Separate control of arm position and velocity demonstrated by vibration of muscle tendon in man

Summary The effect of muscle tendon vibration on the performance of some simple motor tasks and on kinesthesia was studied in normal humans. Subjects performed non-visually-guided slow arm movements to match either the position or the velocity of a visual target. In the experiments designed to study kinesthesia subjects indicated the perceived position or velocity of their passively moved arm. Vibration was applied over either the biceps or the triceps tendon. Position and velocity matching were found to be disturbed by vibration in essentially different ways, as were the perception of imposed position and the perception of imposed velocity. However, the vibration induced disturbance of position matching was congruent with the distortion of position perception. The effect of vibration on velocity matching was in accordance with the effect of vibration on the perception of velocity. It is concluded that the afferent information pathways that give rise to the perception of position and velocity respectively can be used separately in the control of slow movements under different conditions.     

The effect of muscle vibration on human position sense during movements controlled by lengthening muscle contraction

Summary Muscle vibration studies suggest that during voluntary movement limb position is coded by muscle spindle information derived from the lengthening, antagonist muscle. However, these investigations have been limited to movements controlled by shortening contractions. This study further examined this property of kinesthesia during movements controlled by lengthening contraction. Subjects performed a horizontal flexion of the right forearm to a mechanical stop randomly positioned at 30, 50 and 70° from the starting position. The movement was performed against a flexor load (1 kg) requiring contraction of the triceps muscle. Vision was occluded and movements were performed under three conditions: no vibration, vibration of the right biceps and vibration of the right triceps. The perceived position of the right forearm was assessed by instructing subjects to simultaneously match the right limb position with the left limb. Vibration of the shortening biceps muscle had no effect on limb matching accuracy. However, triceps vibration resulted in significant overestimation of the vibrated limb position (10–13°). The variability in movement distance was uninfluenced by muscle vibration. During movements controlled by lengthening contraction, there is a concurrent gamma dynamic fusimotor input that would enhance primary afferent discharge. Despite this additional regulating input to the muscle spindle, it appears that muscle spindle information from the lengthening muscle is important for the accurate perception of limb movement and/or position.     

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.     

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.     

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.     

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.     

Proprioceptive control of cyclical bimanual forearm movements across different movement frequencies as revealed by means of tendon vibration

The effect of unilateral tendon vibration on the performance of cyclical bimanual forearm movements was investigated across different cycling frequencies (from 0.67 to 2.53 Hz). The spatiotemporal features of the individual limb motions as well as their coordination were studied. Tendon vibration was found to result in a substantial reduction in the amplitude of the vibrated arm, leaving the nonvibrated arm unaffected. The vibration-induced amplitude reduction decreased from 26% to 11% as cycling frequency increased even though significant reductions were still observed at the highest cycling frequencies. Tendon vibration was also found to result in an increase of the phase lead of the dominant arm with respect to the nondominant arm, but this effect was not modulated by cycling frequency. The data argue in favor of a closed-loop mode of movement control during cyclical high-speed movements. It is suggested that kinesthetic afferent information is processed and used to guide action up to near-maximal movement speeds, reinforcing recent claims with respect to visual information processing. Electronic Publication     

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     

Some sensory and motor factors influencing the control and appreciation of eye and limb position

Summary Some aspects of the manner in which the central nervous system uses sensory information for the guidance of eye and arm movements were investigated. When subjects experience apparent motion of their restrained forearm, induced by vibration of their biceps muscle in the dark, they are able to pursue with their eyes at least part of this motion and to point with their nonvibrated limb to the apparent location of the vibrated arm. The presence of a small target light on the vibrated hand limits the extent of illusory change in limb position and results in illusory motion of the target light in the same direction as the arm motion. When asked to indicate the spatial position of the light or hand, subjects still point with their nonvibrated arm to the apparent locations. Although visual pursuit of the illusory motion of the forearm can still be elicited in the presence of the target light on the hand, the subjects' eyes remain steadily fixating the stationary target light when they are instructed to track its illusory motion. These findings demonstrate that sensory and motor factors affecting the perception of visual direction and the guidance of arm and eye movements can be differentially employed at several levels of central nervous control.     

