Changes in Cortical Activation Patterns in Language Areas following an Aerobic Exercise Intervention in Older Adults
Joe Nocera, Bruce Crosson, Kevin Mammino, Keith M McGregor, Joe Nocera, Bruce Crosson, Kevin Mammino, Keith M McGregor
Abstract
Previous work has shown that older adults who evidence increased right inferior frontal gyrus (IFG) activity during language tasks show decreased sematic verbal fluency performance. The current study sought to evaluate if an aerobic exercise intervention can alter patterns of brain activity during a semantic verbal fluency task assessed by functional magnetic resonance imaging (fMRI). Thirty-two community-dwelling, sedentary older adults were enrolled to a 12-week aerobic "Spin" exercise group or a 12-week nonaerobic exercise control condition (Balance). Thirty participants completed their assigned intervention (16 Spin; 14 Balance) with pre- and postintervention assessments of a semantic verbal fluency task during fMRI and estimated VO2max testing. There was a significant increase in the change scores for estimated VO2max of the Spin group when compared to the Balance group. Semantic verbal fluency output within the scanner was also improved in the Spin group as compared to controls at postassessment. Group fMRI comparisons of IFG activity showed lower activity in the right IFG following the intervention in the aerobic Spin group when compared to the Balance group. Regression analysis of imaging data with change in both estimated VO2max and semantic verbal fluency was negatively correlated with activity in right IFG. The current work is registered as clinical trial with NCT01787292 and NCT02787655.
Conflict of interest statement
The authors report no financial conflict of interests.
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References
- Kramer A. F., Hahn S., Cohen N. J., et al. Ageing, fitness and neurocognitive function. Nature. 1999;400(6743):418–419. doi: 10.1038/22682.
- Voss M. W., Erickson K. I., Prakash R. S., et al. Neurobiological markers of exercise-related brain plasticity in older adults. Brain, Behavior, and Immunity. 2013;28:90–99. doi: 10.1016/j.bbi.2012.10.021.
- Voss M. W., Weng T. B., Burzynska A. Z., et al. Fitness, but not physical activity, is related to functional integrity of brain networks associated with aging. NeuroImage. 2016;131:113–125. doi: 10.1016/j.neuroimage.2015.10.044.
- Colcombe S., Kramer A. F. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychological Science. 2003;14(2):125–130. doi: 10.1111/1467-9280.t01-1-01430.
- Voelcker-Rehage C., Godde B., Staudinger U. M. Cardiovascular and coordination training differentially improve cognitive performance and neural processing in older adults. Frontiers in Human Neuroscience. 2011;5, article no. 26 doi: 10.3389/fnhum.2011.00026.
- Nocera J. R., McGregor K. M., Hass C. J., Crosson B. Spin exercise improves semantic fluency in previously sedentary older adults. Journal of Aging and Physical Activity. 2015;23(1):90–94. doi: 10.1123/JAPA.2013-0107.
- Prakash R. S., Voss M. W., Erickson K. I., et al. Cardiorespiratory fitness and attentional control in the aging brain. Frontiers in Human Neuroscience. 2011;4, article 229
- Erickson K. I., Voss M. W., Prakash R. S., et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(7):3017–3022. doi: 10.1073/pnas.1015950108.
- Voss M. W., Prakash R. S., Erickson K. I., et al. Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Frontiers in Aging Neuroscience. 2010;2, article 32 doi: 10.3389/fnagi.2010.00032.
- Zlatar Z. Z., Towler S., McGregor K. M., et al. Functional language networks in sedentary and physically active older adults. Journal of the International Neuropsychological Society. 2013;19(6):625–634. doi: 10.1017/s1355617713000246.
- Zlatar Z. Z., McGregor K. M., Towler S., Nocera J. R., Dzierzewski J. M., Crosson B. Self-reported physical activity and objective aerobic fitness: differential associations with gray matter density in healthy aging. Frontiers in Aging Neuroscience. 2015;7, article 5 doi: 10.3389/fnagi.2015.00005.
- Mang C. S., Brown K. E., Neva J. L., Snow N. J., Campbell K. L., Boyd L. A. Promoting motor cortical plasticity with acute aerobic exercise: a role for cerebellar circuits. Neural Plasticity. 2016;2016:12. doi: 10.1155/2016/6797928.6797928
- Singh A. M., Duncan R. E., Neva J. L., Staines W. R. Aerobic exercise modulates intracortical inhibition and facilitation in a nonexercised upper limb muscle. BMC Sports Science, Medicine and Rehabilitation. 2014;6(1, article no. 23) doi: 10.1186/2052-1847-6-23.
- Meinzer M., Seeds L., Flaisch T., et al. Impact of changed positive and negative task-related brain activity on word-retrieval in aging. Neurobiology of Aging. 2012;33(4):656–669. doi: 10.1016/j.neurobiolaging.2010.06.020.
- Golding L. A., Sinning W. E. Y's Way to Physical Fitness: The Complete Guide to Fitness Testing and Instruction. 3rd. YMCA of the USA, Human Kinetics Publishers; 1989.
- Lutkenhoff E. S., Rosenberg M., Chiang J., et al. Optimized brain extraction for pathological brains (optiBET) PLOS ONE. 2014;9(12) doi: 10.1371/journal.pone.0115551.e115551
- Chen G., Adleman N. E., Saad Z. S., Leibenluft E., Cox R. W. Applications of multivariate modeling to neuroimaging group analysis: a comprehensive alternative to univariate general linear model. NeuroImage. 2014;99:571–588. doi: 10.1016/j.neuroimage.2014.06.027.
