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      Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists

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          Abstract

          The mechanism of the compensatory increase in electromyographic activity (EMG) of a cat ankle extensor during walking shortly after paralysis of its synergists is not fully understood. It is possible that due to greater ankle flexion in stance in this situation, muscle spindles are stretched to a greater extent and, thus, contribute to the EMG enhancement. However, also changes in force feedback and central drive may play a role. The aim of the present study was to investigate the short-term (1- to 2-week post-op) effects of lateral gastrocnemius (LG) and soleus (SO) denervation on muscle fascicle and muscle–tendon unit (MTU) length changes, as well as EMG activity of the intact medial gastrocnemius (MG) muscle in stance during overground walking on level (0%), downslope (−50%, presumably enhancing stretch of ankle extensors in stance) and upslope (+50%, enhancing load on ankle extensors) surfaces. Fascicle length was measured directly using sonomicrometry, and MTU length was calculated from joint kinematics. For each slope condition, LG-SO denervation resulted in an increase in MTU stretch and peak stretch velocity of the intact MG in early stance. MG muscle fascicle stretch and peak stretch velocity were also higher than before denervation in downslope walking. Denervation significantly decreased the magnitude of MG fascicle shortening and peak shortening velocity during early stance in level and upslope walking. MG EMG magnitude in the swing and stance phases was substantially greater after denervation, with a relatively greater increase during stance of level and upslope walking. These results suggest that the fascicle length patterns of MG muscle are significantly altered when two of its synergists are in a state of paralysis. Further, the compensatory increase in MG EMG is likely mediated by enhanced MG length feedback during downslope walking, enhanced feedback from load-sensitive receptors during upslope walking and enhanced central drive in all walking conditions.

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          Most cited references39

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          Dynamic sensorimotor interactions in locomotion.

          Locomotion results from intricate dynamic interactions between a central program and feedback mechanisms. The central program relies fundamentally on a genetically determined spinal circuitry (central pattern generator) capable of generating the basic locomotor pattern and on various descending pathways that can trigger, stop, and steer locomotion. The feedback originates from muscles and skin afferents as well as from special senses (vision, audition, vestibular) and dynamically adapts the locomotor pattern to the requirements of the environment. The dynamic interactions are ensured by modulating transmission in locomotor pathways in a state- and phase-dependent manner. For instance, proprioceptive inputs from extensors can, during stance, adjust the timing and amplitude of muscle activities of the limbs to the speed of locomotion but be silenced during the opposite phase of the cycle. Similarly, skin afferents participate predominantly in the correction of limb and foot placement during stance on uneven terrain, but skin stimuli can evoke different types of responses depending on when they occur within the step cycle. Similarly, stimulation of descending pathways may affect the locomotor pattern in only certain phases of the step cycle. Section ii reviews dynamic sensorimotor interactions mainly through spinal pathways. Section iii describes how similar sensory inputs from the spinal or supraspinal levels can modify locomotion through descending pathways. The sensorimotor interactions occur obviously at several levels of the nervous system. Section iv summarizes presynaptic, interneuronal, and motoneuronal mechanisms that are common at these various levels. Together these mechanisms contribute to the continuous dynamic adjustment of sensorimotor interactions, ensuring that the central program and feedback mechanisms are congruous during locomotion.
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            The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion.

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              Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance.

              1. The length of muscle fibres in the medial gastrocnemius (MG) muscle of the anaesthetized cat was measured using ultrasound techniques. During the course of 'isometric' contractions, the muscle fibres shortened by stretching the compliant tendons, until the muscle fibres could no longer produce enough force to stretch the tendons further. At optimal muscle length (Lo) the maximal shortening of muscle fibres was 28%. 2. At muscle lengths much longer than Lo, 'isometric' contractions produced a slow shortening of the muscle fibres as the tendons were stretched and this resulted in a slow rise in tension. This phenomenon, usually referred to as 'creep', is due to low power at long muscle fibre length. This study shows that the series compliance present in the tendons is the major contributor to 'creep' in the cat MG muscle. As the tendons stretched during the course of the contraction, the average sarcomere length became shorter providing greater filament overlap and increasing power. 3. Slow to medium speed stretches applied shortly after the onset of contraction, as occurs in cat MG during walking and trotting, were entirely taken up in the tendons and the muscle fibres actually shortened throughout the imposed muscle stretch. 4. When early stretches were applied at muscle lengths longer than Lo, stretch of the muscle resulted in a peak force that was less than if the stretch had not been applied. This was the reverse of the situation for stretches at lengths less than Lo. When stretch was applied after attaining peak force, the force was greatly enhanced and the muscle fibres were also stretched. 5. Using the same techniques in a freely walking cat, the muscle fibres shortened by 1.0 +/- 0.3 mm during the stance phase of the step-cycle when the muscle was being stretched, in 198 consecutive step-cycles. 6. The tendons act as a mechanical buffer to protect muscle fibres from damage during eccentric contractions. 7. Since stretches of the MG muscle are not faithfully imposed on the muscle fibres, studies of muscle spindle function during locomotion need to take into consideration these effects of tendon compliance. The dominant view, when the foot lands on the ground during normal locomotion, is that muscle spindles are stretched along with the muscle resulting in reflex enhancement of contractile force. This study shows that the muscle fibres do not stretch under these circumstances, except at high speeds of locomotion when the stretch rate is also high.
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                Author and article information

                Contributors
                h.maas@fbw.vu.nl
                Journal
                Exp Brain Res
                Experimental Brain Research. Experimentelle Hirnforschung. Experimentation Cerebrale
                Springer-Verlag (Berlin/Heidelberg )
                0014-4819
                1432-1106
                11 May 2010
                11 May 2010
                June 2010
                : 203
                : 4
                : 681-692
                Affiliations
                [1 ]School of Applied Physiology, Georgia Institute of Technology, Atlanta, GA USA
                [2 ]Research Institute MOVE, Faculty of Human Movement Sciences, VU University Amsterdam, Van der Boechorststraat 9, 1081 Amsterdam, The Netherlands
                [3 ]Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA USA
                [4 ]Institute of Biomedical Research into Human Health and Movement, Manchester Metropolitan University, Manchester, UK
                [5 ]Department of Cell Biology, Emory University School of Medicine, Atlanta, GA USA
                Article
                2279
                10.1007/s00221-010-2279-2
                2880237
                20458472
                877a5933-cefc-4bcf-9fd5-41d8ae278b14
                © The Author(s) 2010
                History
                : 24 December 2009
                : 21 April 2010
                Categories
                Research Article
                Custom metadata
                © Springer-Verlag 2010

                Neurosciences
                plasticity,emg,muscle spindle,locomotion,nerve injury,proprioceptive feedback,muscle length,denervation

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