The sensory origins of human position sense.

KEY POINTS: Position sense at the human forearm can be measured in blindfolded subjects by matching positions of the arms or by a subject pointing to the perceived position of an unseen arm. Effects on position sense tested were: elbow muscle conditioning with a voluntary contraction, muscle vibration, loading the arm and elbow skin stretch. Conditioning contractions and vibration produced errors in a matching task, consistent with the action of muscle spindles as position sensors. Position errors in a pointing task were not consistent with the action of muscle spindles. Loading the arm or skin stretch had no effect in either matching or pointing tasks. It is proposed that there are two kinds of position sense: (i) indicating positions of different body parts relative to one another, using signals from muscle spindles; and (ii) indicating position of the body in extrapersonal space, using signals from exteroceptors, vision, touch and hearing. ABSTRACT: Human limb position sense can be measured in two ways: in a blindfolded matching task, position of one limb is indicated with the other limb. Alternatively, position of a limb, hidden from view, is indicated with a pointer, moved by pressing a lever. These experiments examined the sensory basis of position sense measured in these two ways. Position errors were measured in 14 subjects after elbow flexors or extensors had been conditioned with a half-maximum voluntary contraction. In agreement with previous studies, in the matching trials, position errors were distributed according to a pattern consistent with the action of muscle spindles as the position sensors. In the pointing trials, all errors lay in the direction of extension of the true position of the hidden arm and their distribution was inconsistent with influences arising in muscle spindles. Vibration of elbow muscles produced an illusion of muscle lengthening during a matching task, while during the pointing task no illusion was present. Finally, the matching-pointing error difference was preserved, even when one arm was loaded with a weight or skin over the elbow was stretched. It is proposed that there are two kinds of position sense. One is signalled by muscle spindles, indicating position of one part of the body relative to another. A second provides information about the position of the body in extrapersonal space and here we hypothesise that exteroceptors, including vision, touch and hearing, acting via a central map of the body, provide the spatial information.

Position sense at the human forearm after conditioning elbow muscles with isometric contractions.

These experiments were designed to test the idea that, in a forearm position-matching task, it is the difference in afferent signals coming from the antagonist muscles of the forearm that determines the perceived position of the arm. In one experiment, flexor and then extensor muscles of the reference arm were conditioned by isometric voluntary contractions while the arm was held at the test angle, approximately 45° from the horizontal. At the same time, indicator arm flexor muscles were contracted while the arm was flexed, or extensors were contracted while it was extended. After an indicator flexor contraction, during matching, subjects made large errors in the direction of flexion, by 9.3° relative to the reference arm and after an indicator extensor contraction by 7.4° in the direction of extension. In the second experiment, with reference muscles conditioned as before, slack was introduced in indicator muscles by a combination of muscle contraction and stretch. This was expected to lower levels of afferent activity in indicator muscles. The subsequent matching experiment yielded much smaller errors than before, 1.4° in the direction of flexion. In both experiments, signal levels coming from the reference arm remained the same and what changed was the level of indicator signal. The fact that matching errors were small when slack was introduced in indicator muscles supported the view that the signal coming from reference muscles was also small. It was concluded that the brain is concerned with the signal difference from the antagonist pair of each arm and with the total signal difference between the two arms.

The senses of active and passive forces at the human ankle joint.

