Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-26T15:53:36.459Z Has data issue: false hasContentIssue false
  • English
  • Français

The Effect of Self-Paced Exercise Intensity and Cardiorespiratory Fitness on Frontal Grey Matter Volume in Cognitively Normal Older Adults: A Randomised Controlled Trial

Published online by Cambridge University Press:  22 September 2021

Natalie J. Frost Open the ORCID record for Natalie J. Frost [Opens in a new window] ,
Michael Weinborn Open the ORCID record for Michael Weinborn [Opens in a new window] ,
Gilles E. Gignac ,
Ying Xia ,
Vincent Doré ,
Stephanie R. Rainey-Smith ,
Shaun Markovic ,
Nicole Gordon ,
Hamid R. Sohrabi  and
Simon M. Laws
...Show all authors
Natalie J. Frost*
Affiliation:
School of Psychological Science, University of Western Australia, Crawley, Western Australia, Australia School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia Ageing, Cognition and Exercise (ACE) Research Group, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
Michael Weinborn
Affiliation:
School of Psychological Science, University of Western Australia, Crawley, Western Australia, Australia Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
Gilles E. Gignac
Affiliation:
School of Psychological Science, University of Western Australia, Crawley, Western Australia, Australia
Ying Xia
Affiliation:
The Australian e-Health Research Centre, CSIRO Health and Biosecurity, Brisbane, Queensland, Australia
Vincent Doré
Affiliation:
The Australian e-Health Research Centre, CSIRO Health and Biosecurity, Brisbane, Queensland, Australia Department of Molecular Imaging and Therapy, Austin Health, 145 Studley Road, Heidelberg, Victoria, Australia
Stephanie R. Rainey-Smith
Affiliation:
School of Psychological Science, University of Western Australia, Crawley, Western Australia, Australia Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia Ageing, Cognition and Exercise (ACE) Research Group, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
Shaun Markovic
Affiliation:
School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia Ageing, Cognition and Exercise (ACE) Research Group, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
Nicole Gordon
Affiliation:
School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia
Hamid R. Sohrabi
Affiliation:
Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia School of Biomedical Sciences, Faculty of Medicine and Health Sciences, Macquarie University, New South Wales, Australia Centre for Healthy Ageing, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia
Simon M. Laws
Affiliation:
Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia Co-operative Research Centre for Mental Health, Carlton, Victoria, Australia Collaborative Genomics Group, School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia School of Biomedical Sciences, Faculty of Health Sciences, Curtin Health Innovation Research Institute, Curtin University, Bentley, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
Ralph N. Martins
Affiliation:
Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia School of Biomedical Sciences, Faculty of Medicine and Health Sciences, Macquarie University, New South Wales, Australia
Jeremiah J. Peiffer
Affiliation:
School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Ageing, Cognition and Exercise (ACE) Research Group, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia
Belinda M. Brown
Affiliation:
School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Australian Alzheimer’s Research Foundation, Sarich Neuroscience Research Institute, Nedlands, Western Australia, Australia Ageing, Cognition and Exercise (ACE) Research Group, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Centre for Healthy Ageing, School of Psychology and Exercise Science, Murdoch University, Murdoch, Western Australia, Australia Lifestyle Approaches towards Cognitive Health (LATCH) Research Group, Perth, Western Australia, Australia
*
*Correspondence and reprint requests to: Natalie J. Frost, School of Psychology & Exercise Science, Murdoch University, 90 South Street, Murdoch WA6150, Australia. Email: natalie.frost@murdoch.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Exercise has been found to be important in maintaining neurocognitive health. However, the effect of exercise intensity level remains relatively underexplored. Thus, to test the hypothesis that self-paced high-intensity exercise and cardiorespiratory fitness (peak aerobic capacity; VO2peak) increase grey matter (GM) volume, we examined the effect of a 6-month exercise intervention on frontal lobe GM regions that support the executive functions in older adults.

