Abstract
Purpose
Intra-limb and muscular coordination during gait are the result of the organisation of the neuromuscular system, which have been widely studied on a flat terrain. Environmental factors, such as the inclination of the terrain, is a challenge for the postural control system to maintain balance. Therefore, we hypothesised that the central nervous system flexibly modifies its control strategies during locomotion on slopes.
Methods
Ten subjects walked on an inclined treadmill at different slopes (from − 9° to + 9°) and speeds (from 0.56 to 2.22 m s−1). Intra-limb coordination was investigated via the Continuous Relative Phase, whereas muscular coordination was investigated by decomposing the coordinated muscle activation profiles into Basic Activation Patterns.
Results
A greater stride to stride variability of kinematics was observed during walking on slopes, as compared to walking on the level. On positive slopes, the stride period and width present a greater variability without modification of the time-pattern of the muscular activation and of the variability of intersegmental coordination. On negative slopes, the stride width is larger, the variability of the stride period and of the inter-segmental coordination is greater and the basic activation patterns become broader, especially at slow speeds.
Conclusion
Our findings suggest that the control strategy of downhill walking corresponds to a more conservative gait pattern, which could be adopted to lower the risk of falling at the cost of a greater energy consumption. In uphill walking, where metabolic demands are high, the strategy adopted may be planned to minimise energy expenditure.
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Abbreviations
- CRP:
-
Continuous relative phase
- GRF:
-
Ground reaction force
- EMG:
-
Records of the electrical activity produced by skeletal muscles
- TO:
-
Toe off
- COP:
-
Centre of pressure
- FC:
-
Foot contact
- Fx, Fy, Fz :
-
Lateral, fore-aft and vertical component of the GRF
- d y , d x :
-
Lateral and fore-aft position of the COP
- ωi, θi :
-
Lower-limb segment angular velocity and position
- φ iN :
-
Phase angle
- ϕ iN :
-
CRP angle
- MARP:
-
Mean absolute relative phase
- DP:
-
Deviation phase of the CRP
- FWHM:
-
Full width at half maximum
- CI:
-
Co-activation index
- NNMF:
-
Non-negative matrix factorisation
- P, W:
-
Basic activation patterns and associated weighting components
- VAF:
-
Variability accounted for
References
Allen JL, Franz JR (2018) The motor repertoire of older adult fallers may constrain their response to balance perturbations. J Neurophysiol 120(5):2368–2378. https://doi.org/10.1152/jn.00302.2018
Baggen RJ, van Dieën JH, Van Roie E et al (2020) Age-related differences in muscle synergy organization during step ascent at different heights and directions. Appl Sci 10:1987. https://doi.org/10.3390/app10061987
Bernstein NA (1967) The Co-ordination and regulation of movements. Pergamon Press, Oxford
Bianchi L, Angelini D, Orani GP, Lacquaniti F (1998) Kinematic coordination in human gait: relation to mechanical energy cost. J Neurophysiol 79(4):2155–2170. https://doi.org/10.1152/jn.1998.79.4.2155
Biewener AA, Daley MA (2007) Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control. J Exp Biol 210(17):2949–2960. https://doi.org/10.1242/jeb.005801
Birn-Jeffery AV, Higham TE (2014) The scaling of uphill and downhill locomotion in legged animals. Integr Comp Biol 54(6):1159–1172. https://doi.org/10.1093/icb/icu015
Borghese NA, Bianchi L, Lacquaniti F (1996) Kinematic determinants of human locomotion. J Physiol 494(3):863–879. https://doi.org/10.1113/jphysiol.1996.sp021539
Buzzi UH, Ulrich BD (2004) Dynamic stability of gait cycles as a function of speed and system constraints. Mot Control 8(3):241–254. https://doi.org/10.1123/mcj.8.3.241
