White matter microstructural organization and gait stability in older adults

Understanding age-related decline in gait stability and the role of alterations in brain structure is crucial. Here, we studied the relationship between white matter microstructural organization using Diffusion Tensor Imaging (DTI) and advanced gait stability measures in 15 healthy young adults (range 18–30 years) and 25 healthy older adults (range 62–82 years). Among the different gait stability measures, only stride time and the maximum Lyapunov exponent (which quantifies how well participants are able to attenuate small perturbations) were found to decline with age. White matter microstructural organization (FA) was lower throughout the brain in older adults. We found a strong correlation between FA in the left anterior thalamic radiation and left corticospinal tract on the one hand, and step width and safety margin (indicative of how close participants are to falling over) on the other. These findings suggest that white matter FA in tracts connecting subcortical and prefrontal areas is associated with the implementation of an effective stabilization strategy during gait.

[1]  M. Woollacott,et al.  Attention and the control of posture and gait: a review of an emerging area of research. , 2002, Gait & posture.

[2]  Peter J Beek,et al.  Online gait event detection using a large force platform embedded in a treadmill. , 2008, Journal of biomechanics.

[3]  P. Beek,et al.  Maximum Lyapunov exponents as predictors of global gait stability: a modelling approach. , 2012, Medical engineering & physics.

[4]  Daniel P. Ferris,et al.  Electrocortical activity is coupled to gait cycle phase during treadmill walking , 2011, NeuroImage.

[5]  A. Hof.  The 'extrapolated center of mass' concept suggests a simple control of balance in walking. , 2008, Human movement science.

[6]  Arthur D. Kuo,et al.  Stabilization of Lateral Motion in Passive Dynamic Walking , 1999, Int. J. Robotics Res..

[7]  Richard Beare,et al.  Cerebral White Matter Lesions, Gait, and the Risk of Incident Falls: A Prospective Population-Based Study , 2009, Stroke.

[8]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[9]  S. Resnick,et al.  Longitudinal Magnetic Resonance Imaging Studies of Older Adults: A Shrinking Brain , 2003, The Journal of Neuroscience.

[10]  Peter J Beek,et al.  Speeding up or slowing down?: Gait adaptations to preserve gait stability in response to balance perturbations. , 2012, Gait & posture.

[11]  H. Fukuyama,et al.  Brain functional activity during gait in normal subjects: a SPECT study , 1997, Neuroscience Letters.

[12]  R. Baloh,et al.  A longitudinal study of gait and balance dysfunction in normal older people. , 2003, Archives of neurology.

[13]  I. Deary,et al.  Brain white matter lesions detected by magnetic resosnance imaging are associated with balance and gait speed , 2003 .

[14]  Yei-Yu Yeh,et al.  Cortical control of gait in healthy humans: an fMRI study , 2008, Journal of Neural Transmission.

[15]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  Jonathan B Dingwell,et al.  Voluntarily changing step length or step width affects dynamic stability of human walking. , 2012, Gait & posture.

[17]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[18]  Jean-Marc Constans,et al.  Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging , 2009, Neurobiology of Aging.

[19]  I. Rosenberg,et al.  Clinical prediction of fall risk and white matter abnormalities: a diffusion tensor imaging study. , 2012, Archives of neurology.

[20]  Stephen M. Smith,et al.  Crossing fibres in tract-based spatial statistics , 2010, NeuroImage.

[21]  F. Schmitt,et al.  Age and gender effects on human brain anatomy: A voxel-based morphometric study in healthy elderly , 2007, Neurobiology of Aging.

[22]  J. Dingwell,et al.  Dynamic stability of human walking in visually and mechanically destabilizing environments. , 2011, Journal of biomechanics.

[23]  Martin Wiesmann,et al.  Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging , 2004, NeuroImage.

[24]  Henry Brodaty,et al.  Brain white matter hyperintensities, executive dysfunction, instability, and falls in older people: a prospective cohort study. , 2012, The journals of gerontology. Series A, Biological sciences and medical sciences.

[25]  A. Pfefferbaum,et al.  Diffusion tensor imaging and aging , 2006, Neuroscience & Biobehavioral Reviews.

[26]  B. E. Maki,et al.  Gait Changes in Older Adults: Predictors of Falls or Indicators of Fear? , 1997, Journal of the American Geriatrics Society.

[27]  Jesse C. Dean,et al.  The Effect of Lateral Stabilization on Walking in Young and Old Adults , 2007, IEEE Transactions on Biomedical Engineering.

[28]  M S Buchsbaum,et al.  Regional and global changes in cerebral diffusion with normal aging. , 2001, AJNR. American journal of neuroradiology.

[29]  Ronald C Petersen,et al.  Normative spatiotemporal gait parameters in older adults. , 2011, Gait & posture.

[30]  A. Kuo,et al.  Direction-dependent control of balance during walking and standing. , 2009, Journal of neurophysiology.

[31]  Sebastiaan Overeem,et al.  Gait-related cerebral alterations in patients with Parkinson's disease with freezing of gait. , 2011, Brain : a journal of neurology.

[32]  Jonathan B. Dingwell,et al.  A direct comparison of local dynamic stability during unperturbed standing and walking , 2006, Experimental Brain Research.

[33]  Daniel S. Margulies,et al.  Long-term effects of motor training on resting-state networks and underlying brain structure , 2011, NeuroImage.

[34]  Jonathan B Dingwell,et al.  The effects of sensory loss and walking speed on the orbital dynamic stability of human walking. , 2007, Journal of biomechanics.

[35]  F Fazekas,et al.  Deep frontal and periventricular age related white matter changes but not basal ganglia and infratentorial hyperintensities are associated with falls: cross sectional results from the LADIS study , 2009, Journal of Neurology, Neurosurgery, and Psychiatry.

