Summary
Locomotor patterns of human infants were studied during stepping in the newborn period (first two months of life), during supported locomotion (6–12 months of age) and during independent locomotion in children who just were able to walk by themselves without external support (10–18 months of age). Leg movements, pattern of muscular activity and reaction forces were studied by a computerized system. The locomotor pattern during the newborn period lacked the specific functions that are unique for human plantigrade locomotion. There was no heel strike in front of the body; the foot was placed instead on its forepart straight under the body. Hip and knee joints were hyperflexed during the whole step cycle and flexed synchronously during swing. The specific knee-ankle coordination of human adults was missing. The ankle extensors were activated prior to touch down together with other extensor muscles. There was no propulsive force. A similar immature non-plantigrade pattern recurred after an inactive period. During the subsequent period of supported locomotion there was a gradual transformation of the infantile pattern towards the plantigrade pattern continuing after establishment of independent locomotion. It is suggested that innate pattern generators in the spinal cord produce the infant stepping and also generate the basic locomotor rhythm in adults, but that neural circuits specific for humans develop late in ontogeny and transform the original, non-plantigrade motor activity to a plantigrade locomotor pattern.
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References
Andre'-Thomas, Autgarden S (1966) Locomotion from pre- to postnatal life. Clin Dev Med, Spastics Society, Lavenham, Suffolk
Bernstein N (1967) The coordination and regulation of movements. Pergamon Press, Oxford
Bresler B, Frankel JP (1950) The forces and moments in the leg during level walking. Trans Am Soc Mech Eng 72: 27–36
Brown TG (1911) The intrinsic factors in the act of progression in the mammal. Proc R Soc B 84: 308–319
Bruner JS, Bruner MB (1968) On voluntary action and its hierarchical structure. Int J Psychol 3: 239–255
Burnett CN, Johnson EW (1971) Development of gait in childhood: Part II. Develop Med Child Neurol 13: 207–215
Cavagna GA, Margaria R (1966) Mechanics of walking. J Appl Physiol 21: 271–278
Darwin C (1872) The descent of man
Eberhardt HD, Tuman VT, Bresler B (1954) The principal elements in human locomotion. In: Klopsteg PE, Wilson PD (eds) Human Limbs and their Substitutes. McGraw-Hill, New York, pp 437–471
Engberg I (1964) Reflexes to foot muscles in the cat. Acta Physiol Scand Suppl 235
Engberg I, Lundberg A (1969) An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Acta Physiol Scand 75: 614–630
Elftman H (1944) The bipedal walking of the chimpanzee. J Mammology 25: 67–71
Elftman H, Manter J (1935) Chimpanzee and human feet in bipedal walking. Am J Phys Anthrop 20: 69–79
Forssberg H (1982) Spinal locomotor functions and descending control. In: Sjölund B, Björklund A (eds) Brain Stem Control of Spinal Mechanisms. Elsevier Biomedical Press, Amsterdam, pp 253–271
Forssberg H, Grillner S (1973) The locomotion of the acute spinal cat injected with Clonidine i.v. Brain Res 50: 184–186
Forssberg H, Grillner S, Halbertsma J (1980a) The locomotion of the spinal cat. 1. Coordination within a hindlimb. Acta Physiol Scand 108: 269–281
Forssberg H, Grillner S, Halbertsma J, Rossignol S (1980b) The locomotion of the spinal cat. 2. Interlimb coordination. Acta Physiol Scand 108: 283–295
Forssberg H, Wallberg H (1980) Infant locomotion: A preliminary movement and electromyografic study. In: Berg K, Eriksson BO (eds) Children and Exercise IX. University Park Press, Baltimore, pp 32–40
Forssberg H, Johnels B, Steg G (1984) Is Parkinsonian gait caused by a regression to a more immature walking pattern? Adv Neurol 40: 375–379
Goslow JR, Reinking RM, Stuart DG (1973) The cat step cycle: Hindlimb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141: 1–42
Gottlieb GL, Myklebust BM, Penn RD, Agarwall GC (1982) Reciprocal excitation of muscle antagonists by primary afferent pathway. Exp Brain Res 46: 454–456
Gray J (1968) Animal locomotion. William Clowes & Sons, London
Griffin PP, Wheelhouse WW, Shiavi R, Bass W (1977) Habitual toe-walkers. J Bone Joint Surg 59: 97–101
Grillner S, Zangger P (1979) On the central generation of locomotion in the low spinal cat. Exp Brain Res 34: 241–262
Halbertsma J (1983) The stride cycle of the cat. A computarized analysis and modelling of locomotor movements in the cat. Thesis Technische Hogeschool Delft
Jankowska E, Jukes MGM, Lund S, Lundberg A (1967) The effect of DOPA on the spinal cord. 6. Halfcenter organization of inteneurones transmitting effects from the flexor reflex afferents. Acta Physiol Scand 70: 389–402
