perturbation of a skilled action 1. the responses of neurologically normal and cerebral palsied...

Human Movement Science 6 (1987) 37-65

North-Holland

31

PERTURBATION OF A SKILLED ACTION 1. THE RESPONSES OF NEUROLOGICALLY NORMAL AND CEREBRAL PALSIED INDIVIDUALS *

Ann HARRISON and Roy KRUZE Kuwait University, Safat, Kuwait

Harrison, A. and R. Kruze, 1987. Perturbation of a skilled action 1. The responses of neurologically normal and cerebral palsied individuals. Human Movement Science 6, 37-65.

Subjects were trained to execute rhythmical forward and backward arm swings, with consistent timing and displacement characteristics. A DC servomotor was used to introduce brief perturba-

tions, opposing elbow extension. Pilot studies indicated that: (1) Weak disturbances tended to

foreshorten the voluntary action, while larger perturbations (strong enough to reverse the ongoing

action) caused positional overshooting. (2) When prolonged ( > 500 msec) perturbations were

investigated, there was no evidence that EMG responses within the first 100 msec provided much

force to counter the disturbance. (3) Subjects were unable to learn to curb the steep rises in

velocity observed when strong perturbations were released, despite extensive feedback experience.

The main study confirmed that electromyographic and movement parameters reflect the magni-

tude of the perturbation. The actions of cerebral palsied subjects were more disrupted by

perturbations, abnormal antagonist activity and clonus were recorded. Models of compensation

are discussed.

Introduction

The experiments reported below investigated the reactions of neurologically normal and cerebral palsied adults to perturbations intro-

* 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)

38 A. Harrison, R. Kruze / Perturbation of an amon

duced while they were executing very accurate arm swings. Our aim was to study the magnitude and time-course of compensations achieved, explore what mechanisms are deployed, and characterise any abnormalities observed.

When a posture is disturbed, compensation involves reinstating the original limb configuration. Efficiency is assessed in terms of the speed and accuracy with which this is completed, and the energy and attention expended in doing so. When an ongoing movement is disturbed, effective compensation is more problematic to define. Take, for example, the current action of rhythmically and repeatedly flexing and extending the elbow. The arc of movement and velocity profile are prescribed. When such an action is interrupted, what form should compensation take ? Detecting an error and responding to it cannot occur instantaneously, and so reinstating all movement parameters following a disruption is impossible. Given the delay, there is an inevitable compromise between recapturing position, velocity and timing. If preserving the end-point of the swing is judged to be vital, doing so on time will necessitate altering the velocity profile in order to compensate for the interruption. If the force and speed of the action are considered its prime aspects, the most effective compensation would be to preserve these and foreshorten swing amplitude. If it does not matter whether the current arm swing is salvaged, the most efficient overall strategy may be to neglect it and resume movement on the return swing, thereby avoiding all reprogramming demands. Which aspect of a performance is safeguarded is likely to vary from action to action. When playing tennis, it is crucial to try and preserve the instant and force with which the ball is struck, but when a hand-held object is being resited all that may matter is final limb position. Flexibility in enstating whatever compensation is judged most appropriate implies cognitive reappraisal following a disruption or contingency prepro- gramming. A unitary definition of compensation, applicable for all actions and all circumstances, appears unrealistic. The operational definition of compensation adopted in the current studies was that subjects should recapture the originally planned action as quickly and completely as possible. Specifically, they were instructed not to trade-off inaccuracy of the current swing in order to simplify future reprogramming demands.

A. Harrison, R. Kruze / Perturbation of an action 39

Physiological responses to perturbation

A good deal of research, especially during the past decade, has been concerned with tracing central and peripheral responses to perturbation. In most studies, a maintained posture rather than an ongoing action was disrupted. In terms of electromyographic activity, an early three-phase (Ml, M2, M3) response pattern has been described. This is usually completed within 100 msec of perturbation onset, and precedes the main EMG updating (Lee and Tatton 1975). Ml, M2 and M3 responses are sensitive to factors such as the intensity of the perturbation (Dufresne et al. 1979; Marsden et al. 1978; Vilis and Cooke 1976), and the force profile and duration of the movement interrupted (Des- medt and Godaux 1978; Hallett et al. 1981; Lee and Tatton 1975). Unfortunately the tripartite pattern is not always observed, and its components cannot always be unambiguously identified (Jaeger et al. 1982a; Lee and Tatton 1975 and 1982; Seguin and Cooke 1983). There is general agreement that Ml is subserved by a spinal mechanism (Wiesendanger and Miles 1982), but the reaction is more complex than the tendon jerk (Kearney and Chan 1982)._It is a matter of continuing debate, however, whether M2 and M3 responses involve supraspinal pathways (Chan et al. 1979; Eklund et al. 1982b; Ghez and Shinoda 1978; Mackay and Murphy 1979; Marsden et al. 1976; 1977; 1978; Miller and Brooks 1981; Tatton et al. 1975). In man, there is mounting evidence that M2 and M3 responses could be accounted for by purely spinal mechanisms, e.g., phased spindle discharges (Hagbarth et al. 1981), muscle oscillations (Eklund et al. 1982a and b), or different afferent pathways (Appelberg et al. 1977). It is possible that spinal and supraspinal mechanisms coexist (Appelberg et al. 1977), and that spinal mechanisms are evident functionally only when lesioning interferes with descending inhibition. Phillips (1978) argues that the transcortical loop has supplanted segmental servo action. Reasoning that this pro- vides an explanation of how pyramidal tract neuron activity is modulated when increased loads are encountered, and because otherwise there seems no reason for such a fast descending pathway.

