Associations between age, motor function, and resting state sensorimotor network connectivity in healthy older adults

NeuroImage

Volumn 108, Issue , 2015, Pages 47-59

  Seidler, Rachael ^a   Erdeniz, Burak ^a   Koppelmans, Vincent ^a   Hirsiger, Sarah ^b   Mérillat, Susan ^b   Jäncke, Lutz ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cerebellum; Grip force; Healthy aging; Motor cortex; MRI; Resting state functional connectivity; Tapping speed

Indexed keywords

ADULT; AGE; AGED; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; BRAIN SIZE; CEREBELLAR LOBULE V; CEREBELLAR LOBULE VIII; CINGULATE GYRUS; CONTROLLED STUDY; CORRELATION ANALYSIS; DIASTOLIC BLOOD PRESSURE; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; GRIP STRENGTH; HEAD MOVEMENT; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; INSULA; LEFT HEMISPHERE; MALE; MIDDLE CINGULUM; MIDDLE FRONTAL GYRUS; MIDDLE ORBITOFRONTAL GYRUS; MOTOR CORTEX; MOTOR PERFORMANCE; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; POSTCENTRAL GYRUS; PRECUNEUS; PRIMARY MOTOR CORTEX; PUTAMEN; RESTING STATE FUNCTIONAL CONNECTIVITY MRI; RESTING STATE NETWORK; RESTING STATE SENSORIMOTOR FUNCTIONAL CONNECTIVITY; RIGHT HEMISPHERE; SENSORIMOTOR CORTEX; SMOKING; SUPERIOR PARIETAL LOBULE; SUPERIOR TEMPORAL GYRUS; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; TEMPORAL CORTEX; WHITE MATTER; AGING; BRAIN; BRAIN MAPPING; IMAGE PROCESSING; MIDDLE AGED; MOTOR ACTIVITY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; REST;

AGED; AGING; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR ACTIVITY; NEURAL PATHWAYS; REST;

EID: 84920181277     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.12.023     Document Type: Article

References (59)

