Is muscle–tendon unit length a valid indicator for muscle spindle output?

摘要

An important role of feedback from muscle and cutaneous receptors is to regulate the magnitude and timing of muscle activity to satisfy the mechanical demands during locomotion (Rossignol et al. 2006). Such sensory information can be used to modulate the walking system of the central nervous system, but it is also suitable to compensate for acute mechanical perturbations via rapid spinal pathways. The latter is likely to be important during walking on uneven surfaces, preventing the body from getting off balance and in the worst case falling. This hypothesis was tested in a well-designed study by af Klint et al. (2008), who assessed changes in within-step activity of the triceps surae muscles during over-ground walking. In this study, natural variations in ground surface were mimicked with small (i.e. ± 3 deg) slope changes of a robotic platform that was embedded in the walkway. Modulation of proprioceptive feedback as a result of an altered ground was assessed by changes in muscle–tendon unit (MTU) length, Achilles tendon force (ATF) and electromyography. MTU length was calculated using kinematic data of the ankle and knee joints as well as regression equations from the literature. ATF was assessed using a E-shaped buckle transducer externally clamped to the tendon. It was found that stepping on an inclined surface increased triceps surae activity as well as MTU length and ATF. The opposite occurred during steps on a negative slope. These results clearly show acute modulation of neural drive to the muscle. As the slopes were imposed in a random order, these compensatory responses most likely rely on within-step reflex pathways (through proprioceptive and/or cutaneous afferents) in contrast to feed-forward control. This significant finding opens the door for our understanding of which of the reflex pathways might be critical for maintaining stability during walking on uneven terrain. Relating mechanical variables to potential feedback from peripheral afferents is a frequently used approach for studying the neural control of locomotion (specific references can be found in the extensive review of Rossignol et al. 2006). The role of length feedback is typically based on changes in MTU length, assuming constant gamma activation and presynaptic inhibition. Based on our experience with in vivo measurements of MTU and muscle fascicle length changes, we discuss the following question: Is MTU length a valid indicator of muscle spindle output? As the muscle spindles lie in parallel with the extrafusal skeletal muscle fibres, muscle fascicle length changes are more representative of the strains that muscle spindles ‘sense’. In the discussion, af Klint et al. (2008) state: ‘The muscle–tendon length was directly changed by the inclination of the platform and concomitant changes in ATF were recorded. While these estimates are subject to error, the general pattern is most likely present at muscle fibre level.’ However, MTU length changes can be profoundly different from fascicles length changes in triceps sureae muscles, as we have shown in humans (Lichtwark & Wilson, 2006) and cats (Maas et al. 2005). In cats, sonomicrometry has been used to measure muscle fascicle length during overground walking at various slopes. In the early stance phase during walking on a level surface and on a positive slope (25–100%, 14–45 deg), the muscle fascicles of medial gastrocnemius (MG) are consistently shortening while MTU length is increasing. Note that sensory information from this part of the step cycle (close to heel or paw contact) can still be used to alter muscle activity levels within the same step. The general pattern of length changes in MG fascicles and MTU is similar only during walking on a negative slope (−25% and −50%). Such MTU-fascicle similarity was found for all slope conditions in soleus (SO) muscle. Note that this muscle has a different architecture (parallel instead of pinnate, lower tendon-to-fibre length ratio) and crosses only one j