Cardiorespiratory fitness and attentional control in the aging brain

Frontiers in Human Neuroscience

Volumn , Issue JANUARY, 2011, Pages 1-12

  Prakash, Ruchika Shaurya ^a   Voss, Michelle W ^b   Erickson, Kirk I ^c   Lewis, Jason M ^b   Chaddock, Laura ^b   Malkowski, Edward ^b   Alves, Heloisa ^b   Kim, Jennifer ^b   Szabo, Amanda ^b   White, Siobhan M ^b   Wójcicki, Thomas R ^b   Klamm, Emily L ^b   Mcauley, Edward ^b   Kramer, Arthur F ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiorespiratory fitness; Cognitive and attentional control references; Stroop task

Indexed keywords

AGED; AGING; ARTICLE; ATTENTION; BRAIN REGION; CARDIORESPIRATORY FITNESS; CONTROLLED STUDY; FEMALE; FITNESS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL PERFORMANCE; MENTAL TASK; NERVE CELL NETWORK; NEUROMODULATION; NEUROPHYSIOLOGICAL RECRUITMENT; NORMAL HUMAN; PARIETAL CORTEX; PHYSICAL CAPACITY; PREFRONTAL CORTEX; RESPONSE TIME; SELF CONTROL; STROOP TEST; UPREGULATION; VISUAL CORTEX; VISUAL DISCRIMINATION;

EID: 79955765950     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: None     Document Type: Article

References (87)

1. Banich, M. T., Milhalm, M. P., Atchley, R., Cohen, N. J., Webb, A., Wszalek, T., Kramer, A. F., Liang, Z., Wright, A., Shenker, J., and Magin, J. (2000). FMRI studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. J. Cogn. Neurosci. 12, 988-1000.
2. Banich, M. T., Milhalm, M. P., Jacobson, B. L., Webb, A., Wszalek, T., and Cohen, N. J. (2001). Attentional selection and the processing of task-irrelevant information: insights from fMRI examinations of the Stroop task. Prog. Brain Res. 134, 450-470.
3. Bar, M. (2003). A cortical mechanism for triggering top-down facilitation in visual object recognition. J. Cogn. Neurosci. 15, 600-609.
4. Barcelo, F., Suwazono, S., and Knight, R. T. (2000). Prefrontal modulation of visual processing in humans. Nat. Neurosci. 3, 399-403.
5. Beckmann, C. F., Jenkinson, M., and Smith, S. M. (2003). General multi-level linear modeling for group analysis in FMRI. Neuroimage 20, 1052-1063.
6. Bench, C. J., Frith, C. D., Grasby, P. M., Friston, K. J., Paulesu, E., Frackowiak, R. S. J., and Dolan, R. J. (1993). Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia 31, 907-922.
7. Black, J. E., Isaacs, K. R., Anderson, B. J., Alcantara, A. A., and Greenough, W. T. (1990). Learning causes synaptogen-esis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. U.S.A. 87, 5568-5572.
8. Blomstrand, E., Perret, D., Parry-Billings, M., and Newsholme, E. A. (1989). Effect of sustained exercise on plasma amino acid concentrations on 5-hy-droxy-tryptamine metabolism in six different brain regions in the rat. Acta Physiol. Scand. 136, 473-481.
9. Borg, G. (1998). Borg's Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics.
10. Brown, G. G., Kinderman, S. S., Siegle, G. J., Granholm, E., Wong, E. C., and Buxton, R. B. (1999). Brain activation and pupil response during covert performance of the Stroop Color Word task. J. Int. Neuropsychol. Soc. 5, 308-319.
11. Bush, G., Whalen, P. J., Rosen, B. R., Jenike, M. A., McInerney, S. C., and Rauch, S. L. (1998). The counting Stroop: an interference task specialized for functional neuroimaging - validation study with functional MRI. Hum. Brain Mapp. 6, 270-282.
12. Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17, 85-100.
13. Cabeza, R., Anderson, N. D., Locantore, J. K., and McIntosh, A. R. (2002). Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17, 1394-1402.