Upper limb kinesthetic asymmetries: Gender and handedness effects

Proprioceptive and motor information contribute to movement representation; however, the equivalence of homologous contralateral sensorimotor processes as a function of gender and handedness has received little attention. The present work investigated asymmetry in contralateral reproductions of movements elicited by tendon vibration in right and left handed young adults of both genders. With eyes closed, illusions of elbow flexion movement elicited by a 100 Hz vibration applied to the distal tendon of the right or left triceps muscle were matched concurrently with the opposite limb. Overall, movement velocity was larger for females than males, asymmetric and handedness dependent in males. Conversely, consistent symmetry was found between left and right-handed females. These findings lead us to suggest that hand preference and gender contribute to differences in movement representation that may result from the combination of cortical structural differences and information processing specific to each hemisphere and gender.     

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.     

Post-movement beta synchronization after kinesthetic illusion, active and passive movements.

After the completion of a voluntary movement or in response to somatosensory stimulation, a short-lasting burst of beta oscillations (post movement beta ERS, beta rebound) can be observed. In the present study, we investigated if this is also true for the illusion of movements, induced by a vibration at 80 Hz on the biceps tendon. We compared the post-movement synchronization of EEG beta rhythms induced by active and passive movements and illusion in eight right-handed healthy subjects. As a result, a short-lasting post-movement beta ERS was present over motor areas after both active and passive and also after illusion of movement in all subjects. These results suggested a possible role of MI and the somatosensory cortex in the somatic perception of limb movement in humans.     

Centrally programmed patterns of muscle activity in voluntary motor behavior of humans

Summary Rapid voluntary limb movements are accompanied by a triphasic electromyogram (EMG): the agonist muscle discharges briefly to generate the initial limb displacement and then, in sequence, an antagonist and second agonist burst occur. The origins of these bursts of EMG have been attributed to both peripheral and central sources. We attempted to determine in human subjects whether somesthetic afferent inputs related to passive muscle stretch or joint rotation were necessary for the appearance of the three bursts. EMGs were recorded while subjects performed rapid isotonic movements before and after forearm afferent function was blocked by ischemia. EMG patterns were also studied during phasic and sustained isometric contractions of forearm muscles.When the forearm was ischemically deafferented the triphasic EMG pattern persisted though the amplitudes of the three bursts were modified. In separate experiments, a similar three burst pattern was also observed while phasic isometric contractions were performed, but not when rapid-onset sustained isometric contractions were executed.These data support the view that somesthetic afferent information related to muscle length or joint rotation is not necessary for the occurrence of the three burst pattern during rapid motor behaviors. Since bursts of EMG activity were observed when torque rose and fell quickly during fast isotonic movements and phasic isometric contractions, the triphasic pattern appears to be a fundamental property of the central program underlying such rapid motor behaviors.     

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.     

Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study

Summary The activities of single proprioceptive fibres were recorded from the lateral peroneal nerve using transcutaneously implanted tungsten microelectrodes. Unitary discharges originating from muscle spindle primary and secondary endings and Golgi tendon organs were identified by means of various physiological tests. The sensitivity of proprioceptors to mechanical vibrations with a constant low amplitude (0.2–0.5 mm) applied at various frequencies to the tendon of the receptor-bearing muscle was studied. Muscle spindle primary endings (Ia fibres) were found to be the most sensitive to this mechanical stimulus. In some cases their discharge could be driven in a one-to-one manner up to 180 Hz. Most of them also fired harmonically with the vibration up to 80 Hz and then discharged in a subharmonic manner (1/2–1/3) with increasing vibration frequencies. Muscle spindle secondary endings (II fibres) and Golgi tendon organs (Ib fibres) were found to be either insensitive or only slightly sensitive to tendon vibration in relaxed muscles. The effects of tendon vibration on muscle spindle sensory endings response to muscle lengthening and shortening induced by imposed constant velocity or sinusoidal movements of the ankle joint were studied. Modulation of the proprioceptive discharge frequency coding the various joint movement parameters was either completely or partly masked by the receptor response to vibration, depending on the vibration frequency. Moreover, vibrations combined with sinusoidal joint movements elicited quantitatively erroneous proprioceptive messages concerning the movement parameters (amplitude, velocity). The sensitivity of the Golgi tendon organs to vibration increased greatly when the receptor-bearing muscle was tonically contracted. These data confirm that vibration is able to preferentially activate the Ia afferent channel, even when the vibration amplitude is low. They define the frequency sensitivity of the muscle spindle primary and secondary endings and the Golgi tendon organs. They also show that the physiological messages triggered by ongoing motor activities undergo a series of changes during the exposure of muscles to vibration.     

