The effect of agonist/antagonist muscle vibration on human position sense

Summary During voluntary movement, muscle spindles of both the agonist and antagonist muscles potentially can supply information about position of the limb. Muscle vibration is known to increase muscle spindle discharge and cause systematic distortions of limb position sense in humans. The following two experiments attempted to examine these contributions by separately vibrating over the triceps and biceps muscles during forearm positioning. In the first experiment, subjects performed a horizontal flexion or extension of the right arm to a mechanical stop randomly positioned at 20, 40 or 60°. Vision was occluded and vibration was applied to the right arm. The perceived position of the right limb was assessed by instructing subjects to simultaneously match the right arm position with the left limb. Vibration of the shortening, agonist muscle had no effect on limb matching accuracy. However, antagonist muscle vibration resulted in a significant overestimation of the vibrated limb position by 6–13°. The procedures for the second experiment were similar to the first, except that movements of the right limb were self-terminated and only flexion movements were performed. A screen was mounted over the arms and subjects were instructed to move the right arm until it was positioned beneath a marker on the screen. Vibration of the shortening agonist muscle had no effect on either the positioning accuracy of the right limb or matching accuracy of the left limb. However, antagonist muscle vibration resulted in significantly shorter movements (6–10°) by the right limb and an overestimation of right limb position by the left, matching limb. These findings support the hypothesis that muscle spindle afferent information from the lengthening antagonist muscle contributes to limb position sense during voluntary movement.     

Vibration-induced changes in movement-related EMG activity in humans

The effect of muscle tendon vibration during voluntary arm movement was studied in normal humans. Subjects made alternating step flexion and extension movements about the elbow. A small vibrator was mounted over either the biceps or the triceps muscle and vibration was applied during flexion or extension movements. The vibrator was turned off between movements. After a period of practice, subjects learned the required movements and were able to make them with their eyes closed. Application of vibration to the muscle antagonist to the movement being performed produced an undershoot of the required end-movement position. The undershoot was 20-30% of the total movement amplitude. In contrast, vibration of the muscle agonist to the movement resulted in no change in movement end position. The vibration-induced undershoot was associated with an increase in the EMG activity of the vibrated (antagonist) muscle and a resultant increase in the ratio of the antagonist to agonist EMG activity. The increase in antagonist EMG produced by the vibration occurred with a latency of approximately 60 ms from vibration onset. The observed results are consistent with vibration-induced activation of muscle spindle receptors in the lengthening muscle during movement. It is suggested that, during movement, the sensitivity of the spindle receptors in the shortening muscle is decreased and the information concerning limb position during movement comes primarily from the lengthening muscle.     

The effects of wrist muscle vibration on human voluntary elbow flexion-extension movements

Summary The effect of forearm muscle tendon vibration during alternating step flexion-extension movements about the elbow was studied in normal humans. In one experiment, a vibrator was mounted over either the forearm flexor or the extensor muscle. In a second experiment, a vibrator was mounted over either the forearm muscle or the biceps muscle. In both experiments, vibration was applied either to a single muscle or simultaneously to both muscles during elbow flexion-extension movements. After a period of practice, subjects learned the required movements and were able to make them with their eyes closed. Application of vibration to the forearm and the biceps muscle during extension movements produced an undershoot of the required end movement position. Moreover, application of high frequency vibration (100 Hz) to the forearm extensor and flexor muscle produced an overshoot of the required end-movement position. The observed results are consistent with vibration induced activation of muscle spindle receptors not only in the lengthening muscle during movement but also in the forearm muscles. It is suggested that the pattern of distribution of muscle spindle afferent from the forearm muscle onto -motoneurons of muscles acting at the elbow has played an important role of alternating step flexion-extension movements.     

