When a muscle relaxes after a contraction, cross-bridges between actin and myosin in sarcomeres detach, but about 1% spontaneously form new, non-force-generating attachments. These bridges give muscle its thixotropic property. They remain in place for long periods if the muscle is left undisturbed and give the muscle a passive stiffness in response to a stretch. They are detached by stretch, but reform at the new length. If the muscle is then shortened, the presence of these bridges prevents muscle fibres from shortening and they fall slack. So, resting muscle can be in one of two states, where it presents in response to a stretch with a high stiffness, if no slack is present, or with a compliant response in the presence of slack. Intrafusal fibres of muscle spindles show thixotropic behaviour. For spindles, after a conditioning contraction, they are left stretch sensitive, with a high level of background discharge. Alternatively, if after the contraction the muscle is shortened, intrafusal fibres fall slack, leaving spindles with a low level of background activity and insensitivity to stretch. Muscle spindles are receptors involved in the senses of human limb position and movement. The technique of muscle conditioning can be used to help understand the contribution of muscle spindles to these senses and how the brain interprets signals arising in spindles. When, in a two-arm position-matching task, elbow muscles of the two arms are deliberately conditioned in opposite ways, the blindfolded subject makes large position errors of which they are unaware. The evidence suggests that the brain is concerned with the difference signal coming from the antagonists acting at the elbow and with the overall difference in signal from the two arms. Another way of measuring position sense is to use a single arm and indicate its perceived position with a pointer. Here, there is no access to a signal from the other limb, and position sense relies on referral to a central map of the body, the postural schema.
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Key pointsr When a blindfolded subject holds his or her arm at a particular angle, its reported position shifts over time; this is known as proprioceptive drift.r Here, we show that in relation to position sense at the elbow, the direction of perceived shifts is consistent with adaptation in discharge levels of sensory receptors in elbow muscles.r Raising or lowering receptor discharge levels by similar amounts in opposing muscles at the elbow using muscle conditioning abolishes proprioceptive drift, but large position errors may result.r The present experiments provide an explanation for proprioceptive drift and indicate that, in a forearm position-matching task, the brain is not concerned with actual discharge levels from arm muscles, but with their difference.Abstract These experiments on the human forearm are based on the hypothesis that drift in the perceived position of a limb over time can be explained by receptor adaptation. Limb position sense was measured in 39 blindfolded subjects using a forearm-matching task. A property of muscle, its thixotropy, a contraction history-dependent passive stiffness, was exploited to place muscle receptors of elbow muscles in a defined state. After the arm had been held flexed and elbow flexors contracted, we observed time-dependent changes in the perceived position of the reference arm by an average of 2.8°in the direction of elbow flexion over 30 s (Experiment 1). The direction of the drift reversed after the arm had been extended and elbow extensors contracted, with a mean shift of 3.5°over 30 s in the direction of elbow extension (Experiment 2). The time-dependent changes could be abolished by conditioning elbow flexors and extensors in the reference arm at the test angle, although this led to large position errors during matching (±10°), depending on how the indicator arm had been conditioned (Experiments 3 and 4). When slack was introduced in the elbow muscles of both arms, by shortening muscles after the conditioning contraction, matching errors became small and there was no drift in position sense (Experiments 5 and 6). These experiments argue for a receptor-based mechanism for proprioceptive drift and suggest that to align the two forearms, the brain monitors the difference between the afferent signals from the two arms.
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