Ontogenesis of head stabilization in space during locomotion in children: influence of visual cues

The main purpose of this study was to investigate the development of the head stabilization in space strategy (HSSS) during various locomotor tasks in 3- to 8-year-old children and adults. The contribution of visual factors to the HSSS was also examined by applying peripheral visual restriction, stroboscopic visual motion cue restriction, and darkness. The kinematics of the head and trunk rotations (pitch, yaw, and roll) were analyzed by means of an optical TV-image processor (ELITE system). For each of the three angular components, an appropriate “head anchoring index” was defined in order to compare the HSSS with a head stabilization on the trunk strategy. Head-trunk correlation rates were also calculated for each angular component in order to evaluate the head-trunk stiffness. The development of head-trunk coordinations during locomotion under normal vision can be said to involve at least three main periods. The first period occurs from the age of 3 to 6 years, when the HSSS is adopted only while walking on the flat ground. While walking on narrow supports, children in this age-group rather tend to increase the head-trunk stiffness, especially at 6 years of age. The second period includes 7- to 8-year-old children. Children of this age become able to adopt the HSSS while walking on narrow supports. During this period, the HSSS is associated with a large decrease in the head-trunk correlations. Lastly, in adulthood the HSSS is commonly adopted but specifically involves the roll component associated with the lateral body oscillations while walking. Vision was found to have little influence on children's HSSS while walking, whatever their age. Moreover, darkness induces an increase in the efficiency of the HSSS in adults. This confirms that the HSSS is the most appropriate strategy available for dealing with an increase in the level of equilibrium difficulty and may reflect a “top-down” organization of the postural control while walking. These results also suggest that the HSSS may be mainly of vestibular origin and presumably serves to facilitate the visual input processing, particularly that of the motion and peripheral visual cues which are involved in the control of body equilibrium during locomotion.

[1]  N. A. Bernshteĭn.  The co-ordination and regulation of movements , 1967 .

[2]  V. J. Wilson,et al.  Mammalian Vestibular Physiology , 1979, Springer US.

[3]  B. Amblard,et al.  Locomotion in adult cats with early vestibular deprivation: Visual cue substitution , 2004, Experimental Brain Research.

[4]  M. Woollacott,et al.  The growth of stability: postural control from a development perspective. , 1985, Journal of motor behavior.

[5]  J. Dichgans,et al.  Die Entwicklung der visuellen Stabilisation des aufrechten Standes beim Kind: Ein Reifezeichen in der Kinderneurologie , 1976, Archiv für Psychiatrie und Nervenkrankheiten.

[6]  Norman M. Wereley,et al.  Visual, vestibular and voluntary contributions to human head stabilization , 2004, Experimental Brain Research.

[7]  Lewis M. Nashner,et al.  Strategies for Organization of Human Posture , 1985 .

[8]  T. Roberts.  The Role of Vestibular and Neck Receptors in Locomotion , 1976 .

[9]  M. Gresty.  Stability of the head in pitch (neck flexion‐extension): Studies in normal subjects and patients with axial rigidity , 1989, Movement disorders : official journal of the Movement Disorder Society.

[10]  M. Igarashi,et al.  Dynamic equilibrium in squirrel monkeys after unilateral and bilateral labyrinthectomy. , 1970, Acta oto-laryngologica.

[11]  Ian P. Howard,et al.  Human visual orientation , 1982 .

[12]  R. Olshen,et al.  The development of mature gait. , 1980, The Journal of bone and joint surgery. American volume.

[13]  C. Assaiante,et al.  Peripheral vision and age-related differences in dynamic balance , 1992 .

[14]  Barnes Gr,et al.  Transmission of Angular Acceleration to the Head in the Seated Human Subject , 1974 .

[15]  B. Amblard,et al.  Role of Foveal and Peripheral Visual Information in Maintenance of Postural Equilibrium in Man , 1980, Perceptual and motor skills.

[16]  M B Dutia,et al.  The sagittal vestibulocollic reflex and its interaction with neck proprioceptive afferents in the decerebrate cat. , 1985, The Journal of physiology.

[17]  C. Assaiante,et al.  Discrete visual samples may control locomotor equilibrium and foot positioning in man. , 1989, Journal of motor behavior.

[18]  M. Dutia.  Interaction between vestibulocollic and cervicocollic reflexes: automatic compensation of reflex gain by muscle afferents. , 1988, Progress in brain research.

[19]  Chantal Bard,et al.  Stabilization of head and eyes on target as a factor in successful basketball shooting , 1986 .

[20]  A. Berthoz,et al.  Head stabilization during various locomotor tasks in humans , 2004, Experimental Brain Research.

[21]  W. P. Huebner,et al.  Performance of the human vestibuloocular reflex during locomotion. , 1989, Journal of neurophysiology.

[22]  S. Lund,et al.  Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. , 1983, Acta physiologica Scandinavica.

[23]  R. Leigh,et al.  Instability of gaze during locomotion in patients with deficient vestibular function , 1990, Annals of neurology.

[24]  Giancarlo Ferrigno,et al.  Elite: A Digital Dedicated Hardware System for Movement Analysis Via Real-Time TV Signal Processing , 1985, IEEE Transactions on Biomedical Engineering.

[25]  R Fontaine,et al.  Analysis of the transition from upright stance to steady state locomotion in children with under 200 days of autonomous walking. , 1989, Journal of motor behavior.

[26]  A M Bronstein,et al.  Evidence for a vestibular input contributing to dynamic head stabilization in man. , 1988, Acta oto-laryngologica.

[27]  André Thomas,et al.  Équilibre et équilibration , 1940 .

[28]  J. Crémieux,et al.  Visual and vestibular control of locomotion in early and late sensory-deprived cats. , 1988, Progress in brain research.

[29]  V. J. Wilson,et al.  DYNAMICS OF VESTIBULO‐OCULAR, VESTIBULO‐COLLIC, AND CERVICOCOLLIC REFLEXES * , 1981, Annals of the New York Academy of Sciences.

[30]  Alain Berthoz,et al.  The Head-neck sensory motor system , 1992 .

[31]  R. J. Leigh,et al.  Frequency and velocity of rotational head perturbations during locomotion , 2004, Experimental Brain Research.

[32]  John Crawford,et al.  LIVING WITHOUT A BALANCING MECHANISM* , 1964, The British journal of ophthalmology.

[33]  C. Assaiante,et al.  Head-Trunk Coordination and Locomotor Equilibrium in 3-to 8-Year-Old Children , 1992 .

[34]  J. Crémieux,et al.  Early sensory determinants of locomotor speed in adult cats: II. Effects of strobe rearing on vestibular functions , 1990, Behavioural Brain Research.

[35]  J. Crémieux,et al.  Lateral orientation and stabilization of human stance: static versus dynamic visual cues , 2004, Experimental Brain Research.

[36]  G. Barnes,et al.  Transmission of angular acceleration to the head in the seated human subject. , 1974, Aerospace medicine.

[37]  J F Baker,et al.  Dynamic and kinematic properties of the vestibulocollic and cervicocollic reflexes in the cat. , 1988, Progress in brain research.