Effect of quadriceps contraction on upper limb position sense errors in humans

Short-length muscle contraction (hold-short conditioning) causes limb position sense errors after the muscle returns to its intermediate length; this is due to intrafusal muscle thixotropy, which raises the muscle spindle sensitivity. In humans, contraction of muscles in the upper body (referred to as the Jendrassik manoeuvre) reinforces tendon reflexes in the lower limbs. However, it is unclear whether such a reinforcement manoeuvre enhances thixotropic position sense errors. We studied the effect of quadriceps contraction on upper limb position sense errors induced by hold-short conditioning of the biceps in 12 healthy men. Quadriceps contraction increased the tonic vibration reflex of the biceps, suggesting that quadriceps contraction has a reinforcing effect similar to that of the Jendrassik manoeuvre. After hold-short conditioning of the right biceps, subjects perceived that the conditioned forearm was placed in a more extended position than it actually was. Such position sense errors were enhanced during quadriceps contraction and the degree of error was increased with the intensity of the quadriceps contraction. These results suggest that limb position sense is affected by remote muscle contraction.     

The effects of muscle vibration on the attainment of intended final position during voluntary human arm movements

Summary Muscle tendon vibration was applied during voluntary step-tracking arm target-movements performed by normal human subjects. Vibration (freq. = 120 Hz) was applied over either the biceps or triceps tendons. During non-visually guided (eyes closed) trials, vibration of the muscle antagonistic to the movement being performed resulted in an undershoot of the required target. Thus, biceps vibration produced an undershoot of the extension target and triceps vibration an undershoot of the flexion target. The same effect occurred if the vibration was applied continuously over several movements or only during the course of individual movements. In contrast, vibration of the muscle acting as the prime mover had no effect on the correct attainment of the required target. It is suggested that the central nervous system may monitor muscle afferent activity of the lengthening (antagonist) muscle during simple, step movements.Supported by the Medical Research Council of Canada, Grant MA-6699     

The attainment of target position during step-tracking movements despite a shift of initial position

Summary Subjects performed a step-tracking forearm movement at maximum velocity without visual guidance. A considerable shift of initial forearm position, which remained unnoticed by the subject, was induced by vibration of the biceps tendon. Notwithstanding the shift of initial position subjects attained the correct final position, irrespective of whether the vibration was switched off before the movement or continued during the movement. Recordings of biceps and triceps electromyograms show that muscle activities were programmed to produce a movement from the actual initial position to the target position. The findings indicate that correct information on forearm position is available to the central nervous system at a subconscious level even if position perception is disturbed through vibration.     

Activity patterns of upper arm muscles in relation to direction of rapid wrist movement in man

Summary Adjustment of arm posture associated with rapid wrist movements was studied by EMG analysis. Seven healthy adults, seated and holding their right arm with the shoulder in a neutral position with the elbow in 90° flexion and the wrist position neutral, were instructted to flex or extend the wrist as fast as possible. To examine whether the activity patterns of the upper arm muscles were related to the prime mover or the direction of the movement in space, the forearm was in two postures, supinate and pronate. The surface EMGs of biceps brachii, brachialis, triceps brachii and the prime movers were recorded along with the angular displacement of the wrist. The sequences of the upper arm muscle activities changed in relation to the direction of the movement. The earliest activities of the upper arm muscles were considered to counteract the dynamic perturbation induced by the rapid wrist movement. The onsets of the earliest activity of the upper arm muscles preceded the movement onset by 50–60 ms. These results revealed that the activity patterns of the arm muscles associated with the rapid wrist movements were functionally compatible with the anticipatory postural adjustment and were controlled according to the direction of the movement in space.     

Effects of tendon vibration on the spatiotemporal characteristics of human locomotion

The present study addressed the involvement of proprioceptive input of the muscle spindles in the spatiotemporal control of human locomotion. Blindfolded subjects walked along a walkway while tendon vibration, a powerful stimulus of Ia afferents, was applied to various muscles of the lower limb. The effects of tendon vibration were measured on joint kinematics and on intralimb and interlimb coordination. Tendon vibration of the tibialis anterior during locomotion led to a decreased plantar flexion at toe-off, whereas vibration of the triceps surae led to a decreased dorsiflexion during swing. Vibration of the quadriceps femoris at the knee led to a decreased knee flexion during swing. These local effects of vibration can be explained in the light of a lengthening illusion of the vibrated muscle in that phase of the gait cycle where the muscle is lengthened. Tendon vibration did not affect the qualitative features of intralimb coordination. With respect to interlimb coordination, only vibration of the biceps femoris showed a significant increase in phase lead of the vibrated limb. The present results suggest the involvement of Ia afferent input in the online control of joint rotations. Additionally it is hypothesized that the proprioceptive input of biceps femoris might be involved in the control of coordination between the limbs, whereas the coordination between the segments of one limb appears to be unaffected by disturbance of muscle spindle input of one muscle.     

