Conservation of Reactive Stabilization Strategies in the Presence of Step Length Asymmetries During Walking
Chang Liu, Lucas De Macedo, James M Finley, Chang Liu, Lucas De Macedo, James M Finley
Abstract
The ability to maintain dynamic balance in response to unexpected perturbations during walking is largely mediated by reactive control strategies. Reactive control during perturbed walking can be characterized by multiple metrics such as measures of whole-body angular momentum (WBAM), which capture the rotational dynamics of the body, and through Floquet analysis which captures the orbital stability of a limit cycle attractor. Recent studies have demonstrated that people with spatiotemporal asymmetries during gait have impaired control of whole-body dynamics as evidenced by higher peak-to-peak ranges of WBAM over the gait cycle. While this may suggest that spatiotemporal asymmetries could impair stability, no studies have quantified how direct modification of asymmetry influences reactive balance control. Here, we used a biofeedback paradigm that allows participants to systematically adopt different levels of step length asymmetry to test the hypothesis that walking asymmetrically impairs the reactive control of balance. In addition, we tested the hypothesis that perturbations to the non-dominant leg would cause less whole-body rotation due to its hypothesized role in weight support during walking. We characterized reactive control strategies in two ways. We first computed integrated angular momentum to characterize changes in whole-body configuration during multi-step responses to perturbations. We also computed the maximum Floquet multipliers (FMs) across the gait cycle, which represent the rate of convergence back to limit cycle behavior. Our results show that integrated angular momentum during the perturbation step and subsequent recovery steps, as well as the magnitude of maximum FMs over the gait cycle, do not change across levels of asymmetry. However, our results showed both limb-dependent and limb-independent responses to unexpected perturbations. Overall, our findings suggest that there is no causal relationship between step length asymmetry and impaired reactive control of balance in the absence of neuromotor impairments. Our approach could be used in future studies to determine if reducing asymmetries in populations with neuromotor impairments, such people post-stroke or amputees improves dynamic stability.
Keywords: angular momentum; asymmetry; locomotion; reactive control; stability.
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References
- Allen J. L., Kautz S. A., Neptune R. R. (2011). Step length asymmetry is representative of compensatory mechanisms used in post-stroke hemiparetic walking. Gait Posture 33, 538–543. 10.1016/j.gaitpost.2011.01.004
- Aprigliano F., Martelli D., Tropea P., Pasquini G., Micera S., Monaco V. (2017). Ageing does not affect the intralimb coordination elicited by slip-like perturbation of different intensities. J. Neurophysiol. 118, 1739–1748. 10.1152/jn.00844.2016
- Awad L. N., Reisman D. S., Pohlig R. T., Binder-Macleod S. A. (2016). Reducing the cost of transport and increasing walking distance after stroke: a randomized controlled trial on fast locomotor training combined with functional electrical stimulation. Neurorehabil. Neural Repair 30, 661–670. 10.1177/1545968315619696
- Balasubramanian C. K., Bowden M. G., Neptune R. R., Kautz S. A. (2007). Relationship between step length asymmetry and walking performance in subjects with chronic hemiparesis. Arch. Phys. Med. Rehabil. 88, 43–49. 10.1016/j.apmr.2006.10.004
- Barth D. G., Schumacher L., Thomas S. S. (1992). Gait analysis and energy cost of below-knee amputees wearing six different prosthetic feet. J. Prosthetics Orthot. 4, 63–75. 10.1097/00008526-199200420-00001
- Beurskens R., Wilken J. M., Dingwell J. B. (2014). Dynamic stability of individuals with transtibial amputation walking in destabilizing environments. J. Biomech. 47, 1675–1681. 10.1016/j.jbiomech.2014.02.033
- Bhatt T., Wening J. D., Pai Y. C. (2006). Adaptive control of gait stability in reducing slip-related backward loss of balance. Exp. Brain Res. 170, 61–73. 10.1007/s00221-005-0189-5
- Bruijn S. M., Meijer O. G., Beek P. J., van Dieën J. H. (2013). Assessing the stability of human locomotion: a review of current measures. J. R. Soc. Interface 10:20120999. 10.1098/rsif.2012.0999
