|
|
||||||||
1 Laboratoire de Neurobiologie Humaine, Unité Mixte de Recherche Centre National de la Recherche Scientifique 6149 "Neurobiologie Intégrative et Adaptative," 13397 Marseille, France; 2 Prince of Wales Medical Research Institute, Randwick, New South Wales 2031, Australia; and 3 The Miami Project to Cure Paralysis, University of Miami School of Medicine, Miami, Florida 33136
| |
ABSTRACT |
|---|
|
|
|---|
One way to improve the weak triceps brachii voluntary forces of people with chronic cervical spinal cord injury may be to excite the paralyzed or submaximally activated fraction of muscle. Here we examined whether elbow extensor force was enhanced by vibration (80 Hz) of the triceps or biceps brachii tendons at rest and during maximum isometric voluntary contractions (MVCs) of the elbow extensors performed by spinal cord-injured subjects. The mean ± SE elbow extensor MVC force was 22 ± 17.5 N (range: 0-23% control force, n = 11 muscles). Supramaximal radial nerve stimuli delivered during elbow extensor MVCs evoked force in six muscles that could be stimulated selectively, suggesting potential for force improvement. Biceps vibration at rest always evoked a tonic vibration reflex in biceps, but extension force did not improve with biceps vibration during triceps MVCs. Triceps vibration induced a tonic vibration reflex at rest in one-half of the triceps muscles tested. Elbow extensor MVC force (when >1% of control force) was enhanced by vibration of the triceps tendon in one-half of the muscles. Thus triceps, but not biceps, brachii tendon vibration increases the contraction strength of some partially paralyzed triceps brachii muscles.
tonic vibration reflex; antagonist vibratory response; muscle weakness; muscle paralysis; maximum voluntary contraction
| |
INTRODUCTION |
|---|
|
|
|---|
MANY PEOPLE WITH CERVICAL spinal cord injury (SCI) have weak triceps brachii muscles (31, 33). This weakness limits their ability to push a wheelchair, to transfer from one place to another, and to reach objects in the environment. The various factors that contribute to this weakness of triceps brachii during voluntary contractions may include disruption of descending inputs from higher centers to the spinal cord, death of motoneurons near the injury site, poor central drive, coactivation of biceps and triceps brachii, and disuse atrophy (30, 31, 33). It is also typical for triceps brachii to be paralyzed partially in these individuals with SCI. That is, only some triceps brachii motor units are activated by voluntary effort. The other triceps brachii motor units are either paralyzed or are not driven at a maximal frequency by voluntary effort, because additional force can often be evoked by magnetic cortical stimulation, radial nerve stimulation, or both sites of stimulation during maximal voluntary triceps contractions (33). One way to compensate for this muscle weakness during voluntary contractions would be to activate additional motor units and/or to drive already active motor units maximally by external inputs.
Radial nerve stimulation can be used to excite triceps brachii, including the fraction of muscle that the subject cannot drive voluntarily. However, after chronic cervical SCI, it is not always easy to stimulate triceps brachii selectively. The associated partial denervation and atrophy of triceps brachii often mean that the stimulation also activates other radial-innervated muscles or antagonists (33). An alternative way to activate triceps brachii may be to vibrate the muscle tendon mechanically.
Muscle tendon vibration excites muscle spindle primary endings (3, 20, 27), which, in turn, induce reflex contractions in healthy muscles at rest. These reflex contractions may be of two types, depending on the context in which the vibratory stimulation is applied. Vibration may evoke a tonic vibratory reflex (TVR) in the parent muscle when the subject looks at his or her arm, a response that can involve both mono- and polysynaptic spinal pathways, as well as supraspinal processes (13, 14, 19, 28). When the subjects close their eyes, tendon vibration induces a sensation of illusory movement, which is accompanied, in 70% of healthy subjects, by a contraction of the muscle(s) antagonistic to the vibrated muscle [antagonist vibratory response (AVR)] (4, 5, 10, 26). Thus a contraction of triceps brachii may result from an illusory sensation of forearm extension due to vibration of the biceps brachii tendon.