Ml and M2 responses are seen when a muscle is stretched, but their size is affected by what preparatory instructions are given (Colebatch et al. 1979; Ebner et al. 1982; Evarts and Granit 1976; Evarts and Vaughn 1978; Hammond 1956; Iles 1977; Lamarre and Lund 1975; Rothwell et al. 1980). If the subject is told to resist the displacement,

40 A. Harmon, R. Kruze / Perturbation of an action

these responses are enhanced. If the subject is told to go with the perturbation, they are reduced. By way of contrast, if contraction of muscle A is demanded in response to perturbation, an M3 response is observed in this muscle’s electromyogram whether or not A was stretched. Wiesendanger and Miles (1982), therefore, differentiate M3 as an ‘intentional’ response, describing Ml and M2 as ‘reflexive’. A question still being debated is whether M3 represents a preprogrammed response or whether current voluntary decision making precedes its execution. Houk (1978) argues that M3 latency is sufficiently long that voluntary initiation cannot be ruled out. This position is strengthened by the very brief voluntary reaction times sometimes logged in man (Lansing and Meyerink 1981; Verrier and Tatton 1982). Any gener- alisation involving reaction time must, however, be treated with caution. Evidence exists that motor programming is not always completed before movement is begun, that motor programming of a given response does not always follow the same sequence, and that anticipatory programming can occur (Bishop and Harrison 1983; Harrison and Bishop 1982 and 1985; Rosenbaum 1983). Such findings suggest that the time taken to muster a voluntary compensatory response after perturbation will vary depending on what immediate and long-term compensatory accuracy is demanded, and what aspects of the response can be prepared in advance.

Even though the magnitude of the early EMG responses reflect the intensity of the perturbation, it is questioned whether they provide much power for countering the opposing force (Allum and Budingen 1979; Allum et al. 1982~). Alternative roles have been suggested for the M2 component: stabilising stiffness (Akazawa et al. 1982; Crago et al. 1976; Kearney and Hunter 1982; Kwan et al. 1979; Nichols and Houk 1976), countering irregularities in movement speed (Hagbarth et al. 1981), and overcoming inertia so that later voluntary movement is not delayed (Nichols and Houk 1976). Allum et al. (1982b) proposed that Ml is responsible for creating a linear response to stretch, while the M2/M3 component constitutes an efferent test signal for calibrating motoneurone excitability (Allum 1975) so that voluntary activity can be tailored accordingly. Information about the current status of the pe- riphery is derived using knowledge about the size of the test signal and the afferent return. The observation that the M2/M3 response is highly variable is not inconsistent with such a role (Marsden et al. 1981), it may simply indicate that there is considerable variation in how a given action is performed electromyographically.


Various experimental techniques have been used to investigate central and peripheral reactions to perturbation. Working with primates, Evarts and Tanji (1976) identified two pyramidal tract neuron responses: a short latency (20-25 msec) reflex component which depended simply on which muscles were stretched, and a longer latency (40-50 msec) response which depended on which muscles would effect the voluntary response demanded. Correlations have been established between central and M2 and M3 EMG components (Cheney and Fetz 1978; Evarts and Tanji 1974 and 1976).

Sensorimotor cortical cells have been shown to reflect the output of muscle spindle receptors (Conrad et al. 1975; Evarts and Vaughn 1978), and could contribute to early and late EMG reactions (Allum et al. 1982a; Capaday and Cooke 1983; Conrad et al. 1974; Jaeger et al. 1982b; Wiesendanger and Miles 1982). When interpreting the physiological data presented, species and task differences must not be ignored (Tatton et al. 1983).

Physiological models

As indicated above, there is still a great deal of contention concern- ing the significance of the various central and peripheral responses recorded when a posture or movement is perturbed. Even more conten- tious is how such components are welded together to effect compensation. It is appropriate to acknowledge that the roles of some components, such as the muscle spindle (Evarts and Fromm 1981; Stein and Oguztoreli 1981), may well differ under conditions of postural and movement perturbation, and that different task demands may make it inappropriate to use common strategies.

