Load modulation of BOLD response and connectivity predicts working memory performance in younger and older adults

Journal of Cognitive Neuroscience

Volumn 23, Issue 8, 2011, Pages 2030-2045

  Nagel, Irene E ^a,b   Preuschhof, Claudia ^a,b   Li, Shu Chen ^a   Nyberg, Lars ^c   Bäckman, Lars ^a,d   Lindenberger, Ulman ^a   Heekeren, Hauke R ^a,b  

^a MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UMEÅ UNIVERSITY   (Sweden)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; BOLD SIGNAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL PERFORMANCE; NERVE CELL; NERVE CELL NETWORK; NEUROMODULATION; NORMAL HUMAN; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE; WORKING MEMORY;

ADULT; AGE FACTORS; AGED; AGING; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CUES; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; NERVE NET; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PSYCHOPHYSICS; REACTION TIME; TIME FACTORS; YOUNG ADULT;

EID: 79957929302     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn.2010.21560     Document Type: Article

References (89)

1. Andrews-Hanna, J. R., Snyder, A. Z., Vincent, J. L., Lustig, C., Head, D., Raichle, M. E., et al. (2007). Disruption of large-scale brain systems in advanced aging. Neuron, 56, 924-935.
2. Axmacher, N., Schmitz, D. P., Wagner, T., Elger, C. E., & Fell, J. (2008). Interactions between medial temporal lobe, prefrontal cortex, and inferior temporal regions during visual working memory: A combined intracranial EEG and functional magnetic resonance imaging study. Journal of Neuroscience, 28, 7304-7312.
3. Babcock, R. L., & Salthouse, T. A. (1990). Effects of increased processing demands on age differences in working memory. Psychology and Aging, 5, 421-428.
4. Bäckman, L., Karlsson, S., Fischer, H., Karlsson, P., Brehmer, Y., Rieckmann, A., et al. (in press). Dopamine D1 receptors and age differences in brain activation during working memory. Neurobiology of Aging.
5. Bäckman, L., Lindenberger, U., Li, S. C., & Nyberg, L. (2010). Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues. Neuroscience and Biobehavioral Reviews, 34, 670-677.
6. Bäckman, L., Nyberg, L., Lindenberger, U., Li, S. C., & Farde, L. (2006). The correlative triad among aging, dopamine, and cognition: Current status and future prospects. Neuroscience and Biobehavioral Reviews, 30, 791-807.
7. Bäckman, L., Small, B. J., Wahlin, A., & Larsson, A. (1999). Cognitive functioning in very old age. In F. I. Craik & T. Salthouse (Eds.), Handbook of aging and cognition (Vol. 2, pp. 499-558). Mahwah, NJ: Erlbaum.
8. Baddeley, A. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4, 829-839.
9. Baltes, P. B., & Lindenberger, U. (1997). Emergence of a powerful connection between sensory and cognitive functions across the adult life span: A new window to the study of cognitive aging? Psychology and Aging, 12, 12-21.
10. Barbas, H., & Pandya, D. N. (1989). Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology, 286, 353-375.
11. Barbas, H., & Zikopoulos, B. (2007). The prefrontal cortex and flexible behavior. Neuroscientist, 13, 532-545.
12. Barch, D. M., Braver, T. S., Nystrom, L. E., Forman, S. D., Noll, D. C., & Cohen, J. D. (1997). Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia, 35, 1373-1380.
13. Bennett, P. J., Sekuler, A. B., McIntosh, A. R., & Della-Maggiore, V. (2001). The effects of aging on visual memory: Evidence for functional reorganization of cortical networks. Acta Psychologica (Amsterdam), 107, 249-273.
14. Braver, T. S., Cohen, J. D., Nystrom, L. E., Jonides, J., Smith, E. E., & Noll, D. C. (1997). A parametric study of prefrontal cortex involvement in human working memory. Neuroimage, 5, 49-62.
15. Burzynska, A., Preuschhof, C., Bäckman, L., Nyberg, L., Li, S.-C., Lindenberger, U., et al. (2010). Age-related differences in white-matter microstructure: Region-specific patterns of diffusivity. Neuroimage, 49, 2104-2112.
16. Cabeza, R., Anderson, N. D., Locantore, J. K., & McIntosh, A. R. (2002). Aging gracefully: Compensatory brain activity I high-performing older adults. Neuroimage, 17, 1394-1402.
17. Cabeza, R., McIntosh, A. R., Tulving, E., Nyberg, L., & Grady, C. L. (1997). Age-related differences in effective neural connectivity during encoding and recall. NeuroReport, 8, 3479-3483.