[36]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[37]  P. Beek,et al.  Assessing the stability of human locomotion: a review of current measures , 2013, Journal of The Royal Society Interface.

[38]  M. Ioffe,et al.  Learning postural tasks in hemiparetic patients with lesions of left versus right hemisphere , 2010, Experimental Brain Research.

[39]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[40]  L. Rubenstein.  Falls in older people: epidemiology, risk factors and strategies for prevention. , 2006, Age and ageing.

[41]  Stephen M. Smith,et al.  Age-related changes in grey and white matter structure throughout adulthood , 2010, NeuroImage.

[42]  Alan C. Evans,et al.  Cortical thickness is associated with gait disturbances in cerebral small vessel disease , 2012, NeuroImage.

[43]  S. Swinnen,et al.  Proprioceptive sensibility in the elderly: Degeneration, functional consequences and plastic-adaptive processes , 2009, Neuroscience & Biobehavioral Reviews.

[44]  J. Dingwell,et al.  Effects of walking speed, strength and range of motion on gait stability in healthy older adults. , 2008, Journal of biomechanics.

[45]  Richard Beare,et al.  The location of white matter lesions and gait—A voxel‐based study , 2010, Annals of neurology.

[46]  S. Swinnen,et al.  Dynamics of hemispheric specialization and integration in the context of motor control , 2006, Nature Reviews Neuroscience.

[47]  David E. Meyer,et al.  Attention and Control , 1993 .

[48]  P. Aerts,et al.  Low vision affects dynamic stability of gait. , 2010, Gait & posture.

[49]  S. Swinnen,et al.  White matter fractional anisotropy predicts balance performance in older adults , 2012, Neurobiology of Aging.

[50]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.

[51]  A. Hof,et al.  Control of lateral balance in walking. Experimental findings in normal subjects and above-knee amputees. , 2007, Gait & posture.

[52]  Roger P. Woods,et al.  Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation , 2004, NeuroImage.

[53]  A L Hof,et al.  The condition for dynamic stability. , 2005, Journal of biomechanics.

[54]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[55]  Jaap H van Dieën,et al.  Local dynamic stability and variability of gait are associated with fall history in elderly subjects. , 2012, Gait & posture.

[56]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[57]  S. Lord,et al.  Impact of White Matter Lesions on Physical Functioning and Fall Risk in Older People: A Systematic Review , 2011, Stroke.

[58]  David G Norris,et al.  Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. , 2011, Brain : a journal of neurology.

[59]  Takashi Hanakawa,et al.  Neuroimaging of standing and walking: Special emphasis on Parkinsonian gait , 2006 .

[60]  A Pfefferbaum,et al.  Neuroradiological characterization of normal adult ageing. , 2007, The British journal of radiology.

[61]  Patricia M McAndrew,et al.  Walking Variability during Continuous Pseudo-random Oscillations of the Support Surface and Visual Field , 2022 .

[62]  B. R. Bloem,et al.  Recent advances in functional neuroimaging of gait , 2007, Journal of Neural Transmission.

[63]  Nicholas Stergiou,et al.  Sensitivity of the Wolf’s and Rosenstein’s Algorithms to Evaluate Local Dynamic Stability from Small Gait Data Sets , 2011, Annals of Biomedical Engineering.

[64]  J. Duysens,et al.  Neural control of locomotion; Part 1: The central pattern generator from cats to humans , 1998 .

[65]  R W Baloh,et al.  Disequilibrium of unknown cause in older people , 1993, Annals of neurology.

[66]  Thomas Brandt,et al.  Real versus imagined locomotion: A [18F]-FDG PET-fMRI comparison , 2010, NeuroImage.

[67]  R. Cubelli,et al.  Impairments of trunk movements following left or right hemisphere lesions: dissociation between apraxic errors and postural instability. , 2003, Brain : a journal of neurology.

[68]  Samuel Patz,et al.  Diffusion Tensor Imaging, White Matter Lesions, the Corpus Callosum, and Gait in the Elderly , 2009, Stroke.

[69]  Jonathan B Dingwell,et al.  Dynamic margins of stability during human walking in destabilizing environments. , 2012, Journal of biomechanics.

[70]  Ichiro Miyai,et al.  Gait capacity affects cortical activation patterns related to speed control in the elderly , 2009, Experimental Brain Research.

[71]  Jonathan B Dingwell,et al.  Voluntary changes in step width and step length during human walking affect dynamic margins of stability. , 2012, Gait & posture.

[72]  Jonathan B Dingwell,et al.  Dynamic stability of superior vs. inferior segments during walking in young and older adults. , 2009, Gait & posture.

[73]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[74]  Y. Laufer,et al.  Standing Balance and Functional Recovery of Patients with Right and Left Hemiparesis in the Early Stages of Rehabilitation , 2003, Neurorehabilitation and neural repair.

[75]  Jaap H. van Dieën,et al.  Identification of elderly fallers by muscle strength measures , 2007, European Journal of Applied Physiology.

[76]  F. Prince,et al.  Comparison of three methods to estimate the center of mass during balance assessment. , 2004, Journal of biomechanics.

[77]  J. Medeiros,et al.  Does fear of falling influence spatial and temporal gait parameters in elderly persons beyond changes associated with normal aging? , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[78]  M. Grabiner,et al.  Variation in trunk kinematics influences variation in step width during treadmill walking by older and younger adults. , 2010, Gait & posture.

[79]  Martin Wiesmann,et al.  Imaging human supraspinal locomotor centers in brainstem and cerebellum , 2008, NeuroImage.