Afferent outputs relay information about muscle length, force of contraction and rate of change of muscle length. Various models have proposed that muscle afference is used to detect perturbation intensity and direction. In theory, postural disturbances can be dealt with effectively and relatively easily because a given change in muscle length will require an invariant response to reinstate the original posture. Diener et al. (1983) demonstrated that when a person adjusts his posture voluntarily, the responses of short-, medium- and long-latency reflexes are modulated. In turn, these changes affect what compensations are produced when disturbances are encountered. It is far less straightforward to plan compensation when a dynamically changing

42 A. Harrison, R. Kruze / Perturbation of an action

pattern of muscle activity is disrupted. The same perturbation may retard or hasten goal attainment depending on precisely when it is encountered. Nor are the aims of compensation necessarily fixed. Sometimes, compensation will involve recapturing the planned pattern of positional changes with minimum delay, while on other occasions the performer will opt to safeguard only selected action parameters. Some models involve a preprogrammed compensatory mechanism (Matthews 1981 and 1982). One such proposal envisages that gamma efferent activity is programmed to complement alpha efferent activity, modulating fusimotor responsiveness so that corrections are triggered automatically at the appropriate time and are of an appropriate magnitude (Appenteng et al. 1982; Dufresne et al. 1978). One possible drawback of a preprogrammed process is that it may have to run its full course, without any chance of modification, even though current circumstances render the selected strategy less than ideal (Chan and Kearney 1982). The cognitive demands involved in setting up the multiple time-locked contingencies required to ensure preprogrammed compensation when a complex movement pattern is disrupted are great (Dufresne et al. 1980) and unless supreme accuracy is needed probably also uneconomic (Connolly and Harrison 1976). An alternative strategy is for expected and contemporary afferent activity to be compared, and measures taken to compensate for any deviations detected. Again, re-establishing a set limb position would seem far less demanding than taking into account the future progress of an action (Appenteng et al. 1982; Conrad et al. 1975; Cooke 1980a). When errors are detected and the required compensation has been identified, it should not be forgot- ten that this must still be translated into the language of muscle efference - identifying which units will be active, selecting whether fresh units will be recruited or firing frequency will be increased, designating a graded or non-threshold pattern of unit recruitment (Phillips 1978), safeguarding synergist and antagonist activity (Lamarre et al. 1981; Matthews and Watson 1981; Smith 1981), and specifying the role of sensory feedback (Desmedt and Godaux 1978; Tatton and Bruce 1981).

‘ If corticospinal “commands” are to bypass, as well as to engage, the elaborate spinal

mechanisms which link the different muscle groups in programmed patterns and sequences of

action, they must impose on the alpha motoneurones, in appropriately selected combinations, at least equally elaborate patterns of action: some of these patterns would be determined de

nooo by unprecedented configurations of environmental stimuli, some would be the result of

recent learning, and some would have been rendered relatively automatic by long practice.’

(Phillips 1978: 4)


Biomechanical contributions to compensation

One aspect of the neuromuscular system’s capacity for coping with disruptions which has received relatively less attention involves the limb’s physical characteristics. A simple analogy is with a rubber band. The rubber band exhibits some resistance to stretch because of its inherent mechanical and thermodynamic properties. If the disturbance is sufficiently weak, the rubber band will not alter its length to any measurable degree. The effect a disruption has will depend on the characteristics of the disturbance and the precise state of the rubber band (length, stretch history, etc.). When a limb is perturbed the mechanical status of the limb, and its potential for absorbing (viscosity) and storing (elasticity) energy (Hunter and Kearney 1982) will contribute to the responses observed. Indeed, fluctuations in intrinsic muscle stiffness have been linked to changing potential demands for load resistance (Akazawa et al. 1982).

Early mechanographic analyses of normal and perturbed movements by Asatyran and Fel’dman led to a mass-spring model of the human arm, and postulation that separate systems control postural maintenance and movement dynamics (Asatyran and Fel’dman 1965; Fel’dman 1966a,b). In a recent position paper, Nashner and McCollum (1985) outlined a three-dimensional graphical analysis of postural movements exploring how biomechanical and neural decision-making constraints could simplify the planning, execution, monitoring and correction of actions. Using this approach, they characterised the performances of patients with various sensorimotor abnormalities. Dis- cussion continues regarding how best to conceptualise and represent spatial movements, what actions to study, what measurements to take and what units of behaviour to use. There is, however, a growing recognition of the need to explore the biomechanical demands of different actions. At the simplest level, to determine what changes can be accounted for in such terms. At the opposite extreme, theorists are exploring redefining how a person plans and executes an action and accommodates errors in physico-mechanical control terms (Bizzi 1980; Cooke 1980b; Kugler et al. 1980).

