. Greenwood P.M. Functional plasticity in cognitive aging: review and hypothesis. Neuropsychology 2007, 21:657-673.
29. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage 2009, 48:63-72.
30. Groves A.R., Smith S.M., Fjell A.M., Tamnes C.K., Walhovd K.B., Douaud G., Woolrich M.W., Westlye L.T. Benefits of multi-modal fusion analysis on a large-scale dataset: life-span patterns of inter-subject variability in cortical morphometry and white matter microstructure. Neuroimage 2012, 63:365-380.
31. Gunning-Dixon F.M., Gur R.C., Perkins A.C., Schroeder L., Turner T., Turetsky B.I., Chan R.M., Loughead J.W., Alsop D.C., Maldjian J., Gur R.E. Age-related differences in brain activation during emotional face processing. Neurobiol. Aging 2003, 24:285-295.
32. Hafkemeijer A., van der Grond J., Rombouts S.A. Imaging the default mode network in aging and dementia. Biochim. Biophys. Acta 2012, 1822:431-441.
33. 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.
34. Koch W., Teipel S., Mueller S., Buerger K., Bokde A.L.W., Hampel H., Coates U., Reiser M., Meindl T. Effects of aging on default mode network activity in resting state fMRI: does the method of analysis matter?. Neuroimage 2010, 51:280-287.
35. Kriegeskorte N., Simmons W.K., Bellgowan P.S.F., Baker C.I. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009, 12:535-540.
36. Lindenberger U., Baltes P.B. Sensory functioning and intelligence in old age: a strong connection. Psychol. Aging 1994, 9:339-355.
37. Lustig C., Snyder A.Z., Bhakta M., O'Brien K.C., McAvoy M., Raichle M.E., Morris J.C., Buckner R.L. Functional deactivations: change with age and dementia of the Alzheimer type. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14504-14509.
38. Madden D.J., Turkington T.G., Provenzale J.M., Hawk T.C., Hoffman J.M., Coleman R.E. Selective and divided visual attention: age-related changes in regional cerebral blood flow measured by H2(15)O PET. Hum. Brain Mapp. 1997, 5:389-409.
39. Meulenbroek O., Petersson K.M., Voermans N., Weber B., Fernandez G. Age differences in neural correlates of route encoding and route recognition. Neuroimage 2004, 22:1503-1514.
40. Nyberg L., Salami A., Andersson M., Eriksson J., Kalpouzos G., Kauppi K., Lind J., Pudas S., Persson J., Nilsson L.-G. Longitudinal evidence for diminished frontal cortex function in aging. Proc. Natl. Acad. Sci. 2010, 107:22682-22686.
41. O'Sullivan M., Jones D.K., Summers P.E., Morris R.G., Williams S.C.R., Markus H.S. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 2001, 57:632-638.
42. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 2009, 60:173-196.
43. Park D.C., Polk T.A., Park R., Minear M., Savage A., Smith M.R. Aging reduces neural specialization in ventral visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13091-13095.
44. Park J., Carp J., Kennedy K.M., Rodrigue K.M., Bischof G.N., Huang C.M., Rieck J.R., Polk T.A., Park D.C. Neural broadening or neural attenuation? Investigating age-related dedifferentiation in the face network in a large lifespan sample. J. Neurosci. 2012, 32:2154-2158.
45. Persson J., Lustig C., Nelson J.K., Reuter-Lorenz P.A. Age differences in deactivation: a link to cognitive control?. J. Cogn. Neurosci. 2007, 19:1021-1032.
46. 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.
47. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:676-682.
48. Raz N. The aging brain observed in vivo: differential changes and their modifiers. The Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging 2005, 19-58. Oxford University Press, New York. R. Cabeza, L. Nyberg, D.C. Park (Eds.).
49. Raz N., Rodrigue K.M. Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 2006, 30:730-748.
50. 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.
51. Sambataro F., Murty V.P., Callicott J.H., Tan H.Y., Das S., Weinberger D.R., Mattay V.S. Age-related alterations in default mode network: impact on working memory performance. Neurobiol. Aging 2010, 31:839-852.
52. Satterthwaite T.D., Wolf D.H., Loughead J., Ruparel K., Elliott M.A., Hakonarson H., Gur R.C., Gur R.E. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 2012, 60:623-632.
53. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
54. Shiffrin R.M., Schneider W. Controlled and automatic human information processing: II. Perceptual learning, automatic attending and a general theory. Psychol. Rev. 1977, 84:127-190.
55. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
56. 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.
57. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:S208-S219.
58. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
59. Smith S.M., Miller K.L., Salimi-Khorshidi G., Webster M., Beckmann C.F., Nichols T.E., Ramsey J.D., Woolrich M.W. Network modelling methods for FMRI. Neuroimage 2011, 54:875-891.
60. Sonuga-Barke E.J.S., Castellanos F.X. Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci. Biobehav. Rev. 2007, 31:977-986.
61. Tomasi D., Volkow N.D. Aging and functional brain networks. Mol. Psychiatry 2012, 17(471):549-558.
62. Van Dijk K.R.A., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
63. Wechsler D. WAIS-III: Administration and Scoring Manual: Wechsler Adult Intelligence Scale 1997, Psychological Corporation, San Antonio, TX.
64. Westlye L.T., Walhovd K.B., Dale A.M., Bjørnerud A., Due-Tønnessen P., Engvig A., Grydeland H., Tamnes C.K., Østby 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.
65. Westlye E.T., Lundervold A., Rootwelt H., Lundervold A.J., Westlye L.T. Increased hippocampal default mode synchronization during rest in middle-aged and elderly APOE epsilon4 carriers: relationships with memory performance. J. Neurosci. 2011, 31:7775-7783.
66. White N., Roddey C., Shankaranarayanan A., Han E., Rettmann D., Santos J., Kuperman J., Dale A. PROMO: real-time prospective motion correction in MRI using image-based tracking. Magn. Reson. Med. 2010, 63:91-105.
67. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.
68. Zuo X.-N., Kelly C., Adelstein J.S., Klein D.F., Castellanos F.X., Milham M.P. Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 2010, 49:2163-2177.