Abstract
In goal-oriented locomotion, healthy adults generate highly stereotyped trajectories and a consistent anticipatory head orienting behaviour, both evidence of top-down, open-loop control. The aim of this study is to describe the typical development of anticipatory orienting strategies and trajectory formation. Our hypothesis is that full-blown anticipatory control requires advanced navigational skills. Twenty-six healthy subjects (14 children: 4–11 years; 6 adolescents: 13–17 years; 6 adults) were asked to walk freely towards one of the three visual targets, in a randomised order. Movement was captured via an optoelectronic system, with 15 body markers. The whole-body displacement, yaw orientation of head, trunk and pelvis, heading direction and foot placements were extracted. Head-heading anticipation, trajectory curvature, indexes of variability of trajectories, foot placements and kinematic profiles were studied. The mean head-heading anticipation time and trajectory curvature did not significantly differ among age groups. In children, however, head anticipation was more often lacking (χ 2 = 9.55, p < 0.01), and there were significant intra- and inter-subject variations. Trajectory curvature was often very high in children, while it became consistently lower in adolescence (χ 2 = 78.59, p < 10−17). The indexes of spatial and kinematic variability all followed a decreasing developmental trend (R 2 > 0.5, p < 0.0001). In conclusion, children under 11 do not perform curvilinear locomotor trajectories as adolescents and adults do. Anticipatory head orientation and trajectory formation develop in late childhood, well after gait maturation. Navigational skills, such as path planning and shifting from ego- to allocentric spatial reference frames, are proposed as necessary requisites for mature locomotor control.
Similar content being viewed by others
References
Adamovich SV, Archambault PS, Ghafouri M, Levin MF, Poizner H, Feldman AG (2001) Hand trajectory invariance in reaching movements involving the trunk. Exp Brain Res 138:288–303
Arechavaleta G, Laumond JP, Hicheur H, Berthoz A (2008) An optimality principle governing human walking. IEEE Trans Robot 24:514
Assaiante C (1998) Development of locomotor balance control in healthy children. Neurosci Biobehav Rev 22:527–532
Assaiante C, Mallau S, Viel S, Jover M, Schmitz C (2005) Development of Postural Control in Healthy Children: a Functional Approach. Neural Plast 12:109–118; discussion 263–272. doi:10.1155/NP.2005.109
Battaglia-Mayer A, Caminiti R, Lacquaniti F, Zago M (2003) Multiple levels of representation of reaching in the parieto-frontal network. Cereb Cortex 13:1009–1022
Beck RJ, Andriacchi TP, Kuo KN, Fermier RW, Galante JO (1981) Changes in the gait patterns of growing children. J Bone Jt Surg Am 63:1452–1457
Bennequin D, Fuchs R, Berthoz A, Flash T (2009) Movement timing and invariance arise from several geometries. PLoS Comput Biol 5:1–27. doi:10.1371/journal.pcbi.1000426
Bernardin D, Kadone H, Bennequin D, Sugar T, Zaoui M, Berthoz A (2012) Gaze anticipation during human locomotion. Exp Brain Res 223:65–78. doi:10.1007/s00221-012-3241-2
Bernstein NA (1967) The co-ordination and regulation of movements, 1st edn. Pergamon Press, Oxford
Bullens J, Iglói K, Berthoz A, Postma A, Rondi-Reig L (2010) Developmental time course of the acquisition of sequential egocentric and allocentric navigation strategies. J Exp Child Psychol 107:337–350. doi:10.1016/j.jecp.2010.05.010
Carrozzo M, Stratta F, McIntyre J, Lacquaniti F (2002) Cognitive allocentric representations of visual space shape pointing Errors. Exp Brain Res 147:426–436
Cheron G, Bouillot E, Dan B, Bengoetxea A, Draye JP, Lacquaniti F (2001a) Development of a kinematic coordination pattern in toddler locomotion: planar covariation. Exp Brain Res 137:455–466
Cheron G, Bengoetxea A, Bouillot E, Lacquaniti F, Dan B (2001b) Early emergence of temporal co-ordination of lower limb segments elevation angles in human locomotion. Neurosci Lett 308:123–127
