A cognitive training intervention increases resting cerebral blood flow in healthy older adults

Frontiers in Human Neuroscience

Volumn 4, Issue , 2010, Pages

  Mozolic, Jennifer L ^a   Hayasaka, Satoru ^a   Laurienti, Paul J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Attention; Distraction; Perfusion; Randomized controlled trial

Indexed keywords

AGED; AGING; ARTICLE; BEHAVIOR MODIFICATION; BRAIN BLOOD FLOW; BRAIN PERFUSION; BRAIN SIZE; COGNITION; COGNITIVE TRAINING; CONTROLLED STUDY; DISTRACTIBILITY; EDUCATION PROGRAM; FEMALE; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PREFRONTAL CORTEX; RANDOMIZED CONTROLLED TRIAL; REST; SENSITIVITY ANALYSIS; SINGLE BLIND PROCEDURE; THERAPY;

EID: 77956279855     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/neuro.09.016.2010     Document Type: Article

References (98)

1. Alain, C., and Woods, D. L. (1999). Agerelated changes in processing auditory stimuli during visual attention: evidence for deficits in inhibitory control and sensory memory. Psychol. Aging 14, 507-519.
2. Arikuni, T., Sako, H., and Murata, A. (1994). Ipsilateral connections of the anterior cingulate cortex with the frontal and medial temporal cortices in the macaque monkey. Neurosci. Res. 21, 19-39.
3. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neuroimage 26, 839-851.
4. Asllani, I., Habeck, C., Borogovac, A., Brown, T. R., Brickman, A. M., and Stern, Y. (2009). Separating function from structure in perfusion imaging of the aging brain. Hum. Brain Mapp. 30, 2927-2935.
5. Ball, K., Berch, D. B., Helmers, K. F., Jobe, J. B., Leveck, M. D., Marsiske, M., Morris, J. N., Rebok, G. W., Smith, D. M., Tennstedt, S. L., Unverzagt, F. W., and Willis, S. L. (2002). Effects of cognitive training interventions with older adults: a randomized controlled trial. JAMA 288, 2271-2281.
6. Bangen, K. J., Restom, K., Liu, T. T., Jak, A. J., Wierenga, C. E., Salmon, D. P., and Bondi, M. W. (2007). Differential age effects on cerebral blood flow and BOLD response to encoding: associations with cognition and stroke risk. Neurobiol. Aging 30, 1276-1287.
7. Barbas, H., and Pandya, D. N. (1989). Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286, 353-375.
8. Beason-Held, L. L, Kraut, M. A., and Resnick, S. M. (2009). Stability of default-mode network activity in the aging brain. Brain Imaging Behav. 3, 123-131.
9. Bentourkia, M., Bol, A., Ivanoiu, A., Labar, D., Sibomana, M., Coppens, A., Michel, C., Cosnard, G., and De Volder, A. G. (2000). Comparison of regional cerebral blood flow and glucose metabolism in the normal brain: effect of aging. J. Neurol. Sci. 181, 19-28.
10. Bertsch, K., Hagemann, D., Hermes, M., Walter, C., Khan, R., and Naumann, E. (2009). Resting cerebral blood flow, attention, and aging. Brain Res. 1267, 77-88.
11. Bherer, L., Kramer, A. F., Peterson, M. S., Colcombe, S., Erickson, K., and Becic, E. (2008). Transfer effects in task-set cost and dual-task cost after dual-task training in older and younger adults: further evidence for cognitive plasticity in attentional control in late adulthood. Exp. Aging Res. 34, 188-219.
12. Bohn, M. J., Babor, T. F., and Kranzler, H. R. (1995). The Alcohol Use Disorders Identification Test (AUDIT): validation of a screening instrument for use in medical settings. J. Stud. Alcohol 56, 423.
13. Botvinick, M. M. (2007). Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn. Affect. Behav. Neurosci. 7, 356-366.
14. Boyke, J., Driemeyer, J., Gaser, C., Buchel, C., and May, A. (2008). Traininginduced brain structure changes in the elderly. J. Neurosci. 28, 7031-7035.
15. Bravo, G., and Hebert, R. (1997). Age and education specific reference values for the Mini-Mental and modified Mini-Mental State Examinations derived from a non-demented elderly population. Int. J. Geriatr. Psychiatry 12, 1008-1018.
