Hippocampal and cerebral blood flow after exercise cessation in master athletes

Frontiers in Aging Neuroscience

Volumn 8, Issue AUG, 2016, Pages

  Alfini, Alfonso J ^a   Weiss, Lauren R ^a   Leitner, Brooks P ^a   Smith, Theresa J ^a   Hagberg, James M ^a   Smith, J Carson ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Aerobic fitness; Arterial spin labeling; Athlete; Cerebral blood flow; Cerebrovascular health; Healthy older adults; Hippocampus; MRI

Indexed keywords

ADULT; ARTERIAL SPIN LABELING; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDURANCE TRAINING; FUSIFORM GYRUS; GRAY MATTER; HUMAN; INFERIOR PARIETAL LOBULE; INFERIOR TEMPORAL GYRUS; LINGUAL GYRUS; MIDDLE AGED; PERFUSION WEIGHTED IMAGING; PRECUNEUS; RIGHT HIPPOCAMPUS; RUNNING; SCREENING; TONSIL; TRAINING;

EID: 84990043612     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2016.00184     Document Type: Article

References (51)

1. Alsop, D. C., Detre, J. A., Golay, X., Günther, M., Hendrikse, J., and Zaharchuk, G. (2014). Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the european consortium for ASL in dementia. Magn. Reson. Med. 116, 102-116. doi: 10.1002/mrm.25197
2. Binder, J. R., Desai, R. H., Graves, W. W., and Conant, L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767-2796. doi: 10.1093/cercor/bhp055
3. Brooks, G., Fahey, T., and White, T. (1996). Exercise Physiology: Human Bioenergetics and Its Applications. Mountain View, CA: Mayfield Publishing Company.
4. Buckner, R. L., Snyder, A. Z., Shannon, B. J., LaRossa, G., Sachs, R., and Mintun, M. A. (2005). Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 25, 7709-7717. doi: 10.1523/jneurosci.2177-05.2005
5. Buxton, R. B. (2005). Quantifying CBF with arterial spin labeling. J. Magn. Reson. Imaging 22, 723-726. doi: 10.1002/jmri.20462
6. Buxton, R. B., Frank, L. R., Wong, E. C., Siewert, B., Warach, S., and Edelman, R. R. (1998). A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn. Reson. Med. 40, 383-396. doi: 10.1002/mrm.1910400308
7. Chapman, S. B., Aslan, S., Spence, J. S., DeFina, L. F., Keebler, M. W., and Lu, H. (2013). Shorter term aerobic exercise improves brain, cognition, and cardiovascular fitness in aging. Front. Aging Neurosci. 5:75. doi: 10.3389/fnagi.2013.00075
8. Chappell, M. A. (2014). Arterial Spin Labeling: Non-Invasive Measurement of Perfusion. FSL Arterial Spin Labelling. 1-76. Available online at: http://fsl.fmrib.ox.ac.uk/fslcourse/physics+apps/FSL_arterial_spin_labelling.pdf
9. Chappell, M. A., Groves, A., and Woolrich, M. W. (2009). Variational bayesian inference for a nonlinear forward model. IEEE Trans. Signal Process. 57, 223-236. doi: 10.1109/TSP.2008.2005752
10. Chappell, M. A., Groves, A. R., MacIntosh, B. J., Donahue, M. J., Jezzard, P., and Woolrich, M. W. (2011). Partial volume correction of multiple inversion time arterial spin labeling MRI data. Magn. Reson. Med. 65, 1173-1183. doi: 10.1002/mrm.22641
11. Convertino, V. A. (1991). Blood volume: its adaptation to endurance training. Med. Sci. Sport Exerc. 23, 1338-1348. doi: 10.1249/00005768-199112000-00004
12. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173. doi: 10.1006/cbmr.1996.0014
13. Coyle, E. F., Hemmert, M. K., and Coggan, A. R. (1986). Effects of detraining on cardiovascular responses to exercise: role of blood volume. J. Appl. Physiol. 60, 95-99.
14. Davranche, K., and McMorris, T. (2009). Specific effects of acute moderate exercise on cognitive control. Brain Cogn. 69, 565-570. doi: 10.1016/j.bandc.2008.12.001
15. Erickson, K. I., Prakash, R. S., Voss, M. W., Chaddock, L., Hu, L., and Kramer, A. F. (2009). Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19, 1030-1039. doi: 10.1002/hipo.20547
16. Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355. doi: 10.1016/s0896-6273(02)00569-x
17. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198. doi: 10.1016/0022-3956(75)90026-6
18. Greicius, M. D., Srivastava, G., Reiss, A. L., and Menon, V. (2004). Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A. 101, 4637-4642. doi: 10.1073/pnas.0308627101
19. Groves, A. R., Chappell, M. A., and Woolrich, M. W. (2009). Combined spatial and non-spatial prior for inference on MRI time-series. Neuroimage 45, 795-809. doi: 10.1016/j.neuroimage.2008.12.027
20. Hall, W., and Degenhardt, L. (2008). SPM8-Statistical Parametric Mapping, World Psychiatry: Official Journal of the World Psychiatric Association (WPA). Available online at: http://www.fil.ion.ucl.ac.uk/spm/software/spm8/
21. Hoekstra, T., Boreham, C. A., Murray, L. J., and Twisk, J. W. R. (2008). Associations between aerobic and muscular fitness and cardiovascular disease risk: the northern Ireland young hearts study. J. Phys. Act. Health 5, 815-829.
22. Intlekofer, K. A., and Cotman, C. W. (2013). Exercise counteracts declining hippocampal function in aging and Alzheimer's disease. Neurobiol. Dis. 57, 47-55. doi: 10.1016/j.nbd.2012.06.011
23. Klausen, K., Andersen, L. B., and Pelle, I. (1981). Adaptive changes in work capacity, skeletal muscle capillarization and enzyme levels during training and detraining. Acta Physiol. Scand. 113, 9-16. doi: 10.1111/j.1748-1716.1981.tb06854.x
24. Kramer, A. F., Colcombe, S. J., McAuley, E., Scalf, P. E., and Erickson, K. I. (2005). Fitness, aging and neurocognitive function. Neurobiol. Aging 26(Suppl. 1), 124-127. doi: 10.1016/j.neurobiolaging.2005.09.009
25. MacIntosh, B. J., Crane, D. E., Sage, M. D., Rajab, A. S., Donahue, M. J., and Middleton, L. E. (2014). Impact of a single bout of aerobic exercise on regional brain perfusion and activation responses in healthy young adults. PLoS ONE 9:e85163. doi: 10.1371/journal.pone.0085163
26. Mcguire, D. K., Levine, B. D., Williamson, J. W., Snell, P. G., Gunnar, C., and Mitchell, J. H. (2001). A 30-year follow-up of the Dallas bed rest and training study I. Effect of age on the cardiovascular response to exercise. Circulation 104, 1350-1357. doi: 10.1161/hc3701.096099
27. Monsch, A. U., Bondi, M. W., Butters, N., Salmon, D. P., Katzman, R., and Thal, L. J. (1992). Comparisons of verbal fluency tasks in the detection of dementia of the Alzheimer type. Arch. Neurol. 49, 1253-1258. doi: 10.1001/archneur.1992.00530360051017
28. Mujika, I., and Padilla, S. (2000a). Detraining: loss of training-induced physiological and performance adaptations. Part II: long term insufficient training stimulus. Sports Med. 30, 145-154. doi: 10.2165/00007256-200030030-00001
29. Mujika, I., and Padilla, S. (2000b). Detraining: loss of training-induced physiological and performance adaptations. Part, I. Sports Med. 30, 79-87. doi: 10.2165/00007256-200030020-00002
30. Mujika, I., and Padilla, S. (2001a). Muscular characteristics of detraining in humans. Med. Sci. Sports Exerc. 33, 1297-1303. doi: 10.1097/00005768-200108000-00009
31. Mujika, I., and Padilla, S. (2001b). Cardiorespiratory and metabolic characteristics of detraining in humans (Caracteristiques cardiorespiratoires et metaboliques du desentrainement chez les humains). Med. Sci. Sports Exerc. 33, 413-421. doi: 10.1097/00005768-200103000-00013
32. Pereira, A. C., Huddleston, D. E., Brickman, A. M., Sosunov, A. A., Hen, R., and Brown, T. R. (2007). An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 104, 5638-5643. doi: 10.1073/pnas.0611721104
33. Petrella, J. R., Sheldon, F. C., Prince, S. E., Calhoun, V. D., and Doraiswamy, P. M. (2011). Default mode network connectivity in stable vs progressive mild cognitive impairment. Neurology 76, 511-517. doi: 10.1212/wnl.0b013e31820af94e
34. 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. doi: 10.1073/pnas.98.2.676
