Experimental Brain Research

, Volume 193, Issue 3, pp 445–454 | Cite as

Gait capacity affects cortical activation patterns related to speed control in the elderly

  • Taeko HaradaEmail author
  • Ichiro Miyai
  • Mitsuo Suzuki
  • Kisou Kubota
Research Article


Functional decline in locomotion is common among the elderly, and the prevalence of gait disorders increases with age. Recently, increasing interest has been focused on the influence of age-related decline in brain function and neurological disorders such as dementia and Alzheimer’s disease on gait capacity. However, the neural mechanisms underlying gait control in the elderly remain poorly understood. We examined whether cortical activation patterns associated with the control of gait speed were related to the walking capacity in elderly subjects. Fifteen healthy elderly subjects participated in the study (mean ± SD 63 ± 4). Using functional near-infrared spectroscopy, we measured the changes in the cortical oxygenated hemoglobin (oxyHb) while the subjects walked on a treadmill at low, moderate, and high speeds corresponding to 30, 50, and 70% intensity of work load in each subject. We found a greater increase in oxyHb in the left prefrontal cortex (PFC) and the supplementary motor area (SMA) during walking at 70% intensity than at 50 or 30%. The degree of medial sensorimotor cortex (mSMC) and SMA activations was correlated with the locomotor speed and cadence. Heart rate response was only related with left PFC activation. Furthermore, at the highest speed, the change in the PFC activation was greater in subjects with low gait capacity than in those with high gait capacity. Our results indicate that the left PFC, SMA, and SMC control gait speed, and that the involvement of the left PFC might depend on an age-related decline in gait capacity in the elderly.


Gait speed Cortical activation Aging Frontal cortex Functional near-infrared spectroscopy 



This study was supported by a grant-in-aid for “The Research Committee for Ataxic Diseases” of the Research on Measures for Intractable Diseases, Funds for Comprehensive Research on Aging and Health from the Ministry of Health, Labour and Welfare, Japan. We are grateful to the members (Mr Goho and Ms Nakai) of the NPO ATRL, Omichikai Medical Group, for their help in recruiting subjects.


