Advertisement

Neuromechanical adjustments when walking with an aiding or hindering horizontal force

  • A. H. Dewolf
  • Y. P. Ivanenko
  • R. M. Mesquita
  • F. Lacquaniti
  • P. A. WillemsEmail author
Original Article

Abstract

Purpose

Walking against a constant horizontal traction force which either hinders or aids the motion of the centre of mass of the body (COM) will create a discrepancy between the positive and negative work being done by the muscles and may thus affect the mechanics and energetics of walking. We aimed at investigating how this imbalance affects the exchange between potential and kinetic energy of the COM and how its dynamics is related to specific spatiotemporal organisation of motor pool activity in the spinal cord. To understand if and how the spinal cord activation may be associated with COM dynamics, we also compared the neuromechanical adjustments brought on by a horizontal force with published data about those brought on by a slope.

Methods

Ten subjects walked on a treadmill at different speeds with different traction forces. We recorded kinetics, kinematics, and electromyographic activity of 16 lower-limb muscles and assessed the spinal locomotor output by mapping them onto the rostrocaudal location of the motoneuron pools.

Results

When walking with a hindering force, the major part of the exchange between potential and kinetic energy of the COM occurs during the first part of stance, whereas with an aiding force exchanges increase during the second part of stance. Those changes occur since limb and trunk orientations remain aligned with the average orientation of the ground reaction force vector. Our results also show the sacral motor pools decreased their activity with an aiding force and increased with a hindering one, whereas the lumbar motor pools increased their engagement both with an aiding and a hindering force.

Conclusion

Our findings suggest that applying a constant horizontal force results in similar modifications of COM dynamics and spinal motor output to those observed when walking on slopes, consistent with common principles of motor pool functioning and biomechanics of locomotion.

Keywords

Neuromechanics Braking and propulsion force Spinal maps Pendular energy exchange COM dynamics 

Abbreviations

\( \beta_{\text{F}} \)

Orientation of the average GRF relative to the vertical

al, av, af

Lateral, vertical and fore–aft acceleration of the COM

BW

Body weight

COM

Centre of mass of the whole body, the point where the weighted relative position of a distributed mass sums to zero

Ekf, Ekv, Ekl

Energy due to the fore–aft, vertical and lateral movement of the COM

EMG

Records of the electrical activity produced by skeletal muscles

\( E_{\text{p}}^{*} \)

Potential energy of the COM

Es

‘Pendular energy savings’, amount of energy saved by the pendular energy exchange

\( \dot{e}\left( t \right) \)

Rate of pendular energy savings, which represents the magnitude of energy exchanged

FC

Foot contact

Ff, Fl, Fv

Fore–aft, lateral and vertical component of the GRF

Ft

Horizontal traction force

GRF

Ground reaction force

L

Stride length

m

Body mass

r (t)

Recovery within the step, which evaluates the EpEk transduction (in %) at each instant of the walking step

h

Vertical displacement of the COM

TO

Toe off

vbelt

Velocity of the belt

vl, vv, vf

Lateral, vertical and fore–aft velocity of the COM

\( {\dot{\text{W}}}_{1}^{ + } \;{\text{and}}\;{\dot{\text{W}}}_{2}^{ + } \)

First and second peak of positive power during a step, respectively

\( \dot{W}^{ - } \)

Major peak of negative power during a step

\( W_{\text{ext}} \)

Work done by the subject to move the COM relative to the surroundings

\( \dot{W}_{\text{ext}} \)

Power used by the subject to move the COM relative to the surroundings

Wt

Work done by the horizontal traction force

Notes

Acknowledgements

This work was supported by the Italian Ministry of Health (Ricerca corrente, IRCCS Fondazione Santa Lucia), Italian Space Agency (Grants I/006/06/0 and 2019-11-U.0), Italian University Ministry (PRIN Grants 2015HFWRYY_002 and 2017CBF8NJ_005).

Author contributions

PAW and AHD: conceptualization. AHD and RMM: data curation. AHD: formal analysis. FL and PAW: funding acquisition. AHD and YPI: investigation. AHD, YPI and RMM: methodology. FL and PAW: project administration. AHD: software. YPI, FL and PAW: supervision. AHD: writing—original draft. AHD, RMM, YPI, FL and PAW: writing—review and editing.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to disclose.