Kinaesthetic role of muscle afferents in man,studied by tendon vibration and microneurography

Summary The characteristics of vibration-induced illusory joint movements were studied in healthy human subjects. Unseen by the subject, constant frequency vibration trains applied to the distal tendon of the Triceps or Biceps induced an almost constant velocity illusory movement of the elbow whose direction corresponded to that of a joint rotation stretching the vibrated muscle. Vibration trains of the same duration and frequency applied alternatively to the Biceps and Triceps evoked alternating flexion-extension illusory movements.During successive application of vibration trains at frequencies from 10 to 120 Hz, the perceived velocity of the illusory movements increased progressively from 10 to 70–80 Hz, then decreased from 80 to 120 Hz. The maximal perceived velocity was three times higher during alternating vibration of the Biceps and Triceps than during single muscle stimulation.Unit activity from 15 muscle spindle primary endings and five secondary endings located in Tibialis anterior and Extensor digitorum longus muscles were recorded using microneurography in order to study their responses to tendon vibration and passive and active movements of the ankle.Primary endings were all activated by low amplitude tendon vibration (0.2–0.5 mm) previously used to induce illusory movements of the elbow. The discharge of some was phase-locked with the vibration cycle up to 120 Hz, while others responded one-to-one to the vibration cycle up to 30–50 Hz, then fired in a sub-harmonic manner at higher frequencies. Secondary endings were much less sensitive to low amplitude tendon vibration.Primary and secondary ending responses to ramp and sinusoïdal movements of the ankle joint were compared. During the movement, the primary ending discharge frequency was almost constant, while the secondary ending activity progressively increased. During ankle movements the primary ending discharge appeared mainly related to velocity, while some secondary activities seemed related to both movement velocity and joint angle position.Muscle spindle sensory ending responses to active and passive ankle movements stretching the receptor-bearing muscle (plantar flexion) were qualitatively and quantitatively similar. During passive reverse movements (dorsiflexion) most of the sensory endings stopped firing when their muscle shortened. Active muscle shortening (isotonic contraction) modulated differently the muscle spindle sensory ending discharge, which could stop completely, decrease or some times increase during active ankle dorsiflexion. During isometric contraction most of the muscle spindle sensory endings were activated.The characteristics of the vibration-induced illusory movements and the muscle spindle responses to tendon vibration and to active and passive joint movements strengthened the possibility of the contribution of primary endings to kinaesthesia, as suggested by several previous works. Moreover, the present results led us to attribute to proprioception in the muscle stretched during joint movement a predominant, but not exclusive, role in this kind of perception.     

Dual response from human muscle spindles in fast voluntary movements

Single-unit impulses were recorded from the radial nerve of attending human subjects using the microneurography technique. The discharge of muscle spindle afferents from the extensor digitorum muscles was analysed while subjects performed fast lengthening and shortening voluntary movements as well as movements of moderate speed at a single metacarpophalangeal joint. Opposing or assisting loads of moderate size were added in some tests. Fast lengthening movements were, in practically all units, associated with acceleration of spindle discharge. However, the responses were modest and in many primary afferents it was of similar size as their response to small irregularities during slower movements. During shortening movements, most spindle afferents stopped firing altogether, whereas some afferents exhibited a distinct burst of impulses at the onset of active shortening followed by silence during the main part of the movement. This initial shortening responses was sometimes more prominent when the parent muscle worked against an opposing load. It was interpreted as a result of fusimotor drive associated with the building up of force in the contracting muscle. The initial shortening response from the contracting muscle and the stretch response from the antagonist constitute a dual signal, describing accurately the onset of joint movement as seen from the two muscles. It remains to be clarified which role this pattern of afferent responses may have in the design of the current motor output and in the capturing of nature and size of the external load.     