Byrne JE, Stergiou N, Blanke D, Houser JJ, Kurz MJ, Hageman PA (2002) Comparison of gait patterns between young and elderly women: an examination of coordination. Percept Mot Skills 94(1):265–280. https://doi.org/10.2466/pms.2002.94.1.265
Cappellini G, Ivanenko YP, Martino G, MacLellan MJ, Sacco A, Morelli D, Lacquaniti F (2016) Immature spinal locomotor output in children with cerebral palsy. Front Physiol. https://doi.org/10.3389/fphys.2016.00478
Catavitello G, Ivanenko YP, Lacquaniti F (2018) A kinematic synergy for terrestrial locomotion shared by mammals and birds. eLife 7:1–28. https://doi.org/10.7554/eLife.38190
Cheung VCK, D’Avella A, Tresch MC, Bizzi E (2005) Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25(27):6419–6434. https://doi.org/10.1523/JNEUROSCI.4904-04.2005
Cheung VCK, Turolla A, Agostini M, Silvoni S, Bennis C, Kasi P, Bizzi E (2012) Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci USA 109(36):14652–14656. https://doi.org/10.1073/pnas.1212056109
Chiu S-L, Chou L-S (2012) Effect of walking speed on inter-joint coordination differs between young and elderly adults. J Biomech 45(2):275–280. https://doi.org/10.1016/j.jbiomech.2011.10.028
Chiu S-L, Chou L-S (2013) Variability in inter-joint coordination during walking of elderly adults and its association with clinical balance measures. Clin Biomech 28(4):454–458. https://doi.org/10.1016/j.clinbiomech.2013.03.001
Clark DJ, Ting LH, Zajac FE, Neptune RR, Kautz SA (2010) Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J Neurophysiol 103(2):844–857. https://doi.org/10.1152/jn.00825.2009
Cruz-Montecinos C, Pérez-Alenda S, Cerda M, Maas H (2019) Neuromuscular control during gait in people with haemophilic arthropathy. Haemophilia 25:e69–e77. https://doi.org/10.1111/hae.13697
da Rosa RG, Gomeñuka NA, de Oliveira HB, Peyré-Tartaruga LA (2018) Inclined weight-loaded walking at different speeds: pelvis-shoulder coordination, trunk movements and cost of transport. J Mot Behav 50:73–79. https://doi.org/10.1080/00222895.2017.1283292
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
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
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(2):642–653. https://doi.org/10.1152/japplphysiol.01020.2017
Dewolf AH, Ivanenko Y, Zelik KE, Lacquaniti F, Willems PA (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
Dominici N, Ivanenko YP, Cappellini G, Zampagni ML, Lacquaniti F (2010) Kinematic strategies in newly walking toddlers stepping over different support surfaces. J Neurophysiol 103(3):1673–1684. https://doi.org/10.1152/jn.00945.2009
Dominici N, Ivanenko YP, Cappellini G, D’Avella A, Mondì V, Cicchese M, Lacquaniti F (2011) Locomotor primitives in newborn babies and their development. Science 334(6058):997–999. https://doi.org/10.1126/science.1210617
Ferraro RA, Pinto-Zipp G, Simpkins S, Clark MA (2013) Effects of an inclined walking surface and balance abilities on spatiotemporal gait parameters of older adults. J Geriatr Phys Ther 36(1):31–38. https://doi.org/10.1519/JPT.0b013e3182510339
Full RJ, Koditschek DE (1999) Templates and anchors: neuromechanical hypotheses of legged locomotion on land. J Exp Biol 202(23):3325–3332
Gambelli CN, Theisen D, Willems PA, Schepens B (2016) Motor control of landing from a countermovement jump in simulated microgravity. J Appl Physiol 120:1230–1240. https://doi.org/10.1152/japplphysiol.00993.2015
Gizzi L, Nielsen JF, Felici F, Ivanenko YP, Farina D (2011) Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients. J Neurophysiol 106(1):202–210. https://doi.org/10.1152/jn.00727.2010