Current study

Subjects were trained to produce accurate radial arm swings. Active, very precise actions were selected because these provide the conditions


under which supraspinal error correction systems are most likely to be recruited (Evarts and Fromm 1978). During testing, a DC servomotor was used to perturb randomly-selected trials, permitting comparisons to be drawn with previous postural disturbance studies. Performance was monitored in terms of the position, velocity and acceleration characteristics of arm swings during uninterrupted and perturbed trials. Biceps and triceps muscle activity were recorded using surface electromyography. An unambiguous definition of how to respond to perturbation was given to subjects: they were asked to compensate as fully and quickly as they could, and complete the current arm swing as nearly as possible as planned. The subject’s ability to do so was assessed in terms of how far the velocity profile, arc length and timing of arm swings from perturbed trials deviated from those recorded when movement was not interrupted. To simplify the subjects’ task and maximise the chances of them setting up effective correctional systems, only the extension phase of a swing was perturbed, never elbow flexion. The approach adopted was to look for reactions attributable to the biomechanical status of the limb, and at the time-course and relative power of later adjustments. A group of individuals exhibiting spasticity was included in an attempt to trace the effects of segmental hyperactiv- ity.

Apparatus

The torque of an RM5622 DC servomotor (Colburn and Evarts 1978) provided a variable opposing force for disturbing arm swings (fig. 1). A custom-built Drive Unit supplied controlled patterns of current to the motor. These consisted of rectangular pulses, variable in amplitude from O-10 amp and duration from 10 msec-10 sec. Each amp of current produced 30 lb in of torque. Maximum torque (300 lb in) was sufficient to halt the strongest subject’s fastest movement. An arm cradle was mounted directly onto the shaft of the motor. Flexion and extension movements of the right elbow were performed. Torque onset was triggered automatically when a preselected arc of elbow extension was reached. Random selection of which trial to perturb and perturbation magnitude were under computer control.

Drive Unit outputs were used to monitor selected parameters of the arm swing performance. A potentiometer in the motor (O-15 v) reg-

A. Harrison, R. Kruze / Perturbation of an actm 45

Servomotor

Fig. 1. Apparatus.

istered degree of shaft rotation. The tachogenerator of the motor provided a movement velocity index. Changes occurring in the direction of the planned action were defined as positive, while movements in the opposite direction were designated as negative. A separate output sampled velocity within 3 msec of torque onset, and this served as a measure of movement velocity at the time of impact. The accuracy of these outputs was assessed at f 1%. A wide range of transitory opposi- tions could be generated using the motor. Subjective reports indicate that these ranged from undetected disturbances of velocity to alarming, powerful knocks capable of halting the voluntary swing and briefly reversing its direction. One subject equated the middle range with moving through a patch of thick molasses.

A number of arm boards were piloted before oscillation artefacts were eliminated. Box girder and other metal prototypes produced oscillations within 100 msec of torque onset, reminiscent of reflex components. The arm board used for the studies reported below was made of wood, and was free of these artefacts. The subject’s forearm was held rigid using a splint cast and strappings across the palm. Surface electromyographic recordings of biceps and triceps activity were made using standard preparation procedures and recording sites (Lippold 1967). A Devices M4 polygraph fitted with AC8 preamplifiers was used (amplification 100 pv/cm, 0 gain). When integration was employed, the shortest available time constant (0.2 set) was selected. Computer assessment of digitahsed EMG and Drive Unit outputs was achieved using a Data General Nova 840 computer, signals were sampled every 4 msec. Hardcopies of EMG and movement parameter plots were obtained from a VDU terminal. Traces contained up to


1,000 data points, representing 4 set of recording or about 3 voluntary to and fro arm swings (0.6 Hz).

Pilot studies

Two 25-yr-old, male, right-handed students with no known neuromuscular abnormality were trained to produce accurate rhythmical arm swings (0.6 Hz, 52” amplitude) using a tracking task. Torque onset was triggered 20” from the prescribed start of the action. Subjects viewed their attempts on an oscilloscope screen, one trace indicated the target and a second the person’s arm swing, providing feedback about timing and positional errors. On-line assessment of trials was available to the experimenter, showing arc length, start and finish points, peak velocity and velocity at perturbation onset. Training was discontinued when a subject could execute highly consistent arm swings, varying by less than 4 deg/sec in velocity and 2 deg in arc, and maintain this consistency over a block of 20 trials. The subject’s arm was below his line of sight, and visual monitoring was excluded. During testing, subjects received no feedback. They wore headphones, and white-noise was used to block all cues that a perturbation was imminent.