The traditional view of the neural basis for the sense of muscle force is that it is generated at least in part within the brain. Recently it has been proposed that force sensations do not arise entirely centrally and that there is a contribution from peripheral receptors within the contracting muscle. Evidence comes from experiments on thumb flexor and elbow flexor muscles. Here we have studied the sense of force in plantar flexor muscles of the human ankle, looking for further evidence for such a mechanism. The active angle-torque curve was measured for muscles of both legs, and for each muscle, ankle angles were identified on the ascending and descending limbs of the curve where active forces were similar. In a plantar flexion force matching task, subjects were asked to match the force in one foot, generated on the ascending limb of the curve, with force in the other foot, generated on the descending limb. It was hypothesised that despite active forces being similar, the sensation generated in the more stretched muscle should be greater because of the contribution from its peripheral stretch receptors, leading to an overestimation of the force in the stretched muscle. It was found that provided that the comparison was between active forces, there was no difference in the forces generated by the two legs, supporting the central hypothesis for the sense of force. When total forces were matched, including a component of passive force due to muscle stretch, subjects seemed to ignore the passive component. Yet subjects had an acute sense of passive force, provided that the muscles remained relaxed. It was concluded that subjects had two senses, a sense of active force, generated centrally, and a sense of passive force, or perhaps muscle stretch, generated within the muscle itself.

Sensing the body in chronic pain: a review of psychophysical studies implicating altered body representation.

There is growing evidence that chronic pain conditions can have an associated central pathology, involving both cortical reorganisation and an incongruence between expected and actual sensory-motor feedback. While such findings are primarily driven by the recent proliferation of neuroimaging studies, the psychophysical tasks that complement those investigations have received little attention. In this review, we discuss the literature that involves the subjective appraisal of body representation in patients with chronic pain. We do so by examining three broad sensory systems that form the foundations of the sense of physical self in patients with common chronic pain disorders: (i) reweighting of proprioceptive information; (ii) altered sensitivity to exteroceptive stimuli; and, (iii) disturbed interoceptive awareness of the state of the body. Such findings present compelling evidence for a multisensory and multimodal approach to therapies for chronic pain disorders.

Limb position sense, proprioceptive drift and muscle thixotropy at the human elbow joint.

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.

The shift in muscle's length-tension relation after exercise attributed to increased series compliance.

Eccentric exercise can produce damage to muscle fibres. Here damage indicators are measured in the medial gastrocnemius muscle of the anaesthetised cat after eccentric contractions on the descending limb of the muscle's length-tension relation, compared with eccentric contractions on the ascending limb and concentric contractions on the descending limb. One damage indicator is a shift of the optimum length for peak active tension, in the direction of longer muscle lengths. The shift has been attributed to an increase in muscle compliance. It is a corollary of a current theory for the mechanism of the damage. With the intention of seeking further support for the theory, in these experiments we test the idea that other damage indicators, specifically the fall in twitch:tetanus ratio and in muscle force are due, in part, to such an increase in compliance. This was tested in an undamaged muscle by insertion of a compliant spring (0.19 mm N(-1)) in series with the muscle. This led to a fall in tetanic tension by 17%, a shift in optimum length of 1.7 mm in the direction of longer muscle lengths and a fall in twitch tetanus ratio by 15%. The fall in tension is postulated to be due to development of non-uniform sarcomere lengths within muscle fibres. It is concluded that after a series of eccentric contractions of a muscle, the fall in force is the result of a number of interdependent factors, not all of which are a direct consequence of the damage process.

Position sense at the human forearm in the horizontal plane during loading and vibration of elbow muscles.

When blindfolded subjects match the position of their forearms in the vertical plane they rely on signals coming from the periphery as well as from the central motor command. The command signal provides a positional cue from the accompanying effort sensation required to hold the arm against gravity. Here we have asked, does a centrally generated effort signal contribute to position sense in the horizontal plane, where gravity cannot play a role? Blindfolded subjects were required to match forearm position for the unloaded arm and when flexors or extensors were bearing 10%, 25% or 40% of maximum loads. Before each match the reference arm was conditioned by contracting elbow muscles while the arm was held flexed or extended. For the unloaded arm conditioning led to a consistent pattern of errors which was attributed to signals from flexor and extensor muscle spindles. When elbow muscles were loaded the errors from conditioning converged, presumably because the spindles had become coactivated through the fusimotor system during the load-bearing contraction. However, this convergence was seen only when subjects supported a static load. When they moved the load differences in errors from conditioning persisted. Muscle vibration during load bearing or moving a load did not alter the distribution of errors. It is concluded that for position sense of an unloaded arm in the horizontal plane the brain relies on signals from muscle spindles. When the arm is loaded, an additional signal of central origin contributes, but only if the load is moved.

