The contribution of muscle spindles to position sense measured with three different methods.

The sense of limb position is important, because it is believed to contribute to our sense of self-awareness. Muscle spindles, including both primary and secondary endings of spindles, are thought to be the principal position sensors. Passive spindles possess a property called thixotropy which allows their sensitivity to be manipulated. Here, thixotropic patterns of position errors have been studied with three commonly used methods of measurement of position sense. The patterns of errors have been used as indicators of the influence exerted by muscle spindles on a measured value of position sense. In two-arm matching, the blindfolded participant indicates the location of one arm by placement of the other. In one-arm pointing, the participant points to the perceived position of their other, hidden arm. In repositioning, one of the blindfolded participant's arms is placed at a chosen angle and they are asked to remember its position and then, after a delay, reproduce the position. The three methods were studied over the full range of elbow angles between 5° (elbow extension) and 125° (elbow flexion). Different outcomes were achieved with each method; in two-arm matching, position errors were symmetrical about zero and thixotropic influences were large, while in one-arm pointing, errors were biased towards extension. In repositioning, thixotropic effects were small. We conclude that each of the methods of measuring position sense comprises different mixes of peripheral and central influences. This will have to be taken into consideration by the clinician diagnosing disturbances in position sense.

Proprioceptive disturbances in weightlessness revisited.

The senses of limb position and movement become degraded in low gravity. One explanation is a gravity-dependent loss of fusimotor activity. In low gravity, position and movement sense accuracy can be recovered if elastic bands are stretched across the joint. Recent studies using instrumented joysticks have confirmed that aiming and tracking accuracy can be recovered in weightlessness by changing viscous and elastic characteristics of the joystick. It has been proposed that the muscle spindle signal, responsible for generating position sense in the mid-range of joint movement, is combined with input from joint receptors near the limits of joint movement to generate a position signal that covers the full working range of the joint. Here it is hypothesised that in low gravity joint receptors become unresponsive because of the loss of forces acting on the joint capsule. This leads to a loss of position and movement sense which can be recovered by imposing elastic forces across the joint.

A reassessment of the role of joint receptors in human position sense.

In the past, the peripheral sense organs responsible for generating human position sense were thought to be the slowly adapting receptors in joints. More recently, our views have changed and the principal position sensor is now believed to be the muscle spindle. Joint receptors have been relegated to the lesser role of acting as limit detectors when movements approach the anatomical limit of a joint. In a recent experiment concerned with position sense at the elbow joint, measured in a pointing task over a range of forearm angles, we have observed falls in position errors as the forearm was moved closer to the limit of extension. We considered the possibility that as the arm approached full extension, a population of joint receptors became engaged and that they were responsible for the changes in position errors. Muscle vibration selectively engages signals of muscle spindles. Vibration of elbow muscles undergoing stretch has been reported to lead to perception of elbow angles beyond the anatomical limit of the joint. The result suggests that spindles, by themselves, cannot signal the limit of joint movement. We hypothesise that over the portion of the elbow angle range where joint receptors become active, their signals are combined with those of spindles to produce a composite that contains joint limit information. As the arm is extended, the growing influence of the joint receptor signal is evidenced by the fall in position errors.

Limb position sense and sensorimotor performance under conditions of weightlessness.

This is a review of the current state of knowledge of the effects of weightlessness on human proprioception. Two aspects have been highlighted: the sense of limb position and performance in sensorimotor tasks. For the sense of position, an important consideration is that there probably exists more than one sense: one measured in a blindfolded, two-limb position matching task, the other, by pointing to the perceived position of a hidden limb. There is evidence that these two senses are supported by distinct central projection pathways. When assessing the effects of weightlessness this must be considered. Whether there is a role for vestibular influences on position sense during changes in gravitational forces is an issue for future experiments. A consideration that has proved helpful for the study of sensorimotor tasks under conditions of weightlessness is to examine the performance of subjects who have lost their proprioceptive senses, either congenitally, or later in life, as a result of disease. In weightlessness, normal subjects appear to have particular difficulties with feedback-controlled tasks. A major factor is the influence of vision on performance. In addition, the stress of working in a weightless environment leads to additional cognitive load, making the execution of even simple everyday tasks difficult.

Secondary endings of muscle spindles: Structure, reflex action, role in motor control and proprioception.

