Skip to main content
SpringerLink
Log in

Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We describe the muscle synergies accompanying steering of walking along curved trajectories, in order to analyze the simultaneous control of progression and balance-threatening emerging forces. For this purpose, we bilaterally recorded in ten subjects the electromyograms (EMGs) of a representative sample of leg and trunk muscles (n=16) during continuous walking along one straight and two curved trajectories at natural speed. Curvilinear locomotion involved a graded, limb-dependent modulation of amplitude and timing of activity of the muscles of the legs and trunk. The turn-related modulation of the motor pattern was highly coordinated amongst muscles and body sides. For all muscles, linear relationships were detected between the spatial and temporal features of muscle EMG activity. The largest modulation of EMG was observed in gastrocnemius medialis and lateralis muscles, which showed opposite changes in timing and amplitude during curve-walking. Moreover, amplitude and timing characteristics of muscle activities were significantly correlated with the spatial and temporal gait adaptations that are associated with curvilinear locomotion. The present results reveal that fine-modulation of the muscle synergies underlying straight-ahead locomotion is enough to generate the adequate propulsive forces to steer walking and maintain balance. These findings suggest that the turn-related command operates by modulation of the phase relationships between the tightly coupled neuronal assemblies that drive motor neuron activity during walking. This would produce the invariant templates for locomotion kinematics that are at the base of human navigation in space.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alexander RM (1989) Optimization and gaits in the locomotion of vertebrates. Physiol Rev 69:1199–1227

    PubMed  CAS  Google Scholar 

  • Arndt A, Bruggemann GP, Koebke J, Segesser B (1999) Asymmetrical loading of the human triceps surae: II. Differences in calcaneal moments. Foot Ankle Int 20:450–455

    PubMed  CAS  Google Scholar 

  • Bent LR, McFadyen BJ, Merkley VF, Kennedy PM, Inglis JT (2000) Magnitude effects of galvanic vestibular stimulation on the trajectory of human gait. Neurosci Lett 279:157–160

    Article  PubMed  CAS  Google Scholar 

  • Bernstein N (1967) The co-ordination and regulation of movements. Pergamon, Oxford

    Google Scholar 

  • Berthoz A, Viaud-Delmon I (1999) Multisensory integration in spatial orientation. Curr Opin Neurobiol 9:708–712

    Article  PubMed  CAS  Google Scholar 

  • Bove M, Diverio M, Pozzo T, Schieppati M (2001) Neck muscle vibration disrupts steering of locomotion. J Appl Physiol 91:581–588

    PubMed  CAS  Google Scholar 

  • Bussel B, Roby-Brami A, Nerris O, Yakovleff A (1996) Evidence for a spinal stepping generator in man. Paraplegia 34:91–92

    PubMed  CAS  Google Scholar 

  • Capaday C (2002) The special nature of human walking and its neural control. Trends Neurosci 25:370–376

    Article  PubMed  CAS  Google Scholar 

  • Cavagna GA, Margaria R (1966) Mechanics of walking. J Appl Physiol 21:271–278

    PubMed  CAS  Google Scholar 

  • Chekirda IF, Bogdashevskiy AV, Yeremin AV, Kolosov IA (1971) Coordination structure of walking of Soyuz-9 crew members before and after flight. Kosmicheskaia Biologiia I Aviakosmicheskaia Meditsina 5:48–52

    Google Scholar 

  • Cheron G, Bouillot E, Dan B, Bengoetxea A, Draye JP, Lacquaniti F (2001) Development of a kinematic coordination pattern in toddler locomotion: planar covariation. Exp Brain Res 137:455–466

    Article  PubMed  CAS  Google Scholar 

  • Clark JE (1995) On becoming skillful: Patterns and constraints. In: Research quarterly for exercise and sport, vol 66, pp 173–183

  • Courtine G, Schieppati M (2003a) Human walking along a curved path. I. Body trajectory, segment orientation and the effect of vision. Eur J Neurosci 18:177–190

    Article  PubMed  Google Scholar 

  • Courtine G, Schieppati M (2003b) Human walking along a curved path. II. Gait features and EMG patterns. Eur J Neurosci 18:191–205

    Article  PubMed  Google Scholar 

  • Courtine G, Pozzo T (2004) Recovery of the locomotor function after prolonged microgravity exposure. I. Head-trunk movement and locomotor equilibrium during various tasks. Exp Brain Res 158:86–99

    Article  PubMed  Google Scholar 

  • Courtine G, Schieppati M (2004) Tuning of a basic coordination pattern constructs straight-ahead and curved walking in humans. J Neurophysiol 91:1524–1535