- Bruijn S. M., van Dieën J. H., Meijer O. G., Beek P. J. (2009). Statistical precision and sensitivity of measures of dynamic gait stability. J. Neurosci. Methods 178, 327–333. 10.1016/j.jneumeth.2008.12.015
- Chen G., Patten C., Kothari D. H., Zajac F. E. (2005). Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds. Gait Posture 22, 51–56. 10.1016/j.gaitpost.2004.06.009
- Dempster W. T. (1955). Space requirements of the seated operator: geometrical, kinematic, and mechanical aspects other body with special reference to the limbs. WADC Tech. Rep. [Epub ahead of print]. 1–254. 10.21236/ad0087892
- Dingwell J. B., Cusumano J. P. (2000). Nonlinear time series analysis of normal and pathological human walking. Chaos 10, 848–863. 10.1063/1.1324008
- Dingwell J. B., Cusumano J. P., Cavanagh P. R., Sternad D. (2001). Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. J. Biomech. Eng. 123, 27–32. 10.1115/1.1336798
- Dingwell J. B., Kang H. G. (2007). Differences between local and orbital dynamic stability during human walking. J. Biomech. Eng. 129, 586–593. 10.1115/1.2746383
- Granata K. P., Lockhart T. E. (2008). Dynamic stability differences in fall-prone and healthy adults. J. Electromyogr. Kinesiol. 18, 172–178. 10.1016/j.jelekin.2007.06.008
- Hanavan E. P., Jr. (1964). A mathematical model of the human body AMRL-TR-64-102. AMRL TR. [Epub ahead of print]. 1–149. 10.1037/e400822004-001
- Hausdorff J. M., Purdon P. L., Peng C. K., Ladin Z., Wei J. Y., Goldberger A. L. (1996). Fractal dynamics of human gait: stability of long-range correlations in stride interval fluctuations. J. Appl. Physiol. 80, 1448–1457. 10.1152/jappl.1996.80.5.1448
- Havens K. L., Mukherjee T., Finley J. M. (2018). Analysis of biases in dynamic margins of stability introduced by the use of simplified center of mass estimates during walking and turning. Gait Posture 59, 162–167. 10.1016/j.gaitpost.2017.10.002
- Heiden T. L., Sanderson D. J., Inglis J. T., Siegmund G. P. (2006). Adaptations to normal human gait on potentially slippery surfaces: the effects of awareness and prior slip experience. Gait Posture 24, 237–246. 10.1016/j.gaitpost.2005.09.004
- Herr H. M., Popovic M. (2008). Angular momentum in human walking. J. Exp. Biol. 211, 467–481. 10.1242/jeb.008573
- Hobbelen D. G. E., Wisse M. (2007). “Limit cycle walking,” in Humanoid Robots: Human-like Machines, ed. Hackel M. (Vienna: Advanced Robotic Systems International; ), 277–294.
- Hof A. L. (2008). The “extrapolated center of mass” concept suggests a simple control of balance in walking. Hum. Mov. Sci. 27, 112–125. 10.1016/j.humov.2007.08.003
- Hof A. L., Gazendam M. G. J., Sinke W. E. (2005). The condition for dynamic stability. J. Biomech. 38, 1–8. 10.1016/j.jbiomech.2004.03.025
- Hurmuzlu Y., Basdogan C. (1994). On the measurement of dynamic stability of human locomotion. J. Biomech. Eng. 116, 30–36. 10.1115/1.2895701
- Hurmuzlu Y., Basdogan C., Stoianovici D. (1996). Kinematics and dynamic stability of the locomotion of post-polio patients. J. Biomech. Eng. 118, 405–411. 10.1115/1.2796024
- Kao P.-C., Dingwell J. B., Higginson J. S., Binder-Macleod S. (2014). Dynamic instability during post-stroke hemiparetic walking. Gait Posture 40, 457–463. 10.1016/j.gaitpost.2014.05.014
- Kuo A. D. (1999). Stabilization of lateral motion in passive dynamic walking. Int. J. Rob. Res. 18, 917–930. 10.1177/02783649922066655
- Kurz M. J., Arpin D. J., Corr B. (2012). Differences in the dynamic gait stability of children with cerebral palsy and typically developing children. Gait Posture 36, 600–604. 10.1016/j.gaitpost.2012.05.029
- Lee S. J., Hidler J. (2008). Biomechanics of overground vs. treadmill walking in healthy individuals. J. Appl. Physiol. 104, 747–755. 10.1152/japplphysiol.01380.2006
- Lewek M. D., Bradley C. E., Wutzke C. J., Zinder S. M. (2014). The relationship between spatiotemporai gait asymmetry and balance in individuals with chronic stroke. J. Appl. Biomech. 30, 31–36. 10.1123/jab.2012-0208
- Martelli D., Monaco V., Bassi Luciani L., Micera S. (2013). Angular momentum during unexpected multidirectional perturbations delivered while walking. IEEE Trans. Biomed. Eng. 60, 1785–1795. 10.1109/TBME.2013.2241434
- McAndrew P. M., Dingwell J. B., Wilken J. M. (2010). Walking variability during continuous pseudo-random oscillations of the support surface and visual field. J. Biomech. 43, 1470–1475. 10.1016/j.jbiomech.2010.02.003