1. 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 aging. Neuron 2007, 56(5):924-935.
2. Bernard J.A., Seidler R.D., Hassevoort K.M., Benson B.L., Welsh R.C., Wiggins J.L., Peltier S.J. Resting state cortico-cerebellar functional connectivity networks: a comparison of anatomical and self-organizing map approaches. Front. Neuroanat. 2012, 6:31. 10.3389/fnana.2012.00031.
3. Bernard J.A., Peltier S.J., Wiggins J.L., Jaeggi S.M., Buschkuehl M., Fling B.W., Seidler R.D. Disrupted cortico-cerebellar connectivity in older adults. Neuroimage 2013, 83:103-119. 10.1016/j.neuroimage.2013.06.042.
4. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34(4):537-541.
5. Bluhm R.L., Osuch E.A., Lanius R.A., Boksman K., Neufeld R.W., Théberge J., Williamson P. Default mode network connectivity: effects of age, sex, and analytic approach. Neuroreport 2008 May 28, 19(8):887-891.
6. Brodtmann A., Puce A., Darby D., Donnan G. Regional fMRI brain activation does correlate with global brain volume. Brain Res. 2009, 1259:17-25. 10.1016/j.brainres.2008.12.044.
7. Burciu R.G., Reinold J., Rabe K., Wondzinski E., Siebler M., Müller O., Theysohn N., Gerwig M., Donchin O., Timmann D. Structural correlates of motor adaptation deficits in patients with acute focal lesions of thecerebellum. Exp Brain Res 2014 Sep, 232(9):2847-2857.
8. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55(1):8-23. 10.1016/j.neuroimage.2010.11.049.
9. Chao-Gan Y., Yu-Feng Z. DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Front. Syst. Neurosci. 2010, 4:13. 10.3389/fnsys.2010.00013.
10. Damoiseaux J.S., Beckmann C.F., Arigita E.J., Barkhof F., Scheltens P., Stam C.J., Rombouts S.A. Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18(8):1856-1864. 10.1093/cercor/bhm207.
11. Di Martino A., Scheres A., Margulies D.S., Kelly A.M., Uddin L.Q., Shehzad Z., Milham M.P. Functional connectivity of human striatum: a resting state FMRI study. Cereb. Cortex 2008, 18(12):2735-2747. 10.1093/cercor/bhn041.
12. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage 2006, 33(1):127-138. 10.1016/j.neuroimage.2006.05.056.
13. Donchin O., Rabe K., Diedrichsen J., Lally N., Schoch B., Gizewski E.R., Timmann D. Cerebellar regions involved in adaptation to force field and visuomotor perturbation. J Neurophysiol 2012 Jan, 107(1):134-144.
14. Ferreira L.K., Busatto G.F. Resting-state functional connectivity in normal brain aging. Neurosci. Biobehav. Rev. 2013, 37(3):384-400. 10.1016/j.neubiorev.2013.01.017.
15. Fling B.W., Seidler R.D. Fundamental differences in callosal structure, neurophysiologic function, and bimanual control in young and older adults. Cerebral Cortex 2012, 22:2643-2652.
16. Fling B.W., Chapekis M., Reuter-Lorenz P.A., Anguera J., Bo J., Langan J., Seidler R.D. Age differences in callosal contributions to cognitive processes. Neuropsychologia 2011, 49(9):2564-2569. 10.1016/j.neuropsychologia.2011.05.004.
17. Fling B.W., Kwak Y., Peltier S.J., Seidler R.D. Differential relationships between transcallosal structural and functional connectivity in young and older adults. Neurobiol. Aging 2012, 33(10):2521-2526. 10.1016/j.neurobiolaging.2011.11.018.
18. 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(3):189-198.
19. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 2004 Mar 30, 101(13):4637-4642.
20. 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 Jul, 14(1 Pt 1):21-36.
21. Hermundstad A.M., Bassett D.S., Brown K.S., Aminoff E.M., Clewett D., Freeman S., Carlson J.M. Structural foundations of resting-state and task-based functional connectivity in the human brain. PNAS 2013, 110(15):6169-6174.
22. Heuninckx S., Wenderoth N., Swinnen S.P. Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J. Neurosci. 2008, 28(1):91-99. (28/1/91 [pii]). 10.1523/JNEUROSCI.3300-07.2008.
23. Ikram M.A., Vrooman H.A., Vernooij M.W., van der Lijn F., Hofman A., van der Lugt A., Niessen W.J., Breteler M.M. Brain tissue volumes in the general elderly population. The Rotterdam Scan Study. Neurobiol Aging. 2008 Jun, 29(6):882-890.
24. Jo H.J., Gotts S.J., Reynolds R.C., Bandettini P.A., Martin A., Cox R.W., Saad Z.S. Effective Preprocessing Procedures Virtually Eliminate Distance-Dependent Motion Artifacts in Resting State FMRI. J Appl Math. 2013 May, 21:2013. 10.1155/2013/935154.
25. Kwak Y., Peltier S., Bohnen N.I., Muller M.L., Dayalu P., Seidler R.D. Altered resting state cortico-striatal connectivity in mild to moderate stage Parkinson's disease. Front. Syst. Neurosci. 2010, 4:143. 10.3389/fnsys.2010.00143.
26. Langan J., Peltier S.J., Bo J., Fling B.W., Welsh R.C., Seidler R.D. Functional implications of age differences in motor system connectivity. Front. Syst. Neurosci. 2010, 4:17. 10.3389/fnsys.2010.00017.
27. Lutz K., Koeneke S., Wüstenberg T., Jäncke L. Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci Lett 2005 Jan 3, 373(1):61-66.
28. Mathys C., Hoffstaedter F., Caspers J., Caspers S., Südmeyer M., Grefkes C., Eickhoff S.B., Langner R. An age-related shift of resting-state functional connectivity of the subthalamic nucleus: a potential mechanism for compensating motor decline in older adults. Frontiers in Aging Neuroscience 2014, 6:178.
29. Mattay V.S., Fera F., Tessitore A., Hariri A.R., Das S., Callicott J.H., Weinberger D.R. Neurophysiological correlates of age-related changes in human motor function. Neurology 2002, 58(4):630-635.