References

  1. Alexander RM (1995) Tendon elasticity and positional control. Behav Brain Sci 18:745.  https://doi.org/10.1017/S0140525X00040711 CrossRefGoogle Scholar
  2. Asmussen E, Bonde-Petersen F (1974) Apparent efficiency and storage of elastic energy in human muscles during exercise. Acta Physiol Scand 92:537–545.  https://doi.org/10.1111/j.1748-1716.1974.tb05776.x CrossRefPubMedGoogle Scholar
  3. Avogadro P, Kyröläinen H, Belli A (2004) Influence of mechanical and metabolic strain on the oxygen consumption slow component during forward pulled running. Eur J Appl Physiol 93:203–209.  https://doi.org/10.1007/s00421-004-1200-8 CrossRefPubMedGoogle Scholar
  4. Bhat SG, Cherangara S, Olson J, Redkar S, Sugar TG (2019) Analysis of a periodic force applied to the trunk to assist walking gait. In: WearRAcon, pp 68–73.  https://doi.org/10.1109/wearracon.2019.8719396
  5. Burnett DR, Campbell-Kyureghyan NH, Cerrito PB, Quesada PM (2011) Symmetry of ground reaction forces and muscle activity in asymptomatic subjects during walking, sit-to-stand, and stand-to-sit tasks. J Electromyogr Kinesiol 21:610–615.  https://doi.org/10.1016/j.jelekin.2011.03.006 CrossRefPubMedGoogle Scholar
  6. Cappellini G, Ivanenko YP, Dominici N et al (2010) Migration of motor pool activity in the spinal cord reflects body mechanics in human locomotion. J Neurophysiol 104:3064–3073.  https://doi.org/10.1152/jn.00318.2010 CrossRefPubMedGoogle Scholar
  7. Cappellini G, Ivanenko YP, Martino G et al (2016) Immature spinal locomotor output in children with cerebral palsy. Front Physiol.  https://doi.org/10.3389/fphys.2016.00478 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cavagna GA (1975) Force platforms as ergometers. J Appl Physiol 39:174–179CrossRefGoogle Scholar
  9. Cavagna GA, Thys H, Zamboni A (1976) The sources of external work in level walking and running. J Physiol 262:639–657.  https://doi.org/10.1113/jphysiol.1976.sp011613 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cavagna GA, Willems PA, Legramandi MA, Heglund NC (2002) Pendular energy transduction within the step in human walking. J Exp Biol 205:3413–3422PubMedGoogle Scholar
  11. Chang Y-H, Kram R (1999) Metabolic cost of generating horizontal forces during human running. J Appl Physiol 86:1657–1662.  https://doi.org/10.1152/jappl.1999.86.5.1657 CrossRefPubMedGoogle Scholar
  12. Chvatal SA, Torres-Oviedo G, Safavynia SA, Ting LH (2011) Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. J Neurophysiol 106:999–1015.  https://doi.org/10.1152/jn.00549.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Conway KA, Bissette RG, Franz JR (2018) The functional utilization of propulsive capacity during human walking. J Appl Biomech 34:474–482.  https://doi.org/10.1123/jab.2017-0389 CrossRefGoogle Scholar
  14. Dewolf AH, Willems PA (2019) Running on a slope: a collision-based analysis to assess the optimal slope. J Biomech 83:298–304.  https://doi.org/10.1016/j.jbiomech.2018.12.024 CrossRefPubMedGoogle Scholar
  15. Dewolf AH, Peñailillo LE, Willems PA (2016) The rebound of the body during uphill and downhill running at different speeds. J Exp Biol 219:2276–2288.  https://doi.org/10.1242/jeb.142976 CrossRefPubMedGoogle Scholar
  16. Dewolf AH, Ivanenko YP, Lacquaniti F, Willems PA (2017) Pendular energy transduction within the step during human walking on slopes at different speeds. PLoS One.  https://doi.org/10.1371/journal.pone.0186963 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dewolf AH, Ivanenko YP, Zelik KE, Lacquaniti F, Willems PA (2018) Kinematic patterns while walking on a slope at different speeds. J Appl Physiol 125:642–653.  https://doi.org/10.1152/japplphysiol.01020.2017 CrossRefPubMedGoogle Scholar