14. Cabeza, R., Daselaar, S. M., Dolcos, F., Prince, S. E., Budde, M., and Nyberg, L. (2004). Task-independent and task-specifc age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 14, 364-375.
15. Chaddock, L., Erickson, K. I., Prakash, R. S., and Kramer, A. F. (2010). Basal ganglia volume is associated with aerobic ftness in preadolescent children. Dev. Neurosci. 32, 249-256.
16. Christie, B. R., Eadie, B. D., Kannangara, T. S., Robillard, J. M., Shin, J., and Titterness, A. K. (2008). Exercising our brains: how physical activity impacts synaptic plasticity in the dentate gyrus. Neuromol. Med. 10, 47-58.
17. Cohen, L., Dehaene, S., Naccache, L., Lehericy, S., Dehaene-Lambertz, G., Henaff, M. A., and Michel, F. (2000). The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 123, 291-307.
18. Colcombe, S., and Kramer, A. F. (2003). Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol. Sci. 14, 125-130.
19. Colcombe, S. J., Erickson, K. I., Raz, N., Webb, A. G., Cohen, N. J., and McAuley, E. (2003). Aerobic ftness reduces brain tissue loss in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 55, 176-180.
20. Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., McAuley, E., Elavsky, S., Marquez, D. X., Hu, L., and Kramer, A. F. (2006). Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1166-1170.
21. Colcombe, S. J., Kramer, A. F., Erickson, K. I., Scalf, P., McAuley, E., and Cohen, N. J. (2004). Cardiovascular ftness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. U.S.A. 101, 3316-3321.
22. Colcombe, S. J., Kramer, A. F., Erickson, K. I., and Scalf, P. (2005). The implications of cortical recruitment and brain morphology for individual differences in inhibitory functioning in aging humans. Psychol. Aging 20, 363-375.
23. Corbetta, M., Miezin, F. M., Dobmeyer, S., Schulman, G. L., and Petersen, S. E. (1990). Attentional modulation of neural processing of shape, color and velocity in humans. Science 248, 1556-1559.
24. Cotman, C. W., and Berchtold, N. C. (2002). Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25, 295-301.
25. Cotman, C. W., Berchtold, N. C., and Christie, L.-A. (2007). Exercise builds brain health: key roles of growth factor cascades and infammation. Trends Neurosci. 30, 464-472.
26. Dale, A. M. (1999). Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8, 109-114.
27. Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S., and Cabeza, R. (2008). Que PASA? The posterior anterior shift in aging. Cereb. Cortex 18,1201-1209.
28. Dennis, N. A., and Cabeza, R. (2008). "Neuroimaging of healthy cognitive aging," in Handbook of Aging and Cognition, 3rd Edn., eds F. I. M. Craik and T. A. Salthouse (Mahwah, NJ: Erlbaum), 1-53.
29. DiGirolamo, G. J., Kramer, A. F., Barad, V., Cepeda, N., Weissman, D. H., Wszalek, T. M., Cohen, N. J., Banich, M., Webb, A., and Beloposky, A. (2001). General and task-specifc frontal lobe recruitment in older adults during executive processes: a fMRI investigation of task switching. Neuroreport 12, 2065-2072.
30. Dolcos, F., Rice, H. J., and Cabeza, R. (2002). Hemispheric asymmetry and aging: right hemisphere decline or hemispheric asymmetry. Neurosci. Biobehav. Rev. 26, 819-825.
31. Erickson, K. I., Colcombe, S. J., Wadhwa, R., Bherer, L., Peterson, M. S., Scalf, P. E., Kim, J. S., Alvarado, M., and Kramer, A. F. (2007). Training-induced plasticity in older adults: effects of training on hemispheric asymmetry. Neurobiol. Aging 28, 272-283.
32. Erickson, K. I., Prakash, R. S., Kim, J. S., Sutton, B. P., Colcombe, S. J., and Kramer, A. F. (2009a). Top-down attentional control in spatially coincident stimuli enhances activity in both task-relevant and task-irrelevant regions of cortex. Behav. Brain Res. 197, 186-197.