16. Buckner, R. L. (2004). Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 44, 195-208.
17. Burgess, P. W., Gilbert, S. J., and Dumontheil, I. (2007). Function and localization within rostral prefrontal cortex (area 10). Philos. Trans. R. Soc. Lond., B, Biol. Sci. 362, 887-899.
18. Burgess, P. W., Quayle, A., and Frith, C. D. (2001). Brain regions involved in prospective memory as determined by positron emission tomography. Neuropsychologia 39, 545-555.
19. Burke, S. N., and Barnes, C. A. (2006). Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 7, 30-40.
20. Buschkuehl, M., Jaeggi, S. M., Hutchison, S., Perrig-Chiello, P., Däpp, C., Müller, M., Breil, F., Hoppeler, H., and Perrig, W. J. (2008). Impact of working memory training on memory performance in old-old adults. Psychol. Aging 23, 743.
21. 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.
22. Cabeza, R., Daselaar, S. M., Dolcos, F., Prince, S. E., Budde, M., and Nyberg, L. (2004). Task-independent and taskspecific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 14, 364-375.
23. Casanova, R., Srikanth, R., Baer, A., Laurienti, P. J., Burdette, J. H., Hayasaka, S., Flowers, L., Wood, F., and Maldjian, J. A. (2007). Biological parametric mapping: a statistical toolbox for multimodality brain image analysis. Neuroimage 34, 137-143.
24. Christoff, K., Ream, J. M., and Gabrieli, J. D. (2004). Neural basis of spontaneous thought processes. Cortex 40, 623-630.
25. Churchill, J. D., Galvez, R., Colcombe, S., Swain, R. A., Kramer, A. F., and Greenough, W. T. (2002). Exercise, experience and the aging brain. Neurobiol. Aging 23, 941-955.
26. 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.
27. 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 function in aging humans. Psychol. Aging 20, 363-375.
28. Colcombe, S. J., Kramer, A. F., Erickson, K. I., Scalf, P., McAuley, E., Cohen, N. J., Webb, A., Jerome, G. J., Marquez, D. X., and Elavsky, S. (2004). Cardiovascular fi tness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. U.S.A. 101, 3316-3321.
29. Corbetta, M., and Shulman, G. L. (2002). Control of goal-directed and stimulusdriven attention in the brain. Nat. Rev. Neurosci. 3, 201-215.
30. Dahlin, E., Nyberg, L., Backman, L., and Neely, A. S. (2008a). Plasticity of executive functioning in young and older adults: immediate training gains, transfer, and long-term maintenance. Psychol. Aging 23, 720.
31. Dahlin, E., Neely, A. S., Larsson, A., Backman, L., and Nyberg, L. (2008b). Transfer of learning after updating training mediated by the striatum. Science 320, 1510-1512.
32. Draganski, B., Gaser, C., Busch, V., Schuierer, G., Bogdahn, U., and May, A. (2004). Neuroplasticity: changes in grey matter induced by training. Nature 427, 311-312.
33. Draganski, B., Gaser, C., Kempermann, G., Kuhn, H. G., Winkler, J., Buchel, C., and May, A. (2006). Temporal and spatial dynamics of brain structure changes during extensive learning. J. Neurosci. 26, 6314-6317.
34. Dreher, J. C., Koechlin, E., Tierney, M., and Grafman, J. (2008). Damage to the fronto-polar cortex is associated with impaired multitasking. PLoS ONE 3:e3227. doi: 10.1371/journal. pone.0003227.
35. 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.
36. Eriksen, B. A., and Eriksen, C. W. (1974). Effects of noise letters upon the identifycation of a target letter in a nonsearch task. Percept. Psychophys. 16, 143-149.
37. Fassbender, C., Murphy, K., Foxe, J. J., Wylie, G. R., Javitt, D. C., Robertson, I. H., and Garavan, H. (2004). A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. Brain Res. Cogn. Brain Res. 20, 132.
38. 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., and Walhovd, K. B. (2009). High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 19, 2001-2012.
39. Golestani, N., and Zatorre, R. J. (2004). Learning new sounds of speech: reallocation of neural substrates. Neuroimage 21, 494.
40. Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., and Frackowiak, R. S. (2001). A voxelbased morphometric study of ageing in 465 normal adult human brains. Neuroimage 14, 21-36.
41. Grady, C. L. (1996). Age-related changes in cortical blood flow activation during perception and memory. Ann. N. Y. Acad. Sci. 777, 14-21.
42. Grady, C. L., McIntosh, A. R., and Craik, F. I. (2005). Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults. Neuropsychologia 43, 1466-1481.
43. Greenough, W. T., McDonald, J. W., Parnisari, R. M., and Camel, J. E. (1986). Environmental conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats. Brain Res. 380, 136-143.
44. Hugenschmidt, C. E., Mozolic, J. L., and Laurienti, P. J. (2009). Suppression of multisensory integration by modalityspecific attention in aging. Neuroreport 20, 349-353.
45. Hugenschmidt, C. E., Peiffer, A. M., Kraft, R. A., Casanova, R., Deibler, A. R., Burdette, J. H., Maldjian, J. A., and Laurienti, P. J. (2008). Relating imaging indices of white matter integrity and volume in healthy older adults. Cereb. Cortex 18, 433-442.
46. Hyde, K. L., Lerch, J., Norton, A., Forgeard, M., Winner, E., Evans, A. C., and Schlaug, G. (2009). Musical training shapes structural brain development. J. Neurosci. 29, 3019-3025.
47. Ilg, R., Wohlschlager, A. M., Gaser, C., Liebau, Y., Dauner, R., Woller, A., Zimmer, C., Zihl, J., and Muhlau, M. (2008). Gray matter increase induced by practice correlates with taskspecific activation: a combined functional and morphometric magnetic resonance imaging study. J. Neurosci. 28, 4210-4215.
48. Isingrini, M., Perrotin, A., and Souchay, C. (2008). Aging, metamemory regulation and executive functioning. Prog. Brain Res. 169, 377-392.
49. Jacobs, B., Schall, M., Prather, M., Kapler, E., Driscoll, L., Baca, S., Jacobs, J., Ford, K., Wainwright, M., and Treml, M. (2001). Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb. Cortex 11, 558-571.
50. Jennings, J., Webster, L., Kleykamp, B., and Dagenbach, D. (2005). Recollection training and transfer effects in older adults: successful use of a repetitionlag procedure. Aging Neuropsychol. Cogn. Neuropsychol. Dev. Cogn. 12, 278-298.
51. Jessberger, S., and Gage, F. H. (2008). Stem-cell-associated structural and functional plasticity in the aging hippocampus. Psychol. Aging 23, 684-691.
52. Kempermann, G., Gast, D., and Gage, F. H. (2002). Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by longterm environmental enrichment. Ann. Neurol. 52, 135-143.
53. Kim, S. G., and Tsekos, N. V. (1997). Perfusion imaging by a flow-sensitive alternating inversion recovery (FAIR) technique: application to functional brain imaging. Magn. Reson. Med. 37, 425-435.
54. Koechlin, E., Basso, G., Pietrini, P., Panzer, S., and Grafman, J. (1999). The role of the anterior prefrontal cortex in human cognition. Nature 399, 148-151.
55. Kramer, A. F., Bherer, L., Colcombe, S. J., Dong, W., and Greenough, W. T. (2004). Environmental infl uences on cognitive and brain plasticity during aging. J. Gerontol. A Biol. Sci. Med. Sci. 59, M940.
56. Kramer, A. F., Larish, J. F., and Strayer, D. L. (1995). Training for attentional control in dual task settings: a comparison of young and old adults. J. Exp. Psychol. Appl. 1, 50-76.
57. Langenecker, S. A., and Nielson, K. A. (2003). Frontal recruitment during response inhibition in older adults replicated with fMRI. Neuroimage 20, 1384.
58. Liu, T. T., and Brown, G. G. (2007). Measurement of cerebral perfusion with arterial spin labeling: part 1. Methods. J. Int. Neuropsychol. Soc. 13, 517-525.
59. Lopez-Luengo, B., and Vazquez, C. (2003). Effects of attention process training on cognitive functioning of schizophrenic patients. Psychiatry Res, 119, 41-53.
