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Gray matter volume covariance patterns associated with gait speed in older adults: a multi-cohort MRI study

Abstract

Accelerated gait decline in aging is associated with many adverse outcomes, including an increased risk for falls, cognitive decline, and dementia. Yet, the brain structures associated with gait speed, and how they relate to specific cognitive domains, are not well-understood. We examined structural brain correlates of gait speed, and how they relate to processing speed, executive function, and episodic memory in three non-demented and community-dwelling older adult cohorts (Overall N = 352), using voxel-based morphometry and multivariate covariance-based statistics. In all three cohorts, we identified gray matter volume covariance patterns associated with gait speed that included brain stem, precuneus, fusiform, motor, supplementary motor, and prefrontal (particularly ventrolateral prefrontal) cortex regions. Greater expression of these gray matter volume covariance patterns linked to gait speed were associated with better processing speed in all three cohorts, and with better executive function in one cohort. These gray matter covariance patterns linked to gait speed were not associated with episodic memory in any of the cohorts. These findings suggest that gait speed, processing speed (and to some extent executive functions) rely on shared neural systems that are subject to age-related and dementia-related change. The implications of these findings are discussed within the context of the development of interventions to compensate for age-related gait and cognitive decline.

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References

  • Abellan van Kan, G., Rolland, Y., Andrieu, S., Bauer, J., Beauchet, O., Bonnefoy, M., Cesari, M., Donini, L. M., Gillette Guyonnet, S., Inzitari, M., Nourhashemi, F., Onder, G., Ritz, P., Salva, A., Visser, M., & Vellas, B. (2009). Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA) task force. The Journal of Nutrition, Health & Aging, 13, 881–889.

    Article  CAS  Google Scholar 

  • Allali, G., van der Meulen, M., Beauchet, O., Rieger, S. W., Vuilleumier, P., & Assal, F. (2014). The neural basis of age-related changes in motor imagery of gait: an fMRI study. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 69, 1389–1398.

    Article  PubMed  Google Scholar 

  • Allali, G., Annweiler, C., Blumen, H., Callisaya, M., De Cock, A.M., Kressig, R., Srikanth, V., Steinmetz, J.P., Verghese, J., Beauchet, O. (2015). Gait phenotype from mild cognitive impairment to moderate dementia: results from the GOOD initiative. European Journal of Neurology.

  • Alvarez, J. A., & Emory, E. (2006). Executive function and the frontal lobes: a meta-analytic review. Neuropsychology Review, 16, 17–42.

    Article  PubMed  Google Scholar 

  • Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38, 95–113.

    Article  PubMed  Google Scholar 

  • Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26, 839–851.

    Article  Google Scholar 

  • Ashby, F. G. (2011). Statistical analysis of fMRI data. In MIT press.

    Google Scholar 

  • Association, A. P. (2000). Diagnostic and statistical manual of mental disorders (revised 4th ed.). Washington, DC: American Psychiatric Association.

    Google Scholar 

  • Atkinson, H. H., Rosano, C., Simonsick, E. M., Williamson, J. D., Davis, C., Ambrosius, W. T., Rapp, S. R., Cesari, M., Newman, A. B., Harris, T. B., Rubin, S. M., Yaffe, K., Satterfield, S., & Kritchevsky, S. B. (2007). Cognitive function, gait speed decline, and comorbidities: the health, aging and body composition study. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62, 844–850.

    Article  Google Scholar 

  • Beauchet, O., Allali, G., Launay, C., Herrmann, F., & Annweiler, C. (2013). Gait variability at fast-pace walking speed: a biomarker of mild cognitive impairment? The Journal of Nutrition, Health & Aging, 17, 235–239.

    Article  CAS  Google Scholar 

  • Beauchet, O., Allali, G., Annweiler, C., & Verghese, J. (2016a). Association of motoric cognitive risk syndrome with brain volumes: results from the gait study. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 71, 1081–1088.

    Article  PubMed  Google Scholar 

  • Beauchet, O., Annweiler, C., Callisaya, M. L., De Cock, A. M., Helbostad, J. L., Kressig, R. W., Srikanth, V., Steinmetz, J. P., Blumen, H. M., Verghese, J., & Allali, G. (2016b). Poor gait performance and prediction of dementia: results from a meta-analysis. Journal of the American Medical Directors Association.

