Early changes in muscle activation patterns of toddlers during walking.

Early locomotor behavior has been the focus of considerable attention by developmentalists over several decades. Few studies have addressed explicitly patterns of muscle activity that underlie this coordination pattern. Our purposes were to illustrate a method to determine objectively the onset and offset of muscle firings during early walking and to investigate the emergence of patterns of activation of the core locomotor muscles. We tested eight toddlers as they walked overground at walking onset (max. of 3-6 independent steps) and after three months of walking experience. Surface electrodes monitored activity of the gastrocnemius, tibialis anterior, quadriceps, and hamstrings. We reduced EMG signals to a frame-by-frame designation of "on-off," followed by muscle state and co-contraction analyses, and probability distributions for each muscle's activity across multiple cycles. Our results clearly show that at walking onset muscle activity was highly variable with few, if any, muscles showing recurring patterns of behavior, within or among toddlers. Variability and co-activation decreased with walking experience but remained inconsistent, in contrast to the significant increase in stability shown for joint coordination and endpoint (foot placement) parameters. We propose this trend emerges because of the high number of options (muscle combinations) available. Toddlers learn first to marshal sufficient force to balance and make forward progress but slowly discover how to optimize these resources.

[1]  M. E. Morbeck Primate morphophysiology, locomotor analyses and human bipedalism , 1986, International Journal of Primatology.

[2]  Hiroshi Shimizu,et al.  Self-organized control of bipedal locomotion by neural oscillators in unpredictable environment , 1991, Biological Cybernetics.

[3]  M. Hanson,et al.  Normal Patterns of Spontaneous Activity Are Required for Correct Motor Axon Guidance and the Expression of Specific Guidance Molecules , 2004, Neuron.

[4]  David A. Winter,et al.  Biomechanics and Motor Control of Human Movement , 1990 .

[5]  Jane E. Clark,et al.  The development of intralimb coordination in the first six months of walking , 1991 .

[6]  A. Hof Scaling gait data to body size , 1996 .

[7]  D. Sutherland,et al.  The Development of mature walking , 1988 .

[8]  H. Forssberg,et al.  Ontogeny of postural adjustments during sitting in infancy: variation, selection and modulation. , 1996, The Journal of physiology.

[9]  R. Platt,et al.  Reducing antibiotic use in children: a randomized trial in 12 practices. , 2001, Pediatrics.

[10]  P. Hodges,et al.  A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. , 1996, Electroencephalography and clinical neurophysiology.

[11]  Annick Ledebt,et al.  Changes in arm posture during the early acquisition of walking , 2000 .

[12]  M T Turvey,et al.  Commentary: development of perception-action systems and general principles of pattern formation. , 1993, Child development.

[13]  M. Hadders‐Algra,et al.  The development of postural adjustments during reaching in 6- to 18-month-old infants Evidence for two transitions , 1999, Experimental Brain Research.

[14]  B. Ulrich,et al.  Treadmill training of infants with Down syndrome: evidence-based developmental outcomes. , 2001, Pediatrics.

[15]  E. Thelen,et al.  A multimuscle state analysis of adult motor learning , 1999, Experimental Brain Research.

[16]  Esther Thelen,et al.  Spatially Specific Changes in Infants' Muscle Coactivity as They Learn to Reach. , 2000, Infancy : the official journal of the International Society on Infant Studies.

[17]  D. Corbetta,et al.  Infants Return to Two-Handed Reaching When They Are Learning to Walk , 2002, Journal of motor behavior.

[18]  J. H. Cocatre-Zilgien,et al.  A new method of depicting animal step patterns , 1993, Animal Behaviour.

[19]  E. Goldfield Emergent Forms: Origins and Early Development of Human Action and Perception , 1995 .

[20]  E. Thelen,et al.  Exploration and selection in the early acquisition of skill. , 1994, International review of neurobiology.

[21]  R N Marshall,et al.  Algorithms to determine event timing during normal walking using kinematic data. , 2000, Journal of biomechanics.

[22]  Jane E. Clark,et al.  A longitudinal study of intralimb coordination in the first year of independent walking: a dynamical systems analysis. , 1993, Child development.

[23]  J Whitall,et al.  A developmental study of the interlimb coordination in running and galloping. , 1989, Journal of motor behavior.

[24]  A. Opstal Dynamic Patterns: The Self-Organization of Brain and Behavior , 1995 .

[25]  E. Gibson Exploratory behavior in the development of perceiving, acting, and the acquiring of knowledge. , 1988 .

[26]  Nancy Bayley,et al.  The development of motor abilities during the first three years : a study of sixty-one infants tested repeatedly , 1936 .

[27]  Tsutomu Okamoto,et al.  Electromyographic developmental changes in one individual from newborn stepping to mature walking. , 2003, Gait & posture.

[28]  Marion A. Eppler,et al.  Crawling versus walking infants' perception of affordances for locomotion over sloping surfaces. , 1993, Child development.

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

[30]  C. Giuliani,et al.  A kinematic and electromyographic analysis of the development of sitting posture in infants. , 1993, Developmental psychobiology.

[31]  G Schöner,et al.  A synergetic theory of quadrupedal gaits and gait transitions. , 1990, Journal of theoretical biology.

[32]  Mijna Hadders-Algra,et al.  Variability in infant motor behavior: A hallmark of the healthy nervous system , 2002 .

[33]  G. Edelman,et al.  Solving Bernstein's problem: a proposal for the development of coordinated movement by selection. , 1993, Child development.

[34]  S. J. Phillips,et al.  Human interlimb coordination: the first 6 months of independent walking. , 1988, Developmental psychobiology.

[35]  E. Thelen,et al.  Hidden skills: a dynamic systems analysis of treadmill stepping during the first year. , 1991, Monographs of the Society for Research in Child Development.

[36]  E. Thelen,et al.  The transition to reaching: mapping intention and intrinsic dynamics. , 1993, Child development.

[37]  H. Forssberg,et al.  Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion , 2004, Experimental Brain Research.