30. Merker B., Podell K. Encyclopedia of Clinical Neuropsychology 2010, vol. 1:1176-1178. Springer, New York. D.J., J. Kreutzer, B. Caplan (Eds.).
31. Noble J.W., Eng J.J., Kokotilo K.J., Boyd L.A. Aging effects on the control of grip force magnitude: an fMRI study. Exp. Gerontol. 2011, 46(6):453-461. 10.1016/j.exger.2011.01.004.
32. O'Brien L.M., Ziegler D.A., Deutsch C.K., Kennedy D.N., Goldstein J.M., Seidman L.J., Herbert M.R. Adjustment for whole brain and cranial size in volumetric brain studies: a review of common adjustment factors and statistical methods. Harv. Rev. Psychiatry 2006, 14(3):141-151. 10.1080/10673220600784119.
33. Onoda K., Ishihara M., Yamaguchi S. Decreased functional connectivity by aging is associated with cognitive decline. J. Cogn. Neurosci. 2012, 24(11):2186-2198. 10.1162/jocn_a_00269.
34. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 2009, 60:173-196. 10.1146/annurev.psych.59.103006.093656.
35. Podell K. Encyclopedia of Clinical Neuropsychology 2010, vol. 1:1208-1209. Springer, New York. D.J., J. Kreutzer, B. Caplan (Eds.).
36. Rizzolatti G., Wolpert D.M. Motor systems. Curr. Opin. Neurobiol. 2005, 15(6):623-625. 10.1016/j.conb.2005.10.018.
37. Roski C., Caspers S., Langner R., Laird A.R., Fox P.T., Zilles K., Eickhoff S.B. Adult age-dependent differences in resting-state connectivity within and between visual-attention and sensorimotor networks. Front. Aging Neurosci. 2013, 5:67. 10.3389/fnagi.2013.00067.
38. Schatz P. Finger tapping test. Encyclopedia of Clinical Neuropsychology 2010, vol. 1:1050-1051. Springer, New York.
39. Schufried G. Special Ability Tests; Two-Hand Coordination. Vienne Test System - Psychological Assessment 2011, Schuhfried GmbH, Moedling, Austria. D.J., J. Kreutzer, B. Caplan (Eds.).
40. Seidler R.D., Bernard J.A., Burutolu T.B., Fling B.W., Gordon M.T., Gwin J.T., Lipps D.B. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 2010, 34(5):721-733. (S0149-7634(09)00159-6 [pii]). 10.1016/j.neubiorev.2009.10.005.
41. Spraker M.B., Yu H., Corcos D.M., Vaillancourt D.E. Role of individual basal ganglia nuclei in force amplitude generation. J Neurophysiol 2007 Aug, 98(2):821-834.
42. Song X.W., Dong Z.Y., Long X.Y., Li S.F., Zuo X.N., Zhu C.Z., Zang Y.F. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 2011, 6(9):e25031. 10.1371/journal.pone.0025031.
43. Song J., Birn R.M., Boly M., Meier T.B., Nair V.A., Meyerand M.E., Prabhakaran V. Age-related reorganizational changes in modularity and functional connectivity of human brain networks. Brain Connect 2014 Nov, 4(9):662-676.
44. Sorg C., Riedl V., Mühlau M., Calhoun V.D., Eichele T., Läer L., Drzezga A., Förstl H., Kurz A., Zimmer C., Wohlschläger A.M. Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 2007 Nov 20, 104(47):18760-18765.
45. 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 Mar, 6(3):309-315.
46. Stillman C.M., Gordon E.M., Simon J.R., Vaidya C.J., Howard D.V., Howard J.H. Caudate resting connectivity predicts implicit probabilistic sequence learning. Brain Connectivity 2013, 3(6):601-610.
47. Tomasi D., Volkow N.D. Aging and functional brain networks. Mol. Psychiatry 2012, 17(5):458-549. (471). 10.1038/mp.2011.81.
48. Tustison N.J., Avants B.B., Cook P.A., Zheng Y., Egan A., Yushkevich P.A., Gee J.C. N4ITK: improved N3 bias correction. IEEE Trans. Med. Imaging 2010, 29(6):1310-1320. 10.1109/TMI.2010.2046908.
49. van der Zwaag W., Kusters R., Magill A., Gruetter R., Martuzzi R., Blanke O., Marques J.P. Digit somatotopy in the human cerebellum: a 7T fMRI study. Neuroimage. 2013 Feb 15, 67:354-362. Epub 2012 Dec 11. 10.1016/j.neuroimage.2012.11.041.
50. Wang K., Liang M., Wang L., Tian L., Zhang X., Li K., Jiang T. Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum Brain Mapp 2007 Oct, 28(10):967-978.
51. Wang L., Negreira A., LaViolette P., Bakkour A., Sperling R.A., Dickerson B.C. Intrinsic interhemispheric hippocampus functional connectivity predicts individual differences in memory performance ability. Hippocampus 2010, 20(3):345-351.
52. Ward N.S., Frackowiak R.S. Age-related changes in the neural correlates of motor performance. Brain 2003, 126(Pt 4):873-888.
53. Ward N.S., Swayne O.B., Newton J.M. Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol. Aging 2008, 29(9):1434-1446. 10.1016/j.neurobiolaging.2007.04.017.
54. Wiestler T., McGonigle D.J., Diedrichsen J. Integration of sensory and motor representations of single fingers in the human cerebellum. J. Neurophysiol. 2011, 105(6):3042-3053. 10.1152/jn.00106.2011.
55. Witt S.T., Laird A.R., Meyerand M.E. Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. Neuroimage 2008, 42(1):343-356. 10.1016/j.neuroimage.2008.04.025.
56. Wu T., Zang Y., Wang L., Long X., Hallett M., Chen Y., Chan P. Aging influence on functional connectivity of the motor network in the resting state. Neurosci. Lett. 2007, 422(3):164-168. 10.1016/j.neulet.2007.06.011.
57. Ystad M., Hodneland E., Adolfsdottir S., Haász 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(1):24-31.
58. Yu R., Liu B., Wang L., Chen J., Liu X. Enhanced functional connectivity between putamen and supplementary motor area in Parkinson's disease patients. PLoS One 2013, 8(3):e59717. 10.1371/journal.pone.0059717.
59. Zollig J., Merillat S., Eschen A., Rocke C., Martin M., Jancke L. Plasticity and imaging research in healthy aging: core ideas and profile of the International Normal Aging and Plasticity Imaging Center (INAPIC). Gerontology 2011, 57(2):190-192. 10.1159/000324307.