  1. Armstrong DM (1988) The supraspinal control of mammalian locomotion. J Physiol 405:1–37PubMedGoogle Scholar
  2. Atkinson HH, Rosano C, Simonsick EM, Williamson JD, Davis C, Ambrosius WT, Rapp SR, Cesari M, Newman AB, Harris TB, Rubin SM, Yaffe K, Satterfield S, Kritchevsky SB (2007) Health ABC study. Cognitive function, gait speed decline, and comorbidities: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 62:844–850PubMedGoogle Scholar
  3. Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2002) Parallel processing of serial movements in prefrontal cortex. Proc Natl Acad Sci USA 99:13172–13177PubMedCrossRefGoogle Scholar
  4. Ble A, Volpato S, Zuliani G, Guralnik JM, Bandinelli S, Lauretani F, Bartali B, Maraldi C, Fellin R, Ferrucci L (2005) Executive function correlates with walking speed in older persons: the InCHIANTI study. J Am Geriatr Soc 53:410–415PubMedCrossRefGoogle Scholar
  5. Borg GA (1982) Physiological basis of perceived exertion. Med Sci Sports Exerc 14:377–381PubMedGoogle Scholar
  6. Cabeza R, Grady CL, Nyberg L, McIntosh AR, Tulving E, Kapur S, Jennings JM, Houle S, Craik FI (1997) Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci 17:391–400PubMedGoogle Scholar
  7. Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L (2000) Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J Cogn Neurosci 12:197–206PubMedCrossRefGoogle Scholar
  8. Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L, Cabeza R, Anderson ND, Locantore JK, McIntosh AR (2002) Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17:1394–1402PubMedCrossRefGoogle Scholar
  9. Carlson MC, Fried LP, Xue QL, Bandeen-Roche K, Zeger SL, Brandt J (1999) Association between executive attention and physical functional performance in community-dwelling older women. J Gerontol B Psychol Sci Soc Sci 54:S262–S270PubMedGoogle Scholar
  10. Catalan MJ, Honda M, Weeks RA, Cohen LG, Hallett M (1998) The functional neuroanatomy of simple and complex sequential finger movements: a PET study. Brain 121:253–264PubMedCrossRefGoogle Scholar
  11. Cunnington R, Iansek R, Bradshaw JL, Phillips JG (1995) Movement-related potentials in Parkinson’s disease. Presence and predictability of temporal and spatial cues. Brain 118:935–950PubMedCrossRefGoogle Scholar
  12. Cunnington R, Windischberger C, Deecke L, Moser E (2002) The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 15:373–385PubMedCrossRefGoogle Scholar
  13. Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RSJ (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402PubMedCrossRefGoogle Scholar
  14. Deiber MP, Honda M, Ibanez V, Sadato N, Hallett M (1999) Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 81:3065–3077PubMedGoogle Scholar
  15. D’Esposito M, Deouell LY, Gazzaley A (2003) Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 4:863–872PubMedCrossRefGoogle Scholar
  16. Dietz V, Muller R, Colombo G (2002) Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 125:2626–2634PubMedCrossRefGoogle Scholar
  17. Drew T (1988) Motor cortical cell discharge during voluntary gait modification. Brain Res 457:181–187PubMedCrossRefGoogle Scholar
  18. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626PubMedGoogle Scholar
  19. Esposito G, Kirkby BS, Van Horn JD, Ellmore TM, Berman KF (1999) Context-dependent, neural system-specific neurophysiological concomitants of ageing: mapping PET correlates during cognitive activation. Brain 122:963–979PubMedCrossRefGoogle Scholar
  20. Farkas E, Luiten PG (2001) Cerebral microvascular pathology in aging and Alzheimer’s disease. Prog Neurobiol 64:575–611PubMedCrossRefGoogle Scholar
  21. Fife TD, Baloh RW (1993) Disequilibrium of unknown cause in older people. Ann Neurol l34:694–702CrossRefGoogle Scholar
  22. Fitzpatrick AL, Buchanan CK, Nahin RL, Dekosky ST, Atkinson HH, Carlson MC, Williamson JD (2007) Ginkgo evaluation of memory (GEM) study investigators. Associations of gait speed and other measures of physical function with cognition in a healthy cohort of elderly persons. J Gerontol A Biol Sci Med Sci 62:1244–1251PubMedGoogle Scholar
  23. Frith CD (2000) The role of dorsolateral prefrontal cortex in the selection of action. In: Monsell S, Driver J (eds) Control of cognitive processes: attention and performance. MIT, Cambridge, pp 549–565Google Scholar
  24. Frith CD, Friston K, Liddle PF, Frackowiak RS (1991) Willed action and the prefrontal cortex in man: a study with PET. Proc Biol Sci 244:241–246PubMedCrossRefGoogle Scholar
  25. Fukuyama H, Ouchi Y, Matsuzaki S, Nagahama Y, Yamauchi H, Ogawa M, Kimura J, Shibasaki H (1997) Brain functional activity during gait in normal subjects: a SPECT study. Neurosci Lett 228:183–186PubMedCrossRefGoogle Scholar
  26. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1997) Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. Brain 120:1587–1602PubMedCrossRefGoogle Scholar
  27. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1998) The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain 121:1695–1709PubMedCrossRefGoogle Scholar