  • Beauchet, O., Blumen, H.M., Callisaya, M.L., De Cock, A.M., Kressig, R.W., Srikanth, V., Steinmetz, J.P., Annweiler, C., Allali, G., 2016c. Times are changing; researchers need to change too. European Journal of Neurology 23, e10.

  • Blumen, H. M., Holtzer, R., Brown, L. L., Gazes, Y., & Verghese, J. (2014). Behavioral and neural correlates of imagined walking and walking while talking in the elderly. Human Brain Mapping, 35, 4090–4104.

    Article  PubMed  PubMed Central  Google Scholar 

  • Buracchio, T., Dodge, H. H., Howieson, D., Wasserman, D., & Kaye, J. (2010). The trajectory of gait speed preceding mild cognitive impairment. Archives of Neurology, 67, 980–986.

    Article  PubMed  PubMed Central  Google Scholar 

  • Burnham, K.P., Anderson, D.R. (2002). Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media.

  • Buschke, H. (1973). Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12, 543–550.

    Article  Google Scholar 

  • Callisaya, M. L., Beare, R., Phan, T. G., Blizzard, L., Thrift, A. G., Chen, J., & Srikanth, V. K. (2013). Brain structural change and gait decline: a longitudinal population-based study. Journal of the American Geriatrics Society, 61, 1074–1079.

    Article  PubMed  Google Scholar 

  • Callisaya, M. L., Beare, R., Phan, T. G., Chen, J., & Srikanth, V. K. (2014). Global and regional associations of smaller cerebral gray and white matter volumes with gait in older people. PLoS One, 9, e84909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Callisaya, M. L., Blizzard, C. L., Wood, A. G., Thrift, A. G., Wardill, T., & Srikanth, V. K. (2015). Longitudinal relationships between cognitive decline and gait slowing: the tasmanian study of cognition and gait. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 70, 1226–1232.

    Article  Google Scholar 

  • Ceccarelli, A., Rocca, M. A., Pagani, E., Falini, A., Comi, G., & Filippi, M. (2009). Cognitive learning is associated with gray matter changes in healthy human individuals: a tensor-based morphometry study. NeuroImage, 48, 585–589.

    Article  PubMed  Google Scholar 

  • Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., McAuley, E., Elavsky, S., Marquez, D. X., Hu, L., & Kramer, A. F. (2006). Aerobic exercise training increases brain volume in aging humans. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 61, 1166–1170.

    Article  Google Scholar 

  • Cosentino, S., Brickman, A. M., Griffith, E., Habeck, C., Cines, S., Farrell, M., Shaked, D., Huey, E. D., Briner, T., & Stern, Y. (2015). The right insula contributes to memory awareness in cognitively diverse older adults. Neuropsychologia, 75, 163–169.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cummings, S. R., Studenski, S., & Ferrucci, L. (2014). A diagnosis of dismobility--giving mobility clinical visibility: a mobility working group recommendation. JAMA, 311, 2061–2062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doi, T., Shimada, H., Makizako, H., Tsutsumimoto, K., Uemura, K., Anan, Y., & Suzuki, T. (2014). Cognitive function and gait speed under normal and dual-task walking among older adults with mild cognitive impairment. BMC Neurology, 14, 67.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dumurgier, J., Crivello, F., Mazoyer, B., Ahmed, I., Tavernier, B., Grabli, D., Francois, C., Tzourio-Mazoyer, N., Tzourio, C., & Elbaz, A. (2012). MRI atrophy of the caudate nucleus and slower walking speed in the elderly. NeuroImage, 60, 871–878.

    Article  PubMed  Google Scholar 

  • Efron, B., Tibshirani, R.J. (1994). An introduction to the bootstrap. CRC press.

  • Elderkin-Thompson, V., Ballmaier, M., Hellemann, G., Pham, D., & Kumar, A. (2008). Executive function and MRI prefrontal volumes among healthy older adults. Neuropsychology, 22, 626–637.

    Article  PubMed  Google Scholar 

  • Erickson, K. I., Voss, M. W., Prakash, R. S., Basak, C., Szabo, A., Chaddock, L., Kim, J. S., Heo, S., Alves, H., White, S. M., Wojcicki, T. R., Mailey, E., Vieira, V. J., Martin, S. A., Pence, B. D., Woods, J. A., McAuley, E., & Kramer, A. F. (2011). Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences, 108, 3017–3022.