Earlier studies in people with SCI have shown that tendon vibration generally induces either no TVR or a weak response in the parent muscle (2, 8, 9, 13, 16). The AVR was not explored. Sometimes only electromyographic (EMG) signals and/or joint angles were recorded. When both the agonist and antagonist muscles were excited simultaneously by vibration, it was unclear how contraction strength was changed. Other studies have focused only on leg muscles or have provided case reports.
Given the evidence that the maximal triceps brachii voluntary force-generating capacity is significantly less in subjects with chronic cervical SCI than in controls (mean ± SD: 18 ± 22% of control force), but the force-generating capacity of the entire triceps brachii muscle was predicted to be greater (i.e., the strength of the voluntary contraction; the fraction activated poorly by voluntary effort and/or the paralyzed muscle fraction was 30 ± 26% of control force; Ref. 33), we hypothesized that the maximal voluntary elbow extensor force of individuals with chronic cervical SCI could be increased by exciting the triceps brachii motor pool with tendon vibration. Thus the primary aim of the present study was to determine whether vibration of either the triceps or biceps brachii tendons during a maximum voluntary contraction (MVC) of triceps brachii was a way to enhance the elbow extension force. To address this aim, it was necessary to answer two preliminary questions. First, we analyzed whether there was the potential to improve the elbow extensor force in the present subject population with chronic SCI (>1 yr). The maximal voluntary force of each triceps brachii muscle tested was compared with the predicted force-generating capacity of the entire muscle by using the twitch interpolation technique (1, 17, 23, 33). Second, for tendon vibration to improve maximum voluntary elbow extensor force, it was necessary that the vibration-induced inputs excited the triceps brachii motoneurons. The effectiveness of the vibration was tested by analysis of whether a tonic vibration reflex and/or AVR was induced in each of the triceps brachii muscles at rest. If a reflex response was induced by vibration before or during the voluntary triceps contraction, vibration may facilitate the initiation, maintenance, and/or strength of the voluntary contraction.
| |
MATERIALS AND METHODS |
|---|
|
|
|---|
Subjects.
Experiments were performed on eight volunteers (mean ± SE age:
40 ± 4 yr) who had sustained a SCI at C7 or higher,
as assessed by the criteria of the American Spinal Injury Association
(21). Table 1 gives some
characteristics of each person, in particular his or her injury level
and American Spinal Injury Association classification, the time since
injury, and the cause of injury. These subjects were chosen because
they had weak or completely paralyzed triceps brachii muscles when
evaluated by a manual examination. Only one arm was studied in five
people due to time constraints. Both arms (usually paralyzed to
different extents) were studied in the other three subjects
(n = 11 muscles in total). All but one subject
(subject 8, Table 1) had normal biceps function in the arm
tested, as assessed by manual muscle examination (i.e., a score of 5).
All subjects gave their informed, written consent to participate in
this study, which was approved by the University of Miami Institutional
Review Board and conducted according to the Declaration of Helsinki.
|
Experimental setup.
Each subject sat in his or her wheelchair. The arm rest of the
wheelchair was removed on the test side. The test arm lay palm up on an
inclined support, such that the elbow was flexed to ~90°, an
optimal angle for generating isometric force in triceps brachii (Del
Valle A, Bigland-Ritchie B, and Thomas CK, unpublished observations) (Fig. 1A). The subject's
forearm and hand were held against the support with Velcro. The
test shoulder was always strapped with a car seatbelt attached to the
subject's wheelchair at a point just behind the shoulder of the
contracting arm. The strap was bound firmly across the chest to a point
on the other side of the wheelchair at waist level. This setup gave
stability to the trunk during the contractions and immobilized the test
shoulder. Thus most of the force that we measured was attributed to
elbow extensor muscles (triceps brachii, anconeus). A transducer (FT10, Astro-Med, West Warwick, RI) was used to record the forces applied in
both the extension and flexion directions. The transducer lay beneath
the incline of the support, just proximal to the wrist, as during the
previous experiments involving able-bodied control subjects (31,
33).