Cinelli M, Warren WH (2012) Do walkers follow their heads? Investigating the role of head rotation in locomotor control. Exp Brain Res 219:175–190. doi:10.1007/s00221-012-3077-9
Courtine G, Schieppati M (2003) Human walking along a curved path. I. Body trajectory, segment orientation and the effect of vision. Eur J Neurosci 18:177–190. doi:10.1046/j.1460-9568.2003.02736.x
Dominici N, Ivanenko YP, Cappellini G, D’Avella A, Mondì V, Cicchese M, Fabiano A, Silei T, Di Paolo A, Giannini C, Poppele RE, Lacquaniti F (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999. doi:10.1126/science.1210617
Fajen BR, Warren WH (2003) Behavioral dynamics of steering, obstacle avoidance, and route selection. J Exp Psychol Hum Percept Perform 29:343–362
Forssberg H (1985) Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res 57:480–493
Grasso R, Assaiante C, Prévost P, Berthoz A (1998a) Development of anticipatory orienting strategies during locomotor tasks in children. Neurosci Biobehav Rev 22:533–539
Grasso R, Prévost P, Ivanenko YP, Berthoz A (1998b) Eye-head coordination for the steering of locomotion in humans: an anticipatory synergy. Neurosci Lett 253:115–118
Grillner S, Wallén P, Saitoh K, Kozlov A, Robertson B (2008) Neural bases of goal-directed locomotion in vertebrates—an overview. Brain Res Rev 57:2–12. doi:10.1016/j.brainresrev.2007.06.027
Hicheur H, Vieilledent S, Berthoz A (2005a) Head motion in humans alternating between straight and curved walking path: combination of stabilizing and anticipatory orienting mechanisms. Neurosci Lett 383:87–92. doi:10.1016/j.neulet.2005.03.046
Hicheur H, Vieilledent S, Richardson MJE, Flash T, Berthoz A (2005b) Velocity and curvature in human locomotion along complex curved paths: a comparison with hand movements. Exp Brain Res 162:145–154
Hicheur H, Pham QC, Arechavaleta G, Laumond JP, Berthoz A (2007) The formation of trajectories during goal-oriented locomotion in Humans. I. A stereotyped behaviour. Eur J Neurosci 26:2376–2390. doi:10.1111/j.1460-9568.2007.05836.x
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. doi:10.1007/s002210100811
Hollands MA, Patla AE, Vickers JN (2002) Look where you’re going!’: gaze behaviour associated with maintaining and changing the direction of locomotion. Exp Brain Res 143:221–230. doi:10.1007/s00221-001-0983-7
Imai T, Moore ST, Raphan T, Cohen B (2001) Interaction of body, head, and eyes during walking and turning. Exp Brain Res 136:1–18
Ivanenko YP, Dominici N, Cappellini G, Lacquaniti F (2005) Kinematics in newly walking toddlers does not depend upon postural stability. J Neurophysiol 94:754–763. doi:10.1152/jn.00088.2005
Ivanenko YP, D’Avella A, Poppele RE, Lacquaniti F (2008) On the origin of planar covariation of elevation angles during human locomotion. J Neurophysiol 99:1890–1898. doi:10.1152/jn.01308.2007
Jahn K, Wagner J, Deutschländer A, Kalla R, Hüfner K, Stephan T, Strupp M, Brandt T (2009) Human hippocampal activation during stance and locomotion fMRI study on healthy, blind, and vestibular-loss subjects. Ann N Y Acad Sci 1164:229–235. doi:10.1111/j.1749-6632.2009.03770.x
Marigold DS, Patla AE (2007) Gaze fixation patterns for negotiating complex ground terrain. Neurosci 144:302–313
Marigold DS, Patla AE (2008) Visual information from the lower visual field is important for walking across multi-surface terrain. Exp Brain Res 188:23–31. doi:10.1007/s00221-008-1335-7
Massion J (1998) Postural control systems in developmental perspective. Neurosci 22:465–472
Messier J, Adamovich S, Berkinblit M, Tunik E, Poizner H (2003) Influence of movement speed on accuracy and coordination of reaching movements to memorized targets in three-dimensional space in a deafferented subject. Exp Brain Res 150:399–416. doi:10.1007/s00221-003-1413-9
