Age-related reduction of BOLD modulation to cognitive difficulty predicts poorer task accuracy and poorer fluid reasoning ability

NeuroImage

Volumn 147, Issue , 2017, Pages 262-271

  Rieck, Jenny R ^a   Rodrigue, Karen M ^a   Boylan, Maria A ^a   Kennedy, Kristen M ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Adult lifespan; Aging; Cognitive control; fMRI; Reasoning

Indexed keywords

ACCURACY; ADULT; AGE DISTRIBUTION; AGED; AGING; ANGULAR GYRUS; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; DECISION MAKING; DEFAULT MODE NETWORK; DORSAL ANTERIOR CINGULATE CORTEX; ELECTROENCEPHALOGRAM; EXECUTIVE FUNCTION; FEMALE; FLUID REASONING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL CORTEX; LEFT ANGULAR GYRUS; LIFESPAN; MALE; MEDIAL FRONTAL CORTEX; MENTAL CAPACITY; MIDDLE FRONTAL GYRUS; NEUROMODULATION; NORMAL HUMAN; POSTERIOR CINGULATE; PRECUNEUS; PRIORITY JOURNAL; RESPONSE TIME; TASK PERFORMANCE; TEMPOROPARIETAL JUNCTION; VENTROMEDIAL PREFRONTAL CORTEX; BRAIN CORTEX; BRAIN MAPPING; DIAGNOSTIC IMAGING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; THINKING; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; AGING; BRAIN MAPPING; CEREBRAL CORTEX; EXECUTIVE FUNCTION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; THINKING; YOUNG ADULT;

EID: 85007271407     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.12.022     Document Type: Article

References (58)