Study I. Responses to perturbations of different magnitudes

The subject performed repeated arm swings, aware that on a propor- tion of occasions extension would be interrupted by an opposing force. The instruction given to subjects was to minimise the effects of the disturbance, and as far as possible to salvage the planned extension movement. Perturbed trials were randomly distributed among non- perturbed trials. About 10% of extension trials were perturbed. Per- turbations of 1.0, 2.0, 3.0, 4.0, 5.0 and 6.0 amp (duration 100 msec) were tested in randomised order. Subjects’ responses depended on the magnitude of the disturbance (fig. 2). Small amplitude perturbations slowed down the voluntary action, movement was foreshortened, but the timing of the reversal was well maintained. As torque magnitude was increased, foreshortening became more pronounced. Once the perturbation was powerful enough to halt the arm swing and reverse its direction (i.e., stretch the contracting muscle), overshooting of the swing terminus was observed. The rise in velocity which accompanied


non-perturbed trial Peak Velocity

$ 01.. time 114 units

lamp, 100 msec perturbation

4amp, 100 msec perturbation

h .Z

z O --- -- > A t ----- ____ time 154 units

6 amp, 100 msec perturbation

h .Z $ 0 -__ __ ____ ___ time

>

A

I 179 units

m 100 msecs

Fig. 2. Velocity profiles of perturbed and non-perturbed trials.

the overshoot was large, far greater than that used to perform the test action. When smaller torques were used, relative stretching of the contracting muscle was produced, i.e., interruption meant that the muscle was longer than it otherwise would have been. In models of alpha-gamma coactivation (Granit 1975), both actual and relative stretch should trigger afferent activity because goal attainment has been retarded. In the current study, responses to actual and relative stretch were very different. Stimulus magnitude is a confounded variable, and it may be that the differences in receptor activation, which compensatory mechanisms are deployed or the efficiency of compensatory mechanisms used may contribute to the differences observed. The results do, however, strongly suggest a biomechanical contribution. With small torques, undershooting of the target position was observed. As relative stretch increased, so too did positional undershooting,



3 ._

; 0 >

m time

period of torque opposition

Fig. 3. Velocity response to a sustained perturbation.

which is consistent with more and more energy being taken out of the system. Once the perturbation was forceful enough to reverse the arm swing and produce actual stretch, overcompensation was recorded in the form of overshooting the target position. This is consistent with the sudden release of stored energy when the torque is switched off. Overshooting also increased with torque magnitude.

Study 2. Response to a sustained perturbation

In an attempt to separate reflexive and biomechanical reactions following perturbation, the current study investigated how subjects responded to torques lasting more than 500 msec. The rationale being that this gives time for reflexive electromyographic responses to occur and for their corrective power to be assessed before the opposing torque is removed and putative biomechanical responses are expressed. No effective countering of the torque was evident until 150-200 msec after torque onset (fig. 3) which is sufficiently long to involve voluntary reprogramming. There was no clear evidence of compensation within the first 100 msec. As in study 1, when the torque was switched off, a rapid rise in velocity was recorded.

Study 3. Voluntary attempts to curb overshooting after high amplitude perturbation

The current study investigated whether people can learn to curb the overshooting that occurs when a large amplitude opposing torque is switched off. The purpose being to investigate whether the overshoot is the expression of a mechanism which is subject to voluntary modulation. It was stipulated that the performance of non-perturbed trials

A. Harrison. R. Krure / Perturbation of an action 49

BEFORE TRAIKIKG

non-perturbed trial

6.5 amp, 80 msec perturbation

F.a .1: g 0 ____ ___ - _ _--_ __ l/ii\ time

f

AFTER TRAISIXG

non-perturbed trial

f 0 I_*__ time

6.5 amp, 80 msec perturbation

+a .1: ‘: 0 14 _ ___ _ _ -- ___ ___ time

f

Peak Velocity

125 units

19-l units

131 units

212 units

I

100 msecs

Fig. 4. Velocity profiles of perturbed and non-perturbed trials before and after feedback

experience to curb overshooting.

should not be altered, in order to prevent the person adopting a different pattern of alpha efferent activity or antagonist involvement. During training, the subject was provided with oscilloscope feedback of arm position. He experienced more than 1,000 test trials over a period of two days, divided into five 15-min training sessions. About a third of trials were perturbed. A 6.5-amp, 80-msec torque was used throughout. Before and after training, the subject’s reaction to a 6.5-amp, 80-msec perturbation was assessed during the method outlined in study 1. Typical trials (fig. 4) indicate that the subject salvaged the action more effectively after training. There was no evidence, however, that the subject was able to reduce peak velocity following torque release. He salvaged the action more effectively by decelerating more rapidly, but

50 A. Harrison, R. Kmze / Perturbation of an action

only after velocity had peaked. The subject reported that he was unable to latch onto his arm quickly enough to prevent the springback. The literature reviewed indicated that subjects are able to modulate early EMG response components. If such reflexes played a major role in producing the overshoot observed, then modulation of peak velocity would have been expected. While it is always possible that the subject failed to isolate the optimal strategy for modulating reflex correction, the results are compatible with a biomechanical explanation for the overshoot.