NEW FINDINGS: What is the topic of this review? We describe the structure and function of secondary sensory endings of muscle spindles, their reflex action and role in motor control and proprioception. What advances does it highlight? In most mammalian skeletal muscles, secondary endings of spindles are more or much more numerous than primary endings but are much less well studied. By focusing on secondary endings in this review, we aim to redress the balance, draw attention to what is not known and stimulate future research. ABSTRACT: Kinaesthesia and the control of bodily movement rely heavily on the sensory input from muscle spindles. Hundreds of these sensory structures are embedded in mammalian muscles. Each spindle has one or more sensory endings and its own complement of small muscle fibres that are activated by the CNS via fusimotor neurons, providing efferent control of sensory responses. Exactly how the CNS wields this influence remains the subject of much fascination and debate. There are two types of sensory endings, primary and secondary, with differing development, morphology, distribution and responsiveness. Spindle primary endings have received more attention than secondaries, although the latter usually outnumber them. This review focuses on the secondary endings. Their location within the spindle, their response properties, the projection of their afferents within the CNS and their reflex actions all suggest that secondaries have certain separate roles from the primaries in proprioception and motor control. Specifically, spindle secondaries seem more adapted than primaries to signalling slow and maintained changes in the relative position of bodily segments, thereby contributing to position sense, postural control and static limb positioning. By highlighting, in this way, the roles of secondary endings, a final aim of the review is to broaden understanding of muscle spindles more generally and of the important contributions they make to both sensory and motor mechanisms.

Two senses of human limb position: methods of measurement and roles in proprioception.

The sense of position of the body and its limbs is a proprioceptive sense. Proprioceptors are concerned with monitoring the body's own actions. Position sense is important because it is believed to contribute to our self-awareness. This review discusses recent developments in the debate about the sources of peripheral afferent signals contributing to position sense and describes different methods of measurement of position sense under conditions where vision does not participate. These include pointing to or verbal reporting of the perceived position of a hidden body part, alignment of one body part with the perceived position of another, or using memory-based repositioning tasks. The evidence suggests that there are at least two different mechanisms involved in the generation of position sense, mechanisms using different central processing pathways. The principal sensory receptor responsible for position sense is believed to be the muscle spindle. One criterion for identifying mechanism is whether position sense can be manipulated by controlled changes in spindle discharge rates. Position sense measured in two-limb matching is altered in a predictable way by such changes, while values for pointing and verbal reporting remain unresponsive. It is proposed that in two-limb matching the sensation generated is limb position in postural space. In pointing or verbal reporting, information is provided about limb position in extrapersonal space. Here vision is believed to play a role. The evidence suggests that we are aware, at the same time, of sensations of limb position in postural space as well as in extrapersonal space.

Position sense at the human forearm over a range of elbow angles.

Ten adult participants carried out two experiments on position sense at the forearm, one a two-arm matching task, the other a one-arm pointing task. For matching, both forearms were strapped to paddles which moved in the vertical plane between 0° and 90°. At the start of each trial, the arms were conditioned with a contraction sequence to control for the thixotropic property of muscle and muscle spindles. In the matching task, the blindfolded participant moved their indicator arm from 45° into flexion or extension to match the position of the reference arm placed at one of five test angles, between 5° and 85°. In the pointing task, only the reference arm was strapped to a paddle and conditioned. Participants indicated the position of the arm, hidden by a screen, by moving a pointer paddle or choosing one of a series of trajectory lines drawn on the screen. In matching, where test angles were in the direction of flexion of 45°, errors were small; in the direction of extension larger errors were made, up to 8° into flexion. In pointing trials, except at the most extended position, all errors lay in the direction of extension. It is argued that position sense by matching is concerned with the relative positions of the body and its parts, position sense by pointing gives information about position of the body and limbs in external space.

Exercise, fatigue and proprioception: a retrospective.

