Split-Belt Treadmill Stepping in Infants Suggests Autonomous Pattern Generators for the Left and Right Leg in Humans

The behavior of the pattern generator for walking in human infants (7-12 months of age) was studied by supporting the infants to step on a split-belt treadmill. The treadmill belts could be run at the same speed (tied-belt), different speeds, or in different directions (split-belt). We determined whether the legs could operate independently under these conditions, as demonstrated by taking different numbers of steps or by stepping in different directions. Video, surface electromyography, electrogoniometry, and force platform data were recorded. The majority of infants who could step under tied-belt conditions also stepped under split-belt conditions. During forward stepping at low speed differentials between the two belts (ratio, <4), infants adopted a step cycle duration that was intermediate between that expected from tied-belt stepping at each of the speeds. At large speed differentials between the two belts (ratio, 7-22), the infants took extra steps on the fast leg during the stance phase on the slow leg. When the two belts ran in opposite directions, one leg stepped forward, and the other stepped backward. During all forms of stepping, the legs maintained a reciprocal relationship, so that swing phase occurred in one leg at a time. Timing of muscle activity suggests a strong inhibition between the flexor-generating centers on each side and a weaker inhibition between the extensor-generating centers. The stepping behavior resembled that reported for other animals under similar conditions, suggesting that the pattern generator for each limb is autonomous but interacts with its counterpart for the contralateral limb.

[1]  U. Bässler,et al.  Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor-driven belt , 1985, Biological Cybernetics.

[2]  P. Stein,et al.  Modular Organization of Turtle Spinal Interneurons during Normal and Deletion Fictive Rostral Scratching , 2002, The Journal of Neuroscience.

[3]  Kristin Musselman,et al.  Infant stepping: a window to the behaviour of the human pattern generator for walking. , 2004, Canadian journal of physiology and pharmacology.

[4]  P. Jacobs,et al.  Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man. , 1994, Brain : a journal of neurology.

[5]  J. Nielsen.  How we Walk: Central Control of Muscle Activity during Human Walking , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[6]  J. F. Yang,et al.  Could different directions of infant stepping be controlled by the same locomotor central pattern generator? , 2000, Journal of neurophysiology.

[7]  C. Capaday,et al.  Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. , 1999, Journal of neurophysiology.

[8]  J. Halbertsma.  The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. , 1983, Acta physiologica Scandinavica. Supplementum.

[9]  M. Dimitrijevic,et al.  Evidence for a Spinal Central Pattern Generator in Humans a , 1998, Annals of the New York Academy of Sciences.

[10]  P. Stein,et al.  Example of 2:1 interlimb coordination during fictive rostral scratching in a spinal turtle. , 1998, Journal of neurophysiology.

[11]  Robert D. Martin,et al.  The Behavioural Physiology of Animals and Man. , 1974 .

[12]  P. Stein,et al.  Spinal cord coordination of hindlimb movements in the turtle: intralimb temporal relationships during scratching and swimming. , 1997, Journal of neurophysiology.

[13]  J. F. Yang,et al.  The initiation of the swing phase in human infant stepping: importance of hip position and leg loading , 2000, The Journal of physiology.

[14]  K. Pearson,et al.  Contribution of hind limb flexor muscle afferents to the timing of phase transitions in the cat step cycle. , 1996, Journal of neurophysiology.

[15]  J. Nielsen,et al.  Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking , 2001, The Journal of physiology.

[16]  D. Graham.  Pattern and Control of Walking in Insects , 1985 .

[17]  J. Duysens,et al.  Human neuronal interlimb coordination during split-belt locomotion , 2004, Experimental Brain Research.

[18]  Jaynie F Yang,et al.  Sensory Gating for the Initiation of the Swing Phase in Different Directions of Human Infant Stepping , 2002, The Journal of Neuroscience.

[19]  S. Soffe.  Roles of Glycinergic Inhibition and N‐Methyl‐D‐Aspartate Receptor Mediated Excitation in the Locomotor Rhythmicity of One Half of the Xenopus Embryo Central Nervous System , 1989, The European journal of neuroscience.

[20]  E Thelen,et al.  Bilateral coordination in human infants: stepping on a split-belt treadmill. , 1987, Journal of experimental psychology. Human perception and performance.

[21]  N. Kudo,et al.  Morphological and physiological studies of development of the monosynaptic reflex pathway in the rat lumbar spinal cord. , 1987, The Journal of physiology.

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

[23]  P. Stein,et al.  Spinal cord coordination of hindlimb movements in the turtle: interlimb temporal relationships during bilateral scratching and swimming. , 1997, Journal of neurophysiology.

[24]  S. Grillner,et al.  On the central generation of locomotion in the low spinal cat , 1979, Experimental Brain Research.

[25]  W. Zijlstra,et al.  Adaptational and learning processes during human split-belt locomotion: interaction between central mechanisms and afferent input , 2004, Experimental Brain Research.

[26]  S. Grillner.  Control of Locomotion in Bipeds, Tetrapods, and Fish , 1981 .

[27]  S. Rossignol,et al.  The locomotion of the low spinal cat. II. Interlimb coordination. , 1980, Acta physiologica Scandinavica.

[28]  C. Capaday.  The special nature of human walking and its neural control , 2002, Trends in Neurosciences.

[29]  R. Stein,et al.  Identification, Localization, and Modulation of Neural Networks for Walking in the Mudpuppy (Necturus Maculatus) Spinal Cord , 1998, The Journal of Neuroscience.

[30]  V. Reggie Edgerton,et al.  Neurobiological basis of human locomotion , 1991 .

[31]  L. Jordan.  Brain stem and spinal cord mechanisms for the initiation of locomotion , 1991 .

[32]  V. Dietz,et al.  Adaptational effects during human split-belt walking: influence of afferent input , 1998, Experimental Brain Research.

[33]  O. Kiehn,et al.  Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord , 2003, Progress in Neurobiology.

[34]  P. Stein,et al.  Variations in motor patterns during fictive rostral scratching in the turtle: knee-related deletions. , 2004, Journal of neurophysiology.

[35]  P. Stein.  Neuronal control of turtle hindlimb motor rhythms , 2005, Journal of Comparative Physiology A.

[36]  J. F. Yang,et al.  Infant stepping: a method to study the sensory control of human walking , 1998, The Journal of physiology.