A perceptual analysis of viscosity

The perception of viscosity was studied using the contralateral limb-matching procedure in which subjects adjusted the viscosity of a motor connected to the wrist of one (matching) arm until it was perceived to be the same as that of the motor attached to the other (reference) arm. Two servo-controlled electromagnetic linear motors with computer-controlled viscosity were used to present viscosities ranging in amplitude from 2 to 1024 N · s/m to 11 subjects. Ten different viscosities were matched by subjects, and there were ten repetitions of each stimulus amplitude. The psychophysical function relating the reference to matching viscosity was linear (99% variance accounted for), and the accuracy with which the viscosities were matched (slope of 0.88) paralleled that reported previously for force, limb position and stiffness. The Weber fraction for viscosity was 0.34, which is 50% larger than that measured for stiffness and over twice that reported for force. An analysis of the movements and forces generated to perceive the reference viscosity revealed that subjects did not vary the amplitude of the movements and typically made very small excursions of the forearm, but that both the velocity of the movements and force changed significantly as a function of the reference viscosity. These findings were interpreted as indicating that the human proprioceptive system is capable of integrating information regarding force and movement velocity so as to perceive the viscosity of a mechanical system connected to the limbs, but that its sensitivity to changes in viscosity is much less than would be predicted from its capacity to detect variations in muscle force and limb movement.     

Relationship between the velocity of illusory hand movement and strength of MEG signals in human primary motor cortex and left angular gyrus

We studied the relationship between the velocity of movement illusion and the activity level of primary motor area (M1) and of the left angular gyrus (AG) in humans. To induce illusory movement perception, we applied co-vibration at different frequencies on tendons of antagonistic muscle groups. Since it is well established that the velocity of illusory movement is related to the difference in vibration frequency applied to two antagonistic muscles, we compared magnetoencephalography (MEG) signals recorded in two conditions of co-vibration: in the “fast illusion” condition a frequency difference of 80 Hz was applied on the tendons of the right wrist extensor and flexor muscle groups, whereas in the “slow illusion” condition a frequency difference of 40 Hz was applied on the same muscle groups. The dipole strength, reflecting the activity level of structures, was measured over M1 and the left AG in two different time-periods: 0–400 and 400–800 ms in each condition. Our results showed that the activity level of the AG was similar in both conditions whatever the time-period, whereas the activity level of M1 was higher in the “fast illusion” condition compared to the “slow illusion” condition from 400 ms after the vibration onset only. The data suggest that the two structures differently contributed to the perception of illusory movements. Our hypothesis is that M1 would be involved in the coding of cinematic parameters of the illusory movement but not the AG.     

Reduced effects of tendon vibration with increased task demand during active, cyclical ankle movements

Tendon vibration can alter proprioceptive feedback, one source of sensory information which humans can use to produce accurate movements. However, the effects of tendon vibration during functional movement vary depending on the task. For example, ankle tendon vibration has considerably smaller effects during walking than standing posture. The purpose of this study was to test whether the effects of ankle tendon vibration are predictably influenced by the mechanical demands of a task, as quantified by peak velocity. Twelve participants performed symmetric, cyclical ankle plantar flexion/dorsiflexion movements while lying prone with their ankle motion unconstrained. The prescribed movement period (1, 3 s) and peak-to-peak amplitude (10°, 15°, 20°) were varied across trials; shorter movement periods or larger amplitudes increased the peak velocity. In some trials, vibration was continuously and simultaneously applied to the right ankle plantar flexor and dorsiflexor tendons, while the left ankle tendons were never vibrated. The vibration frequency (40, 80, 120, 160 Hz) was varied across trials. During trials without vibration, participants accurately matched the movement of their ankles. The application of 80 Hz vibration to the right ankle tendons significantly reduced the amplitude of right ankle movement. However, the effect of vibration was smaller during more mechanically demanding (i.e., higher peak velocity) movements. Higher vibration frequencies had larger effects on movement accuracy, possibly due to parallel increases in vibration amplitude. These results demonstrate that the effects of ankle tendon vibration are dependent on the mechanical demand of the task being performed, but cannot definitively identify the underlying physiological mechanism.