Patla AE, Vickers JN (2003) How far ahead do we look when required to step on specific locations in the travel path during locomotion? Exp Brain Res 148:133–138. doi:10.1007/s00221-002-1246-y
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
Pham QC, Hicheur H (2011) On the open-loop and feedback processes that underlie the formation of trajectories during visual and nonvisual locomotion in humans. J Neurophysiol 102:2800–2815. doi:10.1152/jn.00284.2009
Pham QC, Hicheur H, Arechavaleta G, Laumond JP, Berthoz A (2007) The formation of trajectories during goal-oriented locomotion in humans. II. A maximum smoothness model. Eur J Neurosci 26:2391–2403. doi:10.1111/j.1460-9568.2007.05835.x
Pham QC, Berthoz A, Hicheur H (2011) Invariance of locomotor trajectories across visual and gait direction conditions. Exp Brain Res 210:207–215. doi:10.1007/s00221-011-2619-x
Poirel N, Vidal M, Pineau A, Lanoë C, Leroux G, Lubin A, Turbelin MR, Berthoz A, Houdé O (2011) Evidence of different developmental trajectories for length estimation according to egocentric and allocentric viewpoints in children and adults. Exp Psychol 58:142–146. doi:10.1027/1618-3169/a000079
Pozzo T, McIntyre J, Cheron G, Papaxanthis C (1998a) Hand trajectory formation during whole body reaching movements in man. Neurosci Lett 240:159–162
Pozzo T, Papaxanthis C, Stapley P, Berthoz A (1998b) The sensorimotor and cognitive integration of gravity. Brain Res Rev 28:92–101
Prévost P, Ivanenko Y, Grasso R, Berthoz A (2002) Spatial invariance in anticipatory orienting behaviour during human navigation. Neurosci Lett 339:243–247
Richardson MJE, Flash T (2002) Comparing smooth arm movements with the two-thirds power law and the related segmented-control hypothesis. J Neurosci 22:8201–8211
Roncesvalles MN, Schmitz C, Zedka M, Assaiante C, Woollacott M (2005) From egocentric to exocentric spatial orientation: development of posture control in bimanual and trunk inclination Tasks. J Mot Behav 37:404–416
Sreenivasa MN, Frissen I, Souman JL, Ernst MO (2008) Walking along curved paths of different angles: the relationship between head and trunk turning. Exp Brain Res 191:313–320. doi:10.1007/s00221-008-1525-3
Sutherland DH, Olshen R, Cooper L, Woo SL (1980) The development of mature gait. J Bone Jt Surg Am 62:336–353
Vallis LA, McFadyen BJ (2005) Children use different anticipatory control strategies than adults to circumvent an obstacle in the travel path. Exp Brain Res 167:119–127. doi:10.1007/s00221-005-0054-6
Vaughan CL, Langerak NG, Omalley MJ (2003) Neuromaturation of human locomotion revealed by non-dimensional scaling. Exp Brain Res 153:123–127. doi:10.1007/s00221-003-1635-x
Vieilledent S, Hicheur H, Ducourant T, Kerlirzin Y, Berthoz A (2005) La Génération De Trajectoires Locomotrices Chez L’homme. In: Thinus-Blanc C, Bullier J (eds) Agir Dans L’espace. Edition de la maison des sciences de l’homme, Paris, pp 169–191
Viviani P, Terzuolo C (1982) Trajectory determines movement dynamics. Neurosci 7:431–437
Wagner J, Stephan T, Kalla R, Brückmann H, Strupp M, Brandt T, Jahn K (2008) Mind the bend: cerebral activations associated with mental imagery of walking along a curved path. Exp Brain Res 191:247–255. doi:10.1007/s00221-008-1520-8
Winter DA (2009) Biomechanics and motor control of human movement, 4th edn. Wiley, Hoboken
Acknowledgments
This research was made possible by PACE grant from La Fondation Motrice—Sodiaal (Paris, France) to AB and GC, by RC 2011 grant from the Italian Ministry of Health to GC and by scholarship support to VB from La Fondation Motrice. The authors thank Vincent Corsentino for reviewing the English of the manuscript.
Conflict of interest
The authors declare they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Belmonti, V., Cioni, G. & Berthoz, A. Development of anticipatory orienting strategies and trajectory formation in goal-oriented locomotion. Exp Brain Res 227, 131–147 (2013). https://doi.org/10.1007/s00221-013-3495-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-013-3495-3