    Article  Google Scholar 

  • Ezzati, A., Katz, M. J., Lipton, M. L., Lipton, R. B., & Verghese, J. (2015). The association of brain structure with gait velocity in older adults: a quantitative volumetric analysis of brain MRI. Neuroradiology, 57, 851–861.

    Article  PubMed  PubMed Central  Google Scholar 

  • Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.

    Article  CAS  PubMed  Google Scholar 

  • Friston, K. J., Holmes, A. P., Poline, J. B., Grasby, P. J., Williams, S. C., Frackowiak, R. S., & Turner, R. (1995). Analysis of fMRI time-series revisited. NeuroImage, 2, 45–53.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Rill, E. (1991). The pedunculopontine nucleus. Progress in Neurobiology, 36, 363–389.

    Article  CAS  PubMed  Google Scholar 

  • Habeck, C., & Stern, Y. (2007). Neural network approaches and their reproducibility in the study of verbal working memory and Alzheimer's disease. Clinical Neuroscience Research, 6, 381–390.

    Article  PubMed  PubMed Central  Google Scholar 

  • Habeck, C., & Stern, Y. (2010). Multivariate data analysis for neuroimaging data: overview and application to Alzheimer’s Disease. Cell Biochemistry and Biophysics, 58, 53–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Habeck, C., Krakauer, J. W., Ghez, C., Sackeim, H. A., Eidelberg, D., Stern, Y., & Moeller, J. R. (2005a). A new approach to spatial covariance modeling of functional brain imaging data: ordinal trend analysis. Neural Computation, 17, 1602–1645.

    Article  PubMed  Google Scholar 

  • Habeck, C., Rakitin, B. C., Moeller, J., Scarmeas, N., Zarahn, E., Brown, T., & Stern, Y. (2005b). An event-related fMRI study of the neural networks underlying the encoding, maintenance, and retrieval phase in a delayed-match-to-sample task. Brain Research. Cognitive Brain Research, 23, 207–220.

    Article  PubMed  Google Scholar 

  • Habeck, C., Foster, N. L., Perneczky, R., Kurz, A., Alexopoulos, P., Koeppe, R. A., Drzezga, A., & Stern, Y. (2008). Multivariate and univariate neuroimaging biomarkers of Alzheimer's disease. NeuroImage, 40, 1503–1515.

    Article  PubMed  PubMed Central  Google Scholar 

  • Habeck, C., Gazes, Y., Razlighi, Q., Steffener, J., Brickman, A., Barulli, D., Salthouse, T., & Stern, Y. (2016). The reference ability neural network study: life-time stability of reference-ability neural networks derived from task maps of young adults. NeuroImage, 125, 693–704.

    Article  CAS  PubMed  Google Scholar 

  • Haber, S.N. (2016). Corticostriatal circuitry. Neuroscience in the 21st Century, 1–21.

  • Holtzer, R., Verghese, J., Xue, X., & Lipton, R. B. (2006). Cognitive processes related to gait velocity: results from the Einstein aging study. Neuropsychology, 20, 215–223.

    Article  PubMed  Google Scholar 

  • Holtzer, R., Wang, C., Lipton, R., & Verghese, J. (2012). The protective effects of executive functions and episodic memory on gait speed decline in aging defined in the context of cognitive reserve. Journal of the American Geriatrics Society, 60, 2093–2098.

    Article  PubMed  PubMed Central  Google Scholar 

  • Holtzer, R., Epstein, N., Mahoney, J. R., Izzetoglu, M., & Blumen, H. M. (2014a). Neuroimaging of mobility in aging: a targeted review. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 69, 1375–1388.

    Article  PubMed  PubMed Central  Google Scholar 

  • Holtzer, R., Mahoney, J., & Verghese, J. (2014b). Intraindividual variability in executive functions but not speed of processing or conflict resolution predicts performance differences in gait speed in older adults. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 69, 980–986.

    Article  PubMed  Google Scholar 

  • Holtzer, R., Wang, C., & Verghese, J. (2014c). Performance variance on walking while talking tasks: theory, findings, and clinical implications. Age, 36, 373–381.

    Article  PubMed  Google Scholar 

  • Iseki, K., Hanakawa, T., Shinozaki, J., Nankaku, M., & Fukuyama, H. (2008). Neural mechanisms involved in mental imagery and observation of gait. NeuroImage, 41, 1021–1031.