This is an account of experiments carried out in my laboratory over more than 20 years, exploring the influence of exercise on human limb position sense. It is known that after intense exercise we are clumsy in the execution of skilled movements. The first question we posed concerned eccentric exercise, where the contracting muscle is forcibly lengthened. Such exercise produces muscle damage, and the damage might extend to the muscle's proprioceptors, the muscle spindles, producing a disturbance of limb position sense. However, provided the exercise was sufficiently severe (20-30% fall in muscle force), comparing eccentric exercise with concentric exercise, where no damage ensues, there was no difference in the effects on position sense. After exercise of elbow muscles, the forearm was always perceived as more extended than its actual position. It led to a new hypothesis: after exercise, did the extra effort required to lift the fatigued arm provide a position signal? Findings based on spindles' thixotropic behaviour did not support such a proposition for the elbow joint, although at the wrist an effort signal may contribute. Spindle thixotropy has also been proposed to explain the poor proprioception experienced under conditions of weightlessness. After exercise of elbow extensors or flexors, the position errors were always in the direction of forearm extension. At the knee, after exercise the lower leg was always perceived as more flexed. These findings led to the conclusion that disturbances to position sense, post-exercise, did not involve peripheral receptors, and that the effect arose within the brain.

The neural basis of the senses of effort, force and heaviness.

Effort, force and heaviness are related terms, having in common that they are all sensations associated with the generation of voluntary muscle contractions. Traditionally they have been thought to originate in the brain, as a result of copies of motor commands relayed to sensory areas. A stumbling block for the central hypothesis has been the lack of proportionality between the fall in muscle force from fatigue or paralysis and the increase in sensation generated while trying to achieve the required force. In recent times growing evidence has accumulated supporting a role for peripheral sensory receptors, in particular the muscle spindles, as contributing to these sensations. The review discusses the evidence for participation of sensory receptors and what this means for proprioception. In particular, it is not straightforward to envisage how muscle spindles might provide a reliable force signal in a contracting muscle, with or without support from the fusimotor system. An important additional consideration is the method of measurement. It has emerged that there is evidence of a task-dependency in the composition of the afferent signals contributing to the sense of force. The evidence suggests that the signal used in a two-arm force matching task is not the same as in a one-arm task. It will be important, in the future, to try and obtain more direct evidence about the afferent origins of the senses of effort, force and heaviness, how they might change from one task to another and what implications this has for motor control.

Kinesthetic Senses.

The kinesthetic senses are the senses of position and movement of the body, senses we are aware of only on introspection. A method used to study kinesthesia is muscle vibration, which engages afferents of muscle spindles to trigger illusions of movement and changed position. When vibrating elbow flexors, it generates sensations of forearm extension, when vibrating extensors, sensations of forearm flexion. Vibrating the elbow joint produces no illusion. Vibrating flexors and extensors together at the same frequency also produces no illusion, because what is perceived is the signal difference between antagonist muscles of each arm and between arms. The size of the illusion depends on how the muscle has been conditioned beforehand, due to a property of muscle called thixotropy. When measuring the illusion, blindfolded subjects may carry out a matching or pointing task. In pointing, signals from muscle spindles are less important than in matching. Afferent signals from kinesthetic receptors project to areas of somatosensory cortex to generate sensations of detection and location. This is referred to the body model, which provides information about size and shape of body parts. Kinesthesia, together with vision and touch, is associated with the sense of body ownership. All three can combine or each, on its own, can generate ownership. Related is the sense of agency, the sense of being responsible for one's own actions. In recent times, much progress has been made using neuroimaging techniques to identify the various areas of the brain likely to be responsible for generating these sensations. © 2017 American Physiological Society. Compr Physiol 8:1157-1183, 2018.

Muscle damage produced by isometric contractions in human elbow flexors.

Isometric exercise is often prescribed during rehabilitation from injury to maintain muscle condition and prevent disuse atrophy. However, such exercise can lead to muscle soreness and damage. Here we investigate which parameters of isometric contractions are responsible for the damage. Bouts of 30 repetitions of maximum voluntary contractions of elbow flexors in 38 subjects were carried out and peak force, soreness, and tenderness were measured before the exercise, immediately afterwards, at 2 h, and at 24 h postexercise. When one arm was held near the optimum angle for force generation (90°), the force it produced was greater by 28% than by the other arm held at a longer length (155°). However, despite the smaller contraction forces of the muscle held at the longer length, after the exercise it exhibited a greater fall in force that persisted out to 24 h (20% fall) and more delayed soreness than the muscle exercised at 90° (7% fall at 24 h). The result indicates a length dependence of the damage process for isometric contractions at maximum effort. In four additional experiments, evidence was provided that the damage occurred during the plateau of the contraction and not the rising or relaxation phases. The damage had a prompt onset and was cumulative, continuing for the duration of the contraction. We interpret our findings in terms of the nonuniform lengthening of sarcomeres during the plateau of the contractions and conclude that muscle damage from isometric exercise is minimized if carried out at lengths below the optimum, using half-maximum or smaller contractions. NEW & NOTEWORTHY Isometric exercise, where muscle contracts while the limb is held fixed, is often possible for individuals rehabilitating from injury and can help maintain muscle condition. Such exercise has been reported to cause some muscle damage and soreness. We confirm this and show that to minimize damage, exercising muscles should be held at shorter than the optimum length for force and carried out at half-maximum effort or less.