Methods:

Ninety-eight cognitively normal participants (age = 69.06 ± 5.2 years; n = 54 female) were randomised into either a self-paced high- or moderate-intensity cycle-based exercise intervention group, or a no-intervention control group. Participants underwent magnetic resonance imaging and fitness assessment pre-intervention, immediately post-intervention, and 12-months post-intervention.

Results:

The intervention was found to increase fitness in the exercise groups, as compared with the control group (F = 9.88, p = <0.001). Changes in pre-to-post-intervention fitness were associated with increased volume in the right frontal lobe (β = 0.29, p = 0.036, r = 0.27), right supplementary motor area (β = 0.30, p = 0.031, r = 0.29), and both right (β = 0.32, p = 0.034, r = 0.30) and left gyrus rectus (β = 0.30, p = 0.037, r = 0.29) for intervention, but not control participants. No differences in volume were observed across groups.

Conclusions:

At an aggregate level, six months of self-paced high- or moderate-intensity exercise did not increase frontal GM volume. However, experimentally-induced changes in individual cardiorespiratory fitness was positively associated with frontal GM volume in our sample of older adults. These results provide evidence of individual variability in exercise-induced fitness on brain structure.

Keywords

ExercisePhysical activityFitnessBrain volumeCognitionInterventionMRI
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 9 , October 2022 , pp. 902 - 915
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ABS. (2016). Australian Bureau of Statistics. Census of Population and Housing: Reflecting Australia - Stories from the Census, 2016. Retrieved from https://www.abs.gov.au/ausstats/abs@.nsf/Lookup/by%20Subject/2071.0˜2016˜Main%20Features˜Educational%20Qualifications%20Data%20Summary%20˜65 Google Scholar
Alosco, M. L., Brickman, A. M., Spitznagel, M. B., Griffith, E. Y., Narkhede, A., Raz, N., … Gunstad, J. (2013). Poorer physical fitness is associated with reduced structural brain integrity in heart failure. Journal of the Neurological Sciences, 328(1–2), 51–57. doi: 10.1016/j.jns.2013.02.015 CrossRefGoogle ScholarPubMed
Arenaza-Urquijo, E. M., Landeau, B., La Joie, R., Mevel, K., Mézenge, F., Perrotin, A., … Chételat, G. (2013). Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage, 83, 450–457. doi: 10.1016/j.neuroimage.2013.06.053 CrossRefGoogle ScholarPubMed
Banerjee, A., Chitnis, U. B., Jadhav, S. L., Bhawalkar, J. S., & Chaudhury, S. (2009). Hypothesis testing, type I and type II errors. Industrial Psychiatry Journal, 18(2), 127–131. doi: 10.4103/0972-6748.62274 CrossRefGoogle ScholarPubMed
Barde, Y. A. (1994). Neurotrophins: a family of proteins supporting the survival of neurons. Progress in Clinical and Biological Research, 390, 45–56.Google ScholarPubMed
Best, J. R., Chiu, B. K., Liang Hsu, C., Nagamatsu, L. S., & Liu-Ambrose, T. (2015). Long-Term Effects of Resistance Exercise Training on Cognition and Brain Volume in Older Women: Results from a Randomized Controlled Trial. Journal of the International Neuropsychological Society, 21(10), 745–756. doi: 10.1017/s1355617715000673 CrossRefGoogle ScholarPubMed
