Distinct muscle fascicle length changes in feline medial gastrocnemius and soleus muscles during slope walking.

On the basis of differences in physiology, e.g., histochemical properties and spindle density, and the structural design of the cat soleus (SO) and medial gastrocnemius (MG) muscles, we hypothesized that 1) fascicle length changes during overground walking would be both muscle and slope dependent, which would have implications for the muscles' force output as well as sensory function, and that 2) muscle-tendon unit (MTU) and fascicle length changes would be different, in which case MTU length could not be used as an indicator of muscle spindle strain. To test these hypotheses, we quantified muscle fascicle length changes and compared them with length changes of the whole MTU in the SO and MG during overground walking at various slopes (0, +/- 25, +/- 50, +75, and +100%). The SO and MG were surgically instrumented with sonomicrometry crystals and fine-wire electromyogram electrodes to measure changes in muscle fascicle length and muscle activity, respectively. MTU lengths were calculated using recorded ankle and knee joint angles and a geometric model of the hindlimb. The resultant joint moments were calculated using inverse dynamics analysis to infer muscle loading. It was found that although MTU length and velocity profiles of the SO and MG appeared similar, length changes and velocities of muscle fascicles were substantially different between the two muscles. Fascicle length changes of both SO and MG were significantly affected by slope intensity acting eccentrically in downslope walking (-25 to -50%) and concentrically in upslope walking (+25 to +100%). The differences in MTU and fascicle behaviors in both the SO and MG muscles during slope walking were explained by the three distinct features of these muscles: 1) the number of joints spanned, 2) the pennation angle, and 3) the in-series elastic component. It was further suggested that the potential role of length feedback from muscle spindles is both task and muscle dependent.

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

[2]  J. Hoffer,et al.  Velocity of ultrasound in active and passive cat medial gastrocnemius muscle. , 1992, Journal of biomechanics.

[3]  R L Marsh,et al.  Activation patterns and length changes in hindlimb muscles of the bullfrog Rana catesbeiana during jumping. , 1998, The Journal of experimental biology.

[4]  W Herzog,et al.  Force-sharing between cat soleus and gastrocnemius muscles during walking: explanations based on electrical activity, properties, and kinematics. , 1994, Journal of biomechanics.

[5]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.

[6]  M. Sirota,et al.  Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. , 2005, Journal of neurophysiology.

[7]  P. Carlson-Kuhta,et al.  Forms of forward quadrupedal locomotion. III. A comparison of posture, hindlimb kinematics, and motor patterns for downslope and level walking. , 1998, Journal of neurophysiology.

[8]  S. Rossignol,et al.  Dynamic sensorimotor interactions in locomotion. , 2006, Physiological reviews.

[9]  W. Herzog,et al.  Coordination of medial gastrocnemius and soleus forces during cat locomotion , 2003, Journal of Experimental Biology.

[10]  Uwe Windhorst,et al.  Muscle spindles are multi-functional , 2008, Brain Research Bulletin.

[11]  R. Burke Motor Units: Anatomy, Physiology, and Functional Organization , 1981 .

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

[13]  J. Eng,et al.  Regional variability of stretch reflex amplitude in the cat medial gastrocnemius muscle during a postural task. , 1997, Journal of neurophysiology.

[14]  R. Gregor,et al.  The effects of self-reinnervation of cat medial and lateral gastrocnemius muscles on hindlimb kinematics in slope walking , 2007, Experimental Brain Research.

[15]  R. Gregor,et al.  Hindlimb Kinetics and Neural Control during Slope Walking in the Cat: Unexpected Findings , 2001 .

[16]  R. Roy,et al.  Architecture of the hind limb muscles of cats: Functional significance , 1982, Journal of morphology.

[17]  T. Roberts,et al.  Mechanical function of two ankle extensors in wild turkeys: shifts from energy production to energy absorption during incline versus decline running , 2004, Journal of Experimental Biology.

[18]  D. Denny-Brown,et al.  The Histological Features of Striped Muscle in Relation to Its Functional Activity , 1929 .

[19]  M. Hoy,et al.  Modulation of limb dynamics in the swing phase of locomotion. , 1984, Journal of biomechanics.