Gomeñuka NA, Bona RL, da Rosa RG, Peyré-Tartaruga LA (2014) Adaptations to changing speed, load, and gradient in human walking: cost of transport, optimal speed, and pendulum. Scand J Med Sci Sports 24:e165–173. https://doi.org/10.1111/sms.12129
Gomeñuka NA, Bona RL, da Rosa RG, Peyré-Tartaruga LA (2016) The pendular mechanism does not determine the optimal speed of loaded walking on gradients. Hum Mov Sci 47:175–185. https://doi.org/10.1016/j.humov.2016.03.008
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
Grasso R, Zago M, Lacquaniti F (2000) Interactions between posture and locomotion: Motor patterns in humans walking with bent posture versus erect posture. J Neurophysiol 83(1):288–300. (Retrieved from Scopus)
Hak L, Houdijk H, Steenbrink F, Mert A, Van der Wurff P, Beek PJ, Van Dieën JH (2012) Speeding up or slowing down?: Gait adaptations to preserve gait stability in response to balance perturbations. Gait Posture 36(2):260–264. https://doi.org/10.1016/j.gaitpost.2012.03.005
Hausdorff JM (2007) Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci 26(4):555–589. https://doi.org/10.1016/j.humov.2007.05.003
Hausdorff JM, Rios DA, Edelberg HK (2001) Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 82(8):1050–1056. https://doi.org/10.1053/apmr.2001.24893
Hunter LC, Hendrix EC, Dean JC (2010) The cost of walking downhill: Is the preferred gait energetically optimal? J Biomech 43(10):1910–1915. https://doi.org/10.1016/j.jbiomech.2010.03.030
Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556(1):267–282. https://doi.org/10.1113/jphysiol.2003.057174
Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25(31):7238–7253. https://doi.org/10.1523/JNEUROSCI.1327-05.2005
Ivanenko YP, Poppele RE, Lacquaniti F (2006) Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds. J Neurophysiol 95(2):602–618. https://doi.org/10.1152/jn.00767.2005
Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2007) Modular control of limb movements during human locomotion. J Neurosci 27:11149–11161. https://doi.org/10.1523/JNEUROSCI.2644-07.2007
Janshen L, Santuz A, Ekizos A, Arampatzis A (2017) Modular control during incline and level walking in humans. J Exp Biol 220(Pt 5):807–813. https://doi.org/10.1242/jeb.148957
Kendall F, McCreary E, Provance P, Rodgers M, Romani W (2005) Muscles: testing and function with posture and pain, 5th edn. Lippincott Williams and Wilkins, Baltimore, MD
Lay AN, Hass CJ, Gregor RJ (2006) The effects of sloped surfaces on locomotion: a kinematic and kinetic analysis. J Biomech 39(9):1621–1628. https://doi.org/10.1016/j.jbiomech.2005.05.005
Lay AN, Hass CJ, Richard Nichols T, Gregor RJ (2007) The effects of sloped surfaces on locomotion: an electromyographic analysis. J Biomech 40(6):1276–1285. https://doi.org/10.1016/j.jbiomech.2006.05.023
Lee DD, Seung HS (2001) Algorithms for non-negative matrix factorization. Presented at the Advances in Neural Information Processing Systems. Retrieved from https://www.scopus.com/inward/record.uri?eid=2-s2.0-84898964201&partnerID=40&md5=d1974c80e29ec37759872f4a8ce6d823. Accessed 7 June 2020
Leroux A, Fung J, Barbeau H (2002) Postural adaptation to walking on inclined surfaces: I. Normal strategies. Gait Posture 15(1):64–74. https://doi.org/10.1016/S0966-6362(01)00181-3
Maki BE (1997) Gait changes in older adults: predictors of falls or indicators of fear? J Am Geriatr Soc 45(3):313–320. https://doi.org/10.1111/j.1532-5415.1997.tb00946.x
Margaria R (1968) Positive and negative work performances and their efficiencies in human locomotion. Int Z Angew Physiol Einschl Arbeitsphysiol 25(4):339–351. https://doi.org/10.1007/BF00699624
Mari S, Serrao M, Casali C, Conte C, Martino G, Ranavolo A, Pierelli F (2014) Lower limb antagonist muscle co-activation and its relationship with gait parameters in cerebellar ataxia. Cerebellum 13(2):226–236. https://doi.org/10.1007/s12311-013-0533-4
