Mechanical and neural stretch responses of the human soleus muscle at different walking speeds

During human walking, a sudden trip may elicit a Ia afferent fibre mediated short latency stretch reflex. The aim of this study was to investigate soleus (SOL) muscle mechanical behaviour in response to dorsiflexion perturbations, and to relate this behaviour to short latency stretch reflex responses. Twelve healthy subjects walked on a treadmill with the left leg attached to an actuator capable of rapidly dorsiflexing the ankle joint. Ultrasound was used to measure fascicle lengths in SOL during walking, and surface electromyography (EMG) was used to record muscle activation. Dorsiflexion perturbations of 6 deg were applied during mid‐stance at walking speeds of 3, 4 and 5 km h−1. At each walking speed, perturbations were delivered at three different velocities (slow: ∼170 deg s–1, mid: ∼230 deg s–1, fast: ∼280 deg s–1). At 5 km h−1, fascicle stretch amplitude was 34–40% smaller and fascicle stretch velocity 22–28% slower than at 3 km h−1 in response to a constant amplitude perturbation, whilst stretch reflex amplitudes were unchanged. Changes in fascicle stretch parameters can be attributed to an increase in muscle stiffness at faster walking speeds. As stretch velocity is a potent stimulus to muscle spindles, a decrease in the velocity of fascicle stretch at faster walking speeds would be expected to decrease spindle afferent feedback and thus stretch reflex amplitudes, which did not occur. It is therefore postulated that other mechanisms, such as altered fusimotor drive, reduced pre‐synaptic inhibition and/or increased descending excitatory input, acted to maintain motoneurone output as walking speed increased, preventing a decrease in short latency reflex amplitudes.

[1]  Thomas Sinkjær,et al.  Mobile ankle and knee perturbator , 2003, IEEE Transactions on Biomedical Engineering.

[2]  R G Soule,et al.  Energy cost of loads carried on the head, hands, or feet. , 1969, Journal of applied physiology.

[3]  J. Nielsen,et al.  Afferent feedback in the control of human gait. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[4]  P V Komi,et al.  The role of the stretch reflex in the gastrocnemius muscle during human locomotion at various speeds. , 2007, Journal of applied physiology.

[5]  C. Capaday,et al.  Difference in the amplitude of the human soleus H reflex during walking and running. , 1987, The Journal of physiology.

[6]  Uwe Proske,et al.  Kinesthesia: The role of muscle receptors , 2006, Muscle & nerve.

[7]  A A Biewener,et al.  In Vivo and In Vitro Heterogeneity of Segment Length Changes in the Semimembranosus Muscle of the Toad , 2003, The Journal of physiology.

[8]  A Prochazka,et al.  Muscle afferent function and its significance for motor control mechanisms during voluntary movements in cat, monkey, and man. , 1983, Advances in neurology.

[9]  U Proske,et al.  The role of muscle receptors in the detection of movements , 2000, Progress in Neurobiology.

[10]  T. Fukunaga,et al.  Superficial aponeurosis of human gastrocnemius is elongated during contraction: implications for modeling muscle-tendon unit. , 2002, Journal of biomechanics.

[11]  J. Nielsen,et al.  Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man , 2000, The Journal of physiology.

[12]  Thomas Sinkjær,et al.  An actuator system for investigating electrophysiological and biomechanical features around the human ankle joint during gait , 1995 .

[13]  T Finni,et al.  Behaviour of vastus lateralis muscle-tendon during high intensity SSC exercises in vivo. , 2003, Acta physiologica Scandinavica.

[14]  J. Nielsen,et al.  Positive force feedback in human walking , 2007, The Journal of physiology.

[15]  G. Lichtwark,et al.  Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. , 2007, Journal of biomechanics.

[16]  R Durbaba,et al.  Static and dynamic γ‐motor output to ankle flexor muscles during locomotion in the decerebrate cat , 2006, The Journal of physiology.

[17]  R. Stein,et al.  Regulation of soleus muscle spindle sensitivity in decerebrate and spinal cats during postural and locomotor activities. , 1996, The Journal of physiology.

[18]  R. Stein,et al.  Nonlinear behavior of muscle reflexes at the human ankle joint. , 1995, Journal of neurophysiology.

[19]  Vasilios Baltzopoulos,et al.  Predictability of in vivo changes in pennation angle of human tibialis anterior muscle from rest to maximum isometric dorsiflexion , 1999, European Journal of Applied Physiology and Occupational Physiology.

[20]  Michael Voigt,et al.  Effects of contraction intensity on muscle fascicle and stretch reflex behavior in the human triceps surae. , 2008, Journal of applied physiology.

[21]  M. Voigt,et al.  Modulation of short latency stretch reflexes during human hopping. , 1998, Acta physiologica Scandinavica.

[22]  Peggy Arnell,et al.  The Biomechanics and Motor Control of Human Gait , 1988 .

[23]  Andrew A Biewener,et al.  Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight , 2005, Journal of Experimental Biology.

[24]  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.

[25]  Andrew A Biewener,et al.  Functional diversification within and between muscle synergists during locomotion , 2008, Biology Letters.

[26]  R B Stein,et al.  Impulse rates and sensitivity to stretch of soleus muscle spindle afferent fibers during locomotion in premammillary cats. , 1985, Journal of neurophysiology.

[27]  Yasuo Kawakami,et al.  Architecture of contracting human muscles and its functional significance , 2000 .

[28]  T. Sinkjaer,et al.  Soleus stretch reflex modulation during gait in humans. , 1996, Journal of neurophysiology.

[29]  E. Simonsen,et al.  Amplitude of the human soleus H reflex during walking and running , 1999, The Journal of physiology.

[30]  Michael J Grey,et al.  Ankle extensor proprioceptors contribute to the enhancement of the soleus EMG during the stance phase of human walking. , 2004, Canadian journal of physiology and pharmacology.

[31]  Huub Maas,et al.  Distinct muscle fascicle length changes in feline medial gastrocnemius and soleus muscles during slope walking. , 2009, Journal of applied physiology.

[32]  G. Lichtwark,et al.  Is muscle–tendon unit length a valid indicator for muscle spindle output? , 2009, The Journal of physiology.

[33]  M. Kjaer,et al.  Load‐displacement properties of the human triceps surae aponeurosis in vivo , 2001, The Journal of physiology.

[34]  R. Stein,et al.  Fusimotor control of muscle spindle sensitivity during respiration in the cat. , 1990, The Journal of physiology.

[35]  P. Rack,et al.  Elastic properties of the cat soleus tendon and their functional importance. , 1984, The Journal of physiology.

[36]  R. Kram,et al.  The effects of adding mass to the legs on the energetics and biomechanics of walking. , 2007, Medicine and science in sports and exercise.

[37]  R. Stein,et al.  Factors that determine the magnitude and time course of human H- reflexes in locomotion , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  P. Rack,et al.  Reflex responses at the human ankle: the importance of tendon compliance. , 1983, The Journal of physiology.

[39]  P V Komi,et al.  Significance of passively induced stretch reflexes on achilles tendon force enhancement , 1998, Muscle & nerve.