History-dependence of muscle slack length following contraction and stretch in the human vastus lateralis.

KEY POINTS: In reduced muscle preparations, the slack length and passive stiffness of muscle fibres have been shown to be influenced by previous muscle contraction or stretch. In human muscles, such behaviours have been inferred from measures of muscle force, joint stiffness and reflex magnitudes and latencies. Using ultrasound imaging, we directly observed that isometric contraction of the vastus lateralis muscle at short lengths reduces the slack lengths of the muscle-tendon unit and muscle fascicles. The effect is apparent 60 s after the contraction. These observations imply that muscle contraction at short lengths causes the formation of bonds which reduce the effective length of structures that generate passive tension in muscles. ABSTRACT: In reduced muscle preparations, stretch and muscle contraction change the properties of relaxed muscle fibres. In humans, effects of stretch and contraction on properties of relaxed muscles have been inferred from measurements of time taken to develop force, joint stiffness and reflex latencies. The current study used ultrasound imaging to directly observe the effects of stretch and contraction on muscle-tendon slack length and fascicle slack length of the human vastus lateralis muscle in vivo. The muscle was conditioned by (a) strong isometric contractions at long muscle-tendon lengths, (b) strong isometric contractions at short muscle-tendon lengths, (c) weak isometric contractions at long muscle-tendon lengths and (d) slow stretches. One minute after conditioning, ultrasound images were acquired from the relaxed muscle as it was slowly lengthened through its physiological range. The ultrasound image sequences were used to identify muscle-tendon slack angles and fascicle slack lengths. Contraction at short muscle-tendon lengths caused a mean 13.5 degree (95% CI 11.8-15.0 degree) shift in the muscle-tendon slack angle towards shorter muscle-tendon lengths, and a mean 5 mm (95% CI 2-8 mm) reduction in fascicle slack length, compared to the other conditions. A supplementary experiment showed the effect could be demonstrated if the muscle was conditioned by contraction at short lengths but not if the relaxed muscle was held at short lengths, confirming the role of muscle contraction. These observations imply that muscle contraction at short lengths causes the formation of bonds which reduce the effective length of structures that generate passive tension in muscles.

Anaesthesia changes perceived finger width but not finger length.

The brain needs information about the size of the body to control our interactions with the environment. No receptor signals this information directly; the brain must determine body size from multiple sensory inputs and then store this information. This process is poorly understood, but somatosensory information is thought to play a role. In particular, anaesthetising a body part has been reported to make it feel bigger. Here, we report the first study to measure whether changes in body size following anaesthesia are uniform across dimensions (e.g. width and length). We blocked the digital nerves of ten human subjects with a clinical dose of local anaesthetic (1 % lignocaine) and again in separate sessions with a weaker dose (0.25 % lignocaine) and a saline control. Subjects reported the perceived size of their index finger by selecting templates from a set that varied in size and aspect ratio. We also measured changes in sensory signals that might contribute to the anaesthetic-induced changes using quantitative sensory testing. Subjects perceived their finger to be up to 32 % wider during anaesthesia when compared to during a saline control condition. However, changes in perceived length of the finger were much smaller (<5 %). Previous studies have shown a change in perceived body size with anaesthesia, but have assumed that the aspect ratio is preserved. Our data show that this is not the case. We suggest that nonuniform changes in perceived body size might be due to the brain increasing the body's perimeter to protect it from further injury.

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.

Is this my finger? Proprioceptive illusions of body ownership and representation.