Boccardi, M., Bocchetta, M., Morency, F. C., Collins, D. L., Nishikawa, M., Ganzola, R., … Frisoni, G. B. (2015). Training labels for hippocampal segmentation based on the EADC-ADNI harmonized hippocampal protocol. Alzheimer’s & Dementia: The Journal of the Alzheimer’s Association, 11(2), 175–183. doi: 10.1016/j.jalz.2014.12.002 CrossRefGoogle ScholarPubMed
Borg, G. (1998). Borg’s perceived exertion and pain scales: Human kinetics.Google Scholar
Brockett, A. T., LaMarca, E. A., & Gould, E. (2015). Physical exercise enhances cognitive flexibility as well as astrocytic and synaptic markers in the medial prefrontal cortex. PLoS ONE, 10(5), e0124859. doi: 10.1371/journal.pone.0124859 CrossRefGoogle ScholarPubMed
Brown, B. M., Frost, N., Rainey-Smith, S. R., Doecke, J., Markovic, S., Gordon, N., … Peiffer, J. J. (2021). High-intensity exercise and cognitive function in cognitively normal older adults: a pilot randomised clinical trial. Alzheimer’s Research & Therapy, 13(1), 33. doi: 10.1186/s13195-021-00774-y CrossRefGoogle ScholarPubMed
Brown, B. M., Rainey-Smith, S. R., Castalanelli, N., Gordon, N., Markovic, S., Sohrabi, H. R., … Peiffer, J. J. (2017). Study protocol of the Intense Physical Activity and Cognition study: The effect of high-intensity exercise training on cognitive function in older adults. Alzheimer’s & Dementia: Translational Research & Clinical Interventions, 3(4), 562–570. doi: 10.1016/j.trci.2017.09.003 Google ScholarPubMed
Bugg, J. M., & Head, D. (2011). Exercise moderates age-related atrophy of the medial temporal lobe. Neurobiology of Aging, 32(3), 506–514. doi: 10.1016/j.neurobiolaging.2009.03.008 CrossRefGoogle ScholarPubMed
Cabral, D. F., Rice, J., Morris, T. P., Rundek, T., Pascual-Leone, A., & Gomes-Osman, J. (2019). Exercise for Brain Health: An Investigation into the Underlying Mechanisms Guided by Dose. Neurotherapeutics, 16(3), 580–599. doi: 10.1007/s13311-019-00749-w CrossRefGoogle Scholar
Cañas, A., Juncadella, M., Lau, R., Gabarrós, A., & Hernández, M. (2018). Working Memory Deficits After Lesions Involving the Supplementary Motor Area. Frontiers in Psychology, 9(765). doi: 10.3389/fpsyg.2018.00765 CrossRefGoogle ScholarPubMed
Chow, T. W. (2000). Personality in frontal lobe disorders. Current Psychiatry Reports, 2(5), 446–451. doi: 10.1007/s11920-000-0031-5 CrossRefGoogle ScholarPubMed
Colcombe, S., Erickson, K., Raz, N., Webb, A., Cohen, N., McAuley, E., & Kramer, A. F. (2003). Aerobic fitness reduces brain tissue loss in aging humans. Journals of Gerontology Series A-Biological Sciences And Medical Sciences, 58(2), 176–180.CrossRefGoogle ScholarPubMed
Colcombe, S., Erickson, K., Scalf, P., Kim, J., Prakash, R., McAuley, E., … Kramer, A. F. (2006). Aerobic Exercise Training Increases Brain Volume in Aging Humans. In (Vol. 61, pp. 1166–1170): Oxford University Press.Google Scholar
Colcombe, S., & Kramer, A. F. (2003). Fitness Effects on the Cognitive Function of Older Adults: A Meta-Analytic Study. Psychological Science, 14(2), 125–130. doi: 10.1111/1467-9280.t01-1-01430 CrossRefGoogle ScholarPubMed
Cotman, C. W., & Berchtold, N. C. (2002). Exercise: a behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences, 25(6), 295–301. doi: 10.1016/s0166-2236(02)02143-4 CrossRefGoogle Scholar