  18. Dewolf AH, Ivanenko Y, Zelik KE et al (2019) Differential activation of lumbar and sacral motor pools during walking at different speeds and slopes. J Neurophysiol.  https://doi.org/10.1152/jn.00167.2019 CrossRefPubMedGoogle Scholar
  19. Dionisio VC, Hurt CP, Brown DA (2018) Effect of forward-directed aiding force on gait mechanics in healthy young adults while walking faster. Gait Posture 64:12–17.  https://doi.org/10.1016/j.gaitpost.2018.05.018 CrossRefPubMedGoogle Scholar
  20. Ellis RG, Sumner BJ, Kram R (2014) Muscle contributions to propulsion and braking during walking and running: insight from external force perturbations. Gait Posture 40:594–599.  https://doi.org/10.1016/j.gaitpost.2014.07.002 CrossRefPubMedGoogle Scholar
  21. Franz JR, Kram R (2013) Advanced age affects the individual leg mechanics of level, uphill, and downhill walking. J Biomech 46:535–540.  https://doi.org/10.1016/j.jbiomech.2012.09.032 CrossRefPubMedGoogle Scholar
  22. Fuchioka S, Iwata A, Higuchi Y et al (2015) The forward velocity of the center of pressure in the midfoot is a major predictor of gait speed in older adults. Int J Gerontol 9:119–122.  https://doi.org/10.1016/j.ijge.2015.05.010 CrossRefGoogle Scholar
  23. Gill ML, Grahn PJ, Calvert JS et al (2018) Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia. Nat Med 24:1677–1682.  https://doi.org/10.1038/s41591-018-0175-7 CrossRefPubMedGoogle Scholar
  24. Gimenez P, Arnal PJ, Samozino P et al (2014) Simulation of uphill/downhill running on a level treadmill using additional horizontal force. J Biomech 47:2517–2521.  https://doi.org/10.1016/j.jbiomech.2014.04.012 CrossRefPubMedGoogle Scholar
  25. Gottschall JS, Kram R (2003) Energy cost and muscular activity required for propulsion during walking. J Appl Physiol 94:1766–1772.  https://doi.org/10.1152/japplphysiol.00670.2002 CrossRefPubMedGoogle Scholar
  26. Gottschall JS, Kram R (2006) Mechanical energy fluctuations during hill walking: the effects of slope on inverted pendulum exchange. J Exp Biol 209:4895–4900.  https://doi.org/10.1242/jeb.02584 CrossRefPubMedGoogle Scholar
  27. Grabowski AM, Kram R (2008) Running with horizontal pulling forces: the benefits of towing. Eur J Appl Physiol 104:473–479.  https://doi.org/10.1007/s00421-008-0785-8 CrossRefPubMedGoogle Scholar
  28. Hsiao H, Knarr BA, Higginson JS, Binder-Macleod SA (2015) Mechanisms to increase propulsive force for individuals poststroke. J Neuroeng Rehabilit.  https://doi.org/10.1186/s12984-015-0030-8 CrossRefGoogle Scholar
  29. Ivanenko YP, Poppele RE, Lacquaniti F (2006) Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds. J Neurophysiol 95:602–618.  https://doi.org/10.1152/jn.00767.2005 CrossRefPubMedGoogle Scholar
  30. Ivanenko YP, Cappellini G, Poppele RE, Lacquaniti F (2008) Spatiotemporal organization of α-motoneuron activity in the human spinal cord during different gaits and gait transitions. Eur J Neurosci 27:3351–3368.  https://doi.org/10.1111/j.1460-9568.2008.06289.x CrossRefPubMedGoogle Scholar
  31. Ivanenko YP, Dominici N, Cappellini G et al (2013) Changes in the spinal segmental motor output for stepping during development from infant to adult. J Neurosci 33:3025–3036aCrossRefGoogle Scholar
  32. Kendall F, McCreary E, Provance P et al (2005) Muscles. Testing and function with posture and pain. Lippincott Williams and Wilkins, BaltimoreGoogle Scholar