    Article  PubMed  Google Scholar 

  • Courtine G, Papaxanthis C, Laroche D, Pozzo T (2003) Gait-dependent integration of neck muscle afferent input. Neuroreport 14:2365–2368

    Article  PubMed  Google Scholar 

  • Dietz V, Zijlstra W, Duysens J (1994) Human neuronal interlimb coordination during split-belt locomotion. Exp Brain Res 101:513–520

    Article  PubMed  CAS  Google Scholar 

  • Dietz V, Leenders KL, Colombo G (1997) Leg muscle activation during gait in Parkinson’s disease: influence of body unloading. Electroencephalogr Clin Neurophysiol 105:400–405

    Article  PubMed  CAS  Google Scholar 

  • Dimitrijevic M, Gerasimenko Y, Pinter M (1998) Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 860:360–376

    Article  PubMed  CAS  Google Scholar 

  • Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187:321–332

    Article  PubMed  CAS  Google Scholar 

  • Duysens J, van Wezel BM, Prokop T, Berger W (1996) Medial gastrocnemius is more activated than lateral gastrocnemius in sural nerve induced reflexes during human gait. Brain Res 727:230–232

    Article  PubMed  CAS  Google Scholar 

  • Duysens J, van Wezel BM, van de Crommert HW, Faist M, Kooloos JG (1998) The role of afferent feedback in the control of hamstrings activity during human gait. Eur J Morphol 36:293–299

    Article  PubMed  CAS  Google Scholar 

  • Duysens J, Clarac F, Cruse H (2000) Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80:83–133

    PubMed  CAS  Google Scholar 

  • Edgerton VR, Roy RR (2002) Paralysis recovery in humans and model systems. Curr Opin Neurobiol 12:658–667

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick RC, Wardman DL, Taylor JL (1999) Effects of galvanic vestibular stimulation during human walking. J Physiol 517:931–939

    Article  PubMed  CAS  Google Scholar 

  • Gramsbergen A, Hadders-Algra M (1998) Development of postural control, a basic aspect of neuro-ontogeny. Neurosci Biobehav Rev 22:463–464

    Article  PubMed  CAS  Google Scholar 

  • Grasso R, Glasauer S, Takei Y, Berthoz A (1996) The predictive brain: anticipatory control of head direction for the steering of locomotion. Neuroreport 7:1170–1174

    Article  PubMed  CAS  Google Scholar 

  • Grasso R, Bianchi L, Lacquaniti F (1998) Motor patterns for human gait: backward versus forward locomotion. J Neurophysiol 80:1868–1885

    PubMed  CAS  Google Scholar 

  • Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR (1997) Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 77:797–811

    PubMed  CAS  Google Scholar 

  • Hollands MA, Sorensen KL, Patla AE (2001) Effects of head immobilization on the coordination and control of head and body reorientation and translation during steering. Exp Brain Res 140:223–233

    Article  PubMed  CAS  Google Scholar 

  • Imai T, Moore ST, Raphan T, Cohen B (2001) Interaction of the body, head, and eyes during walking and turning. Exp Brain Res 136:1–18

    Article  PubMed  CAS  Google Scholar 

  • Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282

    Article  PubMed  CAS  Google Scholar 

  • Ivanenko YP, Dominici N, Cappellini G, Lacquaniti F (2005) Kinematics in newly walking toddlers does not depend upon postural stability. J Neurophysiol 94(1):754–763

    Article  PubMed  Google Scholar 

  • Jensen L, Prokop T, Dietz V (1998) Adaptational effects during human split-belt walking: influence of afferent input. Exp Brain Res 118:126–130

    Article  PubMed  CAS  Google Scholar 

  • Kuo AD (2001) A simple model of bipedal walking predicts the preferred speed-step length relationship. J Biomech Eng 123:264–269

    Article  PubMed  CAS  Google Scholar 

  • Lacquaniti F, Grasso R, Zago M (1999) Motor patterns in walking. News Physiol Sci 14:168–174

    PubMed  Google Scholar 

  • Lacquaniti F, Ivanenko YP, Zago M (2002) Kinematic control of walking. Arch Ital Biol 140:263–272

    PubMed  CAS  Google Scholar 

  • Ma YY, Ryou JW, Kim BH, Wilson FA (2004) Spatially directed movement and neuronal activity in freely moving monkey. Prog Brain Res 143:513–520