Position sense at the human elbow joint measured by arm matching or pointing.

Position sense at the human elbow joint has traditionally been measured in blindfolded subjects using a forearm matching task. Here we compare position errors in a matching task with errors generated when the subject uses a pointer to indicate the position of a hidden arm. Evidence from muscle vibration during forearm matching supports a role for muscle spindles in position sense. We have recently shown using vibration, as well as muscle conditioning, which takes advantage of muscle's thixotropic property, that position errors generated in a forearm pointing task were not consistent with a role by muscle spindles. In the present study we have used a form of muscle conditioning, where elbow muscles are co-contracted at the test angle, to further explore differences in position sense measured by matching and pointing. For fourteen subjects, in a matching task where the reference arm had elbow flexor and extensor muscles contracted at the test angle and the indicator arm had its flexors conditioned at 90°, matching errors lay in the direction of flexion by 6.2°. After the same conditioning of the reference arm and extension conditioning of the indicator at 0°, matching errors lay in the direction of extension (5.7°). These errors were consistent with predictions based on a role by muscle spindles in determining forearm matching outcomes. In the pointing task subjects moved a pointer to align it with the perceived position of the hidden arm. After conditioning of the reference arm as before, pointing errors all lay in a more extended direction than the actual position of the arm by 2.9°-7.3°, a distribution not consistent with a role by muscle spindles. We propose that in pointing muscle spindles do not play the major role in signalling limb position that they do in matching, but that other sources of sensory input should be given consideration, including afferents from skin and joint.

The role of muscle proprioceptors in human limb position sense: a hypothesis.

In this mini-review I have proposed that there are two kinds of position sense, one a sense of the position of one part of the body relative to another, the other a sense of the location in space of our body and its limbs. A common method used to measure position sense is to ask subjects to match with one arm the position adopted by the other. Here all of the evidence points to muscle spindles as the major proprioceptors, with cutaneous receptors acting as proprioceptors providing a supporting role. Other senses such as vision do not play a major role. The sense of localisation in space measured by pointing to the arm, rather than matching its position, I propose, is not served by proprioceptors but by exteroceptors, vision, touch and hearing. Here the afferent input is relayed to sensory areas of the brain, to address the postural schema, a cortical map of the body and limbs, specifying its size and shape. It is here that spatial location is computed. This novel interpretation of position sense as two separate entities has the advantage of proposing new, future experiments and if it is supported by the findings, it will represent an important step forward in our understanding of the central processing of spatial information.

Muscle thixotropy as a tool in the study of proprioception.

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.

The contribution of motor commands to position sense differs between elbow and wrist.

Recent studies have suggested that centrally generated motor commands contribute to the perception of position and movement at the wrist, but not at the elbow. Because the wrist and elbow experiments used different methods, this study was designed to resolve the discrepancy. Two methods were used to test both the elbow and wrist (20 subjects each). For the wrist, subjects sat with their right arm strapped to a device that restricted movement to the wrist. Before each test, voluntary contraction of wrist flexor or extensor muscles controlled for muscle spindle thixotropy. After relaxation, the wrist was moved to a test angle. Position was indicated either with a pointer, or by matching with the contralateral wrist, under two conditions: when the reference wrist was relaxed or when its muscles were contracted isometrically (30% maximum). The elbow experiment used the same design to measure position sense in the passive elbow and with elbow muscles contracting (30% maximum). At the wrist when using a pointer, muscle contraction altered significantly the perceived wrist angle in the direction of contraction by 7 deg [3 deg, 12 deg] (mean [95% confidence interval]) with a flexor contraction and 8 deg [4 deg, 12 deg] with an extensor contraction. Similarly, in the wrist matching task, there was a change of 13 deg [9 deg, 16 deg] with a flexor contraction and 4 deg [1 deg, 8 deg] with an extensor contraction. In contrast, contraction of elbow flexors or extensors did not alter significantly the perceived position of the elbow, compared with rest. The contribution of central commands to position sense differs between the elbow and the wrist.

