Stride-time variability and sensorimotor cortical activation during walking

The time it takes between consecutive foot contacts from the same leg is referred to as the stride-time interval. Several investigations have shown that the variations that are present in the stride time intervals are linked to walking balance. In this study, functional near infrared spectroscopy (fNIRS) was utilized to evaluate whether activation in the medial sensorimotor cortices reflects the amount of variations seen in the stride-time intervals. Thirteen healthy adults (Age=23.7 ± 1.4 yrs.) walked forwards and backwards on a programmable treadmill. Each walking condition consisted of two sessions, with each being comprised of five alternating blocks of standing still or walking at 0.45 m/s. Activation in the medial sensorimotor cortices was measured using an fNIRS system, which consisted of a 4 × 4 grid of infrared optode emitter/detector pairs. The optodes were positioned on the participant's head using the International 10/20 system with Cz located beneath the center of the front two rows of optodes. We evaluated the block-wise changes in the amount of oxygenated (oxyHb) and deoxygenated hemoglobin (deoxyHb) in the channels that were located over the supplementary motor area, pre-central gyrus, post-central gyrus and superior parietal lobule. Throughout the experiment, a footswitch system was used to concurrently measure the amount of variation present in the stride-time intervals. Our results showed that oxyHb was greater in the supplementary motor area, pre-central gyrus, and superior parietal lobule when participants walked backwards rather than forwards, which suggests that backward walking presents more of a challenge to the nervous system as it controls the stepping pattern. Additionally, there was a significant decrease in the amount of deoxyHb present in the supplementary motor area while walking backward. Consistent with previous investigations, we noted that the amount of variability present in the stride-time intervals was greater during backward walking compared to forward walking. In addition, the amount of variation in the stride-time intervals while walking forward was positively correlated with the maximum oxyHb response found in the pre-central gyrus and supplementary motor area, which has not been previously shown. This neurobehavioral relationship supports the notion that the subtle variations found in the stride-time intervals are partly associated with processing demands by the motor cortices for regulating the forward temporal kinematics.

[1]  Martin Wolf,et al.  Task complexity relates to activation of cortical motor areas during uni- and bimanual performance: A functional NIRS study , 2009, NeuroImage.

[2]  Makoto Ito,et al.  Time courses of brain activation and their implications for function: A multichannel near-infrared spectroscopy study during finger tapping , 2007, Neuroscience Research.

[3]  Anders M. Dale,et al.  Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy , 2004, NeuroImage.

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

[5]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[6]  Raymond F Reynolds,et al.  Visual guidance of the human foot during a step , 2005, The Journal of physiology.

[7]  J. Donelan,et al.  Mechanical and metabolic requirements for active lateral stabilization in human walking. , 2004, Journal of biomechanics.

[8]  T G Deliagina,et al.  Activity of motor cortex neurons during backward locomotion. , 2011, Journal of neurophysiology.

[9]  V. Edgerton,et al.  Robotic training and spinal cord plasticity , 2009, Brain Research Bulletin.

[10]  Jeffrey M. Hausdorff Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. , 2007, Human movement science.

[11]  K. Kubota,et al.  Longitudinal Optical Imaging Study for Locomotor Recovery After Stroke , 2003, Stroke.

[12]  S. Studenski,et al.  Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed , 2005, Journal of NeuroEngineering and Rehabilitation.

[13]  David A. Boas,et al.  A Quantitative Comparison of Simultaneous BOLD fMRI and NIRS Recordings during Functional Brain Activation , 2002, NeuroImage.

[14]  Joel Vilensky,et al.  A kinematic comparison of backward and forward walking in humans , 1987 .

[15]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[16]  Nicholas Stergiou,et al.  Aging and partial body weight support affects gait variability , 2008, Journal of NeuroEngineering and Rehabilitation.

[17]  J. F. Yang,et al.  Backward walking: a simple reversal of forward walking? , 1989, Journal of motor behavior.

[18]  A. Thorstensson How is the normal locomotor program modified to produce backward walking? , 2004, Experimental Brain Research.

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

[20]  Y. Laufer,et al.  Effect of age on characteristics of forward and backward gait at preferred and accelerated walking speed. , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[21]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[22]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[23]  Nicholas Stergiou,et al.  The aging humans neuromuscular system expresses less certainty for selecting joint kinematics during gait , 2003, Neuroscience Letters.

[24]  A. Minetti,et al.  The transmission efficiency of backward walking at different gradients , 2001, Pflügers Archiv.