Body 'ownership' defines which things belong to us and can be manipulated by signals from cutaneous or muscle receptors. Whether signals from muscle proprioceptors on their own influence perceived ownership is unknown. We used finger-joint movement to induce illusory ownership of an artificial finger without vision. We coupled the subject's index finger to an artificial finger 12 cm above it. The experimenter held the subject's other index finger and thumb on the artificial finger and passively moved them congruently or incongruently for 3 min with the index finger and the grasping index finger and thumb intact or anaesthetised. When intact, congruent movement (19 subjects) reduced perceived vertical distance between index fingers to 1.0 (0.0, 2.0) cm [median (IQR)] from 3.0 (3.0, 4.0) cm with incongruent movement (P < 0.01). Simply grasping the artificial finger reduced perceived spacing between the grasping and test index fingers from 6.0 (5.0, 9.0) cm to 3.0 (3.0, 6.0) cm (P < 0.01), a new grasp illusion. Digital anaesthesia eliminated this grasp effect, after which congruent movement still reduced the perceived spacing between the index fingers to 1.0 (0.0, 2.75) cm compared to 4.0 (3.25, 6.0) cm with incongruent movement (P < 0.001). Subjects more strongly agreed that they were holding their own finger after congruent but not incongruent movement (P < 0.01). We propose that the brain generates possible scenarios and tests them against available sensory information. This process can function without vision or motor commands, and with only one channel of somatic information.

Tongue acceleration in humans evoked with intramuscular electrical stimulation of genioglossus.

Genioglossus was stimulated intramuscularly to determine the effect of regional activation of the muscle on tongue movement in eight healthy adults. Stimulation at motor threshold was delivered with a needle electrode inserted to different depths in the anterior and posterior regions of genioglossus. The current amplitude that induced muscle contraction was ∼80% higher for anterior than posterior sites. Evoked tongue movements were determined from stimulus-triggered averages (150 pulses) of the outputs from an accelerometer fixed to the posterosuperior surface of the tongue. The median amplitude [95% confidence intervals] for the resultant acceleration was 0.0 m/s2 [0.0, 0.2] for anterior and 0.6 m/s2 [0.1, 2.8] for posterior sites. There was a positive relationship between acceleration amplitude and stimulation depth in the posterior of genioglossus (p < 0.001), but acceleration amplitude did not vary with stimulation depth in the anterior region (p = 0.83). This heterogeneity in acceleration responses between muscle regions may contribute to differences in collapsibility of the upper airway.

Overestimation of force during matching of externally generated forces.

If a weight is applied to a finger and the subject asked to produce the same force, the subject generates a force larger than the weight. That is, subjects overestimate the force applied by an external target when matching it. Details of this force overestimation are not well understood. We show that subjects overestimate small target weights, but not larger ones. Furthermore we show for the first time that the force overestimation consists of two components. The first component is a constant. The second component depends on the precise magnitude of the weight and is only present when subjects hold the target weight against gravity. We suggest that the two components are generated in different phases of the force-matching task, are due to different processes, and must have an influence on all proprioceptive judgements of force.

Proprioceptive signals contribute to the sense of body ownership.

The sense of body ownership, knowledge that parts of our body 'belong' to us, is presumably developed using sensory information. Cutaneous signals seem ideal for this and can modify the sense of ownership. For example, an illusion of ownership over an artificial rubber hand can be induced by synchronously stroking both the subject's hidden hand and a visible artificial hand. Like cutaneous signals, proprioceptive signals (e.g. frommuscle receptors) exclusively signal events occurring in the body, but the influence of proprioceptors on the sense of body ownership is not known. We developed a technique to generate an illusion of ownership over an artificial plastic finger, using movement at the proximal interphalangeal joint as the stimulus. We then examined this illusion in 20 subjects when their index finger was intact and when the cutaneous and joint afferents from the finger had been blocked by local anaesthesia of the digital nerves. Subjects still experienced an illusion of ownership, induced by movement, over the plastic finger when the digital nerves were blocked. This shows that local cutaneous signals are not essential for the illusion and that inputs arising proximally, presumably from receptors in muscles which move the finger, can influence the sense of body ownership. Contrary to other studies, we found no evidence that voluntary movements induce stronger illusions of body ownership than those induced by passive movement. It seems that the congruence of sensory stimuli ismore important to establish body ownership than the presence of multiple sensory signals.

Illusory movements of a phantom hand grade with the duration and magnitude of motor commands.