60. Luh, W. M., Wong, E. C., Bandettini, P. A., and Hyde, J. S. (1999). QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn. Reson. Med. 41, 1246-1254.
61. Mahncke, H. W., Connor, B. B., Appelman, J., Ahsanuddin, O. N., Hardy, J. L., Wood, R. A., Joyce, N. M., Boniske, T., Atkins, S. M., and Merzenich, M. M. (2006). Memory enhancement in healthy older adults using a brain plasticity-based training program: a randomized, controlled study. Proc. Natl. Acad. Sci. U.S.A. 103, 12523-12528.
62. Marchal, G., Rioux, P., Petit-Taboue, M. C., Sette, G., Travere, J. M., Le Poec, C., Courtheoux, P., Derlon, J. M., and Baron, J. C. (1992). Regional cerebral oxygen consumption, blood flow, and blood volume in healthy human aging. Arch. Neurol. 49, 1013-1020.
63. Martin, A. J., Friston, K. J., Colebatch, J. G., and Frackowiak, R. S. (1991). Decreases in regional cerebral blood flow with normal aging. J. Cereb. Blood Flow Metab. 11, 684-689.
64. May, A., Hajak, G., Ganssbauer, S., Steffens, T., Langguth, B., Kleinjung, T., and Eichhammer, P. (2007). Structural Brain Alterations following 5 Days of Intervention: Dynamic Aspects of Neuroplasticity. Cereb. Cortex 17, 205-210.
65. Mazoyer, B., Houde, O., Joliot, M., Mellet, E., and Tzourio-Mazoyer, N. (2009). Regional cerebral blood flow increases during wakeful rest following cognitive training. Brain Res. Bull. 80, 133-138.
66. Meltzer, C. C., Cantwell, M. N., Greer, P. J., Ben-Eliezer, D., Smith, G., Frank, G., Kaye, W. H., Houck, P. R., and Price, J. C. (2000). Does cerebral blood flow decline in healthy aging? A PET study with partial-volume correction. J. Nucl. Med. 41, 1842-1848.
67. Mora, F., Segovia, G., and del Arco, A. (2007). Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res. Rev. 55, 78-88.
68. Mozolic, J. L., Long, A. B., Morgan, A. R., Rawley-Payne, M., and Laurienti, P. J. (2009). A cognitive training intervention improves modality-specific attention in a randomized controlled trial of healthy older adults. Neurobiol. Aging. [Epub ahead of print].
69. Nyberg, L., Sandblom, J., Jones, S., Neely, A. S., Petersson, K. M., Ingvar, M., and Backman, L. (2003). Neural correlates of training-related memory improvement in adulthood and aging. Proc. Natl. Acad. Sci. U.S.A. 100, 13728-13733.
70. Olesen, P. J., Westerberg, H., and Klingberg, T. (2004). Increased prefrontal and parietal activity after training of working memory. Nat. Neurosci. 7, 75-79.
71. Park, D. C., Lautenschlager, G., Hedden, T., Davidson, N. S., Smith, A. D., and Smith, P. K. (2002). Models of visuospatial and verbal memory across the adult life span. Psychol. Aging 17, 299-320.
72. Parkes, L. M., Rashid, W., Chard, D. T., and Tofts, P. S. (2004). Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magn. Reson. Med. 51, 736-743.
73. Pereira, A. C., Huddleston, D. E., Brickman, A. M., Sosunov, A. A., Hen, R., McKhann, G. M., Sloan, R., Gage, F. H., Brown, T. R., and Small, S. A. (2007). An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 104, 5638-5643.
74. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
75. Ramnani, N., and owen, A. M. (2004). Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat. Rev. Neurosci. 5, 184-194.
76. Raz, N., Gunning-Dixon, F., Head, D., Rodrigue, K. M., Williamson, A., and Acker, J. D. (2004). Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol. Aging 25, 377-396.
77. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., and Acker, J. D. (2005). Regional brain changes in aging healthy adults: general trends, individual differences and modifi ers. Cereb. Cortex 15, 1676-1689.
78. Resnick, S. M., Pham, D. L., Kraut, M. A., Zonderman, A. B., and Davatzikos, C. (2003). Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J. Neurosci. 23, 3295-3301.
79. Reuter-Lorenz, P. A., Jonides, J., Smith, E. E., Hartley, A., Miller, A., Marshuetz, 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.
