Abstract
To prevent falls, adjustment of foot placement is a frequently used strategy to regulate and restore gait stability. While foot trajectory adjustments have been studied during discrete stepping, online corrections during walking are more common in daily life. Here, we studied quick foot placement adjustments during gait, using an instrumented treadmill equipped with a projector, which allowed us to project virtual stepping stones. This allowed us to shift some of the approaching stepping stones in a chosen direction at a given moment, such that participants were forced to adapt their step in that specific direction and had varying time available to do so. Thirteen healthy participants performed six experimental trials all consisting of 580 stepping stones, and 96 of those stones were shifted anterior, posterior or lateral at one out of four distances from the participant. Overall, long-step gait adjustments were performed more successfully than short-step and side-step gait adjustments. We showed that the ability to execute movement adjustments depends on the direction of the trajectory adjustment. Our findings suggest that choosing different leg movement adjustments for obstacle avoidance comes with different risks and that strategy choice does not depend exclusively on environmental constraints. The used obstacle avoidance strategy choice might be a trade-off between the environmental factors (i.e., the cost of a specific adjustment) and individuals’ ability to execute a specific adjustment with success (i.e., the associated execution risk).
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References
Chen HC, Ashton-Miller JA, Alexander NB, Schultz AB (1994) Effects of age and available response time on ability to step over an obstacle. J Gerontol 49:M227–M233. doi:10.1093/geronj/49.5.M227
Day BL, Lyon IN (2000) Voluntary modification of automatic arm movements evoked by motion of a visual target. Exp Brain Res 130:159–168. doi:10.1007/s002219900218
Den Otter AR, Geurts AC, de Haart M, Mulder T, Duysens J (2005) Step characteristics during obstacle avoidance in hemiplegic stroke. Exp Brain Res 161:180–192
Fonteyn EMR, Schmitz-Hübsch T, Verstappen CC et al (2010) Falls in spinocerebellar ataxias: results of the EuroSCA fall study. Cerebellum 9:232–239. doi:10.1007/s12311-010-0155-z
Fonteyn EM, Heeren A, Engels JJ, Boer JJ, van de Warrenburg BP, Weerdesteyn V (2014) Gait adaptability training improves obstacle avoidance and dynamic stability in patients with cerebellar degeneration. Gait Posture 40:247–251. doi:10.1016/j.gaitpost.2014.04.190
Forster A, Young J (1995) Incidence and consequences of falls due to stroke: a systematic inquiry. BMJ 311:83–86. doi:10.1136/bmj.311.6997.83
Goodale MA, Pelisson D, Prablanc C (1986) Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320:748–750. doi:10.1038/320748a0
Heeren A, van Ooijen M, Geurts AC, Day BL, Janssen TW, Beek PJ, Roerdink M, Weerdesteyn V (2013) Step by step: a proof of concept study of C-Mill gait adaptability training in the chronic phase after stroke. J Rehabil Med 45:616–622. doi:10.2340/16501977-1180
Heijnen MJH, Romine NL, Stumpf DM, Rietdyk S (2014) Memory-guided obstacle crossing: more failures were observed for the trail limb versus lead limb. Exp Brain Res 232:2131–2142. doi:10.1007/s00221-014-3903-3
Hof AL, Gazendam MGJ, Sinke WE (2005) The condition for dynamic stability. J Biomech 38:1–8. doi:10.1016/j.jbiomech.2004.03.025
Hofstad CJ, van der Linde H, Nienhuis B, Weerdesteyn V, Duysens J, Geurts AC (2006) High failure rates when avoiding obstacles during treadmill walking in patients with a transtibial amputation. Arch Phys Med Rehabil 87:1115–1122. doi:10.1016/j.apmr.2006.04.009
Hofstad CJ, Weerdesteyn V, van der Linde H, Nienhuis B, Geurts AC, Duysens J (2009) Evidence for bilaterally delayed and decreased obstacle avoidance responses while walking with a lower limb prosthesis. Clin Neurophysiol 120:1009–1015. doi:10.1016/j.clinph.2009.03.003
Kim H-D, Brunt D (2009) The effect of a sensory perturbation on step direction or length while crossing an obstacle from quiet stance. Gait Posture 30:1–4. doi:10.1016/j.gaitpost.2009.02.016
Kim H-D, Brunt D (2013) Effect of a change in step direction from a forward to a lateral target in response to a sensory perturbation. J Electromyogr Kinesiol 23:851–857. doi:10.1016/j.jelekin.2013.03.001
Laroche DP, Cook SB, Mackala K (2012) Strength asymmetry increases gait asymmetry and variability in older women. Med Sci Sports Exerc 44:2172–2181. doi:10.1249/MSS.0b013e31825e1d31
Moraes R, Patla AE (2006) Determinants guiding alternate foot placement selection and the behavioral responses are similar when avoiding a real or a virtual obstacle. Exp Brain Res 171:497–510. doi:10.1007/s00221-005-0297-2
Moraes R, Allard F, Patla AE (2007) Validating determinants for an alternate foot placement selection algorithm during human locomotion in cluttered terrain. J Neurophysiol 98:1928–1940. doi:10.1152/jn.00044.2006
Nagano H, Begg RK, Sparrow WA, Taylor S (2011) Ageing and limb dominance effects on foot-ground clearance during treadmill and overground walking. Clin Biomech 26:962–968. doi:10.1016/j.clinbiomech.2011.05.013
Nonnekes JH, Talelli P, de Niet M, Reynolds RF, Weerdesteyn V, Day BL (2010) Deficits underlying impaired visually triggered step adjustments in mildly affected stroke patients. Neurorehabil Neural Repair 24:393–400. doi:10.1177/1545968309348317
O’Loughlin JL, Robitaille Y, Boivin JF, Suissa S (1993) Incidence of and risk factors for falls and injurious falls among the community-dwelling elderly. Am J Epidemiol 137:342–354
Patla AE (2003) Strategies for dynamic stability during adaptive human locomotion. IEEE Eng Med Biol Mag 22:48–52. doi:10.1109/MEMB.2003.1195695
Patla AE, Prentice SD, Rietdyk S, Allard F, Martin C (1999) What guides the selection of alternate foot placement during locomotion in humans. Exp Brain Res 128:441–450. doi:10.1007/s002210050867
Pélisson D, Prablanc C, Goodale MA, Jeannerod M (1986) Visual control of reaching movements without vision of the limb. II. Evidence of fast unconscious processes correcting the trajectory of the hand to the final position of a double-step stimulus. Exp Brain Res 62:303–311. doi:10.1007/BF00238849
Pisella L, Gréa H, Tilikete C, Vighetto A, Desmurget M, Rode G, Boisson D, Rossetti Y (2000) An “automatic pilot” for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 3:729–736. doi:10.1038/76694
Potocanac Z, de Bruin J, van der Veen S, Verschueren S, van Dieën J, Duysens J, Pijnappels M (2014a) Fast online corrections of tripping responses. Exp Brain Res 232:3579–3590. doi:10.1007/s00221-014-4038-2
Potocanac Z, Hoogkamer W, Carpes FP, Pijnappels M, Verschueren SM, Duysens J (2014b) Response inhibition during avoidance of virtual obstacles while walking. Gait Posture 39:641–644. doi:10.1016/j.gaitpost.2013.07.125
Reynolds RF, Day BL (2005) Rapid visuo-motor processes drive the leg regardless of balance constraints. Curr Biol 15:R48–R49. doi:10.1016/j.cub.2004.12.051
Reynolds RF, Day BL (2007) Fast visuomotor processing made faster by sound. J Physiol 583:1107–1115. doi:10.1113/jphysiol.2007.136192
Rietdyk S, Drifmeyer JE (2010) The rough-terrain problem: accurate foot targeting as a function of visual information regarding target location. J Mot Behav 42:37–48. doi:10.1080/00222890903303309
Robinovitch SN, Hsiao ET, Sandler R, Cortez J, Liu Q, Paiement GD (2000) Prevention of falls and fall-related fractures through biomechanics. Exerc Sport Sci Rev 28:74–79
Roerdink M (2008) Anchoring: moving from theory to therapy. Dissertation. VU University Amsterdam, Amsterdam
Roerdink M, Coolen BH, Clairbois BHE, Lamoth CJ, Beek PJ (2008) Online gait event detection using a large force platform embedded in a treadmill. J Biomech 41:2628–2632. doi:10.1016/j.jbiomech.2008.06.023
Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258
Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675