- Eklund A., Nichols T. E., Knutsson H. Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(28):7900–7905. doi: 10.1073/pnas.1602413113.
- Meinzer M., Lindenberg R., Sieg M. M., Nachtigall L., Ulm L., Flöel A. Transcranial direct current stimulation of the primary motor cortex improves word-retrieval in older adults. Frontiers in Aging Neuroscience. 2014;6, article no. 253 doi: 10.3389/fnagi.2014.00253.
- Baker L. D., Frank L. L., Foster-Schubert K., et al. Effects of aerobic exercise on mild cognitive impairment: a controlled trial. Archives of Neurology. 2010;67(1):71–79. doi: 10.1001/archneurol.2009.307.
- Barnes D. E., Santos-Modesitt W., Poelke G., et al. The mental activity and exercise (MAX) trial: a randomized controlled trial to enhance cognitive function in older adults. JAMA Internal Medicine. 2013;173(9):797–804. doi: 10.1001/jamainternmed.2013.189.
- Colcombe S. J., Kramer A. F., Erickson K. I., Scalf P. The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans. Psychology and Aging. 2005;20(3):363–375. doi: 10.1037/0882-7974.20.3.363.
- Best J. R., Nagamatsu L. S., Liu-Ambrose T. Improvements to executive function during exercise training predict maintenance of physical activity over the following year. Frontiers in Human Neuroscience. 2014;8, article no. 353 doi: 10.3389/fnhum.2014.00353.
- Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychology and Aging. 2002;17(1):85–100. doi: 10.1037//0882-7974.17.1.85.
- Hu S., Chao H. H.-A., Winkler A. D., Li C.-S. R. The effects of age on cerebral activations: internally versus externally driven processes. Frontiers in Aging Neuroscience. 2012;4, article 4 doi: 10.3389/fnagi.2012.00004.
- Sebastian A., Baldermann C., Feige B., et al. Differential effects of age on subcomponents of response inhibition. Neurobiology of Aging. 2013;34(9):2183–2193. doi: 10.1016/j.neurobiolaging.2013.03.013.
- Turner G. R., Spreng R. N. Executive functions and neurocognitive aging: dissociable patterns of brain activity. Neurobiology of Aging. 2012;33(4):826.e1–826.e13. doi: 10.1016/j.neurobiolaging.2011.06.005.
- Di X., Rypma B., Biswal B. B. Correspondence of executive function related functional and anatomical alterations in aging brain. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 2014;48:41–50. doi: 10.1016/j.pnpbp.2013.09.001.
- Northoff G., Walter M., Schulte R. F., et al. GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nature Neuroscience. 2007;10(12):1515–1517. doi: 10.1038/nn2001.
- McGregor K. M., Nocera J. R., Sudhyadhom A., et al. Effects of aerobic fitness on aging-related changes of interhemispheric inhibition and motor performance. Frontiers in Aging Neuroscience. 2013;5, article no. 66 doi: 10.3389/fnagi.2013.00066.
- Levin O., Netz Y. Aerobic training as a means to enhance inhibition: what’s yet to be studied? European Review of Aging and Physical Activity. 2015;12(1):1–4. doi: 10.1186/s11556-015-0160-9.
- Thomas B. P., Yezhuvath U. S., Tseng B. Y., et al. Life-long aerobic exercise preserved baseline cerebral blood flow but reduced vascular reactivity to CO2. Journal of Magnetic Resonance Imaging. 2013;38(5):1177–1183. doi: 10.1002/jmri.24090.
- Heise K.-F., Zimerman M., Hoppe J., Gerloff C., Wegscheider K., Hummel F. C. The aging motor system as a model for plastic changes of GABA-mediated intracortical inhibition and their behavioral relevance. Journal of Neuroscience. 2013;33(21):9039–9049. doi: 10.1523/JNEUROSCI.4094-12.2013.
- Fujiyama H., Hinder M. R., Schmidt M. W., Tandonnet C., Garry M. I., Summers J. J. Age-related differences in corticomotor excitability and inhibitory processes during a visuomotor RT task. Journal of Cognitive Neuroscience. 2012;24(5):1253–1263. doi: 10.1162/jocn_a_00201.
- Fling B. W., Seidler R. D. Fundamental differences in callosal structure, neurophysiologic function, and bimanual control in young and older adults. Cerebral Cortex. 2012;22(11):2643–2652. doi: 10.1093/cercor/bhr349.
- Levin O., Fujiyama H., Boisgontier M. P., Swinnen S. P., Summers J. J. Aging and motor inhibition: a converging perspective provided by brain stimulation and imaging approaches. Neuroscience and Biobehavioral Reviews. 2014;43:100–117. doi: 10.1016/j.neubiorev.2014.04.001.
- McGregor K. M., Zlatar Z., Kleim E., et al. Physical activity and neural correlates of aging: a combined TMS/fMRI study. Behavioural Brain Research. 2011;222(1):158–168. doi: 10.1016/j.bbr.2011.03.042.
- Baciu M., Boudiaf N., Cousin E., et al. Functional MRI evidence for the decline of word retrieval and generation during normal aging. Age. 2016;38, article 3:1–22. doi: 10.1007/s11357-015-9857-y.
- Antonenko D., Brauer J., Meinzer M., et al. Functional and structural syntax networks in aging. NeuroImage. 2013;83:513–523. doi: 10.1016/j.neuroimage.2013.07.018.
- Colcombe S. J., Kramer A. F., Erickson K. I., et al. Cardiovascular fitness, cortical plasticity, and aging. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(9):3316–3321. doi: 10.1073/pnas.0400266101.
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