Martino G, Ivanenko YP, Serrao M, Ranavolo A, d’Avella A, Draicchio F, Lacquaniti F (2014) Locomotor patterns in cerebellar ataxia. J Neurophysiol 112(11):2810–2821. https://doi.org/10.1152/jn.00275.2014
Martino G, Ivanenko YP, d’Avella A, Serrao M, Ranavolo A, Draicchio F, Lacquaniti F (2015) Neuromuscular adjustments of gait associated with unstable conditions. J Neurophysiol 114(5):2867–2882. https://doi.org/10.1152/jn.00029.2015
McAndrew PM, Dingwell JB, Wilken JM (2010) Walking variability during continuous pseudo-random oscillations of the support surface and visual field. J Biomech 43(8):1470–1475. https://doi.org/10.1016/j.jbiomech.2010.02.003
McIntosh AS, Beatty KT, Dwan LN, Vickers DR (2006) Gait dynamics on an inclined walkway. J Biomech 39(13):2491–2502. https://doi.org/10.1016/j.jbiomech.2005.07.025
Minetti AE, Ardigò LP, Saibene F (1993) Mechanical determinants of gradient walking energetics in man. J Physiol 472(1):725–735. https://doi.org/10.1113/jphysiol.1993.sp019969
Monaco V, Ghionzoli A, Micera S (2010) Age-related modifications of muscle synergies and spinal cord activity during locomotion. J Neurophysiol 104(4):2092–2102. https://doi.org/10.1152/jn.00525.2009
Monsch ED, Franz CO, Dean JC (2012) The effects of gait strategy on metabolic rate and indicators of stability during downhill walking. J Biomech 45(11):1928–1933. https://doi.org/10.1016/j.jbiomech.2012.05.024
Neptune RR, Clark DJ, Kautz SA (2009) Modular control of human walking: a simulation study. J Biomech 42:1282–1287. https://doi.org/10.1016/j.jbiomech.2009.03.009
Noble JW, Prentice SD (2008) Intersegmental coordination while walking up inclined surfaces: age and ramp angle effects. Exp Brain Res 189(2):249–255. https://doi.org/10.1007/s00221-008-1464-z
Ogaya S, Iwata A, Higuchi Y, Fuchioka S (2016) The association between intersegmental coordination in the lower limb and gait speed in elderly females. Gait Posture 48:1–5. https://doi.org/10.1016/j.gaitpost.2016.04.018
Peyré-Tartaruga LA, Coertjens M (2018) Locomotion as a powerful model to study integrative physiology: efficiency, economy, and power relationship. Front Physiol. https://doi.org/10.3389/fphys.2018.01789
Pickle NT, Grabowski AM, Auyang AG, Silverman AK (2016) The functional roles of muscles during sloped walking. J Biomech 49(14):3244–3251. https://doi.org/10.1016/j.jbiomech.2016.08.004
Prentice SD, Hasler EN, Groves JJ, Frank JS (2004) Locomotor adaptations for changes in the slope of the walking surface. Gait Posture 20(3):255–265. https://doi.org/10.1016/j.gaitpost.2003.09.006
Ranavolo A, Donini LM, Mari S, Serrao M, Silvetti A, Iavicoli S, Draicchio F (2013) Lower-limb joint coordination pattern in obese subjects. Biomed Res Int. https://doi.org/10.1155/2013/142323
Rozumalski A, Steele KM, Schwartz MH (2017) Muscle synergies are similar when typically developing children walk on a treadmill at different speeds and slopes. J Biomech 64:112–119. https://doi.org/10.1016/j.jbiomech.2017.09.002
Rudolph KS, Axe MJ, Snyder-Mackler L (2000) Dynamic stability after ACL injury: who can hop? Knee Surg Sports Traumatol Arthrosc 8:262–269
Saito A, Tomita A, Ando R, Watanabe K, Akima H (2018) Similarity of muscle synergies extracted from the lower limb including the deep muscles between level and uphill treadmill walking. Gait Posture 59:134–139. https://doi.org/10.1016/j.gaitpost.2017.10.007
Santuz A, Ekizos A, Eckardt N, Kibele A, Arampatzis A (2018) Challenging human locomotion: stability and modular organisation in unsteady conditions. Sci Rep. https://doi.org/10.1038/s41598-018-21018-4
Santuz A, Brüll L, Ekizos A et al (2020) Neuromotor dynamics of human locomotion in challenging settings. iScience 23:100796. https://doi.org/10.1016/j.isci.2019.100796