  33. Kurz MJ, Stergiou N (2007) Do horizontal propulsive forces influence the nonlinear structure of locomotion? J Neuroeng Rehabilit.  https://doi.org/10.1186/1743-0003-4-30 CrossRefGoogle Scholar
  34. La Scaleia V, Ivanenko YP, Zelik KE, Lacquaniti F (2014) Spinal motor outputs during step-to-step transitions of diverse human gaits. Front Hum Neurosci 8:305.  https://doi.org/10.3389/fnhum.2014.00305 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lejeune TM, Willems PA, Heglund NC (1998) Mechanics and energetics of human locomotion on sand. J Exp Biol 201(13):2071–2080PubMedGoogle Scholar
  36. Lenzo B, Zanotto D, Vashista V et al (2014) A new constant pushing force device for human walking analysis. In: IEEE international conference on robotics and automation, pp 6174–6179.  https://doi.org/10.1109/ICRA.2014.6907769 CrossRefGoogle Scholar
  37. Maclellan MJ, Ivanenko YP, Massaad F et al (2014) Muscle activation patterns are bilaterally linked during split-belt treadmill walking in humans. J Neurophysiol 111:1541–1552.  https://doi.org/10.1152/jn.00437.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Margaria R (1968) Positive and negative work performances and their efficiencies in human locomotion. Int Z Angew Physiol Einschl Arbeitsphysiol 25:339–351.  https://doi.org/10.1007/BF00699624 CrossRefGoogle Scholar
  39. Martino G, Ivanenko Y, Serrao M, Ranavolo A, Draicchio F, Rinaldi M, Casali C, Lacquaniti F (2018) Differential changes in the spinal segmental locomotor output in hereditary spastic paraplegia. Clin Neurophysiol 129:516–525.  https://doi.org/10.1016/j.clinph.2017.11.028 CrossRefPubMedGoogle Scholar
  40. Meurisse GM, Dierick F, Schepens B, Bastien GJ (2016) Determination of the vertical ground reaction forces acting upon individual limbs during healthy and clinical gait. Gait Posture 43:245–250.  https://doi.org/10.1016/j.gaitpost.2015.10.005 CrossRefPubMedGoogle Scholar
  41. Mignardot J-B, Le Goff CG, Van Den Brand R et al (2017) A multidirectional gravity-assist algorithm that enhances locomotor control in patients with stroke or spinal cord injury. Sci Transl Med.  https://doi.org/10.1126/scitranslmed.aah3621 CrossRefPubMedGoogle Scholar
  42. Minetti AE, Ardigò LP, Saibene F (1993) Mechanical determinants of gradient walking energetics in man. J Physiol 472:725–735.  https://doi.org/10.1113/jphysiol.1993.sp019969 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Na K-P, Kim YL, Lee SM (2015) Effects of gait training with horizontal impeding force on gait and balance of stroke patients. J Phys Ther Sci 27:733–736.  https://doi.org/10.1589/jpts.27.733 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Naidu A, Graham SA, Brown D (2019) Fore-aft resistance applied at the center of mass using a novel robotic interface proportionately increases propulsive force generation in healthy nonimpaired individuals walking at a constant speed. J Neuroeng Rehabil 16:111CrossRefGoogle Scholar
  45. Penke K, Scott K, Sinskey Y, Lewek MD (2019) Propulsive forces applied to the body’s center of mass affect metabolic energetics poststroke. Arch Phys Med Rehabil 100:1068–1075.  https://doi.org/10.1016/j.apmr.2018.10.010 CrossRefPubMedGoogle Scholar
  46. Pierotti SE, Brand RA, Gabel RH et al (1991) Are leg electromyogram profiles symmetrical? J Orthop Res 9:720–729.  https://doi.org/10.1002/jor.1100090512 CrossRefPubMedGoogle Scholar
  47. Prampero PED, Fusi S, Sepulcri L et al (2005) Sprint running: a new energetic approach. J Exp Biol 208:2809–2816.  https://doi.org/10.1242/jeb.01700 CrossRefPubMedGoogle Scholar