|
Procedure. Before the recorded trials, the vibrator was manually applied to the biceps brachii tendon of the test arm, with the arm extended slightly and supported by an experimenter. This permitted each subject to become familiar with tendon vibration and the associated sensation of movement illusions. Then, with the test arm placed in the support, the subject was asked to perform a series of MVCs of the elbow extensors. Visual feedback of the force was provided on an oscilloscope, and verbal encouragement was given to help the subject maintain a maximal force for 6 s. When necessary, auditory feedback of triceps brachii EMG was also provided to facilitate muscle relaxation before the vibration or the voluntary contraction. Auditory feedback was turned off during the test MVCs and vibration.
The test protocol consisted of five different series presented in random order (see Fig. 1B). Each series was composed of five trials. There was a 2-min rest between trials. In one series, the subject was asked to perform a MVC of the elbow extensor muscles for 6 s, with continuous visual feedback of the force and verbal encouragement from the experimenters. Two different auditory cues from the computer were used to signal the beginning and the end of each contraction. To assess the extent to which triceps brachii was under voluntary control, four single supramaximal stimuli were delivered to the radial nerve (2 and 4 s after the beginning of the contraction and 2 and 4 s after the contraction). In two other series ("vibration alone"), vibration was applied perpendicularly to the tendons of either the triceps or the biceps brachii muscles for 9 s. Vibration was delivered at 80 Hz, because this frequency is known to activate muscle spindle primary endings preferentially (27). During the vibration, the subjects were asked to relax as much as possible. They were instructed to watch the vibrated arm during triceps vibration so as to facilitate the TVR. During biceps vibration, they were asked to close their eyes to preferentially evoke an AVR. At the end of each trial, the subject reported whether he or she felt any sensation of movement during the vibration. In the other two series, the subject was asked to perform a MVC of the elbow extensor muscles for 6 s, together with vibration of either the triceps (CVT) or biceps brachii tendons (CVB). The vibration was turned on 3 s before the voluntary contraction so as to initiate a vibration reflex. Vibration was stopped at the end of the voluntary contraction. Both the onset and offset of the vibration were marked by auditory cues from the computer.Data recording and analysis. Surface EMG from the triceps and biceps brachii muscles and force were amplified, filtered (30-300 Hz, direct current 100 Hz, respectively), and sampled on-line (3,200 and 400 Hz, respectively) by using an SC/Zoom data-acquisition and analysis system (Department of Physiology, University of Umeå, Sweden).
Data were analyzed off-line by using Zoom software. EMG signals were rectified and integrated between two target times (see below) and normalized for time to provide average EMG values. Force and integrated triceps and biceps brachii EMG were measured at the following target times during each trial. For the vibration-alone trials, measurements were made for two time windows (each of these and the other time windows were ~2 s) before vibration, three time windows during vibration, and two time windows after vibration. For the trials involving a MVC with or without vibration (see Fig. 3), measures were made for two time windows at rest (Pre1 and Pre2), one time window before the MVC with or without vibration (0), three time windows during the MVC (1, 2, 3), and two time windows after the MVC (Post1 and Post2). The degree of voluntary activation of the elbow extensors was estimated by using the twitch interpolation technique (1, 17, 23). The increment in force produced when the radial nerve stimulus was superimposed on the ongoing voluntary contraction was compared with the twitch forces evoked when the muscles were stimulated at rest
|
|
(12.6/17.7)] × 100}. Thus 71% of this
muscle was paralyzed and/or poorly activated by voluntary effort. The
MVC force for this subject was 36.5 N. With 29% voluntary activation,
these data suggest that 125.8 N could be produced by the entire muscle (36.5/0.29), providing the potential to produce 89.3 N by vibration or
some other external means.
Both the MVC and predicted whole muscle forces were expressed relative
to the average triceps brachii force produced by control women or men
(Fig. 1D) to give an indication of the extent of muscle
weakness in the SCI subjects and the magnitude of the muscle atrophy.