Sartori M, Gizzi L, Lloyd DG, Farina D (2013) A musculoskeletal model of human locomotion driven by a low dimensional set of impulsive excitation primitives. Front Comput Neurosci (JUN). https://doi.org/10.3389/fncom.2013.00079
Sheehan RC, Gottschall JS (2012) At similar angles, slope walking has a greater fall risk than stair walking. Appl Ergon 43(3):473–478. https://doi.org/10.1016/j.apergo.2011.07.004
Steele KM, Rozumalski A, Schwartz MH (2015) Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy. Dev Med Child Neurol 57(12):1176–1182. https://doi.org/10.1111/dmcn.12826
Stergiou N, Scholten SD, Jensen JL, Blanke D (2001) Intralimb coordination following obstacle clearance during running: the effect of obstacle height. Gait Posture 13(3):210–220. https://doi.org/10.1016/S0966-6362(00)00101-6
Torres-Oviedo G, Ting LH (2007) Muscle synergies characterizing human postural responses. J Neurophysiol 98:2144–2156. https://doi.org/10.1152/jn.01360.2006
Torres-Oviedo G, Macpherson JM, Ting LH (2006) Muscle synergy organization is robust across a variety of postural perturbations. J Neurophysiol 96(3):1530–1546. https://doi.org/10.1152/jn.00810.2005
Van Emmerik REA, Wagenaar RC (1996) Effects of walking velocity on relative phase dynamics in the trunk in human walking. J Biomech 29(9):1175–1184. https://doi.org/10.1016/0021-9290(95)00128-X
Vieira MF, Rodrigues FB, de Sá e Souza GS, Magnani RM, Lehnen GC, Campos NG, Andrade AO (2017) Gait stability, variability and complexity on inclined surfaces. J Biomech 54:73–79. https://doi.org/10.1016/j.jbiomech.2017.01.045
Winter DA (1991) The biomechanics and motor control of human gait: normal, elderly and pathological. Waterloo Biomechanics, Waterloo
Winter DA (1992) Foot trajectory in human gait: a precise and multifactorial motor control task. Phys Ther 72(1):45–56. (Retrieved from Scopus)
Xu H, Wang Y, Greenland K, Bloswick D, Merryweather A (2015) The influence of deformation height on estimating the center of pressure during level and cross-slope walking on sand. Gait Posture 42(2):110–115. https://doi.org/10.1016/j.gaitpost.2015.04.015
Yen H-C, Chen H-L, Liu M-W, Liu H-C, Lu T-W (2009) Age effects on the inter-joint coordination during obstacle-crossing. J Biomech 42(15):2501–2506. https://doi.org/10.1016/j.jbiomech.2009.07.015
Yokoyama H, Ogawa T, Kawashima N, Shinya M, Nakazawa K (2016) Distinct sets of locomotor modules control the speed and modes of human locomotion. Sci Rep. https://doi.org/10.1038/srep36275
Yokoyama H, Ogawa T, Shinya M, Kawashima N, Nakazawa K (2017) Speed dependency in α-motoneuron activity and locomotor modules in human locomotion: indirect evidence for phylogenetically conserved spinal circuits. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.0290
Acknowledgements
The authors would like to thank Pr. K. Zelik for his help during the experiment and the Pr. F. Lacquaniti and Dr. I. Ivanenko for their help in Formal analysis.
Funding
This study was funded by the Universite catholique de Louvain (Belgium) and the Fonds de la Recherche Scientifique (Belgium).
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Conceptualisation: PAW; Data curation: PAW; Formal analysis: AHD; Funding acquisition: PAW; Investigation: AHD; Methodology: AHD; Project administration: PAW; Software: AHD; Supervision: PAW; Writing—original draft: AHD; Writing—review and editing: AHD, RMM, PAW.
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Dewolf, A.H., Mesquita, R.M. & Willems, P.A. Intra-limb and muscular coordination during walking on slopes. Eur J Appl Physiol 120, 1841–1854 (2020). https://doi.org/10.1007/s00421-020-04415-4
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DOI: https://doi.org/10.1007/s00421-020-04415-4