    Article  PubMed  Google Scholar 

  • Jahn, K., Deutschlander, A., Stephan, T., Strupp, M., Wiesmann, M., & Brandt, T. (2004). Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. NeuroImage, 22, 1722–1731.

    Article  PubMed  Google Scholar 

  • Kail, R., & Salthouse, T. A. (1994). Processing speed as a mental capacity. Acta Psychologica, 86, 199–225.

    Article  CAS  PubMed  Google Scholar 

  • Karas, G., Scheltens, P., Rombouts, S., Visser, P., Van Schijndel, R., Fox, N., & Barkhof, F. (2004). Global and local gray matter loss in mild cognitive impairment and Alzheimer's disease. NeuroImage, 23, 708–716.

    Article  CAS  PubMed  Google Scholar 

  • Katz, M. J., Lipton, R. B., Hall, C. B., Zimmerman, M. E., Sanders, A. E., Verghese, J., Dickson, D. W., & Derby, C. A. (2012). Age and sex specific prevalence and incidence of mild cognitive impairment, dementia and Alzheimer’s dementia in blacks and whites: a report from the einstein aging study. Alzheimer Disease and Associated Disorders, 26, 335–343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Katzman, R., Brown, T., Fuld, P., Peck, A., Schechter, R., & Schimmel, H. (1983). Validation of a short orientation-memory-concentration test of cognitive impairment. American Journal of Psychiatry, 140, 734–739.

    Article  CAS  PubMed  Google Scholar 

  • Klein, T. A., Endrass, T., Kathmann, N., Neumann, J., von Cramon, D. Y., & Ullsperger, M. (2007). Neural correlates of error awareness. NeuroImage, 34, 1774–1781.

    Article  PubMed  Google Scholar 

  • Koechlin, E., Ody, C., & Kouneiher, F. (2003). The architecture of cognitive control in the human prefrontal cortex. Science, 302, 1181–1185.

    Article  CAS  PubMed  Google Scholar 

  • Kühn, S., Gleich, T., Lorenz, R., Lindenberger, U., & Gallinat, J. (2014). Playing Super Mario induces structural brain plasticity: gray matter changes resulting from training with a commercial video game. Molecular Psychiatry, 19, 265–271.

    Article  PubMed  Google Scholar 

  • la Fougere, C., Zwergal, A., Rominger, A., Forster, S., Fesl, G., Dieterich, M., Brandt, T., Strupp, M., Bartenstein, P., & Jahn, K. (2010). Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. NeuroImage, 50, 1589–1598.

    Article  PubMed  Google Scholar 

  • Lambert, C., Benjamin, P., Zeestraten, E., Lawrence, A. J., Barrick, T. R., & Markus, H. S. (2016). Longitudinal patterns of leukoaraiosis and brain atrophy in symptomatic small vessel disease. Brain.

  • Lee, S., Habeck, C., Razlighi, Q., Salthouse, T., & Stern, Y. (2016). Selective association between cortical thickness and reference abilities in normal aging. NeuroImage, 142, 293–300.

    Article  PubMed  PubMed Central  Google Scholar 

  • Leisman, G., Moustafa, A. A., & Shafir, T. (2016). Thinking, walking, talking: integratory motor and cognitive brain function. Frontiers in Public Health, 4, 94.

    Article  PubMed  PubMed Central  Google Scholar 

  • Levy, B. J., & Wagner, A. D. (2011). Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating. Annals of the New York Academy of Sciences, 1224, 40–62.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marinelli, L., Quartarone, A., Hallett, M., Frazzitta, G., & Ghilardi, M. F. (2017). The many facets of motor learning and their relevance for Parkinson's disease. Clinical Neurophysiology, 128, 1127–1141.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marquis, S., Moore, M. M., Howieson, D. B., Sexton, G., Payami, H., Kaye, J. A., & Camicioli, R. (2002). Independent predictors of cognitive decline in healthy elderly persons. Archives of Neurology, 59, 601–606.

    Article  PubMed  Google Scholar 

  • Mielke, M. M., Roberts, R. O., Savica, R., Cha, R., Drubach, D. I., Christianson, T., Pankratz, V. S., Geda, Y. E., Machulda, M. M., & Ivnik, R. J. (2013). Assessing the temporal relationship between cognition and gait: slow gait predicts cognitive decline in the Mayo Clinic Study of aging. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 68, 929–937.

    Article  Google Scholar 

  • Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.