18. Callicott, J. H., Mattay, V. S., Bertolino, A., Finn, K., Coppola, R., Frank, J. A., et al. (1999). Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cerebral Cortex, 9, 20-26.
19. Cappell, K. A., Gmiendl, L., & Reuter-Lorenz, P. A. (2010). Age differences in prefrontal recruitment during verbal working memory depend on memory load. Cortex, 46, 462-473.
20. Chang, C., Crottaz-Herbette, S., & Menon, V. (2007). Temporal dynamics of basal ganglia response and connectivity during verbal working memory. Neuroimage, 34, 1253-1269.
21. Conway, A. R. A., Jarrold, C., Kane, M. J., Miyake, A., & Towse, J. N. (Eds.) (2008). Variation in working memory. New York: Oxford University Press.
22. Cook, I. A., Bookheimer, S. Y., Mickes, L., Leuchter, A. F., & Kumar, A. (2007). Aging and brain activation with working memory tasks: An fMRI study of connectivity. International Journal of Geriatric Psychiatry, 22, 332-342.
23. Croxson, P. L., Johansen-Berg, H., Behrens, T. E., Robson, M. D., Pinsk, M. A., Gross, C. G., et al. (2005). Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. Journal of Neuroscience, 25, 8854-8866.
24. D'Esposito, M. (2007). From cognitive to neural models of working memory. Philosophical Transaction of the Royal Society of London, Series B, Biological Sciences, 362, 761-772.
25. de Frias, C. M., Lovden, M., Lindenberger, U., & Nilsson, L. G. (2007). Revisiting the dedifferentiation hypothesis with longitudinal multi-cohort data. Intelligence, 35, 381-392.
26. Damoiseaux, J. S., Beckmann, C. F., Arigita, E. J., Barkhof, F., Scheltens, P., Stam, C. J., et al. (2008). Reduced resting-state brain activity in the "default network" in normal aging. Cerebral Cortex, 18, 1856-1864.
27. Della-Maggiore, V., Sekuler, A. B., Grady, C. L., Bennett, P. J., Sekuler, R., & McIntosh, A. R. (2000). Corticolimbic interactions associated with performance on a short-term memory task are modified by age. Journal of Neuroscience, 20, 8410-8416.
28. Duverne, S., Motamedinia, S., & Rugg, M. D. (2009). The relationship between aging, performance, and the neural correlates of successful memory encoding. Cerebral Cortex, 19, 733-744.
29. Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6, 218-229.
30. Gazzaley, A., Cooney, J. W., Rissman, J., & D and #x02BC;Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8, 1298-1300.
31. Gazzaley, A., & D'Esposito, M. (2005). BOLD functional MRI and cognitive aging. In R. Cabeza, L. Nyberg, & D. Park (Eds.), Cognitive neuroscience of aging (pp. 107-131). New York: Oxford University Press.
32. Glabus, M. F., Horwitz, B., Holt, J. L., Kohn, P. D., Gerton, B. K., Callicott, J. H., et al. (2003). Interindividual differences in functional interactions among prefrontal, parietal and parahippocampal regions during working memory. Cerebral Cortex, 13, 1352-1361.
33. Grady, C. L., McIntosh, A. R., Bookstein, F., Horwitz, B., Rapoport, S. I., & Haxby, J. V. (1998). Age-related changes in regional cerebral blood flow during working memory for faces. Neuroimage, 8, 409-425.
34. Gunning-Dixon, F. M., & Raz, N. (2000). The cognitive correlates of white matter abnormalities in normal aging: A quantitative review. Neuropsychology, 14, 224-232.
35. Honey, G. D., Fu, C. H., Kim, J., Brammer, M. J., Croudace, T. J., Suckling, J., et al. (2002). Effects of verbal working memory load on corticocortical connectivity modeled by path analysis of functional magnetic resonance imaging data. Neuroimage, 17, 573-582.
36. Ito, H. T., & Schuman, E. M. (2008). Frequency-dependent signal transmission and modulation by neuromodulators. Frontiers in Neuroscience, 2, 138-144.
37. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 17, 825-841.
38. Jenkinson, M., & Smith, S. (2001). A global optimization method for robust affine registration of brain images. Medical Image Analysis, 5, 143-156.
39. Jonides, J., Lewis, R. L., Nee, D. E., Lustig, C. A., Berman, M. G., & Moore, K. S. (2008). The mind and brain of short-term memory. Annual Review of Psychology, 59, 193-224.
40. Jonides, J., Schumacher, E. H., Smith, E. E., Lauber, E. J., Awh, E., Minoshima, S., et al. (1997). Verbal working memory load affects regional brain activation as measured by PET. Journal of Cognitive Neuroscience, 9, 462-475.
41. Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., & Mintun, M. A. (1993). Spatial working memory in humans as revealed by PET. Nature, 363, 623-625.
42. Kaasinen, V., Vilkman, H., Hietala, J., Nagren, K., Helenius, H., Olsson, H., et al. (2000). Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain. Neurobiology of Aging, 21, 683-688.
43. Kirchhoff, B. A., & Buckner, R. L. (2006). Functional-anatomic correlates of individual differences in memory. Neuron, 51, 263-274.
44. Klingberg, T., O'Sullivan, B. T., & Roland, P. E. (1997). Bilateral activation of fronto-parietal networks by incrementing demand in a working memory task. Cerebral Cortex, 7, 465-471.
45. Kondo, H., Morishita, M., Osaka, N., Osaka, M., Fukuyama, H., & Shibasaki, H. (2004). Functional roles of the cingulo-frontal network in performance on working memory. Neuroimage, 21, 2-14.
46. Kondo, H., Osaka, N., & Osaka, M. (2004). Cooperation of the anterior cingulate cortex and dorsolateral prefrontal cortex for attention shifting. Neuroimage, 23, 670-679.
47. Kray, J., & Lindenberger, U. (2000). Adult age differences in task switching. Psychology and Aging, 15, 126-147.
48. Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., & Baker, C. I. (2009). Circular analysis in systems neuroscience: The dangers of double dipping. Nature Neuroscience, 12, 535-540.
49. Li, S.-C., & Sikström, S. (2002). Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neuroscience & Biobehavioral Reviews, 26, 795-808.
50. Lindenberger, U., & Baltes, P. B. (1997). Intellectual functioning in old and very old age: Cross-sectional results from the Berlin Aging Study. Psychology and Aging, 12, 410-432.
51. Lindenberger, U., & Ghisletta, P. (2009). Cognitive and sensory declines in old age: Gauging the evidence for a common cause. Psychology and Aging, 24, 1-16.
52. Lindenberger, U., Mayr, U., & Kliegl, R. (1993). Speed and intelligence in old-age. Psychology and Aging, 8, 207-220.
53. Lindenberger, U., Scherer, H., & Baltes, P. B. (2001). The strong connection between sensory and cognitive performance in old age: Not due to sensory acuity reductions operating during cognitive assessment. Psychology and Aging, 16, 196-205.
54. Madden, D. J., Bennett, I. J., & Song, A. W. (2009). Cerebral white matter integrity and cognitive aging: Contributions from diffusion tensor imaging. Neuropsychology Review, 19, 415-435.
55. Manoach, D. S., Schlaug, G., Siewert, B., Darby, D. G., Bly, B. M., Benfield, A., et al. (1997). Prefrontal cortex fMRI signal changes are correlated with working memory load. NeuroReport, 8, 545-549.
56. Mattay, V. S., Fera, F., Tessitore, A., Hariri, A. R., Berman, K. F., Das, S., et al. (2006). Neurophysiological correlates of age-related changes in working memory capacity. Neuroscience Letters, 392, 32-37.
57. Mayr, U., & Kliegl, R. (1993). Sequential and coordinative complexity: Age-based processing limitations in figural transformations. Journal of Experimental Psychology: Learning, Memory, & Cognition, 19, 1297-1320.
58. Mesulam, M. M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annals of Neurology, 28, 597-613.
59. Meyer-Lindenberg, A., Nichols, T., Callicott, J. H., Ding, J., Kolachana, B., Buckholtz, J., et al. (2006). Impact of complex genetic variation in COMT on human brain function. Molecular Psychiatry, 11, 867-877.
60. Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167-202.
61. Miyake, A. (2001). Individual differences in working memory: Introduction to the special section. Journal of Experimental Psychology: General, 130, 163-168.
62. Nagano-Saito, A., Leyton, M., Monchi, O., Goldberg, Y. K., He, Y., & Dagher, A. (2008). Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. Journal of Neuroscience, 28, 3697-3706.
63. Nagel, I. E., Preuschhof, C., Li, S.-C., Nyberg, L., Bäckman, L., Lindenberger, L., et al. (2009). Performance level modulates adult age differences in brain activation during a spatial working memory task. Proceedings of the National Academy of Sciences, U.S.A., 106, 22552-22557.
64. Narayanan, N. S., Prabhakaran, V., Bunge, S. A., Christoff, K., Fine, E. M., & Gabrieli, J. D. (2005). The role of the prefrontal cortex in the maintenance of verbal working memory: An event-related fMRI analysis. Neuropsychology, 19, 223-232.