Jankowska E, McCrea D, Mackel R (1981) Oligosynaptic excitation of motoneurones by impulses in group Ia muscle spindle afferents in the cat. J Physiol (Lond) 316: 411–425
Johanson DC, White TD (1979) A systematic assessment of early african hominids. Science 203: 321–330
Kazai N, Okamato T, Kumamato M (1976) Electromyographic study of supported walking of infants in the initial period of learning to walk. In: Komi PV (ed) Biomechanics V-A. University Park Press, pp 311–318
Kondo S (1960) Anthropological study on human posture and locomotion. J Fac Sci Univ Tokyo Anthropol 5: 189–260
Knutsson E, Richards C (1979) Different types of disturbed motor control in gait of hemiparetic patients. Brain 102: 405–430
Kuhn RA (1950) Functional capacity of the isolated human spinal cord. Brain 73: 1–51
Leakey MD, Hay RL (1979) Pliocene footprints in the Laetoli beds at Laetoli, northern Tanzania. Nature 278: 317–323
Manter JT (1938) The dynamics of quadrupedal walking. J Exp Biol 15: 522–540
McGraw MB (1940) Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion. J Pediatr 17: 747–777
McHenry HM (1975) Fossils and the mosaic nature of human evolution. Science 190: 425–430
Mori S, Kawahara K, Sakamoto M, Aoki M, Tomiyama T (1982) Setting and resetting of level of postural muscle tone in decerebrate cat by stimulation of brain stem. J Neurophysiol 48: 737–748
Mori S, Shik ML, Yagodnitsyn AS (1977) Role of pontine tegmentum for locomotor control in mesencephalic cat. J Neurophysiol 40: 284–295
Morrison JB (1970) The mechanics of the knee joint in relation to normal walking. J Biomech 3: 51–61
Okada M, Ishida H, Kimura T (1976) Biomechanical features of bipedal gait in human and nonhuman primates. In: Komi PV (eds) Biomechanics V-A. University Park Press, Baltimore, pp 303–309
Okamoto T, Kumamato M (1972) Electromyographic study of the learning process of walking in infants. Electromyografy 12: 149–158
Oppenheim RW (1981) Ontogenetic adaptations and retrogressive processes in the development of the nervous system and behaviour. In: Prechtl HFR, Conolly K (eds) Maturation and Development. Spastics International Medical Publications and William Heinemann Medical Books, London
Pedotti A (1977) A study of motor coordination and neuromuscular activities in human locomotion. Biol Cybern 26: 53–62
Peiper A (1961) Cerebral functions in infancy and childhood. Consultants Bureau, New York
Perry J, Hoffer MM, Giovan P, Antonelli D, Greenberg R (1974) Gait analysis of the triceps surae in cerebral palsy. J Bone Joint Surg 56: 511–520
Prost JH (1967) Bipedalism of man and gibbon compared using estimates of joint motion. Am J Phys Anthrop 26: 135–148
Riddoch G (1917) The reflex functions of the completely divided spinal cord in man, compared with those associated with less severe lesions. Brain 40: 264–401
Rossignol S, Barbeau H, Provencher J (1982) Locomotion in the adult chronic spinal cat. Soc Neurosci 8: 47.1
Russel D, Zajac F (1979) Effects of stimulating Deiter's nucleus and medial longitudinal fasciculus on the timing of the fictive locomotor rhythm induced in cats by DOPA. Brain Res 177: 588–592
Saunders JB, Inman VT, Eberhardt HD (1953) The major determinants in normal and pathological gait. J Bone Joint Surg 35: 543–558
Sherrington CS (1947) The integrative action of the central nervous system. New Haven, Yale University Press
Shik ML, Orlovsky GN (1976) Neurophysiology of locomotor automatism. Physiol Rev 55: 465–501
Smith JL, Smith LA, Zernicke RF, Hoy M (1982) Locomotion in exercised and non-exercised cats cordotomized at 2 or 12 weeks of age. Exp Neurol 76: 393–413
Statham L, Murray MP (1971) Early walking patterns of normal children. Clin Orthop 79: 8–24
Stelzner DJ, Ershler WB, Weber ED (1975) Effects of spinal transection in neonatal and weanling rats: Survival of function. Exp Neurol 46: 156–177
Sutherland DH, Olshen R, Cooper L, Woo SLY (1980) The development of mature gait. J Bone Joint Surg 62: 336–353
Thelen E, Bradshaw G, Ward JA (1981) Spontaneous kicking in month-old infants: Manifestation of human central locomotor program. Behav Neurol Biol 32: 45–53
Thelen E, Fisher DM (1982) Newborn stepping: An explanation for a “disappearing” reflex. Dev Psychol 18: 760–775
Weber ED, Stelzner DJ (1977) Behavioral effects of spinal cord transection in the developing rat. Brain Res 125: 241–255
White TD (1980) Evolutionary implications of pliocene hominid footprints. Science 208: 175–176
Zelazo PR, Zelazo N, Kolb S (1972) “Walking” in the newborn. Science 176: 314–315
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Forssberg, H. Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res 57, 480–493 (1985). https://doi.org/10.1007/BF00237835
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DOI: https://doi.org/10.1007/BF00237835