Davidson, P. S. R., Gao, F. Q., Mason, W. P., Winocur, G., & Anderson, N. D. (2008). Verbal fluency, Trail Making, and Wisconsin Card Sorting Test performance following right frontal lobe tumor resection. Journal of Clinical and Experimental Neuropsychology, 30(1), 18–32. doi: 10.1080/13803390601161166 CrossRefGoogle ScholarPubMed
Davis, J. C., Liu-Ambrose, T., Marra, C. A., & Najafzadeh, M. (2010). The independent contribution of executive functions to health related quality of life in older women. BMC Geriatrics, 10(1). doi: 10.1186/1471-2318-10-16 CrossRefGoogle ScholarPubMed
Erickson, K., Leckie, R. L., & Weinstein, A. M. (2014). Physical activity, fitness, and gray matter volume. Neurobiology of Aging, 35, S20–S28. doi: 10.1016/j.neurobiolaging.2014.03.034 CrossRefGoogle ScholarPubMed
Erickson, K., Voss, M., Prakash, R., Basak, C., Szabo, A., Chaddock, L., … Kramer, A. (2011). Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences, USA, 108(7), 3017–3022.CrossRefGoogle ScholarPubMed
Fisk, J. E., & Sharp, C. A. (2004). Age-Related Impairment in Executive Functioning: Updating, Inhibition, Shifting, and Access. Journal of Clinical and Experimental Neuropsychology, 26(7), 874–890. doi: 10.1080/13803390490510680 CrossRefGoogle ScholarPubMed
Fjell, A. M., & Walhovd, K. B. (2010). Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci, 21(3), 187–221. doi: 10.1515/revneuro.2010.21.3.187 CrossRefGoogle ScholarPubMed
Flöel, A., Ruscheweyh, R., Krüger, K., Willemer, C., Winter, B., Völker, K., … Knecht, S. (2010). Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link? Neuroimage, 49(3), 2756–2763. doi: 10.1016/j.neuroimage.2009.10.043 CrossRefGoogle ScholarPubMed
Frost, N., Weinborn, M., Gignac, G., Rainey-Smith, S. R., Markovic, S., Gordon, N., … Brown, B. M. (2020). A Randomized Controlled Trial of High Intensity Exercise and Executive Functioning in Cognitively Normal Older Adults. The American Journal of Geriatric Psychiatry. doi:https://doi.org/10.1016/j.jagp.2020.06.015 Google ScholarPubMed
Frost, N., Weinborn, M., Gignac, G. E., Markovic, S., Rainey-Smith, S. R., Sohrabi, H. R., … Brown, B. M. (2019). Higher Cardiorespiratory Fitness Is Associated With Better Verbal Generativity in Community-Dwelling Older Adults. Journal of Aging and Physical Activity, 1–8. doi: 10.1123/japa.2018-0382 Google ScholarPubMed
Füzéki, E., & Banzer, W. (2018). Physical activity recommendations for health and beyond in currently inactive populations. International Journal of Environmental Research and Public Health, 15(5), 1042. doi: 10.3390/ijerph15051042 CrossRefGoogle ScholarPubMed
Hamer, M., & Batty, G. D. (2019). Association of body mass index and waist-to-hip ratio with brain structure: UK Biobank study. Neurology, 92(6), e594–e600. doi: 10.1212/wnl.0000000000006879 CrossRefGoogle ScholarPubMed
Harms, M. P., Wang, L., Campanella, C., Aldridge, K., Moffitt, A. J., Kuelper, J., … Csernansky, J. G. (2010). Structural abnormalities in gyri of the prefrontal cortex in individuals with schizophrenia and their unaffected siblings. The British Journal of Psychiatry, 196(2), 150–157. doi: 10.1192/bjp.bp.109.067314 CrossRefGoogle ScholarPubMed
Hertzog, C., Kramer, A. F., Wilson, R. S., & Lindenberger, U. (2008). Enrichment Effects on Adult Cognitive Development: Can the Functional Capacity of Older Adults Be Preserved and Enhanced? Psychological science in the public interest : a journal of the American Psychological Society, 9(1), 1. doi: 10.1111/j.1539-6053.2009.01034.x CrossRefGoogle ScholarPubMed