The senses of force and heaviness at the human elbow joint.

The present-day view of the neural basis for the senses of muscle force and heaviness is that they are generated centrally, within the brain, from copies of motor commands. A corollary of the motor discharge generates a sense of effort which underlies these sensations. In recent experiments on force and heaviness sensations using thumb flexor muscles, a rather different explanation has been invoked: Subjects were proposed to rely predominantly on inputs of a peripheral origin, in particular, the signals of muscle spindles. The present experiments have been carried out at the elbow joint to determine whether these new ideas apply more widely. The effects of fatigue of elbow flexor muscles have been studied in force and heaviness matching tasks using three exercise regimes, a sustained maximum voluntary contraction (MVC), a maintained contraction of 35 % MVC, and a maintained contraction of 35 % MVC combined with muscle vibration at 80 Hz. In force-matching experiments, subjects were required to contract both arms and while the reference arm generated the target force under visual control, it was matched by the indicator arm without visual feedback. During the 100 % MVC exercise, force in the exercising reference arm fell rapidly to almost a half of its original value over 90 s while force in the indicator did not fall, leading to a significant overestimation of the reference force. During the 35 % MVC exercise, subjects also overestimated the reference force and this persisted at 5 and 10 min after the exercise. When 35 % MVC was combined with vibration, the amount by which the indicator arm overestimated the reference force was significantly reduced. In heaviness matching experiments, subjects could move their arms through a small range. The reference arm was loaded with a weight, and weights were added or removed from the indicator until heaviness felt the same in the two arms. There was a small, but significant fall in the matching weight used after 100 % MVC exercise, that is, the weight held by the fatigued arm felt lighter. The 35 % exercise did not alter heaviness sensation while 35 % MVC exercise with vibration led to a significant reduction in perceived heaviness. To conclude, while the results of these experiments on elbow flexors are not as clear cut as for thumb flexors, the central effort hypothesis falls short, in a number of respects in explaining the data which are able to be interpreted in terms of a peripheral afferent contribution to the senses of force and heaviness.

The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force.

This is a review of the proprioceptive senses generated as a result of our own actions. They include the senses of position and movement of our limbs and trunk, the sense of effort, the sense of force, and the sense of heaviness. Receptors involved in proprioception are located in skin, muscles, and joints. Information about limb position and movement is not generated by individual receptors, but by populations of afferents. Afferent signals generated during a movement are processed to code for endpoint position of a limb. The afferent input is referred to a central body map to determine the location of the limbs in space. Experimental phantom limbs, produced by blocking peripheral nerves, have shown that motor areas in the brain are able to generate conscious sensations of limb displacement and movement in the absence of any sensory input. In the normal limb tendon organs and possibly also muscle spindles contribute to the senses of force and heaviness. Exercise can disturb proprioception, and this has implications for musculoskeletal injuries. Proprioceptive senses, particularly of limb position and movement, deteriorate with age and are associated with an increased risk of falls in the elderly. The more recent information available on proprioception has given a better understanding of the mechanisms underlying these senses as well as providing new insight into a range of clinical conditions.

The fall in force after exercise disturbs position sense at the human forearm.

We reported previously that concentric or eccentric exercise can lead to errors in human limb position sense. Our data led us to conclude that the errors, post-exercise, were not due to an altered responsiveness of the proprioceptive afferents, and we proposed that they resulted from central changes in the processing of the afferent input. However, it remained uncertain what was responsible for triggering those changes, the volume of afferent traffic during the exercise or the developing fatigue. The afferent traffic hypothesis was tested by subjects carrying out a series of 250 lightly loaded concentric contractions of elbow flexors that produced little fatigue (6 %). This did not lead to significant position errors. In a second experiment, a series of fatiguing isometric contractions, which kept movements of the muscle to a minimum, led to a 24 % fall in force and significant position errors (3°, direction of extension). In the third experiment, at 24 h after eccentric exercise, when the short-term effects of fatigue and accumulated metabolites were gone, but force was still 28 % below control values, this was accompanied by significant position errors in the direction of extension, 3.2° in the relaxed arm and 3.3° in the self-supported arm. It is concluded that it is the fall in force accompanying exercise which is responsible for disturbing limb position sense. It is suggested that the exercise effects are generated in the brain, perhaps as a result of an alteration of the body map, triggered by the fall in force.