65. Nyberg, L., Dahlin, E., Stigsdotter Neely, A., & Bäckman, L. (2008). Neural correlates of variable working memory load across adult age and skill: Dissociative patterns within the fronto-parietal network. Scandinavian Journal of Psychology, 50, 41-46.
66. O'Sullivan, M., Jones, D. K., Summers, P. E., Morris, R. G., Williams, S. C., & Markus, H. S. (2001). Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology, 57, 632-638.
67. Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25, 46-59.
68. Park, D. C., Lautenschlager, G., Hedden, T., Davidson, N. S., Smith, A. D., & Smith, P. K. (2002). Models of visuospatial and verbal memory across the adult life span. Psychology and Aging, 17, 299-320.
69. Park, D., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 1-24.
70. Petrides, M., & Pandya, D. N. (1984). Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. Journal of Comparative Neurology, 228, 105-116.
71. Pfefferbaum, A., Sullivan, E. V., Hedehus, M., Lim, K. O., Adalsteinsson, E., & Moseley, M. (2000). Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magnetic Resonance in Medicine, 44, 259-268.
72. Postle, B. R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience, 139, 23-38.
73. Raz, N. (2005). The aging brain observed in vivo. Differential changes and their modifiers. In R. Cabeza, L. Nyberg, & D. C. Park (Eds.), Cognitive neuroscience of aging: Linking cognitive and cerebral aging (pp. 19-57). New York: Oxford University Press.
74. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., et al. (2005). Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex, 15, 1676-1689.
75. Reuter-Lorenz, P. A. (2002). New visions of the aging mind and brain. Trends in Cognitive Sciences, 6, 394-400.
76. Reuter-Lorenz, P. A., & Cappell, K. (2008). Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science, 18, 177-182.
77. Reuter-Lorenz, P. A., & Lustig, C. (2005). Brain aging: Reorganizing discoveries about the aging mind. Current Opinion in Neurobiology, 15, 245-251.
78. Rogers, B. P., Morgan, V. L., Newton, A. T., & Gore, J. C. (2007). Assessing functional connectivity in the human brain by fMRI. Magnetic Resonance Imaging, 23, 1347-1357.
79. Rypma, B., & D'Esposito, M. (1999). The roles of prefrontal brain regions in components of working memory: Effects of memory load and individual differences. Proceedings of the National Academy of Sciences, 96, 6558-6563.
80. Rypma, B., Prabhakaran, V., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. (1999). Load-dependent roles of frontal brain regions in the maintenance of working memory. Neuroimage, 9, 216-226.
81. Sambataro, F., Murty, V. P., Callicott, J. H., Tan, H. Y., Das, S., Weinberger, D. R., et al. (2008). Age-related alterations in default mode network: Impact on working memory performance. Neurobiology of Aging, 31, 839-852.
82. Schmiedek, F., Lövdén, M., & Lindenberger, U. (2009). On the relation of mean reaction time and intraindividual reaction time variability. Psychology and Aging, 24, 841-857.
83. Schneider-Garces, N. J., Gordon, B. A., Brumback-Peltz, C. R., Shin, E., Lee, Y., Sutton, B. P., et al. (2010). Span, CRUNCH and beyond: Working memory capacity and the aging brain. Journal of Cognitive Neuroscience, 22, 655-669.
84. Servan-Schreiber, D., Printz, H., & Cohen, J. D. (1990). A network model of catecholamine effects: Gain, signal-to-noise ratio, and behavior. Science, 249, 892-894.
85. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl. 1), S208-S219.
86. Suhara, T., Fukuda, H., Inoue, O., Itoh, T., Suzuki, K., Yamasaki, T., et al. (1991). Age-related changes in human D1 dopamine receptors measured by positron emission tomography. Psychopharmacology, 103, 41-45.
87. Todd, J. J., & Marois, R. (2005). Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity. Cognitive, Affective & Behavioral Neuroscience, 5, 144-155.
88. Wechsler, D. (1981). The psychometric tradition-Developing the Wechsler Adult Intelligence Scale. Contemporary Educational Psychology, 6, 82-85.
89. West, R. L. (1996). An application of prefrontal cortex function theory to cognitive aging. Psychological Bulletin, 120, 272-292.