33. Erickson, K. I., Prakash, R. S., Voss, M. W., Chaddock, L., Hu, L., Morris, K. S., White, W. M., Wojcicki, T. R., McAuley, E., and Kramer, A. F. (2009b). Aerobic ftness is associated with hip-pocampal volume in elderly humans. Hippocampus 19, 1030-1039.
34. Fabel, K., Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C. J., and Palmer, T. D. (2003). VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812.
35. Farmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F. H., and Christie, B. R. (2004). Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124, 71-79.
36. Fordyce, D. E., and Farrar, R. P. (1991). Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical choliner-gic functioning. Behav. Brain Res. 46, 123-133.
37. Frith, C. (2001). A framework for studying the neural basis of attention. Neuropsychologia 39, 1367-1371.
38. Gazzaley, A., Rissman, J., Cooney, J., Rutman, A., Seibert, T., Clapp, W., and D'Esposito, M. (2007). Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. Cereb. Cortex 17, 125-135.
39. Grady, C. L., Maisog, J. M., Horwitz, B., Ungerleider, L. G., Mentis, M. J., Salerno, J. A., Pietrini, P., Wagner, E., and Haxby, J. V. (1994). Age-related changes in cortical blood fow activation during visual processing of faces and location. J. Neurosci. 14, 1450-1462.
40. Grady, C. L., McIntosh, A. R., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mentis, M. J., Pietrini, P., Schapiro, M. B., and Haxby, J. V. (1995). Age-related reductions in human recognition memory due to impaired encoding. Science 269, 218-221.
41. Gutchess, A. H., Welsh, R. C., Hedden, T., Bangert, A., Minear, M., and Liu, L. L. (2005). Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity. J. Cogn. Neurosci. 17, 84-96.
42. Hertzog, C., Kramer, A. F., Wilson, R. S., and Lindenberger, U. (2009). Enrichment effects on adult cognitive development: can the functional capacity of older adults be preserved and enhanced? Psychol. Sci. Public Interest 9, 1-65.
43. Jenkinson, M. (2003). Fast, automated, N-dimensional phase-unwrapping algorithm. Magn. Reson. Med. 49, 193-197.
44. Jobard, G., Crivello, F., and Tzourio-Mazoyer, N. (2003). Evaluation of the dual route theory of reading: a meta analysis of 35 neuroimaging studies. Neuroimage 20, 693-712.
45. Kastner, S., and Ungerleider, L. G. (2001). The neural bases of biased competition in human visual cortex. Neuropsychologia 39, 1263-1276.
46. Kaufman, A. S., and Kaufman, N. L. (1990). Kaufman Brief Intelligence Test: Manual. Circle Pines, MN: American Guidance Service.
47. Kleim, J. A., Cooper, N. R., and VandenBerg, P. M. (2002). Exercise induces angio-genesis but does not alter movement representations within rat motor cortex. Brain Res. 934, 1-6.
48. Kline, G. M., Porcari, J. P., Hintermeister, R., Freedson, P. S., Ward, A., McCarron, R. F., Ross, J., and Rippe, J. M. (1987). Estimation of VO2 Max from a one mile track walk, gender, age, and body weight. Med. Sci. Sports Exerc. 19, 253-259.
49. Kramer, A. F., Hahn, S., Cohen, N., Banich, M., McAuley, E., Harrison, C., Chason, J., Vakil, E., Bardell, L., Boileau, R. A., and Colcombe, A. (1999). Aging, ft-ness, and neurocognitive function. Nature 400, 418-419.
50. Langenecker, S. A., Nielson, K. A., and Rao, S. M. (2004). FMRI of healthy older adults during Stroop interference. Neuroimage 21, 192-200.
51. Lavie, N., Hirst, A., DeFockert, J. W., and Viding, E. (2004). Load theory of selective attention and cognitive control. J. Exp. Psychol. 133, 339-354.