Contrasting the responses of cerebral palsied and neurologically normal subjects to perturbations of different intensities

Method

Subjects Three male right-handed students (20-25 years) with no known

neurological impairment formed the normal group. Two were highly trained, having participated in the pilot studies. The three cerebral palsied subjects, aged 22-26 years, were employed at a sheltered workshop. Sl, a congenital spastic quadriplegic female, is unable to stand or walk independently. She uses her right arm for tasks such as eating, and her left for gross support. Having taken part in preliminary studies, she had some experience of tracking and of perturbed trials. S2, a congenital spastic quadriplegic male, is able to walk independently and has skilful control of his right arm. S3, a congenital spastic quadriplegic male, walks awkwardly with support. His right arm and leg are the most severely affected, and he uses his right arm only for gross supporting functions. For all subjects, testing involved the right arm. Particular difficulty was experienced fitting S3’s arm into the apparatus: passive manipulation provoked strong opposing contrac- tions. With spastic subjects, care was taken to minimise disruptions from head movements and to give them plenty of time to relax and get comfortable. No subject was currently, or had recently been, on medi- cation.

Training To make comparisons valid, it was vital for subjects to perform

comparable arm movements. The target was a 0.6 Hz, 52” arm swing,


as used in the pilot studies. The naive normal subject required 45 min of training before he achieved a satisfactory performance. Spastic subjects experienced greater difficulty, and it was observed that con- tinuous feedback during the early part of training disrupted rather than helped their performance. The approach adopted was to concentrate first on getting the subject to generate a rhythmical forward and backward action. The experimenter counted aloud to signal the time for changing direction. Gradually, length was adjusted until both the correct periodicity and the correct arc were achieved. Visual feedback sometimes proved helpful for refining the action. Sl and S2 achieved a level of consistency comparable with the normal subjects. S3 was exposed to 4 hrs of training, but was unable to achieve similar reliability. His movements were subject to jerky stops and starts, and occa- sional periods of rigidity when progress became impossible. Training was discontinued when two judges reviewing progress considered that proficiency was unlikely to improve further.

Testing Subjects were asked to make repeated arm swings. Random selection

of which trials to interrupt and what magnitude of disturbance to introduce were under computer control. The opposing torque was activated automatically when the arm reached the preselected position, 20” from the prescribed start of the swing. This was the same for all conditions and subjects. The instruction given to subjects was to execute the action as nearly as possible as planned despite any disturbances experienced. Testing was arranged in 8 blocks. Each block contained 50 forward and backward arm swings, each perturbation magnitude was tested once. Four uninterrupted trials were selected at random from each block to characterise non-perturbed performance. A negligible pulse (0.5 amp, 5 msec) was used to trigger on-line data collection and analysis. Normal subjects were tested with 6 pulse sizes: 1.0, 2.0, 3.0, 4.0, 5.0 and 6.0 amp (duration 100 msec). The larger pulses proved too disruptive for spastic subjects, and so ones of 1.0, 2.0, 3.0 and 3.5 amp were used. After each block, the subject rested until he was ready to continue. If requested, the straps on the arm mould were loosened. Between blocks, the experimenter reviewed performance of non-perturbed trials from the previous block. If periodicity or length were unacceptable, refresher training was given.


Results

On-line recordings of 8 trials of each perturbation size and 32 non-perturbed trials were stored. The following data were derived: the start and end points of the extension sweep, velocity and integrated EMG values when a pulse was switched on, velocity and EMG values when the pulse was switched off, summated integrated EMG activity

non-perturbed trial 4 amp, 100 msec perlurbation

1 amp, 100 msec perturbation 5 amp, 100 msec perturbation

--

2 amp, 100 msee perturbalion

6 amp, 100 msee perturbation

_____e

Tk +J+

3 amp, 100 msee perturbation

KEY

I

100 msecs

Subject Nl

Torque - on -time

Opposition -

+“e

Velocity I ___.--. .-----time

-ve

Integrated

EMG I lime

Fig. 5. Velocity and integrated EMG profiles of perturbed and non-perturbed trials for subject Nl.


for a trial, the maximum velocity attained, the maximum EMG value recorded after pulse onset. In addition, the experimenter was able to review EMG, position and velocity traces and store the value of any other selected data points. This was used, for example, to compute the latency of discrete changes in activity observed following perturbation.