Schaefer SY, Mutha PK, Haaland KY, Sainburg RL (2012) Hemispheric specialization for movement control produces dissociable differences in online corrections after stroke. Cereb Cortex 22:1407–1419. doi:10.1093/cercor/bhr237
Smulders E, Schreven C, van Lankveld W, Duysens J, Weerdesteyn V (2009) Obstacle avoidance in persons with rheumatoid arthritis walking on a treadmill. Clin Exp Rheumatol 27:779–785
Soechting JF, Lacquaniti F (1983) Modification of trajectory of a pointing movement in response to a change in target location. J Neurophysiol 49:548–564
Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707. doi:10.1056/NEJM198812293192604
Tseng S-C, Stanhope SJ, Morton SM (2009) Impaired reactive stepping adjustments in older adults. J Gerontol A Biol Sci Med Sci 64:807–815. doi:10.1093/gerona/glp027
van Ooijen MW, Roerdink M, Trekop M, Visschedijk J, Janssen TW, Beek PJ (2013) Functional gait rehabilitation in elderly people following a fall-related hip fracture using a treadmill with visual context: design of a randomized controlled trial. BMC Geriatr 13:34. doi:10.1186/1471-2318-13-34
van Ooijen MW, Heeren A, Smulders K, Geurts AC, Janssen TW, Beek PJ, Weerdesteyn V, Roerdink M (2015) Improved gait adjustments after gait adaptability training are associated with reduced attentional demands in persons with stroke. Exp Brain Res 233:1007–1018. doi:10.1007/s00221-014-4175-7
van Schooten KS, Pijnappels M, Rispens SM, Elders PJ, Lips P, van Dieën JH (2015) Ambulatory fall-risk assessment: amount and quality of daily-life gait predict falls in older adults. J Gerontol A Biol Sci Med Sci 70:608–615. doi:10.1093/gerona/glu225
van Swigchem R, van Duijnhoven HJ, den Boer J, Geurts AC, Weerdesteyn V (2012) Effect of peroneal electrical stimulation versus an ankle-foot orthosis on obstacle avoidance ability in people with stroke-related foot drop. Phys Ther 92:398–406. doi:10.2522/ptj.20100405
Weerdesteyn V, Nienhuis B, Hampsink B, Duysens J (2004) Gait adjustments in response to an obstacle are faster than voluntary reactions. Hum Mov Sci 23:351–363. doi:10.1016/j.humov.2004.08.011
Weerdesteyn V, Nienhuis B, Duysens J (2005a) Advancing age progressively affects obstacle avoidance skills in the elderly. Hum Mov Sci 24:865–880. doi:10.1016/j.humov.2005.10.013
Weerdesteyn V, Nienhuis B, Mulder T, Duysens J (2005b) Older women strongly prefer stride lengthening to shortening in avoiding obstacles. Exp Brain Res 161:39–46. doi:10.1007/s00221-004-2043-6
Whitwell RL, Milner AD, Cavina-Pratesi C, Byrne CM, Goodale MA (2014) DF’s visual brain in action: the role of tactile cues. Neuropsychologia 55:41–50. doi:10.1016/j.neuropsychologia.2013.11.019
Wood BH, Bilclough JA, Bowron A, Walker RW (2002) Incidence and prediction of falls in Parkinson’s disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 72:721–725. doi:10.1136/jnnp.72.6.721
Young WR, Hollands MA (2012) Evidence for age-related decline in visuomotor function and reactive stepping adjustments. Gait Posture 36:477–481. doi:10.1016/j.gaitpost.2012.04.009
Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361. doi:10.1177/1073858404264680
Acknowledgments
We thank Sjoerd Bruijn, Masood Mazaheri and Melvyn Roerdink for helpful suggestions and stimulating discussions. Special thanks are also due to Marike Odeyn and Christophe Delvaux for assistance with data acquisition and analysis. This work was supported by Research Foundation-Flanders (FWO; Grants G.0756.10 and G.0901.11). JD has been funded by the Interuniversity Attraction Poles Program initiated by the Belgian Science Policy Office (P7/11) and received a Visiting Professor Grant from the National Research Council of Brazil (CNPq 400819/2013-9). ZP was funded by the European Commission through MOVE-AGE, an Erasmus Mundus Joint Doctorate Programme (2011-0015).
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Hoogkamer, W., Potocanac, Z. & Duysens, J. Quick foot placement adjustments during gait: direction matters. Exp Brain Res 233, 3349–3357 (2015). https://doi.org/10.1007/s00221-015-4401-y
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DOI: https://doi.org/10.1007/s00221-015-4401-y