The mean maximal voluntary forces produced during elbow extension
performed by control women and men using the same experimental setup
were 157 and 268 N, respectively (Ref. 31; 18 subjects, 9 women, 29 ± 8 yr; 9 men, 24 ± 6 yr). Thus the MVC force for the female SCI subject shown in Fig. 1C was 23.2% of
control maximal force [(36.5 N/157 N) × 100%], whereas the
estimated force that could be evoked from the entire muscle was 80.1%
of control maximal force [(125.8 N/157 N) × 100%], leaving the
potential to produce 56.8% of control force by vibration. These data
also indicate that 19.9% of control force was attributable to muscle
atrophy {157 N
[(125.8 N/157 N) × 100]; see Ref.
33}, a strength deficit that will not be ameliorated by
vibration or other external stimuli.
Mean ± SE values are given. Data were collected from a total of
11 different arms (8 subjects). Because cervical SCI usually induces
asymmetrical effects on triceps brachii, the function of one or the
other triceps brachii muscles in the same subject is often very
different (n = 52 cases; Ref. 25).
Differential impairment by the injury was also observed in the
present group of subjects, as attested by the different MVC amplitudes
(see Fig. 1D, solid bars), and thus allowed us to consider
data from each arm independently. Improvement in the strength of either triceps brachii muscle is also of functional importance to an individual with chronic cervical SCI.
| |
RESULTS |
|---|
|
|
|---|
Maximum voluntary elbow extensor force and total elbow extensor force. All of the SCI subjects had difficulty in contracting triceps brachii voluntarily. This was reflected both as muscle weakness and as an inability to contract triceps brachii selectively. Figure 3A shows an example of the force from five trials performed by one subject (subject 4l). Her MVCs were weak (~12% of the average control female MVC force), reproducible (18.5 ± 2.6 N), and always involved cocontraction of biceps and triceps brachii. Figure 1D shows the mean forces developed during elbow extensor MVCs for 9 of the 11 muscles tested (solid bars; 2 muscles were totally paralyzed, subjects 7 and 8, Table 1), expressed relative to the mean force exerted by healthy women and men tested with the same apparatus (31). The mean forces developed by the SCI subjects ranged from 23 to 0.2% of control values.
Supramaximal stimulation of the radial nerve gave rise to three different responses: selective activation of triceps brachii (n = 6), contraction of triceps brachii together with other radial-innervated muscles in the forearm (n = 4), and muscle spasms that influenced the elbow extensor force (n = 1). Further stimulation was only delivered to those muscles that showed a selective triceps brachii response. In all six of these muscles, triceps force increments (mean ± SE, 5.4 ± 2.2 N) were produced by radial nerve stimulation during isometric MVCs of the elbow extensor muscles. In five cases, the paralyzed and/or submaximally activated part of the elbow extensor muscles was stronger than the fraction that was under voluntary control (Fig. 1D). The voluntary force exceeded the force from the paralyzed and/or submaximally activated fraction in another muscle. The mean forces from paralyzed and/or submaximally activated muscle ranged from 0.2 to 56.8% of control values, an indication of the extent to which tendon vibration may be able to improve the triceps brachii contraction strength.Response to tendon vibration alone.
With triceps and biceps brachii at rest, vibration was applied either
to the triceps tendon while the subject looked at that arm, or to the
biceps tendon while the subject had his or her eyes closed. Vibration
of the triceps brachii tendon was expected to induce contraction of the
triceps brachii muscle and a clear extension response, as shown for one
SCI subject in Fig. 2A.
|
Effects of tendon vibration during elbow extensor MVCs.