1. Ankudowich, E., Pasvanis, S., Rajah, M.N., Changes in the modulation of brain activity during context encoding vs. context retrieval across the adult lifespan. NeuroImage 139 (2016), 103–113.
2. Baciu, M., Koenig, O., Vernier, M.P., Bedoin, N., Rubin, C., Segebarth, C., Categorical and coordinate spatial relations: fmri evidence for hemispheric specialization. Neuroreport 10 (1999), 1373–1378.
3. Barch, D.M., Braver, T.S., Nystrom, L.E., Forman, S.D., Noll, D.C., Cohen, J.D., Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35 (1997), 1373–1380.
4. Beason-Held, L.L., Kraut, M.A., Resnick, S.M., Stability of default-mode network activity in the aging brain. Brain Imaging Behav. 3 (2009), 123–131.
5. Braver, T.S., Barch, D.M., A theory of cognitive control, aging cognition, and neuromodulation. Neurosci. Biobehav Rev. 26 (2002), 809–817.
6. Braver, T.S., Cohen, J.D., Nystrom, L.E., Jonides, J., Smith, E.E., Noll, D.C., A parametric study of prefrontal cortex involvement in human working memory. NeuroImage 5 (1997), 49–62.
7. Brett, M., Anton, J., Valabregue, R., Poline, J., 2002. Region of interest analysis using the MarsBar toolbox for SPM 99. Poster Session Presented at: the Functional Mapping of the Human Brain, Japan.
8. Burianová, H., Lee, Y., Grady, C.L., Moscovitch, M., Age-related dedifferentiation and compensatory changes in the functional network underlying face processing. Neurobiol. Aging 34 (2013), 2759–2767.
9. Cabeza, R., Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17 (2002), 85–100.
10. Cabeza, R., Nyberg, L., Imaging cognition II: an empirical review of 275 PET and fMRI studies. J. Cogn. Neurosci. 12 (2000), 1–47.
11. Cappell, K.A., Gmeindl, L., Reuter-Lorenz, P.A., Age differences in prefrontal recruitment during verbal working memory maintenance depend on memory load. Cortex. 46 (2010), 462–473.
12. Cattell, R.B., Cattell, A.K.S., 1963. Test of "g": culture fair. Institute for Personality and Ability Testing.
13. Chan, M.Y., Park, D.C., Savalia, N.K., Petersen, S.E., Wig, G.S., Decreased segregation of brain systems across the healthy adult lifespan. Proc. Natl. Acad. Sci. USA 111 (2014), E4997–E5006.
14. Christensen, H., Mackinnon, A., Jorm, A.F., Henderson, A.S., Scott, L.R., Korten, A.E., Age differences and interindividual variation in cognition in community-dwelling elderly. Psychol. Aging 9 (1994), 381–390.
15. Cole, M.W., Reynolds, J.R., Power, J.D., Repovs, G., Anticevic, A., Braver, T.S., Multi-task connectivity reveals flexible hubs for adaptive task control. Nat. Neurosci. 16 (2013), 1348–1355.
16. Craik, F.I.M., Byrd, M., Aging and cognitive deficits. Craik, F.I.M., Trehub, S., (eds.) Aging and Cognitive Processes, 1982, Springer, US, 191–211.
17. Damoiseaux, J.S., Beckmann, C.F., Arigita, E.J.S., 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 18 (2008), 1856–1864.
18. Davis, S.W., Dennis, N.A., Daselaar, S.M., Fleck, M.S., Cabeza, R., Qué PASA? The posterior–anterior shift in aging. Cereb. Cortex 18 (2008), 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 22 (2012), 232–242.
20. de Chastelaine, M., Wang, T.H., Minton, B., Muftuler, L.T., Rugg, M.D., The effects of age, memory performance, and callosal integrity on the neural correlates of successful associative encoding. Cereb. Cortex 21 (2011), 2166–2176.
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 12 (1975), 189–198.
22. Glisky, E.L., Changes in cognitive function in human aging. Riddle, D.R., (eds.) Brain Aging: Models, Methods, and Mechanisms, 2007, 2007, CRC Press, Florida.
23. Grady, C.L., The cognitive neuroscience of ageing. Nat. Rev. Neurosci. 13 (2012), 491–505.
24. 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. 18 (2006), 227–241.
25. Greicius, M.D., Krasnow, B., Reiss, A.L., Menon, V., Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. USA 100 (2003), 253–258.
26. He, X., Qin, W., Liu, Y., Zhang, X., Duan, Y., Song, J., Li, K., Jiang, T., Yu, C., Age-related decrease in functional connectivity of the right fronto-insular cortex with the central executive and default-mode networks in adults from young to middle age. Neurosci. Lett. 544 (2013), 74–79.
27. 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 47 (2009), 916–927.
28. Kennedy, K., Rieck, J., Boylan, M., Rodrigue, K., 2016. Functional magnetic resonance imaging data of incremental increases in visuo-spatial difficulty in a large adult lifespan sample. (submitted for publication).
29. Kennedy, K.M., Rodrigue, K.M., Bischof, G.N., Hebrank, A.C., Reuter-Lorenz, P.A., Park, D.C., Age trajectories of functional activation under conditions of low and high processing demands: an adult lifespan fMRI study of the aging brain. NeuroImage 104 (2015), 21–34.
30. Kwon, D., Maillet, D., Pasvanis, S., Ankudowich, E., Grady, C.L., Rajah, M.N., Context memory decline in middle aged adults is related to changes in prefrontal cortex function. Cereb. Cortex 26 (2015), 2440–2460.