[20]  V R Edgerton,et al.  A technique for estimating mechanical work of individual muscles in the cat during treadmill locomotion. , 1984, Journal of biomechanics.

[21]  P. Huijing Muscular Force Transmission Necessitates a Multilevel Integrative Approach to the Analysis of Function of Skeletal Muscle , 2003, Exercise and sport sciences reviews.

[22]  A. Biewener,et al.  In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. , 1998, The Journal of experimental biology.

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

[24]  P A Huijing,et al.  Influence of muscle geometry on shortening speed of fibre, aponeurosis and muscle. , 1992, Journal of biomechanics.

[25]  J. Houk,et al.  Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. , 1976, Journal of neurophysiology.

[26]  G. Loeb,et al.  Mechanics of feline soleus: I. Effect of fascicle length and velocity on force output , 1996, Journal of Muscle Research and Cell Motility.

[27]  R. Gregor,et al.  Relationship between ankle muscle and joint kinetics during the stance phase of locomotion in the cat. , 1993, Journal of biomechanics.

[28]  W. Herzog,et al.  Forces in gastrocnemius, soleus, and plantaris tendons of the freely moving cat. , 1993, Journal of biomechanics.

[29]  T Richard Nichols,et al.  Three‐dimensional model of the feline hindlimb , 2004, Journal of morphology.

[30]  R. Griffiths Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. , 1991, The Journal of physiology.

[31]  A. Biewener,et al.  Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping , 2004, Journal of Experimental Biology.

[32]  R. Griffiths,et al.  Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. , 1989, Progress in brain research.

[33]  V. Edgerton,et al.  HINDLIMB MUSCLE FIBER POPULATIONS OF FIVE MAMMALS , 1973 .

[34]  P. Rack,et al.  Changes in the length of the human biceps brachii muscle during elbow movements. , 1987, The Journal of physiology.

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

[36]  V. Edgerton,et al.  Muscle architecture and force-velocity characteristics of cat soleus and medial gastrocnemius: implications for motor control. , 1980, Journal of neurophysiology.

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

[38]  E. Perreault,et al.  Modeling short-range stiffness of feline lower hindlimb muscles. , 2008, Journal of biomechanics.

[39]  B. Prilutsky,et al.  Role of the muscle belly and tendon of soleus, gastrocnemius, and plantaris in mechanical energy absorption and generation during cat locomotion. , 1996, Journal of biomechanics.

[40]  T. Sandercock,et al.  Nonlinear summation of force in cat soleus muscle results primarily from stretch of the common-elastic elements. , 2000, Journal of applied physiology.

[41]  W. Smith The Integrative Action of the Nervous System , 1907, Nature.

[42]  A Prochazka,et al.  In‐series compliance of gastrocnemius muscle in cat step cycle: do spindles signal origin‐to‐insertion length? , 1990, The Journal of physiology.

[43]  P. Carlson-Kuhta,et al.  Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. , 1998, Journal of neurophysiology.

[44]  M. Taussig The Nervous System , 1991 .

[45]  B. Prilutsky,et al.  Mechanical power and work of cat soleus, gastrocnemius and plantaris muscles during locomotion: possible functional significance of muscle design and force patterns. , 1996, The Journal of experimental biology.

[46]  H. Sugi,et al.  Stiffness changes in frog skeletal muscle during contraction recorded using ultrasonic waves. , 1988, The Journal of physiology.

[47]  D. W. Smith,et al.  Mechanics of slope walking in the cat: quantification of muscle load, length change, and ankle extensor EMG patterns. , 2006, Journal of neurophysiology.

[48]  V R Edgerton,et al.  Mechanical output of the cat soleus during treadmill locomotion: in vivo vs in situ characteristics. , 1988, Journal of biomechanics.

[49]  A. Biewener,et al.  In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia) , 1998, The Journal of experimental biology.

[50]  M. Fitzgerald Symposium on Muscle Receptors , 1963, Neurology.

[51]  L. Jami,et al.  Muscle afferents and spinal control of movement , 1992 .

[52]  B. Walmsley,et al.  Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. , 1978, Journal of neurophysiology.

[53]  A A Biewener,et al.  Muscle and Tendon Contributions to Force, Work, and Elastic Energy Savings: A Comparative Perspective , 2000, Exercise and sport sciences reviews.