Figure 3 illustrates the general increase
in triceps brachii surface EMG and extension force observed when the
triceps brachii tendon was vibrated during MVCs performed by
subject 4l. Without tendon vibration, the
maximum voluntary elbow extensor force developed by this subject was
~20 N (Fig. 3A), but this force was doubled during triceps
tendon vibration (Fig. 3B). Notice that the period of
vibration preceding the onset of the MVC was also accompanied by an
increase in triceps surface EMG and extension force (Fig. 3B).
|
|
| |
DISCUSSION |
|---|
|
|
|---|
The present data showed that triceps brachii tendon vibration at rest evoked a TVR in just over one-half of the triceps tested, particularly in muscles of SCI subjects with stronger elbow extensor MVC forces. Vibration applied to the tendon of triceps brachii during elbow extensor MVCs (>1% of control force) also enhanced the elbow extension force in one-half of the muscles that were evaluated. Conversely, biceps brachii tendon vibration at rest always evoked a TVR in biceps brachii, but biceps tendon vibration during elbow extensor MVCs resulted in no improvements in the extensor force. These data suggest that triceps, but not biceps brachii, tendon vibration provides a way to increase the contraction strength of some of these elbow extensor muscles that have been weakened and partially paralyzed by chronic cervical SCI.
SCI population. All of the subjects who participated in this study were representative of the SCI population with cervical injuries in that they had difficulty with elbow extension because their triceps brachii MVCs were weak compared with those of control subjects, cocontraction of triceps and biceps brachii was common, only some of the triceps brachii muscles could be activated selectively with radial nerve stimulation, and many of the triceps muscles were paralyzed partially (25, 31, 33). These characteristics suggest that these spinal injuries involved upper and/or lower motoneuron damage. Where there is upper motoneuron injury, vibration may enhance force by a number of mechanisms (e.g., enhanced muscle spindle afferent activity resulting in supraspinal and/or spinal excitatory reflex activation of motoneurons). Subjects with lower motoneuron damage may have denervated portions of muscle, but reinnervation is expected to occur from neighboring axons (30). Stretch reflexes are absent in reinnervated muscles (6), possibly because the afferents reinnervate inappropriate target organs (7), a situation that may impair reflex excitation of motoneurons after SCI. If reinnervation from intact axons fails, the muscle fibers that remain denervated will not be activated either by volition, reflexly by vibration, or by electrical stimulation of the radial nerve.
Tendon vibration at rest.
It is well known that vibration of a muscle tendon at rest gives rise
to a tonic contraction of the parent muscle when the subjects look at
their arm (13, 14). This TVR is due to the high-frequency
activation of muscle spindle primary endings (3, 20, 27),
which, in turn, drive the
-motoneurons through monosynaptic and
polysynaptic spinal pathways, as well as supraspinal pathways (13, 14, 19, 28). This reflex, which is almost always produced in muscles of healthy subjects (8, 14), was
observed in about one-half of the triceps brachii muscles that we
tested in people with chronic cervical SCI. Others have shown
that the TVR is absent or weak in muscles influenced by SCI,
particularly when there is complete cord transection (8,
16). In contrast, Dimitrijevic et al. (9) were
always able to evoke a TVR in the muscles of SCI subjects, even when
muscle paralysis was complete. However, stronger TVR responses occurred
when there was greater preservation of motor and sensory function, as
found in the present study. In hemiplegia, as well as in spastic
muscles, the TVR may also be absent or weak, coexist with the
activation of neighboring muscles, or involve antagonist muscles
(3, 15). In the weaker elbow extensor muscles studied
here, we also commonly saw a reflex response in biceps brachii with
triceps tendon vibration.