  28. Gratton G, Corballis PM (1995) Removing the heart from the brain: compensation for the pulse artifact in the photon migration signal. Psychophysiology 32:292–299PubMedCrossRefGoogle Scholar
  29. Hakim AA, Petrovitch H, Burchfiel CM, Ross GW, Rodriguez BL, White LR, Yano K, Curb JD, Abbott RD (1998) Effects of walking on mortality among nonsmoking retired men. N Engl J Med 338:94–99PubMedCrossRefGoogle Scholar
  30. Hardy SE, Perera S, Roumani YF, Chandler JM, Studenski SA (2007) Improvement in usual gait speed predicts better survival in older adults. J Am Geriatr Soc 55:1727–1734PubMedCrossRefGoogle Scholar
  31. Hatakenaka M, Miyai I, Mihara M, Sakoda S, Kubota K (2007) Frontal regions involved in learning of motor skill—a functional NIRS study. Neuroimage 34:109–116PubMedCrossRefGoogle Scholar
  32. Hesselmann V, Zaro Weber O, Wedekind C, Krings T, Schulte O, Kugel H, Krug B, Klug N, Lackner KJ (2001) Age related signal decrease in functional magnetic resonance imaging during motor stimulation in humans. Neurosci Lett 308:141–144PubMedCrossRefGoogle Scholar
  33. Hikosaka O, Sakai K, Miyauchi S, Takino R, Sasaki Y, Putz B (1996) Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. J Neurophysiol 76:617–621PubMedGoogle Scholar
  34. Holtzer R, Verghese J, Xue X, Lipton RB (2006) Cognitive processes related to gait velocity: results from the Einstein aging study. Neuropsychology 20:215–223PubMedCrossRefGoogle Scholar
  35. Hoshi Y, Kobayashi N, Tamura M (2001) Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. J Appl Physiol 90:1657–1662PubMedGoogle Scholar
  36. Humberstone M, Sawle GV, Clare S, Hykin J, Coxon R, Bowtell R, Macdonald IA, Morris PG (1997) Functional magnetic resonance imaging of single motor events reveals human presupplementary motor area. Ann Neurol 42:632–637PubMedCrossRefGoogle Scholar
  37. Inzitari M, Newman AB, Yaffe K, Boudreau R, de Rekeneire N, Shorr R, Harris TB, Rosano C (2007) Gait speed predicts decline in attention and psychomotor speed in older adults: the health aging and body composition study. Neuroepidemiology 29:156–162PubMedCrossRefGoogle Scholar
  38. Jensen G, Nielsen HB, Ide K, Madsen PL, Svendsen LB, Svendsen UG, Secher NH (2002) Cerebral oxygenation during exercise in patients with terminal lung disease. Chest 122:445–450PubMedCrossRefGoogle Scholar
  39. Karvonen MJ, Kentala E, Mustal D (1957) The effects of training on heart rate: a longitudinal study. Ann Med Exp Biol Fenn 35:307–315PubMedGoogle Scholar
  40. Kerber KA, Ishiyama GP, Baloh RW (2006) A longitudinal study of oculomotor function in normal older people. Neurobiol Aging 27:1346–1353PubMedCrossRefGoogle Scholar
  41. Kuo HK, Leveille SG, Yu YH, Milberg WP (2007) Cognitive function, habitual gait speed, and late-life disability in the National Health and Nutrition Examination Survey (NHANES) 1999–2002. Gerontology 53:102–110PubMedCrossRefGoogle Scholar
  42. Lau HC, Rogers RD, Haggard P, Passingham RE (2004a) Attention to intention. Science 303:1208–1210PubMedCrossRefGoogle Scholar
  43. Lau HC, Rogers RD, Ramnani N, Passingham RE (2004b) Willed action and attention to the selection of action. Neuroimage 21:1407–1415PubMedCrossRefGoogle Scholar
  44. Logan JM, Sanders AL, Snyder AZ, Morris JC, Buckner RL (2002) Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron 33:827–840PubMedCrossRefGoogle Scholar
  45. Malouin F, Richards CL, Jackson PL, Dumas F, Doyon J (2003) Brain activations during motor imagery of locomotor-related tasks: a PET study. Hum Brain Mapp 19:47–62PubMedCrossRefGoogle Scholar
  46. Massion J (1992) Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol 38:35–56PubMedCrossRefGoogle Scholar
  47. Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S (2007) Sustained prefrontal activation during ataxic gait: a compensatory mechanism for ataxic stroke? Neuroimage 37:1338–1345PubMedCrossRefGoogle Scholar
  48. Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, Tsunazawa Y, Suzuki T, Yanagida T, Kubota K (2001) Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 14:1186–1192PubMedCrossRefGoogle Scholar
  49. Miyai I, Yagura H, Oda I, Konishi I, Eda H, Suzuki T, Kubota K (2002) Premotor cortex is involved in restoration of gait in stroke. Ann Neurol 52:188–194PubMedCrossRefGoogle Scholar
  50. Miyai I, Yagura H, Hatakenaka M, Oda I, Konishi I, Kubota K (2003) Longitudinal optical imaging study for locomotor recovery after stroke. Stroke 34:2866–2870PubMedCrossRefGoogle Scholar
  51. Miyai I, Suzuki M, Hatakenaka M, Kubota K (2006) Effect of body weight support on cortical activation during gait in patients with stroke. Exp Brain Res 169:85–91PubMedCrossRefGoogle Scholar
  52. Okamoto M, Dan H, Sakamoto K, Takeo K, Shimizu K, Kohno S, Oda I, Isobe S, Suzuki T, Kohyama K, Dan I (2004) Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. Neuroimage 21:99–111PubMedCrossRefGoogle Scholar