Independent coactivation of shoulder and elbow muscles

 The aim of this study was to examine the possibility of independent muscle coactivation at the shoulder and elbow. Subjects performed rapid point-to-point movements in a horizontal plane from different initial limb configurations to a single target. EMG activity was measured from flexor and extensor muscles acting at the shoulder (pectoralis clavicular head and posterior deltoid) and elbow (biceps long head and triceps lateral head) and flexor and extensor muscles acting at both joints (biceps short head and triceps long head). Muscle coactivation was assessed by measuring tonic levels of electromyographic (EMG) activity after limb position stabilized following the end of the movements. It was observed that tonic EMG levels following movements to the same target varied as a function of the amplitude of shoulder and elbow motion. Moreover, for the movements tested here, the coactivation of shoulder and elbow muscles was found to be independent – tonic EMG activity of shoulder muscles increased in proportion to shoulder movement, but was unrelated to elbow motion, whereas elbow and double-joint muscle coactivation varied with the amplitude of elbow movement and were not correlated with shoulder motion. In addition, tonic EMG levels were higher for movements in which the shoulder and elbow rotated in the same direction than for those in which the joints rotated in opposite directions. In this respect, muscle coactivation may reflect a simple strategy to compensate for forces introduced by multijoint limb dynamics. Received: 7 July 1998 / Accepted: 28 July 1998     

Reduced voluntary activation of human skeletal muscle during shortening and lengthening contractions in whole body hyperthermia

This study examined the effect of whole body hyperthermia on the voluntary activation of exercised and non-exercised skeletal muscle performing a series of lengthening and shortening contractions. Thirteen subjects exercised on a cycle ergometer at 60% of maximal oxygen consumption until voluntary exhaustion in ambient conditions of approximately 40 degrees C and 60% relative humidity. Before and immediately following the cycle protocol, subjects performed a series of 25 continuous isokinetic shortening and lengthening maximal voluntary contractions (MVCs) of the leg extensors and forearm flexors. Voluntary activation for shortening and lengthening contractions for the forearm and leg was assessed prior to and following the 25 MVCs by superimposing a paired electrical stimulus to the femoral nerve and the biceps brachii during additional MVCs. Exercise to exhaustion increased rectal temperature to 39.35+/-0.50 degrees C. Voluntary activation remained unchanged following the prehyperthermia endurance set of shortening and lengthening maximal contractions in both the forearm flexors and leg extensors. Similarly, voluntary activation remained at prehyperthermic levels for the single MVCs immediately following the cycle trial. However, by the time of completion of the posthyperthermia endurance contractions, voluntary activation had declined significantly by 5.87+/-7.56 and 8.46+/-9.26% in the shortening and lengthening phases, respectively, for the leg extensors but not for the forearm flexors. These results indicate that the central nervous system (CNS) reduces voluntary drive to skeletal muscle performing both shortening and lengthening contractions following exercise-induced hyperthermia. The reductions in voluntary activation were only observed following a series of dynamic movements, indicating that the CNS allows for initial and brief 're-activation' of skeletal muscle following exercise-induced hyperthermia.     

Disturbed proprioception following a period of muscle vibration in humans

Forearm position matching tasks were performed by blindfolded subjects before and after applying vibration for 60 s to the biceps or triceps muscle of one arm. Following cessation of vibration, statistically significant alignment (proprioceptive) errors occurred when a movement lengthened the previously vibrated muscle. The error was such that the length of the post-vibrated muscle was greater than the length of the same muscle in the non-vibrated arm. This effect is the opposite to that which occurs during vibration.     

The contribution of afferent information on position and velocity to the control of slow and fast human forearm movements

Summary We applied vibration at various rates to the biceps tendon of a passive, restrained arm in normal human subjects and measured its effect on the perception of forearm position and the perception of forearm velocity. The disturbances of limb position perception and limb velocity perception depended on the vibration rate in distinctly different ways. We thereupon applied vibration at various rates to the biceps tendon during the performances of non-visually-guided slow and fast forearm movements. The vibration-rate-dependence of the disturbance of slow movements matched the vibration-ratedependence of the disturbance of limb position perception. The vibration-rate-dependence of the disturbance of fast limb movements matched the vibration-rate-dependence of the disturbance of limb velocity perception. It is concluded that afferent position information is dominant in the control of slow movements, whereas mainly afferent velocity information is used in the control of fast movements.     