Tendon vibration as a means of facilitating voluntary elbow extension force. In the six muscles in which we could evoke a selective triceps brachii response with radial nerve stimulation, twitches were evident during the MVCs of all of these muscles. Thus some triceps brachii motor units were not recruited or driven maximally by voluntary command. In four of these muscles, we estimated that excitation of the paralyzed or poorly activated fraction of muscle could at least double the force that the subjects could generate by voluntary effort (Fig. 1D). Triceps brachii tendon vibration during elbow extensor MVCs improved the performance in four muscles, but the magnitude of the extensor force enhancement varied between muscles (Fig. 4A). Other studies using subjects with incomplete SCI have reported qualitatively similar results from EMG records (9, 16). In one of the muscles that we studied, both the elbow extensor force and surface EMG doubled. Smaller triceps brachii surface EMG and force increases occurred in two other muscles. The differences in the magnitude of these responses may be explained by the following: 1) more or less overlap between the populations of motor units that were still influenced by muscle spindle inputs and descending voluntary control (24); 2) variations in voluntary drive as opposed to disruption of the inputs to the spinal cord; 3) activation of neighboring muscles, like shoulder extensors with vibration, influencing elbow extensor force production (3, 9); and 4) activation of deep motor units or units that were distant from the recording electrodes, resulting in small changes in triceps brachii surface EMG. The fourth muscle behaved differently in that the increase in MVC elbow extension force was associated with a large decrease in biceps brachii surface EMG, irrespective of whether the triceps or biceps brachii tendons were vibrated. Thus, in this arm, tendon vibration helped by changing the relative magnitudes of the triceps and biceps brachii contractions. The degree of biceps and triceps cocontraction during elbow extensor MVCs performed by this subject was similar to that of the other subjects. Thus particular spinal changes in this subject may have influenced the way in which the vibration acted.
The person in whom the maximum voluntary elbow extensor force was doubled by triceps tendon vibration also differed from the rest of the population in that her injury was incomplete, and she experienced frequent spasms in all of her muscles, despite taking baclofen daily. Although baclofen does not seem to reduce the TVR, it does reduce the amplitude of stretch reflexes, increases the threshold of these reflexes in spastic muscles, and reduces the incidence of spasms and clonus (22, 29). Thus this subject may be less sensitive to this medication, as revealed by the frequency and intensity of her muscle spasms, allowing the vibration to drive the motoneurons effectively through reflex pathways. Conversely, diazepam in healthy subjects abolishes the TVR (18), so this medication may be responsible for the lack of improvement in performance with triceps vibration in two subjects (Table 1) or may have reduced the vibration effects. An absence of elbow extensor force improvement could be expected in those muscles that showed a biceps brachii response at rest during biceps or triceps brachii tendon vibration (Fig. 2). In contrast, the absence of improvement in the muscle that showed the largest TVR in triceps brachii at rest and the strongest superimposed twitches in response to radial nerve stimulation (subject 1r) probably suggests that the same motor units were excited voluntarily and by tendon vibration. Such an overlap in the activated populations of motor units is probably also responsible for the lack of improvement observed in muscles that developed a TVR in triceps brachii at rest but were close to maximally activated voluntarily, as assessed by twitch interpolation (e.g., subject 2l, Fig. 1D).Functional implications. These data show that triceps brachii tendon vibration is a way to activate the triceps brachii muscle at rest in some SCI subjects who retain partial voluntary control of this muscle. It is unclear whether routine application of tendon vibration could prevent or retard the disuse atrophy present in some triceps brachii muscles (30), but vibration-induced contractions may be less uncomfortable than electrically induced contractions. In some subjects, triceps brachii tendon vibration during elbow extensor MVCs also improved the elbow extension force. Use of a miniaturized vibrator might help these individuals with SCI improve their muscle function (16), but this issue also needs quantitative evaluation in relation to the motor and sensory function that is preserved after the injury. Vibration-induced muscle contractions may be more effective in people who have an incomplete SCI without lower motoneuron involvement, so that the absence of stretch reflexes that occurs with muscle reinnervation (6, 7) is not a consideration. Furthermore, systematic investigation of the effects of various medications on these reflex responses induced by tendon vibration would be valuable.
| |
ACKNOWLEDGEMENTS |
|---|
This work was supported by grants from Institut National de la Santé et de la Recherche Médicale, Association Française contre les Myopathies, National Health and Medical Research Council of Australia Neil Hamilton Fairley Fellowship 007148, National Institutes of Health Grant NS-30226, and The Miami Project to Cure Paralysis.
| |
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: E. Ribot-Ciscar, Laboratoire de Neurobiologie Humaine, UMR CNRS 6149 "Neurobiologie Intégrative et Adaptative", 52, Faculté des Sciences de Saint-Jérôme, Case 362, 13397, Marseille Cedex 20, France (E-mail: rc{at}up.univ-mrs.fr).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
First published February 14, 2003;10.1152/japplphysiol.00894.2002
Received 27 September 2002; accepted in final form 5 February 2003.
| |
REFERENCES |
|---|
|
|
|---|
1.
