Top

Published in:

01-04-2006 | Research Article

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

Authors: Grégoire Courtine, Charalambos Papaxanthis, Marco Schieppati

Published in: Experimental Brain Research | Issue 3/2006

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.

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

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

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 279:157–160CrossRefPubMed

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

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

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

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

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

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

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

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 137:455–466CrossRefPubMed

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 18:177–190CrossRefPubMed

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

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 158:86–99CrossRefPubMed

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

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

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

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

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

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

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 727:230–232CrossRefPubMed

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 36:293–299CrossRefPubMed

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

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

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

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

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

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

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

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 140:223–233CrossRefPubMed

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

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

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

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

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

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

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

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

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 28:118–135CrossRefPubMed

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) 16:459–470CrossRef

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 34:1387–1398CrossRefPubMed

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

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 17:603–634CrossRefPubMed

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

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

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 4:190–200CrossRefPubMed

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

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 116:13–20PubMed

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

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

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 31:546–566PubMed

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 97:359–367PubMedCrossRef

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 17:1–17CrossRefPubMed

Title: Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans
Authors: Grégoire Courtine
Charalambos Papaxanthis
Marco Schieppati
Publication date: 01-04-2006
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 3/2006
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-005-0215-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

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

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2006

Persistent monoarthritis of the temporomandibular joint region enhances nocifensive behavior and lumbar spinal Fos expression after noxious stimulation to the hindpaw in rats

Information processing limitations with aging in the visual scaling of isometric force

Two eyes in action

Haptic spatial matching in near peripersonal space

Kinesthetic memory in distance reproduction task: importance of initial hand position information

Relevance of EEG alpha and theta oscillations during task switching