    Article  CAS  PubMed  Google Scholar 

  • Morris, J. C., Heyman, A., Mohs, R. C., Hughes, J. P., van Belle, G., Fillenbaum, G., Mellits, E. D., & Clark, C. (1989). The consortium to establish a registry for Alzheimer's disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology, 39, 1159–1165.

    Article  CAS  PubMed  Google Scholar 

  • Mortimer, J. A., Ding, D., Borenstein, A. R., DeCarli, C., Guo, Q., Wu, Y., Zhao, Q., & Chu, S. (2012). Changes in brain volume and cognition in a randomized trial of exercise and social interaction in a community-based sample of non-demented Chinese elders. Journal of Alzheimer's Disease, 30, 757–766.

    Article  PubMed  Google Scholar 

  • Nadkarni, N. K., Nunley, K. A., Aizenstein, H., Harris, T. B., Yaffe, K., Satterfield, S., Newman, A. B., Rosano, C., & Study, f.t.H.A. (2014). Association between cerebellar gray matter volumes, gait speed, and information-processing ability in older adults enrolled in the health ABC study. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 69, 996–1003.

    Article  Google Scholar 

  • Newman, A. B., Simonsick, E. M., Naydeck, B. L., Boudreau, R. M., Kritchevsky, S. B., Nevitt, M. C., Pahor, M., Satterfield, S., Brach, J. S., Studenski, S. A., & Harris, T. B. (2006). Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability. Journal of the American Medical Association, 295, 2018–2026.

    Article  CAS  PubMed  Google Scholar 

  • Norman, D. A., & Shallice, T. (1980). Attention to action: willed and automatic control of behavior. San Diego, La Jolla, Calif: Center for Human Information Processing, University of California.

    Google Scholar 

  • Panel on Prevention of Falls in Older Persons, A.G.S., British Geriatrics, S. (2011). Summary of the updated American geriatrics society/British geriatrics society clinical practice guideline for prevention of falls in older persons. Journal of the American Geriatrics Society, 59, 148–157.

    Article  Google Scholar 

  • Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56, 303–308.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, R. C., Roberts, R. O., Knopman, D. S., Boeve, B. F., Geda, Y. E., Ivnik, R. J., Smith, G. E., & Jack Jr., C. R. (2009). Mild cognitive impairment: ten years later. Archives of Neurology, 66, 1447–1455.

    Article  PubMed  PubMed Central  Google Scholar 

  • Randolph, C., Tierney, M. C., Mohr, E., & Chase, T. N. (1998). The repeatable battery for the assessment of neuropsychological status (RBANS): preliminary clinical validity. Journal of Clinical and Experimental Neuropsychology, 20, 310–319.

    Article  CAS  PubMed  Google Scholar 

  • Raz, N. (2000). Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. In F. I. M. C. T. A. Salthouse (Ed.), The handbook of aging and cognition (2nd ed., pp. 1–90). Mahwah: Lawrence Erlbaum Associates Publishers.

    Google Scholar 

  • Reitan, R. (1978). Manual for administration of neuropsychological test batteries for adults and children. Tucson: Reitan Neuropsychology Laboratories.

    Google Scholar 

  • Rosano, C., Studenski, S. A., Aizenstein, H. J., Boudreau, R. M., Longstreth Jr., W. T., & Newman, A. B. (2012). Slower gait, slower information processing and smaller prefrontal area in older adults. Age and Ageing, 41, 58–64.

    Article  PubMed  Google Scholar 

  • Rosso, A.L., Studenski, S.A., Chen, W.G., Aizenstein, H.J., Alexander, N.B., Bennett, D.A., Black, S.E., Camicioli, R., Carlson, M.C., Ferrucci, L., Guralnik, J.M., Hausdorff, J.M., Kaye, J., Launer, L.J., Lipsitz, L.A., Verghese, J., Rosano, C. (2013). Aging, the Central Nervous System, and Mobility. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences.

  • Rypma, B., Berger, J. S., Prabhakaran, V., Bly, B. M., Kimberg, D. Y., Biswal, B. B., & D'Esposito, M. (2006). Neural correlates of cognitive efficiency. NeuroImage, 33, 969–979.

    Article  PubMed  Google Scholar 

  • Salthouse, T. A. (1996). The processing-speed theory of adult age differences in cognition. Psychological Review, 103, 403.

    Article  CAS  PubMed  Google Scholar 

  • Shallice, T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S. J., & Dolan, R. J. (1994). Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature, 368, 633–635.