Belanger, AY,
and
McComas AJ.
Extent of motor unit activation during effort.
J Appl Physiol
51:
1131-1135,
1981.
2.
Burke, D,
and
Ashby P.
Are spinal "presynaptic" inhibitory mechanisms suppressed in spasticity?
J Neurol Sci
15:
321-326,
1972.
3.
Burke, D,
Hagbarth KE,
Lofstedt L,
and
Wallin BG.
The responses of human muscle spindle endings to vibration of non-contracting muscles.
J Physiol
261:
673-693,
1976.
4.
Calvin-Figuière, S,
Romaiguère P,
Gilhodes JC,
and
Roll JP.
Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration.
Exp Brain Res
124:
342-350,
1999.
5.
Calvin-Figuière, S,
Romaiguère P,
and
Roll JP.
Relations between the directions of vibration-induced kinesthetic illusions and the pattern of activation of antagonist muscles.
Brain Res
881:
128-138,
2000.
6.
Cope, TC,
Bonasera SJ,
and
Nichols TR.
Reinnervated muscles fail to produce stretch reflexes.
J Neurophysiol
71:
817-820,
1994.
7.
Cope, TC,
Haftel VK,
Nichols TR,
Pinter MJ,
and
Prather JF.
Muscle afferent recovery from nerve injury.
In: Proceedings of the International Symposium on Motoneurones and Muscles: The Output Machinery. Groningen, the Netherlands: Univ. of Groningen, 2002, p. 34.
8.
DeGail, P,
Lance JW,
and
Neilson PD.
Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man.
J Neurol Neurosurg Psychiatry
29:
1-11,
1966.
9.
Dimitrijevic, MR,
Spencer WA,
Trontel JV,
and
Dimitrijevic M.
Reflex effects of vibration in patients with spinal cord lesions.
Neurology
27:
1078-1086,
1977.
10.
Feldman, AG,
and
Latash ML.
Inversions of vibration-induced senso-motor events caused by supraspinal influences in man.
Neurosci Lett
31:
147-151,
1982.
11.
Gillies, JD,
Burke DJ,
and
Lance JW.
Supraspinal control of the tonic vibration reflex.
J Neurophysiol
34:
302-309,
1971.
12.
Goodwin, GM,
Mc Closkey DI,
and
Matthews PBC
The contribution of muscle afferents in kinaesthesia shown by vibration induced illusions of movement and by effects of paralyzing joint afferents.
Brain
95:
705-748,
1972.
13.
Hagbarth, KE,
and
Eklund G.
Tonic vibration reflexes (TVR) in spasticity.
Brain Res
2:
201-203,
1966.
14.
Hagbarth, KE,
and
Eklund G.
Motor effects of vibratory stimuli in man.
In: Muscular Afferents and Motor Control, edited by Granit R.. Stockholm: Almqvist and Wiksell, 1966, p. 177-186.
15.
Hagbarth, KE,
and
Eklund G.
The effects of muscle vibration in spasticity, rigidity, and cerebellar disorders.
J Neurol Neurosurg Psychiatry
31:
207-214,
1968.
16.
Hagbarth, KE,
and
Eklund G.
The muscle vibrator-a useful tool in neurological therapeutic work.
Scand J Rehabil Med
1:
26-34,
1969.
17.
Hales, JP,
and
Gandevia SC.
Assessment of maximal voluntary contraction with twitch interpolation: an instrument to measure twitch responses.
J Neurosci Methods
25:
97-102,
1988.
18.
Lance, JW,
DeGail P,
and
Neilson PD.
Tonic and phasic spinal cord mechanisms in man.