The senses of limb movement and position are critical for accurate control of movement. Recent studies show that central signals of motor command contribute to the sense of limb position but it is not clear whether such signals influence the distinctly different sense of limb movement. Nine subjects participated in two experiments in which we inflated a cuff around their upper arm to produce an ischaemic block, paralysing and anaesthetising the forearm, wrist and hand. This produces an experimental phantom wrist and hand. With their arm hidden from view subjects were asked to make voluntary efforts with their blocked wrist. In the first experiment, efforts were 20 and 40% of maximum and were 2 and 4 s in duration. The second experiment used 1 and 5 s efforts of 5 and 50% of maximum. Subjects signalled perceived movements of their phantom wrist using a pointer. All subjects reported clear perceptions of movement of their phantom hand for all levels and durations of effort. On average, subjects perceived their phantom wrist to move between 16.4 +/- 3.3 deg (mean +/- 95% confidence interval (CI)) and 30.2 +/- 5.4 deg in the first experiment and between 10.3 +/- 3.5 and 38.6 +/- 6.7 deg in the second. The velocity of the movements and total displacement of the phantom graded with the level of effort, and the total displacement also graded with duration. Hence, we have shown that motor command signals have a novel proprioceptive role in the perception of movement of human joints.

Respiratory muscle activity in voluntary breathing tracking tasks: Implications for the assessment of respiratory motor control.

How the involuntary (bulbospinal) and voluntary (corticospinal) pathways interact in respiratory muscle control is not established. To determine the role of excitatory corticobulbar pathways in humans, studies typically compare electromyographic activity (EMG) or evoked responses in respiratory muscles during hypercapnic and voluntary tasks. Although ventilation is matched between tasks by having participants track signals of ventilation, these tasks may not result in matched respiratory muscle activity. The aim of this study was to describe respiratory muscle activity and ribcage and abdominal excursions during two different voluntary conditions, compared to hypercapnic hyperventilation. Ventilation was matched in the voluntary conditions via (i) a simple target of lung volume ('volume tracking') or (ii) targets of both ribcage and abdominal excursions, adjusted to end-expiratory lung volume in hypercapnic hyperventilation ('bands tracking'). Compared to hypercapnic hyperventilation, respiratory parameters such as tidal volume were similar, but the ratio of ribcage to abdominal excursion was higher for both voluntary tasks. Inspiratory scalene and parasternal intercostal muscle activity was higher in volume tracking, but diaphragm and abdominal muscle activity showed little to no change. There were no differences in muscle activity in bands tracking for any muscle, compared to hypercapnic hyperventilation. An elevated ratio of ribcage to abdominal excursion in the bands tracking task indicates that participants could not accurately match the targets in this condition. Inspiratory muscle activity is altered in some muscles in some voluntary tasks, compared to hypercapnia. Therefore, differences in muscle activity should be considered in interpretation of studies that use these protocols to investigate respiratory muscle control.

High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles.

Control of posture and movement requires control of the output from motoneurons. Motoneurons of human lower limb muscles exhibit sustained, submaximal activity to high-frequency electrical trains, which has been hypothesized to be partly triggered by monosynaptic Ia afferents. The possibility to trigger such behavior in upper limb motoneurons and the potential unique role of Ia afferents to trigger such behavior remain unclear. Subjects (n = 9) received high-frequency trains of electrical stimuli over biceps brachii and flexor pollicis longus (FPL). We chose to study the FPL muscle because it has weak monosynaptic Ia afferent connectivity and it is involved in fine motor control of the thumb. Two types of stimulus trains (100-Hz bursts and triangular ramps) were tested at five intensities below painful levels. All subjects exhibited enhanced torque in biceps and FPL muscles after both types of high-frequency train. Torques also persisted after stimulation, particularly for the highest stimulus intensity. To separate the evoked torques that resulted from a peripheral mechanism (e.g., muscle potentiation) and that which resulted from a central origin, we studied FPL responses to high-frequency trains after complete combined nerve blocks of the median and radial nerves (n = 2). During the blocks, high-frequency trains over the FPL did not yield torque enhancements or persisting torques. These results suggest that enhanced contractions of central origin can be elicited in motoneurons innervating the upper limb, despite weak monosynaptic Ia connections for FPL. Their presence in a recently evolved human muscle (FPL) indicates that these enhanced contractions may have a broad role in controlling tonic postural outputs of hand muscles and that they may be available even for fine motor activities involving the thumb.

Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation.

Neuromuscular electrical stimulation (NMES) generates contractions by activation of motor axons (peripheral mechanism), but the afferent volley also contributes by recruiting spinal motoneurons synaptically (central mechanism), which recruits motoneurons according to Henneman's size principle. Thus, we hypothesized that contractions that develop due to a combination of peripheral and central mechanisms will fatigue less rapidly than when electrically evoked contractions are generated by the activation of motor axons alone. Plantar-flexion torque evoked by NMES over the triceps surae was compared in five able-bodied subjects before (Intact) and during (Blocked) a complete anesthetic block of the tibial and common peroneal nerves. In the Blocked condition, plantar-flexion torque could only develop from the direct activation of motor axons beneath the stimulating electrodes. NMES was delivered using three protocols: protocol A, constant 100 Hz for 30 s; protocol B, four 2-s bursts of 100 Hz alternating with 20-Hz stimulation; and protocol C, alternating 100 Hz bursts (1 s on, 1 s off) for 30 s. The percent change in evoked plantar flexion torque from the beginning to the end of the stimulation differed (P < 0.05) between Intact and Blocked conditions for all protocols (Intact: protocol A = +125%, B = +230%, C = +78%; Blocked: protocol A = -79%, B = -15%, C = -35%). These results corroborate previous evidence that NMES can evoke contractions via the recruitment of spinal motoneurons in addition to the direct recruitment of motor axons. We now show that NMES delivered for periods of up to 30 s generates plantar-flexion torque which decreases when only motor axons are recruited and increases when the central nervous system can contribute.

The combined effect of muscle contraction history and motor commands on human position sense.

Along with afferent information, centrally generated motor command signals may play a role in joint position sense. Isometric muscle contractions can produce a perception of joint displacement in the same direction as the joint would move if unrestrained. Contradictory findings of perceived joint displacement in the opposite direction have been reported. As this only occurs if muscle spindle discharge in the contracting muscle is initially low, it may reflect increased muscle spindle firing from fusimotor activation, rather than central motor command signals. Methodological differences including the muscle contraction task and use of muscle conditioning could underlie the opposing findings. Hence, we tested perceived joint position during two contraction tasks ('hold force' and 'hold position') at the same joint (wrist) and controlled muscle spindle discharge with thixotropic muscle conditioning. We expected that prior conditioning of the contracting muscle would eliminate any effect of increased fusimotor activation, but not of central motor commands. Muscle conditioning altered perceived wrist position as expected. Further, during muscle contractions, subjects reported wrist positions displaced ~12 degrees in the direction of contraction, despite no change in wrist position. This was similar for 'hold force' and 'hold position' tasks and occurred despite prior conditioning of the agonist muscle. However, conditioning of the antagonist muscle did reduce the effect of voluntary contraction on position sense. The errors in position sense cannot be explained by fusimotor activation. We propose that central signals combine with afferent signals to determine limb position and that multiple sources of information are weighted according to their reliability.

Proprioceptive measurements of perceived hand position using pointing and verbal localisation tasks.

Previous studies revealed that healthy individuals consistently misjudge the size and shape of their hidden hand during a localisation task. Specifically, they overestimate the width of their hand and underestimate the length of their fingers. This would also imply that the same individuals misjudge the actual location of at least some parts of their hand during the task. Therefore, the primary aim of the current study was to determine whether healthy individuals could accurately locate the actual position of their hand when hidden from view, and whether accuracy depends on the type of localisation task used, the orientation of the hidden hand, and whether the left or right hand is tested. Sixteen healthy right-handed participants performed a hand localisation task that involved both pointing to and verbally indicating the perceived position of landmarks on their hidden hand. Hand position was consistently misjudged as closer to the wrist (proximal bias) and, to a lesser extent, away from the thumb (ulnar bias). The magnitude of these biases depended on the localisation task (pointing vs. verbal), the orientation of the hand (straight vs. rotated), and the hand tested (left vs. right). Furthermore, the proximal location bias increased in size as the duration of the experiment increased, while the magnitude of ulnar bias remained stable through the experiment. Finally, the resultant maps of perceived hand location appear to replicate the previously reported overestimation of hand width and underestimation of finger length. Once again, the magnitude of these distortions is dependent on the task, orientation, and hand tested. These findings underscore the need to control and standardise each component of the hand localisation task in future studies.