    Article  CAS  PubMed  Google Scholar 

  • Society, A. G., Society, G., Of, A. A., & On Falls Prevention, O. S. P. (2001). Guideline for the prevention of falls in older persons. Journal of the American Geriatrics Society, 49, 664–672.

    Article  Google Scholar 

  • Spaniol, J., Davidson, P. S., Kim, A. S., Han, H., Moscovitch, M., & Grady, C. L. (2009). Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia, 47, 1765–1779.

    Article  PubMed  Google Scholar 

  • Spetsieris, P. G., & Eidelberg, D. (2011). Scaled subprofile modeling of resting state imaging data in Parkinson's disease: Methodological issues. NeuroImage, 54, 2899–2914.

    Article  PubMed  Google Scholar 

  • Srikanth, V., Sanders, L., Callisaya, M., Martin, K., & Phan, T. (2010). Brain aging and gait. Aging Health, 6, 123–131.

    Article  Google Scholar 

  • Steffener, J., Brickman, A. M., Habeck, C., Salthouse, T. A., & Stern, Y. (2013). Cerebral blood flow and gray matter volume covariance patterns of cognition in aging. Human Brain Mapping, 34, 3267–3279.

    Article  PubMed  Google Scholar 

  • Stern, Y., Habeck, C., Steffener, J., Barulli, D., Gazes, Y., Razlighi, Q., Shaked, D., & Salthouse, T. (2014). The reference ability neural network study: motivation, design, and initial feasibility analyses. NeuroImage, 103, 139–151.

    Article  PubMed  PubMed Central  Google Scholar 

  • Takeuchi, H., Taki, Y., Sassa, Y., Hashizume, H., Sekiguchi, A., Fukushima, A., & Kawashima, R. (2011). Working memory training using mental calculation impacts regional gray matter of the frontal and parietal regions. PLoS One, 6, e23175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tattersall, T. L., Stratton, P. G., Coyne, T. J., Cook, R., Silberstein, P., Silburn, P. A., Windels, F., & Sah, P. (2014). Imagined gait modulates neuronal network dynamics in the human pedunculopontine nucleus. Nature Neuroscience, 17, 449–454.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, P.M., Hayashi, K.M., de Zubicaray, G., Janke, A.L., Rose, S.E., Semple, J., Herman, D., Hong, M.S., Dittmer, S.S., Doddrell, D.M., Toga, A.W., 2003. Dynamics of Gray Matter Loss in Alzheimer's Disease. The Journal of Neuroscience 23, 994–1005.

  • Tulving, E. (1972). Episodic and semantic memory 1. Organization of Memory (Vol. 381). London: Academic.

    Google Scholar 

  • Tulving, E. (1985). Elements of episodic memory.

    Google Scholar 

  • Turner, G., & Clegg, A. (2014). Best practice guidelines for the management of frailty: a British geriatrics society, age UK and Royal College of general practitioners report. Age and Ageing, 43, 744–747.

    Article  PubMed  Google Scholar 

  • van der Meulen, M., Allali, G., Rieger, S. W., Assal, F., Vuilleumier, P. (2012). The influence of individual motor imagery ability on cerebral recruitment during gait imagery. Human Brain Mapping, 35(2), 455–470.

  • Verghese, J., Lipton, R. B., Hall, C. B., Kuslansky, G., Katz, M. J., & Buschke, H. (2002). Abnormality of gait as a predictor of non-Alzheimer's dementia. New England Journal of Medicine, 347, 1761–1768.

    Article  PubMed  Google Scholar 

  • Verghese, J., LeValley, A., Hall, C. B., Katz, M. J., Ambrose, A. F., & Lipton, R. B. (2006). Epidemiology of gait disorders in community-residing older adults. Journal of the American Geriatrics Society, 54, 255–261.

    Article  PubMed  PubMed Central  Google Scholar 

  • Verghese, J., Wang, C., Lipton, R. B., Holtzer, R., & Xue, X. (2007). Quantitative gait dysfunction and risk of cognitive decline and dementia. Journal of Neurology, Neurosurgery, and Psychiatry, 78, 929–935.

    Article  PubMed  PubMed Central  Google Scholar 

  • Verghese, J., Robbins, M., Holtzer, R., Zimmerman, M., Wang, C., Xue, X., & Lipton, R. B. (2008). Gait dysfunction in mild cognitive impairment syndromes. Journal of the American Geriatrics Society, 56, 1244–1251.