Effect of load level and muscle pain intensity on the motor control of elbow-flexion movements

This study assessed interactions between mild/moderate muscle pain and inertial load on the control of human elbow-flexion movements. It is hypothesized that high inertial load combined with moderate muscle pain intensity affect the motor control more than for low inertial-load combined with low-intensity pain. Fifteen subjects performed horizontal pointing movements (70° range) under three load conditions: 0, 4, and 10 kg. Pain was induced by injection of 0.5 ml and 1.5 ml hypertonic saline into the biceps muscle. Subjects scored the muscle pain intensity on a visual analogue scale (VAS). Elbow joint position, VAS, and the electromyograms (EMG, m. biceps brachii, m. triceps brachii, m. brachioradialis, and m. trapezius) were recorded. Mild and moderate muscle pain attenuated acceleration profiles [6.1(0.9)%], effective movement amplitude [3.2 (0.7)%], peak velocity [5.8 (0.9)%] and prolonged the reaction time [21 (5)%]. No interaction between muscle pain intensity and inertial load was found for the kinematic parameters. EMG profiles from m. biceps brachii, m. triceps brachii, and m. brachioradialis were similarly attenuated [10.2 (0.80)%] by mild and moderate muscle pain in all inertial load conditions. For high inertial load, the initial agonist EMG burst activity was more attenuated [50 (5.3)%] by moderate muscle pain compared with mild muscle pain [34 (4.2)%]. These data suggest that for high effort-demanding tasks muscle pain differently affects the motor planning according to the pain-intensity level. Perturbations of motor planning lead to changes on movement strategies, which might be a potential cause of musculoskeletal problems.     

Electromechanical delay in skeletal muscle under normal movement conditions

Electromechanical delays (EMD), the time from onset of EMG activity to change in acceleration or deceleration of the forearm, were studied in concentric and eccentric contractions of biceps and triceps brachii muscles. Horizontal flexion and extension movements were performed at varying speeds by 10 subjects. EMD time in concentric contractions for biceps was 41 +/- 13 ms and for triceps was 26 +/- 11 ms and was not influenced by the velocity of the movement. In eccentric contractions at the slow velocity the biceps EMD time was 38 +/- 13 ms and shortened to 28 +/- 10 ms at the faster velocity. The eccentric triceps EMD, however, was not significantly altered by movement velocity and averaged 30 +/- 7 ms. The data provided support for the hypothesis that stretching of the series elastic component, to a point where muscle force can be detected, is the primary determinant of the EMD phenomenon. However, there are complex interactions of the effects on EMD of muscle fiber type composition, whether the contraction is concentric or eccentric, and the velocity of the movement as well as possible gamma system influence. These complications require that consideration of electromechanical delay be made when phasic relationships between muscle force or joint torque generation from different muscles are inferred from EMGs.     

Combined effects of preceding muscle vibration and contraction on the tonic vibration reflex

As a result of intrafusal thixotropy, muscle contraction at a short length followed by passive lengthening enhances the subsequent tonic vibration reflex (TVR). We studied the effects of muscle vibration, contraction, and their combination on the subsequent TVR in the left biceps in 20 healthy men. The preceding vibration (20 or 80 Hz) conditioning at a short or long length was applied to the muscle belly with and without a contraction. After conditioning, distal tendon vibration (80 Hz) was used to elicit the TVR at the test length. The strength of the TVR was measured by surface electromyography. Conditioning with 80-Hz vibration at a short length followed by passive lengthening enhanced the subsequent TVR, which was greater in the presence than in the absence of a conditioning contraction. These results suggest that vibration and contraction work synergistically to develop intrafusal thixotropy.     