Effect of eccentric exercise on position sense at the human forearm in different postures.

This is a study of the ability of blindfolded human subjects to match the position of their forearms before and after eccentric exercise. The hypothesis tested was that the sense of effort contributed to forearm position sense. The fall in force after the exercise was predicted to alter the relationship between effort and force and thereby induce position errors. In the arms-in-front posture, subjects had their unsupported reference arm set to one of two angles from the horizontal, 30 or 60 degrees , and they matched its position by voluntary placement of their other arm. Matching errors were compared with a task where the arms were counterweighted, so could be moved in the vertical plane with minimal effort, and where the arms were moved in the horizontal plane. In these latter two tasks, the intention was to test whether removal of an effort sensation from holding the arm against gravity influenced matching performance. It was found that, although absolute errors for counterweighted and horizontal matching were no larger than for unsupported matching, their standard deviations, 6.1 and 6.8 degrees , respectively, were significantly greater than for unsupported matching (4.6 degrees ), indicating more erratic matching. The eccentric exercise led, the next day, to a fall in maximum voluntary muscle torque of >or=15%. This was accompanied by a significant increase in matching errors for the unsupported matching task from 2.7 +/- 0.5 to 0.8 +/- 0.7 degrees but not for counterweighted (1.4 +/- 0.2 to -0.2 degrees +/- 1.1 degrees ) or horizontal matching (-1.3 +/- 0.7 degrees to -1.8 +/- 0.7 degrees ). This, it is postulated, is because the reduced voluntary torque after exercise was accompanied by a greater effort required to support the arms, leading to larger matching errors. However, effort is only able to provide positional information for unsupported matching where gravity plays a role. In gravity-neutral tasks like counterweighted or horizontal matching, a change in the effort-force relationship after exercise leaves matching accuracy unaffected.

Effect of muscle fatigue on the sense of limb position and movement.

We have recently shown that in an unsupported forearm-matching task blindfolded human subjects are able to achieve an accuracy of 2-3 degrees . If one arm was exercised to produce significant fatigue and the matching task was repeated, it led subjects to make position-matching errors. Here that result is confirmed using fatigue from a simple weight-lifting exercise. A 30% drop in maximum voluntary force after the exercise was accompanied by a significant matching error of 1.7 degrees in the direction of extension when the reference arm had been fatigued, and 1.9 degrees in the direction of flexion when the indicator arm had been fatigued. We also tested the effect of fatigue on a simple movement tracking task where the reference forearm was moved into extension at a range of speeds from 10 to 50 degrees s(-1). Fatigue was found not to significantly reduce the movement-tracking accuracy. In a second experiment, movement tracking was measured while one arm was vibrated. When it was the reference arm, the subject perceived the movement to be significantly faster (3.7 degrees s(-1)) than it actually was. When it was the indicator, it was perceived to be slower (4.6 degrees s(-1)). The data supports the view that muscle spindles are responsible for the sense of movement, and that this sense is not prone to the disturbance from fatigue. By contrast, the sense of position can be disturbed by muscle fatigue. It is postulated, that the sense of effort experienced by holding the arm against the force of gravity is able to provide information about the position in space of the limb and that the increased effort from fatigue produces positional errors.

Muscle spindle signals combine with the sense of effort to indicate limb position.