    Article  PubMed  PubMed Central  Google Scholar 

  • Verghese, J., Holtzer, R., Lipton, R. B., & Wang, C. (2009). Quantitative gait markers and incident fall risk in older adults. Journals of Gerontology Series A: Biological Sciences & Medical Sciences, 64A, 896–901.

    Article  Google Scholar 

  • Verghese, J., Mahoney, J., Ambrose, A. F., Wang, C., & Holtzer, R. (2010). Effect of cognitive remediation on gait in sedentary seniors. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 65, 1338–1343.

    Article  Google Scholar 

  • Verghese, J., Annweiler, C., Ayers, E., Barzilai, N., Beauchet, O., Bennett, D. A., Bridenbaugh, S. A., Buchman, A. S., Callisaya, M. L., & Camicioli, R. (2014a). Motoric cognitive risk syndrome multicountry prevalence and dementia risk. Neurology, 83, 718–726.

    Article  PubMed  PubMed Central  Google Scholar 

  • Verghese, J., Ayers, E., Barzilai, N., Bennett, D. A., Buchman, A. S., Aron, S., Holtzer, R., Katz, M., Lipton, R. B., & Wang, C. (2014b). Motoric cognitive risk syndrome: Multicenter incidence study. Neurology, 83, 2278–2284.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wai, Y.-Y., Wang, J.-J., Weng, Y.-H., Lin, W.-Y., Ma, H.-K., Ng, S.-H., Wan, Y.-L., & Wang, C.-H. (2012). Cortical involvement in a gait-related imagery task: comparison between Parkinson’s disease and normal aging. Parkinsonism & Related Disorders, 18, 537–542.

    Article  Google Scholar 

  • Waite, L. M., Grayson, D. A., Piguet, O., Creasey, H., Bennett, H. P., & Broe, G. A. (2005). Gait slowing as a predictor of incident dementia: 6-year longitudinal data from the sydney older persons study. Journal of the Neurological Sciences, 230, 89–93.

    Article  Google Scholar 

  • Wang, L., Larson, E. B., Bowen, J. D., & van Belle, G. (2006). Performance-based physical function and future dementia in older people. Archives of Internal Medicine, 166, 1115–1120.

    Article  PubMed  Google Scholar 

  • Watson, N. L., Rosano, C., Boudreau, R. M., Simonsick, E. M., Ferrucci, L., Sutton-Tyrrell, K., Hardy, S. E., Atkinson, H. H., Yaffe, K., Satterfield, S., Harris, T. B., & Newman, A. B. (2010). Executive function, memory, and gait speed decline in well-functioning older adults. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 65, 1093–1100.

    Article  CAS  Google Scholar 

  • Zwergal, A., Linn, J., Xiong, G., Brandt, T., Strupp, M., & Jahn, K. (2012). Aging of human supraspinal locomotor and postural control in fMRI. Neurobiology of Aging, 33, 1073–1084.

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Melanie Lucas, Syed Sabbir, Susmit Tripathi and Jennifer Yuan for their assistance in manually re-orienting, and ensuring proper segmentation of, neuroimaging data.

Funding

No targeted funding is reported for the secondary analyses performed in this study. The individual studies were supported by the following agencies. The Central Control of Mobility in Aging Study was funded by the NIH/NIA (1R01AG044007-01A1 1RO1AG036920 1R56AG057548-01). The Einstein Aging Study was funded by NIH/NIA (AG03949 AG026728). The GAIT Study was funded by the French Ministry of Health (Projet Hospitalier de Recherche Clinique national 2009-A00533-54). Helena M. Blumen was also supported by a career development award from NIH/NIA 1K01AG049829-01A1.

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Correspondence to Helena M. Blumen.

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All procedures performed in these studies involving human subjects were in accordance with the ethical standards of the institutions, and with the 1964 Helsinki declaration and its later amendments.

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Informed consent was obtained from all individual participants included in each study.

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Blumen, H.M., Brown, L.L., Habeck, C. et al. Gray matter volume covariance patterns associated with gait speed in older adults: a multi-cohort MRI study. Brain Imaging and Behavior 13, 446–460 (2019). https://doi.org/10.1007/s11682-018-9871-7

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Keywords

  • Gait
  • Cognition
  • Magnetic resonance imaging
  • Gray matter
  • Multivariate analyses