Movement-related phasic muscle activation

To test the hypothesis that phasic muscle activation is related to the acceleration-deceleration characteristics of the resulting movement, we examined the relation between the duration of the acceleratory phase of a variety of movement types and the duration of the phasic muscle activity producing the acceleration (the initial agonist burst, AG1). Movements of five types were studied: (1) step-tracking movements of different amplitudes (10–90 deg) and durations (200–800 ms), (2) movements of the same amplitude (40 deg) and duration (600 ms) varying only in their symmetry ratio (SR, ratio of acceleration to deceleration durations), (3) movements in which acceleration duration was changed while acceleration magnitude was held constant, (4) oscillatory movements of different frequencies and peak amplitudes, (5) step-tracking movements against different inertial loads. Subjects made movements about the elbow joint in the horizontal plane. Surface electromyographic (EMG) activity was recorded from the biceps and the lateral head of the triceps muscles. Under all movement conditions tested and with acceleration duration ranging from 100 to 500 ms, acceleration duration varied linearly with the duration of AG1. Correlation coefficients for the linear regression lines ranged from 0.8 to 0.99. The slope of the best fit linear regression lines ranged from 0.5 to 1.6 and tended to be higher for extensions than flexions. The variations in slope may arise from differing mechanical properties of the biceps and triceps muscles, as well as from active forces produced in the antagonist. AG1 duration was unchanged by inertial loading when subjects kept acceleration duration constant. If subjects responded to an increase in inertial load with an increase in acceleration duration, there was a corresponding increase in AG1 duration. The data demonstrate a general relation between one characteristic of muscle activation (AG1 duration) and the resulting movement. The linear form of the relation is invariant across movement amplitude (range 10–90 deg), speed, duration (range 200–800 ms) and temporal profile (SR range 0.3-2.7), and is also independent of movement type (step, oscillatory). Such a general and simple relation between EMG and movement suggests that, at least to a first approximation, the nervous system can rather simply determine the muscle activation patterns needed to produce movements with desired characteristics.     

Proprioceptive illusions created by vibration of one arm are altered by vibrating the other arm

There is some evidence that signals coming from both arms are used to determine the perceived position and movement of one arm. We examined whether the sense of position and movement of one (reference) arm is altered by increases in muscle spindle signals in the other (indicator) arm in blindfolded participants (n = 26). To increase muscle spindle discharge, we applied 70–80 Hz muscle vibration to the elbow flexors of the indicator arm. In a first experiment, proprioceptive illusions in the vibrated reference arm in a forearm position-matching task were compared between conditions in which the indicator arm elbow flexors were vibrated or not vibrated. We found that the vibration illusion of arm extension induced by vibration of reference arm elbow flexors was reduced in the presence of vibration of the indicator elbow flexors. In a second experiment, participants were asked to describe their perception of the illusion of forearm extension movements of the reference arm evoked by vibration of reference arm elbow flexors in response to on/off and off/on transitions of vibration of non-reference arm elbow flexors. When vibration of non-reference arm elbow flexors was turned on, they reported a sensation of slowing down of the illusion of the reference arm. When it was turned off, they reported a sensation of speeding up. To conclude, the present study shows that both the sense of limb position and the sense of limb movement of one arm are dependent to some extent on spindle signals coming from the other arm.     

Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle

This study examined the strength of motor unit synchronisation based on time- and frequency-domain measures during postural, shortening and lengthening contractions of a hand muscle in young adults. Single motor unit activity was recorded with intramuscular electrodes in the left first dorsal interosseus muscle as the subject held the index finger at a constant position while supporting a light load for 2-5 min. The subject then performed slow (1.7 deg s⁻¹) shortening and lengthening contractions to lift and lower the load. The movement required subjects to perform 10-25 constant-velocity contractions with the index finger over a 10 deg range of motion by using 6 s shortening and lengthening contractions. Individual discharge times were obtained from 23 pairs of motor units in 14 subjects to assess the strength of motor unit synchronisation and coherence during the three tasks. The strength of motor unit synchronisation was approximately 50 % greater during the lengthening contractions compared with the postural and shortening contractions, and the width of the central synchronous peak in the cross-correlation histogram was ≈4 ms narrower during shortening contractions. These findings reveal that there is an increase in common input to motoneurones during lengthening contractions and a greater relative contribution of direct common inputs to motoneurones during shortening contractions compared with postural tasks. Furthermore, the amount of motor unit coherence in the low-frequency band (2-12 Hz) was reduced during shortening contractions compared with postural and lengthening contractions. These data indicate that the timing of inputs received by the motoneurones innervating the first dorsal interosseus of young adults differs during postural, shortening and lengthening contractions against a light load.