- McAndrew P. M., Wilken J. M., Dingwell J. B. (2012). Dynamic stability of human walking in visually and mechanically destabilizing environments. J. Biomech. 44, 644–649. 10.1016/j.jbiomech.2010.11.007
- McAndrew Young P. M., Dingwell J. B. (2012). Voluntarily changing step length or step width affects dynamic stability of human walking. Gait PostureInt. 35, 472–477. 10.1016/j.gaitpost.2011.11.010
- Nagano H., Begg R. K., Sparrow W. A., Taylor S. (2011). Ageing and limb dominance effects on foot-ground clearance during treadmill and overground walking. Clin. Biomech. 26, 962–968. 10.1016/j.clinbiomech.2011.05.013
- Nott C. R., Neptune R. R., Kautz S. A. (2014). Relationships between frontal-plane angular momentum and clinical balance measures during post-stroke hemiparetic walking. Gait Posture 39, 129–134. 10.1016/j.gaitpost.2013.06.008
- Õunpuu S., Winter D. A. (1989). Bilateral electromyographical analysis of the lower limbs during walking in normal adults. Electroencephalogr. Clin. Neurophysiol. 72, 429–438. 10.1016/0013-4694(89)90048-5
- Pai Y.-C., Wening J. D., Runtz E. F., Iqbal K., Pavol M. J. (2003). Role of feedforward control of movement stability in reducing slip-related balance loss and falls among older adults. J. Neurophysiol. 90, 755–762. 10.1152/jn.01118.2002
- Patla A. E. (1993). “Age-related changes in visually guided locomotion over different terrains: major issues,” in Sensorimotor Impairment in the Elderly, eds Stelmach G. E., Hömberg V. (Dordrecht: Springer Netherlands; ), 231–252.
- Popovic M., Hofmann A., Herr H. (2004). “Angular momentum regulation during human walking: biomechanics and control,” in Proceedings of IEEE International Conference on Robotics and Automation, 2004 ICRA’04 (New Orleans, LA: IEEE), 2405–2411.
- Reisman D. S., Wityk R., Silver K., Bastian A. J. (2009). Split-belt treadmill adaptation transfers to overground walking in persons poststroke. Neurorehabil. Neural Repair 23, 735–744. 10.1177/1545968309332880
- Sadeghi H., Allard P., Duhaime M. (1997). Functional gait asymmetry in able-bodied subjects. Hum. Mov. Sci. 16, 243–258. 10.1016/s0167-9457(96)00054-1
- Sánchez N., Park S., Finley J. M. (2017). Evidence of energetic optimization during adaptation differs for metabolic, mechanical, and perceptual estimates of energetic cost. Sci. Rep. 7:7682. 10.1038/s41598-017-08147-y
- Silverman A. K., Neptune R. R. (2011). Differences in whole-body angular momentum between below-knee amputees and non-amputees across walking speeds. J. Biomech. 44, 379–385. 10.1016/j.jbiomech.2010.10.027
- Song J., Sigward S., Fisher B., Salem G. J. (2012). Altered dynamic postural control during step turning in persons with early-stage Parkinson’s disease. Parkinsons Dis. 2012:386962. 10.1155/2012/386962
- Stergiou N., Decker L. M. (2011). Human movement variability, nonlinear dynamics, and pathology: is there a connection? Hum. Mov. Sci. 30, 869–888. 10.1016/j.humov.2011.06.002
- Tang P. F., Woollacott M. H., Chong R. K. Y. (1998). Control of reactive balance adjustments in perturbed human walking: roles of proximal and distal postural muscle activity. Exp. Brain Res. 119, 141–152. 10.1007/s002210050327
- Underwood H. A., Tokuno C. D., Eng J. J. (2004). A comparison of two prosthetic feet on the multi-joint and multi-plane kinetic gait compensations in individuals with a unilateral trans-tibial amputation. Clin. Biomech. 19, 609–616. 10.1016/j.clinbiomech.2004.02.005
- Vistamehr A., Kautz S. A., Bowden M. G., Neptune R. R. (2016). Correlations between measures of dynamic balance in individuals with post-stroke hemiparesis. J. Biomech. 49, 396–400. 10.1016/j.jbiomech.2015.12.047
- Winiarski S., Czamara A. (2012). Evaluation of gait kinematics and symmetry during the first two stages of physiotherapy after anterior cruciate ligament reconstruction. Acta Bioeng. Biomech. 14, 91–100. 10.5277/abb120212
- Winter D. A. (2009). Biomechanics and Motor Control of Human Movement. New Jersey, NJ: John Wiley & Sons, Inc.
- Woollacott M. H., Tang P.-F. (1997). Balance control during walking in the older adult: research and its implications. Phys. Ther. 77, 646–660. 10.1093/ptj/77.6.646
- Zmitrewicz R. J., Neptune R. R., Walden J. G., Rogers W. E., Bosker G. W. (2006). The effect of foot and ankle prosthetic components on braking and propulsive impulses during transtibial amputee gait. Arch. Phys. Med. Rehabil. 87, 1334–1339. 10.1016/j.apmr.2006.06.013
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