perturbation of a skilled action 2. normalising the responses of cerebral palsied individuals

Human Movement Science 6 (1987) 133-159

North-Holland

133

PERTURBATION OF A SKILLED ACTION 2. NORMALISING THE RESPONSES OF CEREBRAL PALSIED INDIVIDUALS *

Ann HARRISON and Roy KRUZE

Kuwait University, &fat, Kuwa~i

Harrison, A. and R. Kruze, 1987. Perturbation of a skilled action 2. Normalising the responses of cerebral palsied individuals. Human Movement Science 6, 133-159.

Subjects were trained to execute a radial elbow extension of prescribed arc and velocity profile. A

DC servomotor was used to introduce brief perturbations, opposing extension. Neurologically

normal and cerebral palsied subjects’ reactions to a range of perturbation magnitudes were tested.

The training stage of the study was designed to provide cerebral palsied subjects with an

electromyographic target profile of how to respond to a given perturbation, modelled on the

performances of neurologically normal subjects, but taking account of individual differences in

how non-perturbed arm swings were executed electromyographically. In the event, spastic subjects

were not hyperreactive to perturbations when tested. A follow-up study confirmed the interpreta-

tion that this was a consequence of learning to perform the test arm swing with stringent

precision. The implications of the study for models of spasticity and prospects for rehabilitation

are discussed.

Introduction

Spastic cerebral palsy is characterised clinically by exaggerated reflexes, abnormal muscle tone and alpha motoneurone hyperactivity (Dimitrijevic and Nathan 1967a and b; Jansen 1962; Lance and Burke 1974; Lord 1984; Roberts 1974). At one stage, abnormal fusimotor

* The work reported in this paper formed part of a research program supported by the National

Fund for Research into Crippling Diseases, U.K. (grant 421700) and was carried out at the Dept.

of Psychology, Sheffield University, England. Dr. Kruze was supported by a research studentship

from the Science Research Council. We are indebted to Dr. Chris Brown for his electronic and computing skills, and to our subjects for their patience and interest. Preparation was supported by

Kuwait University Grant MC015.

Mailing address: A. Harrison, Dept. of Community Medicine and Behavioural Sciences,

Faculty of Medicine, Kuwait University, P.O. Box 24923 (Safat), 13110 Safat, Kuwait.

0167-9457/87/$3.50 0 1987, Elsevier Science Publishers B.V. (North-Holland)

134 A. Harrison, R. Kruze / Normalising perturbation responses

drive was thought to be a prime defect, but Burke (1983) argues convincingly that this is not so. Myklebust et al. (1982) believe that reciprocal excitation of antagonist muscles is a defining feature of congenital spasticity. A wide range of procedures, including monitoring of active and passive movements, postural correction and dorsal root stimulation, have revealed abnormal antagonist coactivity (Barolat- Romana and Davis 1980; Knutsson and Martensson 1980; Milner- Brown and Penn 1979; Nashner and McCollum 1985). Congenital central lesions may well interfere with normal maturation and development, resulting in the retention of ‘primitive’ spinal pathways and the development of ‘abnormal’ ones (Bobath 1966). Excessive antagonist activity has been taken to indicate developmental immaturity (Thelen 1985). Other researchers have attributed abnormally high levels of antagonist activity to the movement correction modes, strategies and settings used (Nashner and McCollum 1985; Saltzman and Kelso 1985). Nashner et al. (1983) speculate that exaggerated stretch reflexes are the result of abnormal co-ordination patterns, rather than being their cause. Modern recording techniques, such as microneuronogra- phy, have revealed the extremely complex functioning of spinal interneuronal networks, and their importance in controlling the interplay of antagonist and synergistic muscles (Harrison and Jankowska 1985; Harrison and Johannisson 1983; Harrison and Taylor 1983). This has opened up the prospect of designating precisely how segmental functioning and supraspinal modulation are affected in the cerebral palsied system, and of linking abnormalities to the precise location of the central lesion and its onset during development. Rowlandson and Stephens (1985) point out that not only can supraspinal abnormalities interfere with spinal development, but that movement abnormalities may interfere with future central development, just as abnormal visual experience has been shown to prevent normal tuning of visual cortical cells (Blakemore and Van Sluyters 1975). Work with genetically spastic mice indicates that the growth of affected muscles is abnormal (Ziv et al. 1984). This may well ,affect the power balance of antagonist pairs, the biomechanical properties of joints, and the limb’s capacity for absorbing and storing energy and responding to stretch. Marked imbal- ances in antagonist strength can result in position preferences and fixed deformities (Fulford and Brown 1976) which represent further imped- iments to normal, skilful control. The spastic cerebral palsied syndrome is complex, and much remains to be discovered about which supraspi-

A. Harrison, R. Krure / Normalisingperturbafion responses 135

nal and segmental pathways function abnormally, how these contribute to the functional problems patients display, and which sensory and motor dysfunctions can be remedied or functionally compensated.

In a previous study (Harrison and Kruze 1987) we contrasted the reactions of neurologically normal and spastic individuals to perturbations imposed while a skilled radial arm swing was being executed. Spastic subjects were less able ‘ to ride’ a disturbance and safeguard the planned action. Relatively small opposing forces severely disrupted movements, leaving the subject incapable of continuing. Abnormal antagonist involvement and clonus were commonly observed. While spastic individuals displayed less consistency in their responses to stretch, integrated EMG and movement parameters varied systematically with the magnitude of the perturbation and seem to offer a basis for accurately monitoring such disruptions. Generally, cerebral palsied subjects were more reactive electromyographically, but comparisons were problematic because factors such as electrode placement can affect recorded activity. A major hindrance when contrasting the stretch responses of cerebral palsied and neurologically normal subjects stems from the fact that agonist EMG activity was consistently elevated in spastic subjects even for non-perturbed trials. This is to be expected when there is coactivation of the antagonist, for agonist activity must be powerful enough to both counter antagonist activity and effect the desired arm swing. Extra EMG activity has been shown to prime reflex responses (Dufresne et al. 1978; Hallett et al. 1981), and so cerebral palsied subjects might be expected to be excessively responsive to imposed displacements (Gydikov et al. 1981). Furthermore, coactivation may well alter the biomechanical characteristics of the limb, its capacity for absorbing and storing energy, and the movement characteristics seen when opposition is released (Allum et al. 1982; Pinelli 1981).

Ebner et al. (1982) studied the reactions of spastic monkeys to stretch perturbations, and were able to reproduce the clinical features of stiffness, hyperreflexia, and abnormal patterns of antagonist cocontraction. Cerebellar stimulation enstated more normal functioning: increasing compliance, reducing hyperreflexia, and increasing reciprocal co-ordination. This is encouraging, both because it evidences in the monkey preparation a potential for improvement and because the experimental procedure was able to mirror clinical designations. The latter is not always so. Sometimes, patients who are very different

136 A. Harrison, R. Kruze / Normalisingperturbation responses

in clinical assessment terms are not distinguished by experimental indices (Sanes and Evarts 1985). Double-blind studies with human patients have not provided reliable evidence of clinical improvement with cerebellar stimulation (Penn et al. 1980; Whittaker 1980), but species differences may play a role.

Neilson and McCaughey (1982) investigated the capacity of ‘predominantly spastic’ individuals to learn to modulate tonic stretch reflexes. The subject was provided with two meters, one indicated muscle contraction level and the other reflex responsiveness. Passive, sinusoidal elbow movement was used to provoke tonic stretch reflexes. After a year of regular training, subjects were able to vary reflex responsiveness considerably. As training progressed, uncontrolled spasms became less frequent, and subjects were able to suppress resting tonic stretch reflexes. Only two subjects were studied, and so the results must be interpreted cautiously. Very little improvement in tracking performance was seen following training. A lack of carry-over is not unexpected, however, given the different task demands of active and passive movements (Knutsson 1983; Knutsson and Martensson 1980).

Experimental design

The aims of the current study were to contrast the reactions of cerebral palsied and neurologically normal subjects to stretch perturbations introduced while they are performing a precisely controlled voluntary arm swing, and to investigate whether spastic individuals can learn to alter their responses to imposed stretches. Valid subject comparisons depend on training individuals to execute thoroughly equivalent actions, controlling variables such as impact velocity and programmed arm displacement. Various approaches to improvement are evident in the rehabilitation literature: normalisation of activity, sub- stituting a different mechanism for one which is defective or non-functional, learning to avoid situations which trigger or exacerbate abnormal functioning (Caplan 1982). The aim of the current study was for cerebral palsied subjects to learn to generate an electromyographic response to a given perturbation possessing the global characteristics of that produced by a neurologically normal performer under the same circumstances. The procedure involves modelling a neurologically normal subject’s reaction to each of the perturbations tested. Integrated

A. Harrison, R. Kruze / Normalisingperfurbation responses 137

electromyographic (EMG) activity is sampled every 3 msec during a trial. Point by point, performance of the average non-perturbed and the average perturbed trial (for a fixed opposing force) are compared. A multiple of 1.0 indicates that EMG activity is identical at a given instant for the perturbed and non-perturbed profile. A multiple greater than 1.0 indicates that perturbed trial EMG activity is greater, a multiple less than 1.0 reveals that perturbed trial EMG is lower. A multiplier model, consisting of the multiples computed for consecutive samples during a trial, is derived for each perturbation magnitude. A model of normalised performance for each perturbation size (a normalised perturbation profile) is then derived for each cerebral palsied subject by multiplying the spastic subject’s own non-perturbed trial EMG profile by a multiplier model generated by a neurologically normal subject. The spastic subject’s non-perturbed performance is used to compensate for irrelevant subject differences, such as those arising from differences in electrode placement. Precedents exist for this approach (Lee and Tatton 1975; Lenz et al. 1983; Marsden et al. 1976; Mortimer et al. 1981). During training, the cerebral palsied subject is provided with feedback contrasting his/her performance with the normalised perturbation profile target.

A 4-stage training and testing program was devised. During stage 1, neurologically normal and cerebral palsied subjects learn to execute the test action with stringent precision. The subject’s right arm is firmly attached to an arm board which swings freely in a horizontal plane around a pivot point beneath the elbow. Using elbow flexion and extension, the subject is able to generate to and fro radial arm swings. Subjects are prevented from viewing their arm. A mechanical block indicates the starting point, and the subject’s task is to learn to execute an elbow extension of specified arc and velocity profile. An oscillating target box, presented on an oscilloscope screen, indicates when the action should commence and end. Subjects are required to execute the specified extension in synchrony with the target. Stringent precision is insisted on so that differences in impact velocity and action profile can be ruled out as contributing to any subject differences observed (Dufresne et al. 1978). In an earlier study (Harrison and Kruze 1987), the majority of cerebral palsied subjects achieved acceptable skill performing repeated, successive, rhythmical elbow and flexion elbow movements. A single sweep was selected for the current study in order to avoid any conflict between correcting the perturbed swing and

138 A. Harrison, R. Kruze / Normalising perturbanon responses

safeguarding the next. When perturbations were introduced in the present experiments, subjects were asked to execute the disturbed extension as nearly as possible as planned, permitting adequacy of compensation to be unambiguously assessed. Another potential disad- vantage of a repeated to and fro arm action arises if the prescribed arc is consistently foreshortened or extended. This can systematically shift the start point of a phase, varying the distance traversed before the perturbation is encountered. In the current study, a mechanical block controlled the start point, and perturbations were introduced 30 o after. During stage 2, the responses of neurologically normal and cerebral palsied subjects to stretches of different magnitudes are measured. Selection of which trials to perturb and what opposing force level to use are under computer control. Subjects are, therefore, prevented from predicting whether a trial will be perturbed, and adjusting their performance accordingly. During stage 3, spastic subjects are divided into pairs, an experimental subject who receives normalisation training and a control subject who experiences precisely the same number of perturbation trials as the experimental subject he is yoked to but without feedback. As already described, the experimental subjects’ task is to adjust their performance of perturbed trials to match the normalised profile provided. During stage 4, the responses of spastic subjects to perturbations are tested once more, in order to assess the efficacy of the stage-3 training provided to the experimental group. If training is effective, the responses of the experimental spastic group should evidence less disruption than those of control subjects.

Throughout stages 3 and 4, non-perturbed trial performance precision must be maintained. This is to prevent subjects reducing stretch responsiveness by adopting programming strategies which are antitheti- cal to skilful execution of the prime action, e.g., unloading the spindle, curbing alpha motoneurone activity prior to impact, or marshalling excessive antagonist activity to cushion stretch. To be successful, any change must permit the set action to be executed with high precision and enable perturbations of unpredictable size and onset to be re- sponded to in a more normal fashion. Normalisation of alpha motoneurone responsiveness, of spindle output or antagonist cocontraction, better evaluation of afferent error signals, or a more rapid deployment of EMG updates are the types of adjustment which should lead to improvements in the specific context set and should generalise to better movement control. In designing the training proce-

A. Harrison, R. Krure / Normalismgperturbation responses 139

dure, a major aim was to minimise artificiality (Landau 1974). The action required was a standard elbow extension, and the subject’s task was to learn to deal effectively with interruptions.

Subjects and apparatus

Two right-handed students, one male (Nl, aged 25) and one female (N2, aged 25), with no known neuromuscular impairment formed the normal group. The spastic experimental group consisted of two congenital quadriplegic males. Se1 (aged 21) is able to walk independently, has skilful control over his right arm, is employed at a sheltered workshop, and had participated in earlier studies. Se2, a student (aged 25), is unable to stand or walk independently, he uses his right arm for tasks such as eating, and his left for gross supporting functions. The spastic control group likewise comprised one naive and one experienced subject. Scl, a spastic quadriplegic male (aged 21), is able to walk independently. He has skilful control over his right arm, and was employed doing manual factory work. Sc2, a congenital quadriplegic female (aged 25) is unable to stand or walk independently. She uses her right arm for tasks such as eating, and her left for gross supporting functions. She was employed at a sheltered workshop, and had participated in earlier studies.

The arm board apparatus, the servomotor used to generate variable torque opposition, and the electromyographic and movement recording systems employed are detailed elsewhere (Harrison and Kruze 1987). The target was a 0.5 Hz, 72” radial arm swing with a symmetrical velocity profile about a mid-cycle peak of 150 deg/sec. The action was selected because it could be repeated comfortably many times, and yet was forceful enough to generate discernable changes with the range of perturbations used.

Stage I: Training

Procedure By passively moving the subject’s arm, the experimenter demon-

strated the action required and how to interpret the feedback provided. Training proper began with a period of tracking. A 0.5 Hz oscillating square formed the target, while a second beam of the oscilloscope registered the subject’s elbow movement. The subject’s task was to pick


RMS error=16

I

An arm swing anticipating

the target.

L

::

2 RMS error=21

5 E An arm swing lagging d .;

._ behind the target.

I; a 3 <

RMS error=4

An almost perfect

performance.

Time w

Fig. 1, Position error trace and RMS error score, providing performance feedback during stage 1.

up the square on a clockwise phase, and try and keep the ‘stick’ (indicating his movement) within the target square. A physical block marked the start position. At the end of each trial, post hoc feedback in the form of a position error profile and RMS error score appeared on a subsidiary screen (fig. 1). Subjects completed 50 trials with both continuous and post hoc feedback. During subsequent trials, only the target trace was visible, but post hoc feedback was provided. Training was terminated when a subject generated 10 consecutive arm swings with a mean error score of 12 or less (equivalent to a constant positional error of 2” ).

Results All six subjects attained the specified proficiency. Spastic subjects

generally needed more time (table 1). They spent longer resting between blocks, and took up to 10 hrs to complete training. Subjects Se1 and Sc2 had taken part in earlier studies (Harrison and Kruze 1987), and reported that the to and fro arm swing set previously was easier. This is supported by the fact that they were no quicker at reaching criterion than the naive spastic subjects.

A. Harrison, R. Krure / Normalising periurbation responses 141

Table 1

Total number of trials taken to reach criterion performance.

Normal group

Spastic experimental group

Spastic control group

Nl 133

N2 253

Se 1 293

Se 2 257

SC 1 366

SC 2 332

Stage 2: Perturbation reactions

Procedure Subjects were asked to perform the arm extension learned in stage 1,

repeatedly and without feedback. Subjects knew that sometimes they would encounter temporary opposition, and that this would vary in magnitude. Their task was to complete the elbow extension as nearly as possible as planned. Four magnitudes of perturbation (1.0, 2.0, 3.0 and 4.0 amp, duration 100 msec) were investigated, using the method previously described (Harrison and Kruze 1987). During a test block, each perturbation was tested once, order being randomised. Perturbed trials were randomly dispersed among 40 non-perturbed trials, one of which was selected at random to represent non-perturbed performance for that block. Ten blocks of trials were completed, furnishing an EMG profile and movement data for 10 examples of each perturbation magnitude and 10 non-perturbed trials.

Results Good consistency of performance between and within subjects was

achieved (table 2). Measures of length, impact velocity and peak velocity indicated that subjects had retained the precision achieved during training. Contrasted with the target arc of 72”, Nl was on average 8” long, Se2 and Sc2 were 5 o short, while N2, Se1 and Scl were within 2’. Velocity at impact ranged from 228-247 units, less than 20 deg/sec. The total EMG recorded for non-perturbed trials varied considerably from subject to subject, differences in electrode placement may have played some role. Spastic subjects tended to produce greater EMG activity, which is consistent with antagonist coactivity.

Tab

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2

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8.9

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9.8

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144 A. Harrison, R. Krure / Normalising perturbation responses

Amplitude of 100 mser

perturbation (amps).

Fig. 4. Percent increments in total trial EMG (100 x [perturbed - non-perturbed]/non-perturbed) recorded during stage 2 (mean of 10 trials).

separation of spastic and normal subjects is apparent. The performances of spastic subjects during stage 2 did not differ radically from normal. Clonus was seldom observed, and the highly disrupted responses which had marked the performance of Se1 and Sc2 in previous studies were not seen. Except for Scl, as stretch magnitude increased, EMG and movement indices rose monotonically. The divergent performance of Scl was attributed to his use of a ‘rolling’ arm swing, involving predominantly shoulder movement rather than biceps and triceps activity. When this was rectified, ‘normal’ sharp perturbation reactions were observed. Unfortunately, he found it uncomfortable to perform for long using this action. The electrode placements used were, therefore, not optimal to detect stretch responses for Scl.

Stage 3: Normalising responsiveness

Procedure A specially-written computer program derived a ‘multiplier model

relating the average EMG profile for a given perturbation magnitude and the average EMG profile of non-perturbed trials. The multiplier model was based on samples taken every 3 msec during a trial. A set of multiplier models (one for each magnitude of perturbation) was computed for both normal subjects. A normalised perturbation profile for each of the 4 perturbation magnitudes was then derived for each

A. Harrison, R. Kruze / Normalising perturbation responses 145

spastic experimental subject. The averaged EMG profile of 10 accurate non-perturbed trials recorded at the start of stage 3 served as baseline. The baseline was point by point multiplied by a ‘multiplier model’. The projected course of training was to provide an Se subject with feedback contrasting his performance of perturbed trials with a normalised perturbation profile. Feedback was to be given as in stage I, together with a check on impact velocity.

Results

When spastic subjects’ performances were compared with the derived normalised perturbation profiles, it emerged that they were already less reactive (fig. 5). Not by virtue of stage 3 training or

Normalised Perturbation Profiles

2 amp, 100 msec perturbation performance based on Nl

4 amp, 100 msec perturbation

smance based on Nl

Feedback

RhlS EhlG error=13 Impact Velocity error=3

RhlS EhlG error=17

Impact Velocity error=-21

RhlS EhlG error=27

Impact Velocity error=21

Deviation of

KEYS recorded EMG

from normalised Normalised

Response

(integrated EMG units) T

perturbation profile

(integrated tl -...____ time EMG units) ______.time

Fig. 5. Normalised perturbation profiles for Se1 during stage 3, and computed electromyographic and impact velocity errors recorded when his performances were contrasted with the target.

146 A. Harrison, R. Krure / Normahsing perturbation responses

contemporary adjustments to motor programming, but because spastic subjects were differentially less responsive by the end of stage 2.

Discussion

Spastic subjects were able to achieve and maintain great precision in executing the radial arm action set. It proved more difficult than the to and fro arm swing employed previously (Harrison and Kruze 1987). Subjects had to begin the action precisely with the target, reproduce the velocity profile set, and finish on time having completed the arc specified. Overcoming inertia was a key problem reported by spastic subjects. Task precision was essential so that inter-subject velocity differences would be minimised, and comparisons valid. In the event, when normal and spastic subjects’ performances were compared, there was no evidence of hypersensitivity to stretch. This contrasts with the finding of our earlier study, in which stretch displacements proved very disruptive to spastic performers, and clonus episodes were common.

The normalised perturbation profile presupposes that when baseline EMG activity is elevated, response to a perturbation will be magnified by a similar degree. This is consistent with previous studies (Lee and Tatton 1975; Lenz et al. 1983; Marsden et al. 1976; Mortimer et al. 1981). In normal subjects, the effect of shifting baseline can be compared to working against a greater opposing force. In spastic individuals, the effect of antagonist coactivation may be different. There may be an elevation in prime muscle activity without any boost in stretch responsiveness. It seems very probable that coactivation alters the physical properties of a limb in ways not seen when there is equally high, but isolated, agonist activity. Because of the high performance reliability achieved, peak EMG activity was well preserved in the averaged profiles computed. Any tendency to average out extremes would be expected to diminish the spastic-normal differential. By the same token, however, peaks produced in individual attempts during stage 3 would be more pronounced than in the averaged normalised perturbation profile. The observation that single trial EMG output was consistently below target during stage 3, therefore, reinforces the claim that spastic subjects were not reacting excessively to stretch displacements. It is possible that in order to succeed at stage 1, spastic subjects had to normalise motor programming and responsiveness. That is, the


very stage of the training programme which was designed to quantify group differences may have acted to destroy them.

Investigating the effects of task training

The current study was designed to test the hypothesis that reactivity to stretch diminishes as a consequence of achieving skill in performing the test arm action. The spastic subject selected had taken part in an earlier study (Harrison and Kruze 1987), but his execution of the backward and forward radial arm swing used for testing proved too variable for his stretch responses to be averaged meaningfully. Even low amplitude displacement forces greatly disrupted the action in progress, often leaving him unable to complete the phase interrupted. Clonus episodes were common. The subject is a congenital quadriplegic male, aged 22. He walks awkwardly with assistance and is employed at a sheltered workshop. His right limbs are the most severely affected, he uses his right arm only for gross supporting functions and his left for tasks such as eating. Great difficulty was experienced manipulating the subject’s arm into the arm cradle, passive movement provoked strong opposing contractions.

Procedure

The experimenter began by demonstrating the start and finish points of the arm swing, using passive positioning. The 0.5 Hz oscillating box target already described provided the subject with an index of when to begin and finish an action. When the subject was producing actions of approximately the correct timing and arc, testing was instigated.

Pre-training perturbation responsiveness The subject completed blocks of non-perturbed and perturbed trials

as described in stage 2 above. In the preceding experiment, impact velocity for trained subjects ranged from 228-247 units. It was, therefore, decided to accept for analysis any action with an impact velocity between 200 and 260 units. If impact velocity was outside this range, a trial was not stored. Rests were taken between blocks. After 4 hrs, the subject had produced 5 acceptable examples of each of the four perturbation amplitudes. It was originally intended to sample ten of each, but continuation was considered unjustified.


Task training and retesting The subject was exposed to precisely the same schedule described in

stage 1 above. At the beginning, the subject often complained of problems ‘making his arm go’, overcoming inertia and mirroring the target profile. He spent more than 20 hrs in training, but never achieved the criterion set. On a number of occasions he got very close, but a run was spoiled by one deviant trial. Very accurate movements with RMS error scores of 4 or 5 were common towards the end. Training was terminated when further improvement was considered unlikely. The subject was highly motivated, and his execution of the set action was far less impaired and more accurate than at the beginning. Instances of clonus were rare. His failure to meet criterion was due to occasional inaccurate responses, and reflects the stringency of the criterion set. After training, perturbation responses were tested as before.

Results

Pre- and post-training performance of non-perturbed trials (table 3) indicate that, in terms of length and impact velocity, actions were comparable. After training, there was a dramatic decrease in the total amount of EMG activity recorded during both perturbed and non-perturbed trials (table 3). This is evident in both absolute and percentage increments (fig. 6). Inspection of typical single trials (fig. 7) confirms that EMG and peak velocity responses were lower after training. Before training, perturbations proved highly disruptive, often preclud- ing completion of the action. After training, the subject was able to complete the execution of an arc following perturbation, and clonus episodes were very rare. Both before and after training, increasing the magnitude of the perturbation increased the peak EMG response (fig. 8).

Discussion

Task training dramatically altered responsiveness, and there was a general reduction in the EMG activity generated during perturbed and non-perturbed trials. Electrode placement differences may have played some role, but given the concomitant changes in movement indices, genuine reductions in muscle activity are indicated. Before and after

Tab

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3

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150 A. Harrison, R. Krure / Normalising perturbahn responses

Amplitude of 100 msec

perturbation (amps)

!! : : : : pre-

: : : :

training

: : : : :.

i :**

;i .’

0. .-

.*.a post-

training

Amplitude of 100 msec

perturbation (amps) .

Fig. 6. Absolute and percent increments in total trial EMG recorded before and after training.

training, peak EMG was positively correlated with perturbation magnitude. It is fascinating that, in percentage terms, peak EMG was differentially more affected by changes in perturbation magnitude after

Before training

I amp, 100 msee perturbation

-_

After training

2 amp, 100 msec perturbation

-_

I

100 msecs

impact velocily=239 units impact velocily=210 units

3 amp, 100 msec perturbation 4 amp, 100 mscc perturbation

KEY

Torque - on -time

+ve

Velocity I___._ .._..._ -time

-ve . . . . . . . . . . . . ..1.--..-

impact velocity=2lS uoits Integrated EMG I_____ -___ -.--time impact velocity=200 units

Fig. 7. Velocity and integrated EMG profiles of perturbed trials, before and after training.

A. Harrison, R. Krue / Normalising perturbation responses 151

70 pre- training

50 /-=

.a

$30 ,?- E L- ; 10

*-i post- training

w

w 12 4 G 2 Amplitude of 100

5 !3 i

z perturbation (amps). z ‘Z E

Fig. 8. Absolute and percent increments in

post-

?-..

training

5 /‘

:

$ 3 '.I'- _L t'*

2 pre_ training

:’ w

1 34 & 2 Amplitude of 100 msec

!I 2

perturbation (amps)

‘Z peak EMG recorded before and after

training, just as neurologically normal subjects emerged as differentially more affected than cerebral palsied subjects in the preceding study (Harrison and Kruze 1987). The data support the hypothesis that training renders spastic performance more normal, by reducing prime muscle activity and eliminating excessive antagonist involvement.

Overview

The studies carried out indicate that spastic subjects have a capacity for achieving skilful movement control when provided with suitable feedback, and that this experience contributed to ‘normalising’ their reactions to imposed displacements. As reported previously (Harrison and Kruze 1987), short latency EMG components correlated positively with the magnitude of the perturbation, and offer a possible basis for accurately monitoring disruptions. After training, subjects accommod- ated well to a range of displacements, even though the magnitude and onset of such perturbations were unpredictable. In our earlier study, functional compensation was attributed mainly to the biomechanical responses of the limb to impact, and voluntary updating of EMG activity. Short latency EMG components were observed to provide little power (Milner-Brown and Stein 1975). When spastic subjects performed non-perturbed trials after training, an overall reduction in EMG activity was observed, suggesting that antagonist activity had been curbed. In principle, lowering prime muscle activity could reduce


stretch responsiveness (Dimitrijevic and Nathan 1967a and b) and alter the biomechanical properties of the limb. Reductions in stretch responsiveness are not evident. In terms of percentage increment, neurologically normal subjects were more responsive than spastic individuals, and the spastic subject tested was more responsive after he improved his skill at executing the set arm swing. It is plausible that improperly controlled antagonist activity was an important source of error prior to training: jeopardising the prime movement and com- plicating proprioceptive monitoring. Excessive coactivity may also force the use of primitive or inefficient compensatory mechanisms (Nashner and McCollum 1985). In addition, antagonist activation may act to prime agonist alpha motoneurones, rendering them more responsive to peripheral inputs (Dufresne et al. 1978). Excessive cocontraction would make it difficult to begin the prime action, just as subjects reported, and would produce the jerkiness and clonus observed. Suppression of antagonist activity should increase compliance (Dufresne et al. 1978; Ebner et al. 1982), and may greatly alter biomechanical responsiveness to stretch. Even though peak EMG is elevated, the individual’s capacity to instigate controlled deceleration is also enhanced (Harrison and Kruze 1987). Furthermore, the subject’s ability to decipher afferent signals and decide what EMG update is appropriate will be simpler if antagonist contributions vary only in a controlled, predetermined fashion. Neurologically normal individuals regulate antagonist activity to smooth and brake agonist output. The very skilful responses which spastic subjects dispiayed after training suggest that antagonist activity was used (Lamarre et al. 1981). Indeed, it would be undesirable to encourage the adoption of motor programs which eliminate counter control. Some cerebral palsied patients are dependent on antagonist coactivity to generate sufficient stabilisation of a joint to permit mobility (Young and Delwaide 1981). Various researchers have investigated the interplay of agonist and antagonist activity in skilled actions, and the characteristic burst patterns reported could provide a basis for assessing the ‘normality’ of a performance and what provi- sions have been made for updating the action (Angel 1974; Brown and Cooke 1981; Hallett 1979; Hallett and Marsden 1979; Hallett et al. 1975; Sanes and Jennings 1984).

In the current study, excessive antagonist activity, rather than prim- ing reflex responsiveness, reduced the stimulus differential. Interpreta- tion of this is not clear. It may be that the perturbation forces


introduced were relatively small compared with the opposing force of the antagonist, or that the corrective mechanisms were operating at less than maximal efficiency (Jansen 1962). Based on the power of the perturbations used to disrupt the arm swings of naive subjects, the former does not seem likely. In models of skilful gamma-alpha coactivation, gamma efferent activity is modulated to counter spindle unloading and maximise proprioceptive information (Matthews 1981; Phillips 1969). It is reasonable that as skill increases, responses will become better differentiated (Cooke 1980). Experiments employing pseudo-random pulsing of maintained postures have also shown that as voluntary EMG activity increases, the gain of stretch responses increases, but sensitivity decreases (Dufresne et al. 1978). These changes were attributed to alterations in fusimotor drive.

Major difficulties are encountered when trying to evaluate the implications of the changes in performance achieved following training. Much remains to be discovered about the contributions of different abnormalities in the spastic syndrome, and ways of differentiating for B particular patient which components are functioning normally and which are aberrant. The contributions of different receptors, supraspinal and segmental pathways, efferent and afferent systems have yet to be fully described (Bawa and McKenzie 1981; Burke 1980; Hagbarth et al. 1973; Hagbarth et al. 1975; Jaeger et al. 1982b; Seguin and Cooke 1983; Vallbo et al. 1979; Yap 1967; Young and Delwaide 1981); and also the precise functional impacts, and potential for normalisation or compensation, of the various motor and sensory anomalies differentiated (Connolly and Harrison 1976; Herman 1973; Jones 1976; Sanes and Evarts 1983; Sanes et al. 1984; Tardieu et al. 1984). When a more normal performance is achieved, this cannot be presumed to be created by normalisation of components. Rather, the individual may be producing a more normal output by highly unorthodox means, e.g., using descending activity to mimic spinal contributions or to counter segmental hyperactivity. However segmental hyperactivity is countered, normal functioning which was previously precluded by it (e.g., reciprocal inhibition) is likely to be evidenced (Mizuno et al. 1971; Smith 1981; Young and Delwaide 198.1). Even with the ostensibly simple task currently studied, changes in strategy and changes in motor programming were difficult to separate. When movement parameters are less rigorously controlled, and task aims (e.g., what constitutes a perfect correction) are more ambiguous (Brown and Cooke 1981; Jaeger et al.


1982a; Marsden et al. 1976), parsing component contributions will be even more problematic.

Vibration-induced contraction could be used to simulate abnormal antagonist activity, but this procedure also affects receptor output (Jaeger et al. 1982b; Matthews 1982; Matthews et al. 1982; Matthews and Watson 1981). A purer approach would be to develop an artificial antagonist muscle, attached to the tendons and remotely variable in length. The impact of regulated counter forces on agonist function could then be investigated. Such a preparation is artificial in terms of missing any proprioceptive output or interneuronal control of coactivity, but parsing the contribution of physico-mechanical characteristics to limb responsiveness is worthy of further study (Wieneke and Denier van der Gon 1974). Pharmaceutical modulation offers another approach for studying what changes underlie the improvements achieved. Various studies have used glycine administration in an attempt to boost post-synaptic inhibition which is thought to be deficient in spastic muscles (Burke and Ashby 1972; Werman et al. 1968). The action of glycine is not necessarily limited to post-synaptic inhibition (Pycock and Kerwin 1981); but based on work with animals (Hall et al. 1979; Smith et al. 1979; Stern and Hadzovic 1970) and humans (Barbeau 1974; Stern and Bokonjic 1974) it may be worthwhile to study changes in performance after glycine treatment, particularly with patients where a genetic basis is indicated (Barbeau et al. 1982). Phenol is another agent which has been used with spasticity, selectively to block the gamma efferent (Pedersen and Juul-Jensen 1962). Diazepam and dantrolene, which are commonly used in the clinical management of spasticity, do not modulate enhanced stretch reflexes (Young and Delwaide 1981). Recently developed techniques, such as microneu- rography and intraneural microstimulation, however, would seem to offer the best prospect of tracing what patterns of inputs and outputs create abnormalities in the spastic system, and of describing what changes occur when functional improvements are achieved.

Congenital cerebral palsied spastic patients are a very heterogenous clinical group, but there are no obvious reasons to expect that the improvements achieved by subjects in the current study will prove atypical. The aim of rehabilitation is to provide subjects with training which will generalise to better everyday control. This is not claimed for the current study. No attempt was made to extend training and introduce everyday task demands. Recent work by Wolpaw (1985)


suggests that further improvement, of a nature which is likely to generalise to better everyday control, requires protracted training. His work with primates who were rewarded for enhancing or suppressing spinal stretch reflexes (Wolpaw and O’Keefe 1984) demonstrated that attenuation occurred in two phases. The first phase takes place during the first few hours of training, and is thought to be created by descending modulation. The second phase of attenuation takes many weeks to complete. It is characterised by a gradual shift in responsiveness, and is attributed to the development of persistent, inherent alterations in spinal functioning. Procedures need to be found to engineer comparable long-term tonic shifts for spastic cerebral palsied patients, in order to investigate their full potential for achieving gener- alisable improvements in segmental responsiveness. Although the current training stage which was designed to promote normalisation proved redundant, the general approach of deriving a target action model based on the gestalt of normal performance, but taking account of individual electromyographic differences, seems worth pursuing. The present study provides a further demonstration of spastic individuals’ potential for interpreting more effective sequences Harrison 1977).

References

afferent messages accurately and enstating of motor activity (Harrison 1975a and b;

Allum, J.H., K.-H. Mauri& and H.

reflexes in human triceps surae

Brain Research 48, 153-156.

Vogele, 1982. The mechanical effectiveness of short latency

muscles revealed by ischaemia and vibration. Experimental

Angel, R.W., 1974. Electromyography during voluntary movement: the two bust pattern. Electro-

encephalography and Clinical Neurophysiology 36, 493-498.

Barbeau, A., 1974. Preliminary study of glycine administration in patients with spasticity.

Neurology 24, 392.

Barbeau, A., M. Roy and C. Chouza, 1982. Pilot study of theonine supplementation in human

spasticity. Canadian Journal of Neurological Sciences 9, 141-145.

Barolat-Romana, G. and R. Davis, 1980. Neurophysiological mechanisms in abnormal reflex

activities in cerebral palsy and spinal spasticity. Journal of Neurology, Neurosurgery and

Psychiatry 43, 333-342.

Bawa, P. and D.C. McKenzie, 1981. Contribution of joint and cutaneous afferents to longer-latency reflexes in man. Brain Research 211, 185-189.

Blakemore, C. and T.C. van Sluyters, 1975. Innate and environmental factors in the development

of the kitten’s visual cortex. Journal of Physiology 248, 663-716.

Bobath, K., 1966. Motor deficits in patients with cerebral palsy. London: S.I.M.P. with Heine- mann.

156 A. Harrison, R. Kruze / Normalising perturbatm responses

Brown, S.H. and J.D. Cooke, 1981. Amplitude- and instruction-dependent modulation of move-

ment-related electromyogram activity in humans. Journal of Physiology 316, 97-107.

Brown, S.H. and J.D. Cooke, 1981. Responses to force perturbations preceding voluntary human

arm movements. Brain Research 220, 350-355.

Burke, D., 1980. ‘A reassessment of the muscle spindle contribution to muscle tone in normal and

spastic man’. In: R.G. Feldman, R.R. Young and W.P. Koella (eds.), Spasticity: disordered

motor control. Chicago, IL: Year Book.

Burke, D., 1983. ‘Critical examination of the case for and against fusimotor involvement in

disorders of muscle tone’. In: D.E. Desmedt (ed.), Motor control mechanisms in health and

disease. New York: Raven Press.

Burke, D. and P. Ashby, 1972. Are spinal ‘presynaptic’ inhibitory mechanisms suppressed in

spasticity? Journal of Neurological Sciences 15, 321-326.

Caplan, B., 1982. Neuropsychology in rehabilitation: its role in evaluation and intervention.

Archives of Physical Medicine and Rehabilitation 63, 362-366.

Connolly, K.J. and A. Harrison, 1976. ‘The analysis of skill and its implications for training the

handicapped’. In: D.V. Siva Sankar (ed.), Mental health in children, Vol. 3. New York: PJD

Publications.

Cooke, J.D., 1980. The role of stretch reflexes during active movements. Brain Research 181,

493-497.

DimitriJevic, M.R. and P.W. Nathan, 1967a. Studies of spasticity in man 1. Some features of

spasticity. Brain 90, l-30.

Dimitrijevic, M.R. and P.W. Nathan, 1967b. Studies of spasticity in man 2. Analysis of stretch

reflexes in spasticity. Brain 90, 333-358.

Dufresne, J.R., J.F. Soechting and CA. Terzuolo, 1978. Electromyographic response to pseudo-

random torque disturbances of forearm position. Neuroscience 3, 1213-1226.

Ebner, T.J., J.R. Bloedel, J.L. Vitek and A.B. Schwartz, 1982. The effects of cerebellar stimulation

on the stretch reflex of the spastic monkey. Brain 105, 425-442.

Fulford, G.E. and J.K. Brown, 1976. Position as a cause of deformity in children with cerebral

palsy. Developmental Medicine and Child Neurology 18, 305-314.