Hoaglin, D. C., & Iglewicz, B. (1987). Fine-Tuning Some Resistant Rules for Outlier Labeling. Journal of the American Statistical Association, 82(400), 1147–1149. doi: 10.1080/01621459.1987.10478551 CrossRefGoogle Scholar
Hopkins, M. E., Nitecki, R., & Bucci, D. J. (2011). Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic factor levels. Neuroscience, 194, 84–94. doi: 10.1016/j.neuroscience.2011.07.071 CrossRefGoogle ScholarPubMed
Izzicupo, P., apos, Amico, M. A., Di Blasio, A., Napolitano, G., Nakamura, F. Y., … Ghinassi, B. (2017). Aerobic training improves angiogenic potential independently of vascular endothelial growth factor modifications in postmenopausal women. Frontiers in Endocrinology, 8, 363. doi: 10.3389/fendo.2017.00363 CrossRefGoogle ScholarPubMed
Joo, M. S., Park, D. S., Moon, C. T., Chun, Y. I., Song, S. W., & Roh, H. G. (2016). Relationship between Gyrus Rectus Resection and Cognitive Impairment after Surgery for Ruptured Anterior Communicating Artery Aneurysms. Journal of Cerebrovascular and Endovascular Neurosurgery, 18(3), 223–228. doi: 10.7461/jcen.2016.18.3.223 CrossRefGoogle ScholarPubMed
Knutson, K. M., Dal Monte, O., Schintu, S., Wassermann, E. M., Raymont, V., Grafman, J., & Krueger, F. (2015). Areas of Brain Damage Underlying Increased Reports of Behavioral Disinhibition. The Journal of Neuropsychiatry and Clinical Neurosciences, 27(3), 193–198. doi: 10.1176/appi.neuropsych.14060126 CrossRefGoogle ScholarPubMed
Lezak, M. D. (2012). Neuropsychological assessment (5th ed.). Oxford: Oxford University Press.Google Scholar
Lima, C. F., Krishnan, S., & Scott, S. K. (2016). Roles of Supplementary Motor Areas in Auditory Processing and Auditory Imagery. Trends in Neurosciences, 39(8), 527–542. doi: 10.1016/j.tins.2016.06.003 CrossRefGoogle ScholarPubMed
Mallery, P., & George, D. (2016). IBM SPSS Statistics 23 Step by Step A Simple Guide and Reference. Abingdon: Taylor and Francis.Google Scholar
Mandyam, C. D., Wee, S., Eisch, A. J., Richardson, H. N., & Koob, G. F. (2007). Methamphetamine Self-Administration and Voluntary Exercise Have Opposing Effects on Medial Prefrontal Cortex Gliogenesis. Journal of Neuroscience, 27(42), 11442–11450. doi: 10.1523/jneurosci.2505-07.2007 CrossRefGoogle ScholarPubMed
McAllister, A. K., Katz, L. C., & Lo, D. C. (1999). Neurotrophins and synaptic plasticity. Annual Review of Neuroscience, 22(1), 295–318. doi: 10.1146/annurev.neuro.22.1.295 CrossRefGoogle ScholarPubMed
Miyake, A., & Friedman, N. (2012). The Nature and Organization of Individual Differences in Executive Functions: Four General Conclusions. Current Directions in Psychological Science, 21(1), 8–14. doi: 10.1177/0963721411429458 CrossRefGoogle ScholarPubMed
Mohammady, M., Sadeghi, M., & Janani, L. (2017). Intention to treat analysis in randomized clinical trials: A review. HAYAT, 23(2), 138–151.Google Scholar
Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., … Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment. Journal of the American Geriatrics Society, 53(4), 695–699. doi: 10.1111/j.1532-5415.2005.53221.x CrossRefGoogle ScholarPubMed