31. Linden, D.E.J., Bittner, R.A., Muckli, L., Waltz, J.A., Kriegeskorte, N., Goebel, R., Singer, W., Munk, M.H.J., Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network. NeuroImage 20 (2003), 1518–1530.
32. Mattay, V.S., Fera, F., Tessitore, A., Hariri, A.R., Berman, K.F., Das, S., Meyer-Lindenberg, A., Goldberg, T.E., Callicott, J.H., Weinberger, D.R., Neurophysiological correlates of age-related changes in working memory capacity. Neurosci. Lett. 392 (2006), 32–37.
33. Mazaika, P., Whitfield-Gabrieli, S., Reiss, A., 2007. Artifact repair for fMRI data from high motion clinical subjects. Poster Session Presented at Human Brain Mapping. Chicago, IL.
34. Miller, S.L., Celone, K., DePeau, K., Diamond, E., Dickerson, B.C., Rentz, D., Pihlajamäki, M., Sperling, R.A., Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc. Natl. Acad. Sci. USA. 105 (2008), 2181–2186.
35. Miller, E.K., Cohen, J.D., An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24 (2001), 167–202.
36. Otten, L.J., Rugg, M.D., When more means less: neural activity related to unsuccessful memory encoding. Curr. Biol. 11 (2001), 1528–1530.
37. Park, D.C., Lautenschlager, G., Hedden, T., Davidson, N.S., Smith, A.D., Smith, P.K., Models of visuo-spatial and verbal memory across the adult life span. Psychol. Aging 17 (2002), 299–320.
38. Park, D.C., Polk, T.A., Hebrank, A.C., Jenkins, L.J., Age differences in default mode activity on easy and difficult spatial judgment tasks. Front Hum. Neurosci., 3, 2010, 75.
39. Park, H., Kennedy, K.M., Rodrigue, K.M., Hebrank, A.C., Park, D.C., An fMRI study of episodic encoding across the lifespan: changes in subsequent memory effects are evident by middle-age. Neuropsychologia 51 (2013), 448–456.
40. Park, J., Carp, J., Hebrank, A., Park, D.C., Polk, T.A., Neural specificity predicts fluid processing ability in older adults. J. Neurosci. 30 (2010), 9253–9259.
41. Peirce, J.W., PsychoPy – Psychophysics software in Python. J. Neurosci. Methods 162 (2007), 8–13.
42. Peirce, J.W., Generating stimuli for neuroscience using PsychoPy. Front Neuroinform., 2, 2009, 10.
43. Persson, J., Lustig, C., Nelson, J.K., Reuter-Lorenz, P.A., Age differences in deactivation: a link to cognitive control?. J. Cogn. Neurosci. 19 (2007), 1021–1032.
44. Persson, J., Pudas, S., Nilsson, L.G., Nyberg, L., Longitudinal assessment of default-mode brain function in aging. Neurobiol. Aging 35 (2014), 2107–2117.
45. 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 15 (2005), 1676–1689.
46. Raz, N., Rodrigue, K.M., Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 30 (2006), 730–748.
47. Reuter-Lorenz, P.A., Cappell, K.A., Neurocognitive aging and the compensation hypothesis. Curr. Dir. Psychol. Sci. 17 (2008), 177–182.
48. Reuter-Lorenz, P.A., Lustig, C., Brain aging: reorganizing discoveries about the aging mind. Curr. Opin. Neurobiol. 15 (2005), 245–251.
49. Rieck, J.R., Rodrigue, K.M., Kennedy, K.M., Devous, M.D., Park, D.C., The effect of beta-amyloid on face processing in young and old adults: a multivariate analysis of the BOLD signal. Hum. Brain Mapp. 36 (2015), 2514–2526.
50. Rossi, S., Miniussi, C., Pasqualetti, P., Babiloni, C., Rossini, P.M., Cappa, S.F., Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study. J. Neurosci. 24 (2004), 7939–7944.
51. Salthouse, T.A., Methodological assumptions in cognitive aging research. Craik, F.I.M., Salthouse, T.A., (eds.) The Handbook of Aging and Cognition, 2nd ed, 2000, Lawrence Erlbaum Associates Publishers, Mahwah (NJ), 467–498.
52. 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 31 (2010), 839–852.
53. Schaie, K.W., The course of adult intellectual development. Am. Psychol. 49 (1994), 304–313.
54. Schneider-Garces, N.J., Gordon, B.A., Brumback-Peltz, C.R., Shin, E., Lee, Y., Sutton, B.P., Maclin, E.L., Gratton, G., Fabiani, M., Span, CRUNCH, and beyond: working memory capacity and the aging brain. J. Cogn. Neurosci. 22 (2010), 655–669.
55. Spaniol, J., Grady, C.L., Aging and the neural correlates of source memory: over-recruitment and functional reorganization. Neurobiol. Aging, 33, 2012 (425.e3-425.e18).
56. Spreng, R.N., Stevens, W.D., Chamberlain, J.P., Gilmore, A.W., Schacter, D.L., Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. NeuroImage 53 (2010), 303–317.
57. Turner, G.R., Spreng, R.N., Prefrontal engagement and reduced default network suppression co-occur and are dynamically coupled in older adults: the default-executive coupling hypothesis of aging. J. Cogn. Neurosci. 27 (2015), 2462–2476.
58. Verhaeghen, P., Cerella, J., Bopp, K.L., Basak, C., Aging and varieties of cognitive control: a review of meta-analyses on resistance to interference, coordination, and task switching, and an experimental exploration of age-sensitivity in the newly identified process of focus switching. Engle, R.W., Sedek, G., von Hecker, U., McIntosh, D.N., (eds.) Cognitive limitations in aging and Psychopathology, 2005, Cambridge University Press, Cambridge.