[25]  B. Dobkin,et al.  Human lumbosacral spinal cord interprets loading during stepping. , 1997, Journal of neurophysiology.

[26]  Jeffrey M. Hausdorff Gait dynamics in Parkinson's disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. , 2009, Chaos.

[27]  David A Boas,et al.  Eigenvector-based spatial filtering for reduction of physiological interference in diffuse optical imaging. , 2005, Journal of biomedical optics.

[28]  M S Redfern,et al.  A model of foot placement during gait. , 1994, Journal of biomechanics.

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

[30]  Roland R Roy,et al.  Spinal Cord-Transected Mice Learn to Step in Response to Quipazine Treatment and Robotic Training , 2005, The Journal of Neuroscience.

[31]  D. Delpy,et al.  System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination , 1988, Medical and Biological Engineering and Computing.

[32]  Ichiro Miyai,et al.  Frontal regions involved in learning of motor skill—A functional NIRS study , 2007, NeuroImage.

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

[34]  Jeffrey M. Hausdorff,et al.  Gait variability and fall risk in community-living older adults: a 1-year prospective study. , 2001, Archives of physical medicine and rehabilitation.

[35]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  Guang-Zhong Yang,et al.  Assessment of the cerebral cortex during motor task behaviours in adults: A systematic review of functional near infrared spectroscopy (fNIRS) studies , 2011, NeuroImage.

[37]  Ichiro Miyai,et al.  Effect of body weight support on cortical activation during gait in patients with stroke , 2006, Experimental Brain Research.

[38]  U. Nayak,et al.  The effect of age on variability in gait. , 1984, Journal of gerontology.

[39]  Jeffrey M. Hausdorff,et al.  Rhythmic auditory stimulation modulates gait variability in Parkinson's disease , 2007, The European journal of neuroscience.

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

[41]  David A. Boas,et al.  A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans , 2006, NeuroImage.

[42]  F. Lacquaniti,et al.  Motor patterns for human gait: backward versus forward locomotion. , 1998, Journal of neurophysiology.

[43]  Julia T. Choi,et al.  Adaptation reveals independent control networks for human walking , 2007, Nature Neuroscience.

[44]  Heidi Johansen-Berg,et al.  Brain Activity Changes Associated With Treadmill Training After Stroke , 2009, Stroke.

[45]  M. Honda,et al.  Enhanced lateral premotor activity during paradoxical gait in Parkinson's disease , 1999, Annals of neurology.

[46]  Jeffrey M. Hausdorff,et al.  Increased gait unsteadiness in community-dwelling elderly fallers. , 1997, Archives of physical medicine and rehabilitation.

[47]  Arvind Caprihan,et al.  Ankle dorsiflexion fMRI in children with cerebral palsy undergoing intensive body‐weight‐supported treadmill training: a pilot study , 2006, Developmental medicine and child neurology.

[48]  D. Winter,et al.  Control of whole body balance in the frontal plane during human walking. , 1993, Journal of biomechanics.

[49]  A. Luft,et al.  Treadmill Exercise Activates Subcortical Neural Networks and Improves Walking After Stroke: A Randomized Controlled Trial , 2008, Stroke.

[50]  van Deursen RW,et al.  Does a single control mechanism exist for both forward and backward walking? , 1998, Gait & posture.

[51]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[52]  Gammon M Earhart,et al.  Backward walking in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[53]  Jeffrey M. Hausdorff,et al.  Gait variability and basal ganglia disorders: Stride‐to‐stride variations of gait cycle timing in parkinson's disease and Huntington's disease , 1998, Movement disorders : official journal of the Movement Disorder Society.

[54]  S. Studenski,et al.  Gait Variability Is Associated with Subclinical Brain Vascular Abnormalities in High-Functioning Older Adults , 2007, Neuroepidemiology.

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

[56]  Jeffrey M. Hausdorff,et al.  Effect of gait speed on gait rhythmicity in Parkinson's disease: variability of stride time and swing time respond differently , 2005, Journal of NeuroEngineering and Rehabilitation.

[57]  Susan J Harkema,et al.  The human spinal cord interprets velocity-dependent afferent input during stepping. , 2004, Brain : a journal of neurology.

[58]  M. Hallett,et al.  Virtual Reality–Induced Cortical Reorganization and Associated Locomotor Recovery in Chronic Stroke: An Experimenter-Blind Randomized Study , 2005, Stroke.

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

[60]  M Honda,et al.  Mechanisms underlying gait disturbance in Parkinson's disease: a single photon emission computed tomography study. , 1999, Brain : a journal of neurology.