Gydikov, A., A. Kossev, N. Radicheva and N. Tankov, 1981. Interaction between reflexes and

voluntary motor activity in man revealed by discharges of separate motor units. Experimental

Neurology 73, 331-344.

Hagbarth, K.-E., G. Wallin and L. Lofstedt, 1973. Muscle spindle responses to stretch in normal

and spastic subjects. Scandinavian Journal of Rehabilitation Medicine 5, 156-159.

Hagbarth, K.-E., G. Wallin, L. Lofstedt and S.-M. Aquilonius, 1975. Muscle spindle activity in

alternating tremor of Parkinsonism and clonus. Journal of Neurology, Neurosurgery and

Psychiatry 38, 636-641.

Hall, P.V., J.E. Smith, J. Lane, T. Mote and R. Campbell, 1979. Glycine and experimental spinal

spasticity. Neurology 29, 262-267.

Hallett. M., 1979. Ballistic elbow flexion in patients with amytrophic lateral sclerosis. Journal of

Neurology, Neurosurgery and Psychiatry 42, 232-237.

Hallett, M. and C.D. Marsden, 1979. Ballistic flexion movement of the human thumb. Journal of

Physiology 294, 33-50. Hallett, M., M. Bielawski and CD. Marsden, 1981. Behaviour of the long-latency stretch reflex

prior to voluntary movement. Brain Research 219, 178-185.

Hallett, M., B.T. Shahani and R.R. Young, 1975. EMG analysis of stereotyped voluntary

movements in man. Journal of Neurology, Neurosurgery and Psychiatry 38, 1154-1162.

Harrison, A., 1975a. ‘Studies of neuromuscular control in normal and spastic individuals’. In: K.S. Holt (ed.), Movement and child development. London: S.I.M.P. with Heinemann.

Harrison, A., 1975b. ‘Training spastic individuals to achieve better neuromuscular control using

electromyographic feedback’. In: KS. Holt (ed.), Movement and child development. London:

S.I.M.P. with Heinemann.


Harrison, A., 1977. Augmented feedback training of motor control in cerebral palsy. Developmen-

tal Medicine and Child Neurology 19, 75-78.

Harrison, A. and R. Kruze, 1987. Perturbation of a skilled action 1. The responses of neurologi-

tally normal and cerebral palsied individuals. Human Movement Science 6, 37-65.

Harrison, P.J. and E. Jankowska, 1985. Sources of input to interneurones mediating group 1

non-reciprocal inhibition of motoneurones in the cat. Journal of Physiology 361, 3799401.

Harrison, P.J. and T. Johann&son, 1983. Segmental actions of afferents of the interosseous nerve

in the cat. Journal of Physiology 345, 373-389.

Harrison, P.J. and A. Taylor, 1983. Synaptic noise-triggered averaging as a technique for

investigating the origins of EPSPs. Brain Research 264, 316-319.

Herman, R., 1973. ‘Augmented sensory feedback in the control of limb movements’. In: W.S.

Field (ed.), Neural organisation and its relevance to prosthetics. New York: IMBC.

Jaeger, R.J., G.L. Gottlieb and G.C. Agarwal, 1982a. Myoelectric responses at flexors and

extensors of human wrist to step torque perturbations. Journal of Neurophysiology 48,

388-402.

Jaeger, R.J., G.L. Gottlieb, G.C. Agarwal and A.J. Tahmoush, 1982b. Afferent contributions to

stretch-evoked myoelectric responses. Journal of Neurophysiology 48, 403-418.

Jansen, J.K., 1962. Spasticity - functional aspects. Acta Neurologica Scandinavica 38 (suppl. 3)

41-51.

Jones, B., 1976. The perception of passive joint movements by cerebral palsied children. Develop-

mental Medicine and Child Neurology 18, 25-30.

Knutsson, E., 1983. ‘Analysis of gait and isokinetic movements for evaluation of antispastic drugs

or physical therapies’. In: J.E. Desmedt (ed.), Motor mechanisms in health and disease. New

York: Raven Press.

Knutsson, E. and A. Martensson, 1980. Dynamic motor capacity in spastic paresis and its relation

to prime mover dysfunction, spastic reflexes and antagonist co-activation. Scandinavian

Journal of Rehabilitation Medicine 12(3) 93-106.

Lamarre, Y., G. Spidalieri and G.R. Lund, 1981. Patterns of muscular and motor cortical activity

during a simple arm movement in the monkey. Canadian Journal of Physiology and Phar-

macology 59, 748-756.

Lance, J.W. and D. Burke, 1974. Mechanisms of spasticity. Archives of Physical Medicine and

Rehabilitation 55, 332-337.

Landau, W.M., 1974. Spasticity: the fable of a neurological demon and the emperor’s new therapy

(Editorial). Archives of Neurology 31, 217-219.

Lee, R.G. and W.G. Tatton, 1975. Motor responses to sudden limb displacements in primates

with specific CNS lesions and in human patients with motor system disorders. Canadian

Journal of Neurological Sciences 2, 285-293.

Lenz, F.A., W.G. Tatton and R.R. Tasker, 1983. The effect of cortical lesions on the electromyo-

graphic response to joint displacement in the squirrel monkey forelimb. Journal of Neurosci-

ence 3, 795-805.

Lord, J., 1984. Cerebral palsy: a clinical approach. Archives of Physical Medicine and Rehabihta-

tion 65, 542-548.

Marsden, CD., P.A. Merton and H.B. Morton, 1976. Servo action in the human thumb. Journal of Physiology 251, l-44.

Matthews, P.B., 1981. Evolving views on the internal operation and functional role of the muscle spindle. Journal of Physiology 320, l-30.

Matthews, P.B., 1982. Where does Sherrington’s ‘muscle sense’ originate? Muscles, joints, corollary discharge? Annual Review of Neuroscience 5, 189-218.

Matthews, P.B. and J.D. Watson, 1981. Effects of vibrating agonist or antagonist muscle on the

reflex response to sinusoidal displacement of the human forearm. Journal of Physiology 321,

297-316.

158 A. Harrison, R. Krure / Normalising perturbation responses

Matthews, P.B., P. Bawa and H.R. Matthews, 1982. Synchronisation of motor firing by vibration

during stretch evoked responses of the human wrist flexors. Experimental Brain Research 45,

313-316.

Mimer-Brown, H.S. and R.D. Penn, 1979. Pathophysiological mechanisms in cerebral palsy.

Journal of Neurology, Neurosurgery and Psychiatry 42, 606-618.

Milner-Brown, H.S. and R.B. Stein, 1975. The relationship between the surface electromyogram

and muscular force. Journal of Physiology 246, 549-569.