The normal subjects tested were very consistent in their performance of non-perturbed trials (table 1) and, despite perturbation, reproduced their standard arc of movement with only minor positional errors ( + 1” ). As perturbation amplitude increased, movement was reversed more quickly. Velocity was sampled within 3 msec of torque onset, and even at this stage the velocity profiles of perturbed and non-perturbed trials differed. The peak velocity produced after a perturbation was introduced rose with torque magnitude, and this was true also of peak EMG.

non-perturbed trial 3 amp, 100 msec perturbation


-- 3.5 amp, 100 msec perturbation

_+_._


--

KEY

Torque - on -time

Opposition -

+Ye

Velocity I _____ _.._---- time

-ve

I

100 msecs

Subject Sl

Integrated

EMG I time

Fig. 6. Velocity and integrated EMG profiles of perturbed and non-perturbed trials for subject Sl.

Tab

le

1 F

T

he

resp

onse

s of

no

rmal

an

d sp

astic

gr

oup

subj

ects

to

per

turb

atio

ns

of

diff

eren

t m

agni

tude

s (v

eloc

ity

unit

= 1

deg/

sec;

E

MG

=

inte

grat

ed

EM

G

: un

its).

2 Z

&

(a

) N

orm

al

grou

p re

spon

ses

(mea

n of

10

tri

als)

. 2.

3

Puls

e si

ze (

amp)

N

on-p

ertu

rbed

1.

0 2.

0 3.

0 4.

0 5.

0 6.

0 9 %

2

S.E

. x

S.E

. 52

S.

E.

x S.

E.

57

S.E

. x

S.E

. x

S.E

. R

2

Subj

ect

NI

3

Star

t po

sitio

n (d

eg)

10.3

0.

5 10

.8

1.2

10.6

0.

6 10

.6

1.2

11.3

1.

3 13

.0

1.3

11.3

End

po

sitio

n (d

eg)

76.9

0.

6 76

.0

1.3

76.9

1.

3 78

.6

2.2

17.2

0.

9 78

.4

1.9

74.5

Im

pact

ve

loci

ty

152

2.9

150

4.2

133

16.4

14

2 4.

5 12

9 7.

1 12

5 11

.9

112

Puls

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B

A. Harrison, R. Kruze / Perturbation of an action

non-perturbed trial 3 amp, 100 msec perturbation

--


-- 3.5 amp, 100 msec perturbation


-

KEY

Torque - 00 -time

Opposition

I

100 msecs

Subject 52

+Ye

Velocity I_______ -..---time

-ve

Integrated

EMG I time

Fig. 7. Velocity and integrated EMG profiles of perturbed and non-perturbed trials for subject S2.

EMG activity rose while the opposing force was acting, and was more pronounced the stronger the opposition (fig. 5). Spastic subjects Sl and S2 produced comparable results, with peak EMG reflecting perturbation amplitude (table 1). Sl exhibited noticeable disturbances of velocity following a perturbation. Periods of clonus (high muscle activity with no concomitant change in joint angle) and irregular velocity were recorded (fig. 6). S2, the more practiced subject, exhibited greater movement control (fig. 7). Whereas normal subjects were able to ‘ride’ the disturbance, the arm swings of spastic subjects were often greatly disrupted. Even after a moderate (3.5 amp) perturbation, spastic subjects experienced great difficulty continuing. It should be empha- sised that this was not a voluntary stop by subjects, or a case of giving up, rather it occurred because progress was rendered impossible by clonus. The performance of S3, even on non-perturbed trials, was so variable that his responses cannot be meaningfully averaged or com-


non-perturbed trial 3 amp, 100 msec perlurbation

___&

1 100 msee perturbation amp, 3 amp, 100 msec perturbation

--

-s-_

a A

1 100 msec perturbation amp,

KEY

Torque - 00 -time

Opdosition

.-- +ve -

Velocity I__ _____.----. time

I -ve

100 msecs Integrated

Subject S3 EMG I time

Fig. 8. Velocity and integrated EMG profiles of perturbed and non-perturbed trials for subject S3.

pared. Even small pulses caused distress and exaggerated EMG reactions, periods of clonus were frequent (fig. 8).

Discrete changes in electromyographic activity were often discernible during the 100 msec of torque opposition, before the motor was switched off. With larger perturbations, two peaks were common. The mean latencies for normal subjects were 30-40 msec and 40-70 msec. The first peak tended to be of smaller amplitude. Such changes were not, however, apparent in all traces.

Discussion

The neurologically normal individuals tested displayed great consistency in their performance of the radial arm swing task, standard errors indicate variations of less than 1” of arc length and 3 deg/sec


velocity. Their responses to disruptions were also highly consistent, although more variable with larger perturbations. As torque magnitude was increased, disturbances of position and velocity became more pronounced. The strongest perturbation created an anticlockwise displacement 3-4 times faster than the voluntary action interrupted, and when opposition was switched off velocity was 2-3 times greater than that observed in uninterrupted trials. Consistent increases were seen in the EMG activity pertaining after 100 msec, and in the total amount of EMG activity associated with a trial. As in earlier studies, peak velocity and peak EMG rose monotonically with disturbance magnitude.