    PubMed  Google Scholar 

  • Mergner T, Rosemeier T (1998) Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions–a conceptual model. Brain Res Brain Res Rev 28:118–135

    Article  PubMed  CAS  Google Scholar 

  • Morris ME, Huxham F, McGinley J, Dodd K, Iansek R (2001) The biomechanics and motor control of gait in Parkinson disease. Clin Biomech (Bristol, Avon) 16:459–470

    Article  CAS  Google Scholar 

  • Neptune RR, Kautz SA, Zajac FE (2001) Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J Biomech 34:1387–1398

    Article  PubMed  CAS  Google Scholar 

  • Pang MY, Yang JF (2002) Sensory gating for the initiation of the swing phase in different directions of human infant stepping. J Neurosci 22:5734–5740

    PubMed  CAS  Google Scholar 

  • Patla AE, Prentice SD, Robinson C, Neufeld J (1991) Visual control of locomotion: strategies for changing direction and for going over obstacles. J Exp Psychol Hum Percept Perform 17:603–634

    Article  PubMed  CAS  Google Scholar 

  • Patla AE, Adkin A, Ballard T (1999) Online steering: coordination and control of body center of mass, head and body reorientation. Exp Brain Res 129:629–634

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, De Nunzio AM, Schieppati M (2005) Trunk muscle proprioceptive input assists steering of locomotion. Neurosci Lett 384:127–132

    Article  PubMed  CAS  Google Scholar 

  • Stack E, Ashburn A (1999) Fall events described by people with Parkinson’s disease: implications for clinical interviewing and the research agenda. Physiother Res Int 4:190–200

    Article  PubMed  CAS  Google Scholar 

  • Thigpen MT, Light KE, Creel GL, Flynn SM (2000) Turning difficulty characteristics of adults aged 65 years or older. Phys Ther 80:1174–1187

    PubMed  CAS  Google Scholar 

  • Thorstensson A, Carlson H, Zomlefer MR, Nilsson J (1982) Lumbar back muscle activity in relation to trunk movements during locomotion in man. Acta Physiol Scand 116:13–20

    PubMed  CAS  Google Scholar 

  • Vieilledent S, Kerlirzin Y, Dalbera S, Berthoz A (2001) Relationship between velocity and curvature of a human locomotor trajectory. Neurosci Lett 305:65–69

    Article  PubMed  CAS  Google Scholar 

  • Waters RL, Morris JM (1972) Electrical activity of muscles of the trunk during walking. J Anat 111:191–199

    PubMed  CAS  Google Scholar 

  • Williams GN, Chmielewski T, Rudolph K, Buchanan TS, Snyder-Mackler L (2001) Dynamic knee stability: current theory and implications for clinicians and scientists. J Orthop Sports Phys Ther 31:546–566

    PubMed  CAS  Google Scholar 

  • Winter DA, MacKinnon CD, Ruder GK, Wieman C (1993) An integrated EMG/biomechanical model of upper body balance and posture during human gait. Prog Brain Res 97:359–367

    Article  PubMed  CAS  Google Scholar 

  • Zajac FE, Neptune RR, Kautz SA (2003) Biomechanics and muscle coordination of human walking: part II: lessons from dynamical simulations and clinical implications. Gait Posture 17:1–17

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Conseil Régional de Bourgogne and the Institut National pour la Santé et la Recherche Médicale (INSERM). GC was supported by grants from the French Ministry of Research and MS by the Italian Ministry of University and Research (FIRB 2001 RBNE01FJ4 J, PRIN 2003). The help provided by Davy Laroche during data collection is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Dipartimento di Medicina Sperimentale, Sezione di Fisiologia, Università di Pavia, Pavia, Italy

    Grégoire Courtine & Marco Schieppati

  2. Centro Studi Attività Motorie (CSAM), Fondazione Salvatore Maugeri, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Istituto Scientifico di Pavia, Via Ferrata 8, 27100, Pavia, Italy

    Grégoire Courtine & Marco Schieppati

  3. Equipe de Recherche Mixte 207, Institut National de la Santé et de la Recherche Médicale (INSERM), Motricité et Plasticité, Université de Bourgogne, Dijon, France

    Grégoire Courtine & Charalambos Papaxanthis

Authors
  1. Grégoire Courtine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charalambos Papaxanthis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marco Schieppati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Schieppati.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Courtine, G., Papaxanthis, C. & Schieppati, M. Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans. Exp Brain Res 170, 320–335 (2006). https://doi.org/10.1007/s00221-005-0215-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0215-7

Keywords

Search

Navigation