Experiments were carried out to test the hypothesis that, in the absence of vision, position sense at the human forearm is generated by the combined input from muscle spindles in elbow flexor muscles and signals of central origin giving rise to a sense of effort. In a forearm position-matching task, to remove a possible contribution from the sense of effort, the reference arm was held supported at the test angle. Subjects were less accurate in matching elbow position of the supported forearm than when it was unsupported. Adding a 2 kg weight to the unsupported reference arm led subjects to make matching errors consistent with an increase in the effort signal. Evidence of a contribution from muscle spindles was provided by showing that the direction of position matching errors could be systematically altered by flexion or extension conditioning of the reference arm before its placement at the test angle. Such changes in errors with conditioning could be shown to be present when the reference arm was supported, unsupported, or unsupported and weighted. It is concluded that both peripheral signals from muscle spindles and signals of central origin, associated with the motor command required to maintain arm position against the force of gravity, can provide information about forearm position.

Force matching errors following eccentric exercise.

During eccentric exercise contracting muscles are forcibly lengthened, to act as a brake to control motion of the body. A consequence of eccentric exercise is damage to muscle fibres. It has been reported that following the damage there is disturbance to proprioception, in particular, the senses of force and limb position. Force sense was tested in an isometric force-matching task using the elbow flexor muscles of both arms before and after the muscles in one arm had performed 50 eccentric contractions at a strength of 30% of a maximum voluntary contraction (MVC). The exercise led to an immediate reduction of about 40%, in the force generated during an MVC followed by a slow recovery over the next four days, and to the development of delayed onset muscle soreness (DOMS) lasting about the same time. After the exercise, even though participants believed they were making an accurate match, they made large matching errors, in a direction where the exercised arm developed less force than the unexercised arm. This was true whichever arm was used to generate the reference forces, which were in a range of 5-30% of the reference arm's MVC, with visual feedback of the reference arm's force levels provided to the participant. The errors were correlated with the fall in MVC following the exercise, suggesting that participants were not matching force, but the subjective effort needed to generate the force: the same effort producing less force in a muscle weakened by eccentric exercise. The errors were, however, larger than predicted from the measured reduction in MVC, suggesting that factors other than effort might also be contributing. One factor may be DOMS. To test this idea, force matches were done in the presence of pain, induced in unexercised muscles by injection of hypertonic (5%) saline or by the application of noxious heat to the skin over the muscle. Both procedures led to errors in the same direction as those seen after eccentric exercise.

The influence of fatigue on damage from eccentric contractions in the gastrocnemius muscle of the cat.

Eccentric exercise is unique in that it can lead to muscle damage and soreness. Concentric exercise is not accompanied by evidence of damage. There are reports in the literature that muscle fatigue is a factor determining the amount of damage from eccentric exercise. Our theory for the damage process predicts that susceptibility for damage is independent of fatigue. Experiments were carried out to test this prediction as well as to seek other evidence in support of our theory. Comparisons were made between the effects of eccentric and concentric contractions. The nerve supply to the medial gastrocnemius muscle of the anaesthetized cat was divided into three equal portions in terms of the tension they generated. In the first experiment a muscle portion was fatigued by giving it 200 shortening contractions over 12 mm at a shortening speed of 50 mm s(-1). This led to a mean fall in isometric tension (37 +/- 4%) without a significant shift in the optimum length for peak active tension. Giving the fatigued muscle 10 eccentric contractions, active stretches over 6 mm at 50 mm s(-1), beginning from the muscle's optimum length led to a further fall in tension (11% +/- 7%) and a significant shift in optimum length (3.7 mm +/- 0.6 mm) in the direction of longer muscle lengths. The shift in optimum was taken as an indicator of muscle damage. This shift was not significantly different from that seen after eccentric contractions carried out on an unfatigued muscle. After a series of eccentric or concentric contractions, tension at the end of a ramp shortening of 6 mm at 10 mm s(-1) fell more than isometric tension, and by near equal amounts for the two kinds of contractions. In an unfatigued muscle, if tension was altered by changing the rate of stimulation, the fall in shortening tension was greater than after either concentric or eccentric contractions. These observations were seen to be consistent with predictions of the proposed mechanism for the damage process.

Identifying athletes at risk of hamstring strains and how to protect them.