J Neurol Neurosurg Psychiatry
29:
535-544,
1966.
19.
Malmgren, K,
and
Pierrot-Deseilligny E.
Evidence for non-monosynaptic Ia excitation of human wrist flexor motorneurones, possibly via propriospinal neurons.
J Physiol
405:
747-764,
1988.
20.
Matthews, PBC,
and
Watson JDG
Action of vibration on the response of cat muscle spindle Ia afferents to low frequency sinusoidal stretching.
J Physiol
317:
365-381,
1981.
21.
Maynard, FM,
Bracken MB,
Creasey G,
Ditunno JF,
Donovan WH,
Ducker TB,
Garber SL,
Marino RJ,
Stover SL,
Tator CH,
Waters RL,
Wilberger JE,
and
Young W.
International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association.
Spinal Cord
35:
266-274,
1997.
22.
McLellan, DL.
Effects of baclofen upon monosynaptic and tonic vibration reflexes in patients with spasticity.
J Neurol Neurosurg Psychiatry
36:
555-560,
1973.
23.
Merton, PA.
Voluntary strength and fatigue.
J Physiol
123:
553-564,
1954.
24.
Morita, H,
Baumgarten J,
Petersen N,
Christensen LO,
and
Nielsen J.
Recruitment of extensor-carpi-radialis motor units by transcranial magnetic stimulation and radial-nerve stimulation in human subjects.
Exp Brain Res
128:
557-562,
1999.
25.
Needham-Shropshire, BM,
Klose KJ,
Tucker ME,
and
Thomas CK.
Manual muscle test score and force comparisons after cervical spinal cord injury.
J Spinal Cord Med
20:
324-330,
1997.
26.
Roll, JP,
Gilhodes JC,
and
Tardy-Gervet MF.
Effets perceptifs et moteurs des vibrations musculaires chez l'homme normal: mise en évidence d'une réponse des muscles antagonists.
Arch Ital Biol
118:
51-71,
1980.
27.
Roll, JP,
Vedel JP,
and
Ribot E.
Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study.
Exp Brain Res
76:
213-222,
1989.
28.
Romaiguère, P,
Vedel JP,
Azulay JP,
and
Pagni S.
Differential activation of motor units in the wrist extensor muscles during the tonic vibration reflex in man.
J Physiol
444:
645-667,
1991.
29.
Sachais, BA,
Logue JN,
and
Carey MS.
Baclofen, a new antispastic drug. A controlled, multicenter trial in patients with multiple sclerosis.
Arch Neurol
34:
422-428,
1977.
30.
Thomas, CK,
Broton JG,
and
Calancie B.
Motor unit forces and recruitment patterns after cervical spinal cord injury.
Muscle Nerve
20:
212-220,
1997.
31.
Thomas, CK,
Tucker ME,
and
Bigland-Ritchie B.
Voluntary muscle weakness and co-activation after chronic cervical spinal cord injury.
J Neurotrauma
15:
149-161,
1998.
32.
Thomas, CK,
and
Westling G.
Tactile unit properties after cervical spinal cord injury.
Brain
118:
1547-1556,
1995.
33.
Thomas, CK,
Zaidner EY,
Calancie B,
Broton JG,
and
Bigland-Ritchie B.
Muscle weakness, paralysis and atrophy after human cervical spinal cord injury.
Exp Neurol
148:
414-423,
1997.
This article has been cited by other articles:
![]() |
C. J. Mottram, K. S. Maluf, J. L. Stephenson, M. K. Anderson, and R. M. Enoka Prolonged Vibration of the Biceps Brachii Tendon Reduces Time to Failure When Maintaining Arm Position With a Submaximal Load J Neurophysiol, February 1, 2006; 95(2): 1185 - 1193. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. K. Floeter, P. Zhai, R. Saigal, Y. Kim, and J. Statland Motor Neuron Firing Dysfunction in Spastic Patients With Primary Lateral Sclerosis J Neurophysiol, August 1, 2005; 94(2): 919 - 927. [Abstract] [Full Text] [PDF] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |