Contribution of stretch reflexes to locomotor control: a modeling study

Abstract.It is known that the springlike properties of muscles provide automatic load compensation during weight bearing. How crucial is sensory control of the motor output given these basic properties of the locomotor system? To address this question, a neuromuscular model was used to test two hypotheses. (1) Stretch reflexes are too weak and too delayed to contribute significantly to weight-bearing. (2) The important contributions of sensory input involve state-dependent processing. We constructed a two-legged planar locomotor model with 9 segments, driven by 12 musculotendon actuators with Hill-type force-velocity and monotonic force-length properties. Electromyographic (EMG) profiles of the simulated muscle groups during slow level walking served as actuator activation functions. Spindle Ia and tendon organ Ib sensory inputs were represented by transfer functions with a latency of 35 ms, contributing 30% to the net EMG profile and gated to be active only when the receptor-bearing muscles were contracting. Locomotor stability was assessed by parametric variations of actuator maximum forces during locomotion in open-loop (“deafferented”) trials and in trials with feedback control based on either sensory-evoked stretch reflexes or finite-state rules. We arrived at the following conclusions. (1) In the absence of sensory control, the intrinsic stiffness of limb muscles driven by a stereotyped rhythmical pattern can produce surprisingly stable gait. (2) When the level of central activity is low, the contribution of stretch reflexes to load compensation can be crucial. However, when central activity provides adequate load compensation, the contribution of stretch reflexes is less significant. (3) Finite-state control can greatly extend the adaptive capability of the locomotor system.

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

[2]  P. Rack,et al.  The short range stiffness of active mammalian muscle. , 1973, The Journal of physiology.

[3]  Rack Pm,et al.  The short range stiffness of active mammalian muscle. , 1973 .

[4]  J. F. Yang,et al.  Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans , 2004, Experimental Brain Research.

[5]  C. Capaday,et al.  Amplitude modulation of the soleus H-reflex in the human during walking and standing , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  F Lacquaniti,et al.  Influence of leg muscle vibration on human walking. , 2000, Journal of neurophysiology.

[7]  V. Dietz,et al.  Amplitude modulation of the human quadriceps tendon jerk reflex during gait , 2004, Experimental Brain Research.

[8]  K. Pearson,et al.  Chemical ablation of sensory afferents in the walking system of the cat abolishes the capacity for functional recovery after peripheral nerve lesions , 2003, Experimental Brain Research.

[9]  A. Prochazka,et al.  Adaptive changes in locomotor control after partial denervation of triceps surae muscles in the cat , 2001, Journal of Physiology.

[10]  Nobutoshi Yamazaki,et al.  Generation of human bipedal locomotion by a bio-mimetic neuro-musculo-skeletal model , 2001, Biological Cybernetics.

[11]  T. Brown The intrinsic factors in the act of progression in the mammal , 1911 .

[12]  T. Sinkjaer,et al.  Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. , 1988, Journal of neurophysiology.

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

[14]  G. E. Goslow,et al.  The cat step cycle: Hind limb joint angles and muscle lengths during unrestrained locomotion , 1973, Journal of morphology.

[15]  Sergiy Yakovenko,et al.  Spatiotemporal activation of lumbosacral motoneurons in the locomotor step cycle. , 2002, Journal of neurophysiology.

[16]  I. Engberg,et al.  An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. , 1969, Acta physiologica Scandinavica.

[17]  R B Stein,et al.  Gain of the triceps surae stretch reflex in decerebrate and spinal cats during postural and locomotor activities. , 1996, The Journal of physiology.

[18]  Gentaro Taga,et al.  A model of the neuro-musculo-skeletal system for anticipatory adjustment of human locomotion during obstacle avoidance , 1998, Biological Cybernetics.

[19]  K. G. Pearson,et al.  Comparison of the effects of stimulating extensor group I afferents on cycle period during walking in conscious and decerebrate cats , 1997, Experimental Brain Research.

[20]  K. Akazawa,et al.  Modulation of stretch reflexes during locomotion in the mesencephalic cat , 1982, The Journal of physiology.

[21]  M. Gorassini,et al.  Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats , 1998, The Journal of physiology.

[22]  K. Pearson,et al.  Functional role of muscle reflexes for force generation in the decerebrate walking cat , 2000, The Journal of physiology.

[23]  L. D. Partridge,et al.  Signal-handling characteristics of load-moving skeletal muscle. , 1966, The American journal of physiology.

[24]  A. Prochazka Quantifying proprioception. , 1999, Progress in brain research.

[25]  K. Pearson,et al.  Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. , 1999, Journal of neurophysiology.

[26]  P. Zangger,et al.  Muscle spindle control during locomotor movements generated by the deafferented spinal cord. , 1976, Acta physiologica Scandinavica.

[27]  A. Prochazka,et al.  Comparison of natural and artificial control of movement , 1993 .

[28]  J. He,et al.  Feedback gains for correcting small perturbations to standing posture , 1989, Proceedings of the 28th IEEE Conference on Decision and Control,.

[29]  F. Zajac,et al.  Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. , 2001, Journal of biomechanics.

[30]  M. Gorassini,et al.  Corrective responses to loss of ground support during walking. I. Intact cats. , 1994, Journal of neurophysiology.

[31]  A. Prochazka,et al.  Sensory control of locomotion: reflexes versus higher-level control. , 2002, Advances in experimental medicine and biology.

[32]  T. A. Abelew,et al.  Local loss of proprioception results in disruption of interjoint coordination during locomotion in the cat. , 2000, Journal of neurophysiology.

[33]  B. Andrews,et al.  Improving limb flexion in FES gait using the flexion withdrawal response for the spinal cord injured person. , 1993, Journal of biomedical engineering.

[34]  F. Honegger,et al.  Triggering of balance corrections and compensatory strategies in a patient with total leg proprioceptive loss , 2001, Experimental Brain Research.

[35]  N Teasdale,et al.  Gait of a deafferented subject without large myelinated sensory fibers below the neck , 1996, Neurology.

[36]  A. Prochazka,et al.  Implications of positive feedback in the control of movement. , 1997, Journal of neurophysiology.

[37]  Adolf Bickel,et al.  Ueber den Einfluss der sensibelen Nerven und der Labyrinthe auf die Bewegungen der Thiere , 2005, Archiv für die gesamte Physiologie des Menschen und der Tiere.

[38]  A Prochazka,et al.  Isometric muscle length-tension curves do not predict angle-torque curves of human wrist in continuous active movements. , 2000, Journal of biomechanics.