Abstract
Lateral stability during gait is of utmost importance to maintain balance. This was studied on human subjects walking on a treadmill who were given 100-ms perturbations of known magnitude and timing with respect to the gait cycle by means of a computer-controlled pneumatic device. This method has the advantage that the same perturbations can be given at different phases of the stride cycle, thereby allowing an analysis of the phase dependency of the responses in the primary muscles involved. After an inward push, e.g., a push toward the left during right stance, the left foot in the step to follow is placed more to the left (outward strategy). The hypothesis was that this movement is caused by automatic unvoluntary muscle activity. This turned out to be the case: the abduction movement follows EMG responses in the left abductor muscle, gluteus medius, in response to the push. Two responses, with latencies of 100 and 170 ms, and a late reaction >270 ms can be discerned. All three responses are phase dependent; they show facilitation in swing and no response in stance, in contrast to the normal walking activity (background). This independence of the background activity suggests a premotoneuronal gating of these responses, reminiscent of phase-dependent modulation of electrically elicited reflexes. It is concluded that facilitating pathways are opened independent of normal background activation to enable appropriate actions to restore balance after a mediolateral perturbation.
Similar content being viewed by others
References
Allum JHJ, Carpenter MG, Honegger F, Adkin AL, Bloem BR (2002) Age-dependent variations in the directional sensitivity of balance corrections and compensatory arm movements in man. J Physiol 542:643
Bolton DAE, Misiaszek JE (2009) Contribution of hindpaw cutaneous inputs to the control of lateral stability during walking in the cat. J Neurophysiol 102:1711–1724
Carpenter MG, Allum JHJ, Honegger F (1999) Directional sensitivity of stretch reflexes and balance corrections for normal subjects in the roll and pitch planes. Exp Brain Res 129:93–113
Cronin NJ, Ishikawa M, Grey MJ, af Klint R, Komi PV, Avela J, Sinkjaer T, Voigt M (2009) Mechanical and neural stretch responses of the human soleus muscle at different walking speeds. J Physiol 587:3375–3382
Duysens J, Trippel M, Horstmann GA, Dietz V (1990) Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res 82:351–358
Duysens J, Tax AAM, Trippel M, Dietz V (1992) Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 90:404–414
Duysens J, Bastiaanse CM, Smits-Engelsman BCM, Dietz V (2004) Gait acts as a gate for reflexes from the foot. Can J Physiol Pharmacol 82:715–722
Grey MJ, Nielsen JB, Mazzaro N, Sinkjaer T (2007) Positive force feedback in human walking. J Physiol 581:99–105
Hilliard MJ, Martinez KM, Janssen I, Edwards B, Mille ML, Zhang Y, Rogers ML (2008) Lateral balance factors predict future falls in community-living older adults. Arch Phys Med Rehab 89:1708–1713
Hof AL (1996) Scaling gait data to body size. Gait Posture 4:222–223
Hof AL (2007) The equations of motion for a standing human reveal three mechanisms for balance. J Biomech 40:451–457
Hof AL (2008) The ‘extrapolated center of mass’ concept suggests a simple control of balance in walking. Hum Mov Sci 27:112–125
Hof AL, Elzinga H, Grimmius W, Halbertsma JPK (2002) Speed dependency of averaged EMG profiles in walking. Gait Posture 16:78–86
Hof AL, Vermerris SM, Gjaltema WA (2010) Balance responses to lateral perturbations in human treadmill walking. J Exp Biol 213:2655–2664. doi:10.1242/jeb.042572
Horak FB, Macpherson JM (1996) Postural orientation and equilibrium. In: Dow RS (ed) Handbook of physiology. Exercise: regulation and integration of multiple systems. American Physiological Society, Bethesda, pp 255–292
Inman VT, Ralston HJ, Todd F (1981) Human walking. Williams and Wilkins, Baltimore
Jeka JJ, Kiemel T, Creath R, Horak FB, Peterka RJ (2004) Controlling human upright posture: velocity information is more accurate than position or acceleration. J Neurophysiol 92:2368–2379
Karayannidou A, Zelenin PV, Orlovsky GN, Sirota MG, Beloozerova IN, Deliagina TG (2009) Maintenance of lateral stability during standing and walking in the cat. J Neurophysiol 101:8–19
King DL, Zatsiorsky VM (2002) Periods of extreme ankle displacement during one-legged standing. Gait Posture 15:172–179
Kuo A (1999) Stabilization of lateral motion in passive dynamic walking. Int J Robotics Res 18:917–930
Maki BE, Edmondstone MA, McIlroy WE (2000) Age-related differences in laterally directed compensatory stepping behavior. J Gerontol A Biol Sci Med Sci 55:M270–M277
Matthews PBC (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374:73–90
Misiaszek JE (2006) Control of frontal plane motion of the hindlimbs in the unrestrained walking cat. J Neurophysiol 96:1816–1828. doi:10.1152/jn.00370.2006
Oddsson LIE, Wall C, McPartland M, Krebs DE, Tucker CA (2004) Recovery from perturbations during paced walking 62. Gait Posture 19:24–34
Sinkjaer T, Andersen JB, Ladouceur M, Christensen LO, Nielsen JB (2000) Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523:817–827
Townsend M (1985) Biped gait stabilization via foot placement. J Biomech 18:21–38
Verkerke GJ, Hof AL, Zijlstra W, Ament W, Rakhorst G (2005) Determining the centre of pressure during walking and running using an instrumented treadmill. J Biomech 38:1881–1885
Winter DA (1995) Human balance and posture control during standing and walking. Gait Posture 3:193–214
Winter DA (2005) Biomechanics and motor control of human movement, vol 3, 3rd edn. Wiley, Hoboken
Wu G, Cavanagh PR (1995) ISB recommendations for standardization in the reporting of kinematic data. J Biomech 28:1257–1260
Yang JF, Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117
Zehr EP, Stein RB, Komiyama T (1998) Function of sural nerve reflexes during human walking. J Physiol 507:305–314
Acknowledgments
We thank Welmoed Gjaltema and Marije Vermerris for their work in the execution of the experiments and the anonymous reviewers of this paper for many useful suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hof, A.L., Duysens, J. Responses of human hip abductor muscles to lateral balance perturbations during walking. Exp Brain Res 230, 301–310 (2013). https://doi.org/10.1007/s00221-013-3655-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-013-3655-5