The upper limb Physiological Profile Assessment: Description, reliability, normative values and criterion validity.

A progressive decline in upper limb function is associated with ageing and disease. In this cross-sectional study we assessed the performance of 367 healthy individuals aged of 20 to 95 years across a battery of upper limb clinical tests, which we have termed the upper limb Physiological Profile Assessment (PPA). The upper limb PPA was designed to quantify the performance of the multiple physiological domains important for adequate function in the upper extremities. Included are tests of muscle strength, unilateral movement and dexterity, position sense, skin sensation, bimanual coordination, arm stability, along with a functional task. We report age and gender normative values for each test. Test-retest reliability ranged from good to excellent in all tests (intra-class correlation coefficients from 0.65 to 0.98) with the exception of position sense (0.31). Ten of the thirteen tests revealed differences in performance between males and females, twelve showed a decline in performance with increasing age, and eight discriminated between older people with and without upper limb functional impairment. Furthermore, most tests showed good external validity with respect to age, an upper limb functional test and self-reported function. This profiling approach provides a reference range for clinical groups with upper limb sensory and motor impairments and may assist in identifying undiagnosed deficits in the general population. Furthermore, the tests are sufficiently reliable to detect motor impairments in people with compromised upper limb function and evaluate the effectiveness of interventions.

New display of the timing and firing frequency of single motor units.

The neural control of important rhythmical processes such as breathing and locomotion is complex. It is often necessary to depict the activity of motor (or other) units throughout the cycles. We describe and illustrate a novel method that displays visually seven key variables in a single figure related to the timing and frequencies of the discharge of single motor units. This time-and-frequency plot (TAFPLOT) displays the recruitment time, time of peak discharge frequency and derecruitment time, as well as the onset, peak, and final firing frequencies of each motor unit in a population. The frequency of any tonic firing is also displayed. Using the TAFPLOT it is easy to identify the presence or absence of coordinated activity within and between different motoneuron pools. The method is used to illustrate novel differences in the discharge behavior between populations of single motor units innervating the human diaphragm and genioglossus muscles. This new display provides a simple, qualitative and quantitative tool to study the neural control of rhythmical or repetitive motor tasks.

Warm-up stretches reduce sensations of stiffness and soreness after eccentric exercise.

PURPOSE: A commonly used method for warm-up before exercise is to stretch muscles. How this benefits performance remains uncertain. After a period of eccentric exercise, there is muscle damage accompanied by an increase in passive tension, perceived as a sensation of increased stiffness in the exercised muscles. We have tested the idea that warm-up stretches might reduce levels of passive tension to reduce sensations of stiffness and soreness after eccentric exercise. METHODS: Subjects eccentrically exercised elbow flexors of one arm on an isokinetic dynamometer. The other arm acted as a control. After the exercise, measurements were made of resting elbow angle, as an indication of passive tension levels, before and after one or five large, passive arm extensions. Additional measurements made at 24 h included soreness levels in response to muscle stretch or vibration. RESULTS: After the exercise, the relaxed elbow adopted a more flexed posture than normal, an effect that slowly subsided over the next 4 d. Five rapid arm extensions returned arm posture back to near control levels. The flexed posture then gradually re-developed over the next hour. At 24 h postexercise, extending the arm produced some soreness as did muscle vibration. The pain from arm extension and vibration was reduced after a series of arm extensions. CONCLUSIONS: The flexed posture at the elbow is due to an increase in passive tension in elbow flexors as a result of muscle damage from the eccentric exercise. Stretch reduces passive tension. Benefits from the lower tension are reduced sensations of stiffness and soreness. This represents a new proposal for the mechanism for passive stretches as a warm-up strategy.