1. One common soft-tissue injury in sports involving sprinting and kicking a ball is the hamstring strain. Strain injuries often occur while the contracting muscle is lengthened, an eccentric contraction. We have proposed that the microscopic damage to muscle fibres that routinely occurs after a period of unaccustomed eccentric exercise can lead to a more severe strain injury. 2. An indicator of susceptibility for the damage from eccentric exercise is the optimum angle for torque. When this is at a short muscle length, the muscle is more prone to eccentric damage. It is known that subjects most at risk of a hamstring strain have a previous history of hamstring strains. By means of isokinetic dynamometry, we have measured the optimum angle for torque for nine athletes with a history of unilateral hamstring strains. We also measured optimum angles for 18 athletes with no previous history of strain injuries. It was found that mean optimum angle in the previously injured muscles was at a significantly shorter length than for the uninjured muscles of the other leg and for muscles of both legs in the uninjured group. This result suggests that previously injured muscles are more prone to eccentric damage and, therefore, according to our hypothesis, more prone to strain injuries than uninjured muscles. 3. After a period of unaccustomed eccentric exercise, if the exercise is repeated 1 week later, there is much less evidence of damage because the muscle has undergone an adaptation process that protects it against further damage. We propose that for athletes considered at risk of a hamstring strain, as indicated by the optimum angle for torque, a regular programme of mild eccentric exercise should be undertaken. This approach seems to work because evidence from a group of athletes who have implemented such a programme shows a significant reduction in the incidence of hamstring strains.

Human forearm position sense after fatigue of elbow flexor muscles.

After a period of eccentric exercise of elbow flexor muscles of one arm in young, adult human subjects, muscles became fatigued and damaged. Damage indicators were a fall in force, change in resting elbow angle and delayed onset of soreness. After the exercise, subjects were asked to match the forearm angle of one arm, whose position was set by the experimenter, with their other arm. Subjects matched the position of the unsupported reference arm, when this was unexercised, with a significantly more flexed position in their exercised indicator arm. Errors were in the opposite direction when the reference arm was exercised. The size of the errors correlated with the drop in force. Less consistent errors were observed when the reference arm was supported. A similar pattern of errors was seen after concentric exercise, which does not produce muscle damage. The data suggested that subjects were using as a position cue the perceived effort required to maintain a given forearm angle against the force of gravity. The fall in force from fatigue after exercise meant more effort was required to maintain a given position. That led to matching errors between the exercised and unexercised arms. It was concluded that while a role for muscle spindles in kinaesthesia cannot be excluded, detailed information about static limb position can be derived from the effort required to support the limb against the force of gravity.

Low-frequency depression of tension in the cat gastrocnemius muscle after eccentric exercise.

Subjecting a muscle to a series of eccentric contractions in which the contracting muscle is lengthened results in a number of changes in its mechanical properties. These include a fall in isometric tension that is particularly pronounced during low-frequency stimulation, a phenomenon known as low-frequency depression (LFD). Reports of LFD have not taken into account the shift in optimum length for active tension generation to longer muscle lengths that takes place after eccentric contractions. Given the length dependence of the stimulation frequency-tension curve, we tested the hypothesis that the change in this relationship after eccentric exercise is due to the shift in optimum length. We measured LFD by recording tension in response to a linearly increasing rate of stimulation of the nerve to medial gastrocnemius of anesthetized cats, over the range 0-100 pulses per second. Tension responses were measured before and after 50 eccentric contractions consisting of 6-mm stretches starting at 3 mm below optimum length and finishing at 3 mm above it. An index of LFD was derived from the tension responses to ramp stimulation. It was found that LFD after the eccentric contractions was partly, but not entirely, due to changes in the muscle's optimum length. An additional factor was the effect of fatigue. These observations led to the conclusion that the muscle length dependence of LFD was reduced by eccentric contractions. All of this means that after eccentric exercise the tension deficit at low rates of muscle activation is likely to be less severe than first thought.

Responses of muscle spindles following a series of eccentric contractions.