Mizuno, Y., R. Tanaka and N. Yanagisawa, 1971. Reciprocal group 1 inhibition on triceps surae

motoneurons in man. Journal of Neurophysiology 34, 1010-1017.

Mortimer, J.A., D.D. Webster and T.G. Dukich, 1981. Changes in short and long latency stretch

responses during the transition from posture to movement. Brain Research 229, 337-351.

Myklebust, B.M., G.L. Gottlieb, R.D. Penn and G.C. Agarwal, 1982. Reciprocal excitation of

antagonist muscles as a differentiating feature in spasticity. Annals of Neurology 12, 367-374.

Nashner, L.M. and G. McCollum, 1985. The organization of human postural movements: a

formal basis and experimental synthesis. The Behavioral and Brain Sciences 8, 1355172.

Nashner, L.M., A. Shumway-Cook and 0. Marin, 1983. Stance posture control in select groups of

children with cerebral palsy: deficits in sensory organization and muscular coordination.

Experimental Brain Research 49, 393-409.

Neilson, P.D. and J. McCa&hey, 1982. Self-regulation of spasm and spasticity in cerebral palsy. Journal of Neurology, Neurosurgery and Psychiatry 45, 320-330.

Pedersen, E. and P. Juul-Jensen, 1962. Intrathecal phenol in the treatment of spasticity. Acta

Neurologica Scandinavica 38 (suppl. 3), 69-77.

Penn, R.D., B.M. Myklebust, G.L. Gottlieb, G.C. Agarwal and M.E. Etzel, 1980. Chronic

cerebellar stimulation for cerebral palsy. Prospectives and double-blind studies, Journal of

Neurosurgery 53, 160-165.

Phillips, C.G., 1969. The Ferrier lecture, 1968. Motor apparatus of the baboon’s hand. Proceedings

of the Royal Society of London, Series B: Biological Sciences 173, 141-174.

Pinelli, P., 1981. Neurophysiologists’ and neuropsychologists’ views on motor efficiency and motor

initiation: clinical implications. European Neurology 20, 357-366.

Pycock, C.J. and R.W. Kerwin, 1981. The status of glycine as a supraspinal neurotransmitter. Minireview. Life Sciences 28, 2679-2686.

Roberts, E., 1974. Disinhibition as an organising principle in the nervous system. The role of gamma-aminobutyric acid. Advances in Neurology 5, 127-143.

Rowlandson, P.H. and J.A. Stephens, 1985. Maturation of cutaneous reflex responses recorded in

the lower limb in man. Developmental Medicine and Child Neurology 27, 425-433.

Saltzman, E. and J.A.S. Kelso, 1985, Synergies: stabilities, instabilities and modes. The Behavioral and Brain Sciences 8, 161-163.

Saws, J.N. and E.V. Evarts, 1983. Effects of perturbations on accuracy of arm movements.

Journal of Neuroscience 3, 977-986.

Sanes, J.N. and E.V. Evarts, 1985. ‘Psychomotor performance in Parkinson’s disease’. In: R.G.

Delwarde and A. Agnoli (eds.), Clinical neurophysiology in Parkinsonism. Amsterdam:

Elsevier.

Sanes, J.N. and V.A. Jennings, 1984. Centrally programmed patterns of muscle activity in voluntary motor behaviour of humans. Experimental Brain Research 54, 23-32.

Sanes, J.N., K.-H. Mauritz, E.V. Evarts, M.C. Dalakas and A. Chu, 1984. Motor deficits in

patients with large-fiber sensory neuropathy. Proceedings of the National Academy of Sciences of the United States of America 81, 979-982.

Seguin, J.J. and J.D. Cooke, 1983. The effects of cutaneous mechano-receptor stimulation on the

stretch reflex. Experimental Brain Research 52, 152-154.

Smith, A.M., 1981. The coactivation of antagonist muscles. Canadian Journal of Physiology and

Pharmacology 59, 733-747.

A. Harrison, R. Kruze / Normalisingperturbation responses 159

Smith, J.E., P.V. Hall, M.R. Galvin, A.R. Jones and R.L. Campbell, 1979. Effects of glycine

administration on canine experimental spinal spasticity and the levels of glycine, glutamate,

and aspartate in the lumbar spinal cord. Neurosurgery 4, 152-156. Stem, P. and R. Bokonjic, 1974. Glycine therapy in seven cases of spasticity. A pilot study.

Pharmacology 12, 117-119.

Stern, P. and S. Hadzovic, 1970. Effects of glycine on experimental hindlimbs rigidity in rats. Life

Sciences 9, 955-959.

Tardieu, G., C. Tardieu, A. Lespargot, A. Roby and M.D. Bret, 1984. Can vibration-induced

illusions be useful as a muscle perception test for normal and cerebral-palsied children?

Developmental Medicine and Child Neurology 26, 449-456.

Thelen, E., 1985. Simplifying assumptions: can development help? The Behavioral and Brain

Sciences 8, 165-166.

Vallbo, A.B., K.-E. Hagbarth, H.E. Torebjork and B.G. Wallin, 1979. Somatosensory, propriocep-

tive, and sympathetic activity in human peripheral nerves. Physiological Reviews 59, 919-957.

Werman, R., R.A. Davidoff and M.H. Aprison, 1968. Inhibitory action of glycine on spinal

neurons in the cat. Journal of Neurophysiology 31, 81-95.

Whittaker, C.K., 1980. Cerebellar stimulation for cerebral palsy. Journal of Neurosurgery 52,

648-653.

Wieneke, G.H. and J.J. Denier van der Gon, 1974. Variations in the output impedence of the

human motor system. Kybernetic 15, 159-178.

Wolpaw, J.R., 1985. Adaptive plasticity in the spinal stretch reflex: an accessible substrate of

memory? Cellular and Molecular Neurobiology 5, 147-165.

Wolpaw, J.R. and J.A. G’Keefe, 1984. Adaptive plasticity in the primate spinal stretch reflex:

evidence for a two-phase process. Journal of Neuroscience 4, 2718-2724.

Yap, C-B., 1967. Spinal segmental and long-loop reflexes in spinal motoneurone excitability in

spasticity and rigidity. Brain 90, 887-896.

Young, R.R. and P.J. Delwaide, 1981. Spasticity. New England Journal of Medicine 304, 28-33

and 96-99.

Ziv., I., N. Blackbum, M. Rang and J. Koreska, 1984. Muscle growth in normal and spastic mice.

Developmental Medicine and Child Neurology 26, 94-99.

perturbation of a skilled action 2. normalising the responses of cerebral palsied individuals

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