  48. Pugh LGCE (1971) The influence of wind resistance in running and walking and the mechanical efficiency of work against horizontal or vertical forces. J Physiol 213:255–276.  https://doi.org/10.1113/jphysiol.1971.sp009381 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Sadeghi H, Allard P, Prince F, Labelle H (2000) Symmetry and limb dominance in able-bodied gait: a review. Gait Posture 12:34–45CrossRefGoogle Scholar
  50. Saunders JB, Inman VT, Eberhart HB (1953) The major determinants in normal and pathological gait. J Bone Jt Surg Am 35A:543–558.  https://doi.org/10.2106/00004623-195335030-00003 CrossRefGoogle Scholar
  51. Sayenko DG, Rath M, Ferguson AR et al (2019) Self-assisted standing enabled by non-invasive spinal stimulation after spinal cord injury. J Neurotrauma 36:1435–1450.  https://doi.org/10.1089/neu.2018.5956 CrossRefPubMedGoogle Scholar
  52. Simha SN, Wong JD, Selinger JC, Donelan JM (2019) A mechatronic system for studying energy optimization during walking. IEEE Trans Neural Syst Rehabil Eng 27(7):1416–1425.  https://doi.org/10.1109/TNSRE.2019.2917424 CrossRefPubMedGoogle Scholar
  53. Solopova IA, Sukhotina IA, Zhvansky DS et al (2017) Effects of spinal cord stimulation on motor functions in children with cerebral palsy. Neurosci Lett 639:192–198.  https://doi.org/10.1016/j.neulet.2017.01.003 CrossRefPubMedGoogle Scholar
  54. Sun J, Walters M, Svensson N, Lloyd D (1996) The influence of surface slope on human gait characteristics: a study of urban pedestrians walking on an inclined surface. Ergonomics 39:677–692.  https://doi.org/10.1080/00140139608964489 CrossRefPubMedGoogle Scholar
  55. Tomlinson BE, Irving D (1977) The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 34:213–219CrossRefGoogle Scholar
  56. Usherwood JR, Szymanek KL, Daley MA (2008) Compass gait mechanics account for top walking speeds in ducks and humans. J Exp Biol 211:3744–3749.  https://doi.org/10.1242/jeb.023416 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Van Caekenberghe I, Segers V, Willems P et al (2013) Mechanics of overground accelerated running vs. running on an accelerated treadmill. Gait Posture 38:125–131.  https://doi.org/10.1016/j.gaitpost.2012.10.022 CrossRefPubMedGoogle Scholar
  58. Wagner FB, Mignardot J-B, Le Goff-Mignardot CG et al (2018) Targeted neurotechnology restores walking in humans with spinal cord injury. Nature 563:65–71.  https://doi.org/10.1038/s41586-018-0649-2 CrossRefPubMedGoogle Scholar
  59. Wang J, Hurt CP, Capo-Lugo CE, Brown DA (2015) Characteristics of horizontal force generation for individuals post-stroke walking against progressive resistive forces. Clin Biomech 30:40–45.  https://doi.org/10.1016/j.clinbiomech.2014.11.006 CrossRefGoogle Scholar
  60. Winter DA (1991) The biomechanics and motor control of human gait: normal, elderly and pathological. Waterloo Biomechanics, WaterlooGoogle Scholar
  61. Zirker CA, Bennett BC, Abel MF (2013) Changes in kinematics, metabolic cost and external work during walking with a forward assistive force. J Appl Biomech 29:481–489.  https://doi.org/10.1123/jab.29.4.481 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • A. H. Dewolf
    • 1
    • 2
  • Y. P. Ivanenko
    • 3
  • R. M. Mesquita
    • 1
  • F. Lacquaniti
    • 2
    • 3
  • P. A. Willems
    • 1
    Email author
  1. 1.Laboratory of Biomechanics and Physiology of Locomotion, Institute of NeuroscienceUniversité Catholique de Louvain (UCL-FSM)Louvain-la-NeuveBelgium
  2. 2.Department of Systems Medicine and Center of Space BiomedicineUniversity of Rome Tor VergataRomeItaly
  3. 3.Laboratory of Neuromotor PhysiologyIRCCS Santa Lucia FoundationRomeItaly

Personalised recommendations