  53. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  54. Pochon JB, Levy R, Poline JB, Crozier S, Lehericy S, Pillon B, Deweer B, Le Bihan D, Dubois B (2001) The role of dorsolateral prefrontal cortex in the preparation of forthcoming actions: an fMRI study. Cereb Cortex 11:260–266PubMedCrossRefGoogle Scholar
  55. Rajah MN, D’Esposito M (2005) Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. Brain 128:1964–1983PubMedCrossRefGoogle Scholar
  56. Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Loken WJ, Thornton AE, Acker JD (1997) Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 7:268–282PubMedCrossRefGoogle Scholar
  57. Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD (2004) Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging 25:377–396PubMedCrossRefGoogle Scholar
  58. Reuter-Lorenz PA, Jonides J, Smith EE, Hartley A, Miller A, Marshuetz C, Koeppe RA (2000) Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci 12:174–187PubMedCrossRefGoogle Scholar
  59. Riecker A, Grodd W, Klose U, Schulz JB, Groschel K, Erb M, Ackermann H, Kastrup A (2003) Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. J Cereb Blood Flow Metab 23:565–573PubMedCrossRefGoogle Scholar
  60. Rubino FA (2002) Gait disorders. Neurologist 8:254–262PubMedCrossRefGoogle Scholar
  61. Rypma B, Berger JS, D’Esposito M (2002) The influence of working-memory demand and subject performance on prefrontal cortical activity. J Cogn Neurosci 14:721–731PubMedCrossRefGoogle Scholar
  62. Saager RB, Berger AJ (2005) Direct characterization and removal of interfering absorption trends in two-layer turbid media. J Opt Soc Am A Opt Image Sci Vis 22:1874–1882PubMedCrossRefGoogle Scholar
  63. Schroeter ML, Zysset S, Kruggel F, von Cramon DY (2003) Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy. Neuroimage 19:555–564PubMedCrossRefGoogle Scholar
  64. Secher NH, Seifert T, Van Lieshout JJ (2008) Cerebral blood flow and metabolism during exercise: implications for fatigue. J Appl Physiol 104:306–314PubMedCrossRefGoogle Scholar
  65. Snijders AH, van de Warrenburg BP, Giladi N, Bloem BR (2007) Neurological gait disorders in elderly people: clinical approach and classification. Lancet Neurol 6:63–74PubMedCrossRefGoogle Scholar
  66. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315PubMedCrossRefGoogle Scholar
  67. Strangman G, Franceschini MA, Boas DA (2003) Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters. Neuroimage 18:865–879PubMedCrossRefGoogle Scholar
  68. Studenski S, Perera S, Wallace D, Chandler JM, Duncan PW, Rooney E, Fox M, Guralnik JM (2003) Physical performance measures in the clinical setting. J Am Geriatr Soc 51:314–322PubMedCrossRefGoogle Scholar
  69. Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K (2004) Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23:1020–1026PubMedCrossRefGoogle Scholar
  70. Suzuki M, Miyai I, Ono T, Kubota K (2008) Activities in the frontal cortex and gait performance are modulated by preparation. An fNIRS study. Neuroimage 39:600–607PubMedCrossRefGoogle Scholar
  71. Teng EL, Chui HC (1987) The Modified Mini-Mental State (3MS) examination. J Clin Psychiatry 48:314–318PubMedGoogle Scholar
  72. Verghese J, Wang C, Lipton RB, Holtzer R, Xue X (2007) Quantitative gait dysfunction and risk of cognitive decline and dementia. J Neurol Neurosurg Psychiatry 78:929–935PubMedCrossRefGoogle Scholar
  73. Viallet F, Massion J, Massarino R, Khalil R (1992) Coordination between posture and movement in a bimanual load lifting task: putative role of a medial frontal region including the supplementary motor area. Exp Brain Res 88:674–684PubMedCrossRefGoogle Scholar
  74. Volpato S, Blaum C, Resnick H, Ferrucci L, Fried LP, Guralnik JM (2002) Comorbidities and impairments explaining the association between diabetes and lower extremity disability: the women’s health and aging study. Diabetes Care 25:678–683PubMedCrossRefGoogle Scholar
  75. Waite LM, Grayson DA, Piguet O, Creasey H, Bennett HP, Broe GA (2005) Gait slowing as a predictor of incident dementia: 6-year longitudinal data from the Sydney Older Persons Study. J Neurol Sci 229–230:89–93PubMedCrossRefGoogle Scholar
  76. Ward NS, Frackowiak RS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888PubMedCrossRefGoogle Scholar
  77. Weuve J, Kang JH, Manson JE, Breteler MM, Ware JH, Grodstein F (2004) Physical activity, including walking, and cognitive function in older women. JAMA 292:1454–1461PubMedCrossRefGoogle Scholar
  78. Zhang Q, Brown EN, Strangman GE (2007) Adaptive filtering to reduce global interference in evoked brain activity detection: a human subject case study. J Biomed Opt 12:064009PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Taeko Harada
    • 1
    Email author
  • Ichiro Miyai
    • 2
  • Mitsuo Suzuki
    • 2
  • Kisou Kubota
    • 2
  1. 1.The Research Institute of System SciencesNihon Fukushi UniversityHandaJapan
  2. 2.Neurorehabilitation Research InstituteMorinomiya HospitalOsakaJapan

Personalised recommendations