To investigate the effects of eccentric exercise on the signalling properties of muscle spindles, experiments were done using the medial gastrocnemius muscle of cats anaesthetised with 40 mg/kg sodium pentobarbitone, i.p. Responses were recorded from single afferent nerve fibres in filaments of dorsal root during slow stretch of the passive muscle and during intrafusal contractions at a range of lengths, before and after a series of eccentric contractions. The sensitivity to slow stretch was measured as the average firing rate between muscle lengths 10.5 and 9.5 mm shorter than the physiological maximum (Lm), during stretch at 1 mm/s over the whole physiological range. The mean sensitivity of both primary and secondary spindle endings increased slightly, but not significantly, after a series of 20-150 eccentric contractions consisting of a 6 mm stretch, at 50 mm/s, to a final length of between Lm -7 mm and Lm, during stimulation of the whole muscle or sometimes of single fusimotor fibres. Discharges were recorded from primary endings during fusimotor stimulation at 100-150 pulses/s, and from secondary endings during static bag intrafusal contractures produced by i.v. injection of 0.2 mg/kg succinyl choline. Spindle responses were recorded, over a range of muscle lengths, in steps covering the whole physiological range. About half of the responses showed a peak in the relation between length and net increase in firing rate, while the remainder either progressively increased or progressively decreased over the physiological range. No large or consistent changes were seen after the eccentric contractions. It is concluded that the intrafusal fibres of muscle spindles are not prone to damage of the kind seen in extrafusal fibres after a series of eccentric contractions.

Damage to the human quadriceps muscle from eccentric exercise and the training effect.

Nine participants performed two bouts of a step exercise, during which the quadriceps muscle of one leg acted eccentrically. Before and after the exercise, isokinetic torque was measured over a range of knee angles to determine the optimum angle for torque. Immediately after the first bout of exercise, the quadriceps showed a significant (P < 0.05) shift of 15.6 +/- 1.4 degrees (mean +/-sx) of its optimum angle in the direction of longer lengths, suggesting the presence of damage. A drop in peak torque, together with delayed soreness and swelling, confirmed that damage to muscle fibres had occurred. After the second bout of exercise, 8 days later, the shift in optimum angle was 10.4 +/- 1.0 degrees, which was significantly less than after the first bout (P < 0.05). Other indicators of damage were also reduced. In addition, the muscle exhibited a sustained shift in optimum angle (3.4 +/- 0.9 degrees), suggesting that some adaptation had taken place after the first bout of exercise. We conclude that muscles like the quadriceps can show evidence of damage after a specific programme of eccentric exercise, followed by an adaptation response. This is despite the fact that the quadriceps routinely undergoes eccentric contractions in everyday activities.

Effects of local pressure and vibration on muscle pain from eccentric exercise and hypertonic saline.

In human subjects the triceps surae of one leg was exercised eccentrically by asking subjects to walk backwards on an inclined treadmill. Before the exercise controlled local pressure, applied to the muscle with an electromagnet, produced mild soreness, which was reduced when the pressure was combined with vibration. When delayed-onset muscle soreness (DOMS) had set in, 24-48 h after the exercise, vibration increased pain from local pressure. Vibrating at different frequencies suggested 80 Hz as the optimal frequency. During 2-h testing post-exercise, evidence of a change in character of the effects of vibration was first detected at 6 h. It persisted up to 72 h post-exercise. When muscle pain was generated in an unexercised triceps by injection of hypertonic (5%) saline, controlled local pressure applied to the sore area increased pain levels by 32% while pressure plus vibration reduced this to 11%. In a subject with DOMS, local pressure again increased pain from saline by 32% but combining it with vibration increased pain further by an additional 20%. The effect of vibration on DOMS could be abolished with a large nerve fibre block applied to the sciatic nerve. It is concluded that the vibration effects are the result of stimulation of large-diameter mechanoreceptive afferents in the muscle which, it is speculated, play a role in generating DOMS.