52. Liu, X., Banich, M. T., Jacobson, B. L., and Tanabe, J. L. (2006). Functional dissociation of attentional selection within PFC: response and non-response related aspects of attentional selection as ascertained by fMRI. Cereb. Cortex 16, 827-834.
53. Logan, J. M., Sanders, A. L., Snyder, A. Z., Morris, J. C., and Buckner, R. L. (2002). Under- recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron 33, 827-840.
54. Lopez-Lopez, C., LeRoith, D., and Torres-Aleman, I. (2004). Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc. Natl. Acad. Sci. U.S.A. 101, 9833-9838.
55. Lotscher, F., Loffel, T., Steiner, R., Vogt, M., Klossner, S., Popp, A., Lippuner, K., Hoppeler, H., and Dapp, C. (2007). Biologically relevant sex differences for fitness-related parameters in active octogenarians. Eur. J. Appl. Physiol. 99, 533-540.
56. Madden, D. J., and Hoffman, J. M. (1997). "Application of positron emission tomography to age-related cognitive changes," in Brain Imaging in Clinical Psychiatry, eds K. K. R. Krishnan and P. M. Doraiswamy (New York: Marcel Dekker), 575-613.
57. Madden, D. J., Turkington, T. G., Provenzale, J. M., Denny, L. L., Langley, L. K., Hawk, T. C., and Coleman, R. E. (2002). Aging and attentional guidance during visual search: functional neuro-anatomy by positron emission tomog-r a p h y. Psychol. Aging 17, 24-43.
58. Marks, B. L., Madden, D. J., Bucur, B., Provenzale, J. M., White, L. E., Cabeza, R., and Huettel, S. A. (2007). Role of aerobic ftness and aging on cerebral white matter integrity. Ann. N. Y. Acad. Sci. 1097, 171-174.
59. Meyer, K., Niemann, S., and Abel, T. (2004). Gender differences in physical activity and ftness-association with self-reported health and health-relevant attitudes in a middle-aged Swiss urban population. J. Public Health 12, 283-290.
60. Milham, M. P., Banich, M. T., Webb, A., Barad, V., Cohen, N. J., and Wszalek, T. (2001). The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of confict. Brain Res. Cogn. 12, 1325-1346.
61. Milham, M. P., Erickson, K. I., Banich, M. T., Kramer, A. F., Webb, A., and Wszalek, T., and Cohen, N. J. (2002). Attentional control in the aging brain: insights from an fMRI study of the Stroop task. Brain Cogn. 49, 467-473.
62. Nagel, I. E., Preuschhof, C., Li, S-C., Nyberg, L., Backmann, L., Lindenberger, U., and Heekeren, H. R. (2009). Performance level modulates adult age differences in brain activation during spatial working memory. Proc. Natl. Acad. Sci. U.S.A. 106, 22552-22557.
63. Park, D. C., Polk, T. A., Mikels, J. A., Taylor, S. F., and Marshuetz, C. (2001). Cerebral aging: integration of brain and behavioral models cognitive function. Dialogues Clin. Neurosci. Cereb. Aging 3, 151-165.
64. Park, D. C., Polk, T. A., Park, R., Minear, M., Savage, A., and Smith, M. R. (2004). Aging reduces neural specialization in ventral visual cortex. Proc. Natl. Acad. Sci. U.S.A. 101, 13091-13095.
65. Park, D. C., and Reuter-Lorenz, P. A. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 60, 173-196.
66. Pessoa, L., Kastner, S., and Underleider, L. G. (2003). Neuroimaging studies of attention: from modulation of sensory processing to top-down control. J. Neurosci. 23, 3990-3998.
67. Poulton, N. P., and Muir, G. D. (2005). Treadmill training ameliorates dopamine loss but not behavioral deficits in hemi-parkinsonian rats. Exp. Neurol. 193, 181-197.
68. Prakash, R. S., Erickson, K. I., Colcombe, S. J., Kim, J., Sutton, B., and Kramer, A. F. (2010a). Age-related differences in the involvement of the prefrontal cortex in attentional control. Brain Cogn. 71, 328-335.