Niemann, C., Godde, B., & Voelcker-Rehage, C. (2014). Not only cardiovascular, but also coordinative exercise increases hippocampal volume in older adults. Frontiers In Aging Neuroscience, 6, 170. doi: 10.3389/fnagi.2014.00170 CrossRefGoogle ScholarPubMed
Reifman, A., & Keyton, K. (2010). Winsorize. Encyclopedia of research design, 1636–1638.Google Scholar
Reiter, K., Nielson, K. A., Smith, T. J., Weiss, L. R., Alfini, A. J., & Smith, J. C. (2015). Improved Cardiorespiratory Fitness Is Associated with Increased Cortical Thickness in Mild Cognitive Impairment. Journal of the International Neuropsychological Society : JINS, 21(10), 757–767. doi: 10.1017/S135561771500079X CrossRefGoogle ScholarPubMed
Rueda, A., Acosta, O., Couprie, M., Bourgeat, P., Fripp, J., Dowson, N., … Salvado, O. (2010). Topology-corrected segmentation and local intensity estimates for improved partial volume classification of brain cortex in MRI. Journal of Neuroscience Methods, 188(2), 305–315. doi: 10.1016/j.jneumeth.2010.02.020 CrossRefGoogle ScholarPubMed
Ruscheweyh, R., Willemer, C., Krüger, K., Duning, T., Warnecke, T., Sommer, J., … Flöel, A. (2011). Physical activity and memory functions: an interventional study. Neurobiol Aging, 32(7), 1304–1319. doi: 10.1016/j.neurobiolaging.2009.08.001 CrossRefGoogle Scholar
Schinder, A. F., & Poo, M.-m. (2000). The neurotrophin hypothesis for synaptic plasticity. In Trends in Neurosciences (Vol. 23, pp. 639–645). England: Elsevier Ltd.Google Scholar
Stein, A. M., Silva, T. M. V., Coelho, F. G. d. M., Arantes, F. J., Costa, J. L. R., Teodoro, E., & Santos-Galduróz, R. F. (2018). Physical exercise, IGF-1 and cognition: A systematic review of experimental studies in the elderly. Dementia e Neuropsychologia, 12(2), 114–122. doi: 10.1590/1980-57642018dn12-020003 CrossRefGoogle ScholarPubMed
Stillman, C. M., Esteban-Cornejo, I., Brown, B., Bender, C. M., & Erickson, K. I. (2020). Effects of Exercise on Brain and Cognition Across Age Groups and Health States. Trends in Neurosciences. doi: 10.1016/j.tins.2020.04.010 CrossRefGoogle ScholarPubMed
Van Leemput, K., Maes, F., Vandermeulen, D., & Suetens, P. (1999). Automated model-based tissue classification of MR images of the brain. IEEE Transactions on Medical Imaging, 18(10), 897–908. doi: 10.1109/42.811270 CrossRefGoogle ScholarPubMed
Weinstein, A. M., Voss, M. W., Prakash, R. S., Chaddock, L., Szabo, A., White, S. M., … Erickson, K. I. (2012). The association between aerobic fitness and executive function is mediated by prefrontal cortex volume. Brain Behavior and Immunity, 26(5), 811–819. doi: 10.1016/j.bbi.2011.11.008 CrossRefGoogle ScholarPubMed
Winter, J. E., MacInnis, R. J., Wattanapenpaiboon, N., & Nowson, C. A. (2014). BMI and all-cause mortality in older adults: A meta-analysis. American Journal of Clinical Nutrition, 99(4), 875–890. doi: 10.3945/ajcn.113.068122 CrossRefGoogle ScholarPubMed
Wolz, R., Aljabar, P., Hajnal, J. V., Hammers, A., & Rueckert, D. (2010). LEAP: Learning embeddings for atlas propagation. Neuroimage, 49(2), 1316–1325. doi: 10.1016/j.neuroimage.2009.09.069 CrossRefGoogle ScholarPubMed
Supplementary material: File

Frost et al. supplementary material

Frost et al. supplementary material

Download Frost et al. supplementary material(File)
File 32.9 KB