35. Rhyu, I. J., Bytheway, J. A., Kohler, S. J., Lange, H., Lee, K. J., and Cameron, J. L. (2010). Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 167, 1239-1248. doi: 10.1016/j.neuroscience.2010.03.003
36. Rogers, M. A., King, D. S., Hagberg, J. M., Ehsani, A. A., and Holloszy, J. O. (1990). Effect of 10 days of physical inactivity on glucose tolerance in master athletes. J. Appl. Physiol. (1985) 68, 1833-1837.
37. Saltin, B., Blomqvist, G., Mitchell, J. H., Johnson, R. L., Wildenthal, K., and Chapman, C. B. (1968). Response to exercise after bed rest and after training. Circulation 38, 71-78.
38. Sawada, S., Miyachi, M., Murakami, H., Kawakami, R., Tanaka, S., Ishikawa-Takata, K., et al. (2012). Dose-response relationship between cardiorespiratory fitness and morbidity/mortality: A systematic review and meta-analysis. J. Sci. Med. Sport 15, S25. doi: 10.1016/j.jsams.2012.11.061
39. Seals, D. R., Hagberg, J. M., Hurley, B. F., Ehsani, A. A., Holloszy, J. O., and Hagberg, J. M. (1981). Endurance training in older men and women. I. Cardiovascular responses to exercise. J. Neurol. 234, 634-640.
40. Sheline, Y. I., Raichle, M. E., Snyder, A. Z., Morris, J. C., Head, D., and Mintun, M. A. (2010). Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol. Psychiatry 67, 584-587. doi: 10.1016/j.biopsych.2009.08.024
41. Smith, J. C., Nielson, K. A., Antuono, P. J., Lyons, A., Hanson, R. J., and Verber, M. D. (2013). Semantic memory functional MRI and cognitive function after exercise intervention in mild cognitive impairment. J. Alzheimers Dis. 37, 197-215. doi: 10.3233/JAD-130467
42. Smith, J. C., Nielson, K. A., Woodard, J. L., Seidenberg, M., Durgerian, S., and Rao, S. M. (2014). Physical activity reduces hippocampal atrophy in elders at genetic risk for Alzheimer's disease. Front. Aging Neurosci. 6:61. doi: 10.3389/fnagi.2014.00061
43. Smith, J. C., Paulson, E. S., Cook, D. B., Verber, M. D., and Tian, Q. (2010). Detecting changes in human cerebral blood flow after acute exercise using arterial spin labeling: implications for fMRI. J. Neurosci. Methods 191, 258-262. doi: 10.1016/j.jneumeth.2010.06.028
44. Swain, R. A., Harris, A. B., Wiener, E. C., Dutka, M. V., Morris, H. D., and Greenough, W. T. (2003). Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117, 1037-1046. doi: 10.1016/S0306-4522(02)00664-4
45. ten Brinke, L. F., Bolandzadeh, N., Nagamatsu, L. S., Hsu, C. L., Davis, J. C., Miran-Khan, K., et al. (2015). Aerobic exercise increases hippocampal volume in older women with probable mild cognitive impairment: a 6-month randomised controlled trial. Br. J. Sports Med. 49, 248-254. doi: 10.1136/bjsports-2013-093184
46. Thomas, B. P., Yezhuvath, U. S., Tseng, B. Y., Liu, P., Levine, B. D, and Lu, H. (2013). Life-long aerobic exercise preserved baseline cerebral blood flow but reduced vascular reactivity to CO2. J. Magn. Reson. Imaging 38, 1177-1183. doi: 10.1002/jmri.24090
47. Tomporowski, P. D. (2003). Effects of acute bouts of exercise on cognition. Acta Psychol. (Amst.) 112, 297-324. doi: 10.1016/S0001-6918(02)00134-8
48. 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. doi: 10.1038/6368
49. Voss, M. W., Prakash, R. S., Erickson, K. I., Basak, C., Chaddock, L., and Kramer, A. F. (2010). Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front. Aging Neurosci. 2:32. doi: 10.3389/fnagi.2010.00032
50. Woolrich, M. W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., and Smith, S. M. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage 45, S173-S186. doi: 10.1016/j.neuroimage.2008.10.055
51. Yoshiura, T., Hiwatashi, A., Yamashita, K., Ohyagi, Y., Monji, A., Takayama, Y., et al. (2009). Simultaneous measurement of arterial transit time, arterial blood volume, and cerebral blood flow using arterial spin-labeling in patients with Alzheimer disease. Am. J. Neuroradiol. 30, 1388-1393. doi: 10.3174/ajnr.A1562