There was some evidence of discrete changes in electromyographic activity occurring during the 100 msec of torque opposition. In some traces, two peaks were discriminated. Their latencies and relative size are compatible with Ml and M2/3 responses. Such data must, however, be regarded with caution. An integrated EMG index was used to provide a global index of muscle activity, but this is not ideal for differentiating discrete changes. It is clear, however, that EMG activity occurring within 100 msec of perturbation onset was not of itself sufficient to counter torque opposition. Just as in the final pilot study, subjects failed to marshal sufficient power to prevent immediate expression of the springback when torque was switched off. Rather, what they did was use deceleration after velocity had peaked to counter increased momentum and prevent overshooting of the position where arm direction was scheduled to be reversed. In the first pilot study, a full spectrum of positional disruptions, from undershooting to overshooting of the target arm position, was observed. Possibly because of prolonged experience, subjects in the current study preserved the target arc more effectively.

Theoretically, even though EMG changes occurring within 100 msec of disturbance onset were not powerful enough to reinstate the planned action, had subjects responded to small pulses with the responses generated by more powerful disturbances, compensation would have been more effective. The implication is that the potential power of the early EMG reaction was not or could not be used in this way. Subjects did not know when a disruption would occur or whether it would be large or small. Had the early response been preset to maximum regardless of perturbation magnitude, more effective compensation should have resulted. This suggests that receptor activation is critical for eliciting higher levels of activity, or that such a strategy has

60 A. Harrison, R. Krure / Perturbation of an action

overriding disadvantages. Previous researchers have shown that early reflex components can be voluntarily enhanced or diminished. The contention of Allum et al. (1982~) is that M2/M3 components have insufficient power to effect major compensation, and that they are the expression of signals dispatched to calibrate peripheral responsiveness following a disturbance. If reflex responsiveness was preset to ceiling regardless of input, the calibration function probably would be com- promised. One unusual feature of the current study was that the adequacy of subjects’ reactions following a perturbation was assessed not only in terms of reinstating the original direction of movement but also the scheduled positional shifts and time characteristics of the action interrupted. Under such conditions, calibration may well be essential to assess the mechanical impact of the disturbance, so that EMG updates can be tailored to the current status of the neuromuscular system and the action aimed for. If, as suggested, medium latency reflex responses represent the calibration signal, the data indicate that EMG activity at this time does indeed reflect the magnitude of the perturbation imposed.

Skilled subjects coped effectively with the full range of disruptions introduced, decelerating or boosting momentum as appropriate. The time course of corrections indicates that they can be accounted for in biomechanical and voluntary reprogramming terms. The perturbations employed are artificial, and it may be argued that the human neuromuscular system has not evolved to deal reflexively with disruptions of this type or magnitude. As discussed, the limitation (at least for smaller opposing torques) does not seem to lie in the potential power of the EMG responses to cope. One shortcoming of the present study was in not recording the arm dimensions of subjects, or attempting to adjust perturbation magnitudes so these were functionally equivalent from subject to subject. Retrospectively, there was no suspicion that neurologically normal and cerebral palsied subject groups differed systemati- cally in terms of arm length or mass. Moreover, it seems unlikely that the major features distinguishing the subject groups, namely abnormal antagonist involvement and clonus, could be accounted for in these terms.

The present studies highlight the difficulties of parsing reflexive, voluntary and biomechanical contributions. The development of mathematical models is indicated to delineate the nature (e.g., threshold, operating characteristics, relative efficiency) of corrective mechanisms


available, and to describe how these interact to effect correction under different conditions, considering the precise action or posture disturbed, and the nature of the perturbation introduced. To do so will probably involve the study of artificial limbs and control options, and a more detailed investigation of the physiology of the human operating system. A procedure such as microneuronography in theory makes it possible to trace excitatory and inhibitory influences which cannot be differentiated at the extracellular level (Dimitrijevic et al. 1983; Harri- son and Jankowska 1984). Spike-triggered and noise-triggered averag- ing make it possible to differentiate whether activity in a given channel affects the firing rate of a given neurone, and differentiate which channels are affected when a given neurone fires.

The performance of spastic subjects indicated that perturbation produced greater movement disruptions. The clinical features of abnormal antagonist involvement and clonus were provoked. The nature of the integrated EMG index means that quantitative inter-subject comparisons are not valid, because factors such as electrode placement can radically affect the absolute activity recorded. The question of whether spastic subjects produced elevated EMG responses when perturbations were introduced is addressed in a later paper (Harrison and Kruze 1987). The consistent reactions of Sl and S2 indicate a potential basis for accurately monitoring disturbance effects. Both EMG reactions and velocity changes bore a lawful relationship to pulse amplitude. If afferent signals are centrally available and decipherable, accurate assessment of perturbation magnitude should be’possible for these individuals.

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