80. Rhodes, M. G. (2004). Age-related differences in performance on the Wisconsin card sorting test: a metaanalytic review. Psychol. Aging 19, 482-494.
81. Rowe, G., Valderrama, S., Hasher, L., and Lenartowicz, A. (2006). Attentional disregulation: a benefi t for implicit memory. Psychol. Aging 21, 826-830.
82. Rypma, B., Berger, J. S., Genova, H. M., Rebbechi, D., and D'Esposito, M. (2005). Dissociating age-related changes in cognitive strategy and neural efficiency using event-related fMRI. Cortex 41, 582-594.
83. Salat, D. H., Buckner, R. L., Snyder, A. Z., Greve, D. N., Desikan, R. S., Busa, E., Morris, J. C., Dale, A. M., and Fischl, B. (2004). Thinning of the cerebral cortex in aging. Cereb. Cortex 14, 721-730.
84. Salat, D. H., Greve, D. N., Pacheco, J. L., Quinn, B. T., Helmer, K. G., Buckner, R. L., and Fischl, B. (2009). Regional white matter volume differences in nondemented aging and Alzheimer's disease. Neuroimage 44, 1247-1258.
85. Salat, D. H., Tuch, D. S., Hevelone, N. D., Fischl, B., Corkin, S., Rosas, H. D., and Dale, A. M. (2005). Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann. N. Y. Acad. Sci. 1064, 37-49.
86. Shomstein, S., and Yantis, S. (2004). Control of attention shifts between vision and audition in human cortex. J. Neurosci. 24, 10702-10706.
87. Sohlberg, M. M., and Mateer, C. A. (1987). Effectiveness of an attention-training program. J. Clin. Exp. Neuropsychol. 9, 117-130.
88. Sohlberg, M. M., McLaughlin, K. A., Pavese, A., Heidrich, A., and Posner, M. I. (2000). Evaluation of attention process training and brain injuryeducation in persons with acquired brain injury. J. Clin. Exp. Neuropsychol. 22, 656-676.
89. Tellinghuisen, D. J., and Nowak, E. J. (2003). The inability to ignore auditory distractors as a function of visual task perceptual load. Percept. Psychophys. 65, 817-828.
90. Uludag, K., Dubowitz, D. J., Yoder, E. J., Restom, K., Liu, T. T., and Buxton, R. B. (2004). Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. Neuroimage 23, 148-155.
91. Velanova, K., Jacoby, L. L., Wheeler, M. E., McAvoy, M. P., Petersen, S. E., and Buckner, R. L. (2003). Functionalanatomic correlates of sustained and transient processing components engaged during controlled retrieval. J. Neurosci. 23, 8460-8470.
92. Verhaeghen, P., and Cerella, J. (2002). Aging, executive control, and attention: a review of meta-analyses. Neurosci. Biobehav. Rev. 26, 849-857.
93. Weissman, D. H., Warner, L. M., and Woldorff, M. G. (2004). The neural mechanisms for minimizing crossmodal distraction. J. Neurosci. 24, 10941-10949.
94. Willis, S. L., Tennstedt, S. L., Marsiske, M., Ball, K., Elias, J., Koepke, K. M., Morris, J. N., Rebok, G. W., Unverzagt, F. W., Stoddard, A. M., and Wright, E. (2006). Long-term effects of cognitive training on everyday functional outcomes in older adults. JAMA 296, 2805-2814.
95. Wong, E. C., Buxton, R. B., and Frank, L. R. (1998). Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn. Reson. Med. 39, 702-708.
96. Yang, L., and Hasher, L. (2007). The enhanced effects of pictorial distraction in older adults. J. Gerontol. B Psychol. Sci. Soc. Sci. 62:P230-233.
97. Yang, Y. (2002). Perfusion MR imaging with pulsed arterial spin-labeling: basic principles and applications in functional brain imaging. Concepts Magn. Reson. Imaging 14, 347-357.
98. Yang, Y., Frank, J. A., Hou, L., Ye, F. Q., McLaughlin, A. C., and Duyn, J. H. (1998). Multislice imaging of quantitative cerebral perfusion with pulsed arterial spin labeling. Magn. Reson. Med. 39, 825-832.