69. Prakash, R. S., Snook, E. M., Motl, R. W., and Kramer, A. F. (2010b). Aerobic ftness is associated with gray matter volume and white matter integrity in multiple sclerosis. Brain Res. 1341, 41-51.
70. Prakash, R. S., Snook, E. M., Erickson, K. I., Colcombe, S. J., Webb, M. L., Motl, R. W., and Kramer, A. F. (2007). Cardiorespiratory ftness: a predictor of cortical plasticity in multiple sclerosis. Neuroimage 34, 1238-1244.
71. Reuter-Lorenz, P. A., and Lustig, C. (2005). Brain aging: reorganizing discoveries about the aging mind. Curr. Opin. Neurobiol. 15, 245-251.
72. Reuter-Lorenz, P. A., and Mikels, J. (2006). "The aging brain: implications of enduring plasticity for behavioral and cultural change," in Lifespan Development and the Brain: The Perspective of Biocultural Co-Constructivism, eds P. Baltes, P. A. Reuter-Lorenz, and F. Roesler (Cambridge, UK: Cambridge University Press), 255-276.
73. Reuter-Lorenz, P., Jonides, J., Smith, E. S., Hartley, A., Miller, A., Marscheutz, C., and Koeppe, R. A. (2000). Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J. Cogn. Neurosci. 12, 174-187.
74. Reuter-Lorenz, P., Stanczak, L., and Miller, A. (1999). Neural recruitment and cognitive aging: two hemispheres are better than one, especially as you age. Psychol. Sci. 10, 494-500.
75. Rissman, J., Gazzaley, A., and D'Esposito, M. (2004). Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 23, 752-763.
76. Rypma, B., and D'Esposito, M. (2000). Isolating the neural mechanisms of age-related changes in human working memory. Nat. Neurosci. 3, 509-515.
77. Sheikh, J. I., and Yesavage, J. A. (1986). "Geriatric Depression Scale (GDS): recent evidence and development of a shorter version," in Clinical Gerontology: A Guide to Assessment and Intervention, ed. T. L. Brink (New York: The Haworth Press), 165-173.
78. Smith, S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143-155.
79. Stern, Y., Sano, M., Paulsen, J., and Mayeux, R. (1987). Modified mini-mental state examination: validity and reliability. Neurology 37, 179.
80. Swain, R. A., Harris, A. B., Wiener, E. C., Dutka, M. V., Morris, H. D., Theien, B. E., Konda, S., Engberg, K., Lauterbur, P. C., and Greenough, W. T. (2003). Prolonged exercise induces angio-genesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117, 1037-1046.
81. Trejo, J. L., Carro, E., and Torres-Aleman, I. (2001). Circulating insulin-like growth factor mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21, 1628-1634.
82. Van Essen, D. C. (2005). A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28, 635-662.
83. van Praag, H., Kempermann, G., and Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
84. van Praag, H., Shubert, T., Zhao, C., and Gage, F. H. (2005). Exercise enhances learning and hippocampal neuro-genesis in aged mice. J. Neurosci. 25, 8680-8685.
85. Vaynman, S., Ying, Z., and Gomez-Pinilla, F. (2004). Hippocampal BDNF mediates the effcacy of exercise on synap-tic plasticity and cognition. Eur. J. Neurosci. 20, 2580-2590.
86. Voss, M. W., Erickson, K. I., Prakash, R. S., Chaddock, L., Malkowski, E., Alves, H., Kim, J. S., Morris, K. S., White, S. M., Wójcicki, T. R., Hu, L., Szabo, A., Klamm, E., McAuley, E., and Kramer, A. F. (2010). Functional connectivity: a source of variance in the relationship between cardiorespiratory ftness and cognition. Neuropsychologia 48, 1394-1406.
87. Woolrich, M. W., Behrens, T. E., Beckmann, C. F., Jenkinson, M., and Smith, S. M. (2004). Multi-level linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21, 1732-1747.