Experimental BrainResearch
Exp Brain Res (1989) 77:337-348
9 Springer-Verlag 1989
Acquisition of co-ordination between posture and movement in a bimanual task Y. Paulignan i ,, M. Dufoss~ 1, M. Hugon 2, and J. Massion 1 1 Laboratoire de Neurosciences Fonctionnelles, C N R S - L N F 3, 31 Chemin Joseph Aiguier, F-13402 Marseille Cedex 9, France 2 Laboratoire de Psychophysiologie, Universit~ de Provence, UA-CNRS 372, F-13397 Marseille Cedex 13, France
Summary. The acquisition of co-ordination between posture and movement was investigated in human subjects performing a load lifting task. Sitting subjects held their left (postural) forearm in a horizontal position while supporting a 1 kg load via an electromagnet. Perturbation of the postural forearm position consisted of the load release triggered either by the experimenter (control) or by the subject voluntarily moving the other arm. In the latter case, the movement involved the elbow joint (load lifting (A), isometric force change at the wrist level (B), elbow rotation (C) and pressing a button with the wrist (D)) or the fingers (grip isometric force change). We recorded the maximal amplitude and maximal velocity of the rotation of the postural forearm, the E M G of the forearm flexors on both sides and the force exerted either by the load on the postural arm or by the isometric contraction of the moving arm. The maximal forearm angular velocity after unloading was known to be related to the level of muscle contraction before unloading. 1. In the control situation, repetition of the imposed unloading test resulted in a progressive reduction in the maximal forearm rotation without any decrease in the maximal velocity. The amplitude and duration of the unloading reflex were found to increase in parallel. These results suggest that an adaptive mechanism took place which increased the gain of the unloading reflex loop and reduced the mechanical effect of the perturbation. This mechanism was found to come into play not only in the control situation but also in other paradigms where the perturbation was expected by the subjects.
2. A decrease in both maximal amplitude and velocity of forearm rotation together with a weak "anticipatory" deactivation of the forearm postural flexors was observed when the unloading was caused by an elbow movement (situations A, B, C) which indicates that a feedforward postural control took place. An interlimb coordination was built up and stabilized after 40-60 trials. Pressing a button with the wrist (weak force and displacement) was a less effective means of inducing an anticipatory control of the flexors of the postural forearm, which indicates that the intensity of the central control plays a role in the building up of the coordination. 3. A distal grip action exerting either weak (100 g) or a high (1 kg) force was able to reduce the maximal amplitude of the forearm rotation, but not the maximal velocity, which indicates that an improved reflex action takes place, but not a feedforward anticipatory postural control. 4. It is concluded that both feedback and feedforward phasic postural controls play a role in the stabilization of the forearm position when a postural perturbation is caused by a voluntary movement. The acquisition of the feedforward postural control depends on the central command per se rather than on the resulting movement parameters. In addition, proximal joints are more appropriate for building up the coordination than the finger joints.
Key words: Posture - Movement - Co-ordination Bimanual task
Introduction * Present address: I N S E R M U 94, 16 Avenue du Doyen L& pine, F-69500 Bron, France Offprint requests to: J. Massion (address see above)
Central commands are responsible for the muscle contractions which determine movement parame-
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ters. These commands take into account the predictable consequences of the action, such as the sensory input related to the movement execution and the postural disturbance likely to be caused by the movement. A parallel feedforward control is present, which takes into account the expected consequences of the action in order to improve general performance. A feedforward control of the forearm position has been observed to take place in human subjects performing a bimanual load lifting task (Hugon et al. 1982). In this task, one postural forearm was initially loaded with a 1 kg weight whereas the other voluntary arm lifted the load. During this task, the position of the postural forearm remained unchanged because a phasic decrease in the forearm flexor EMG activity took place prior to the onset of the load lifting. On the other hand, when the load lifting was carried out by the experimenter, no anticipatory inhibition of the postural forearm flexors could occur and an upward rotation of the postural forearm was observed due to the spring properties of the flexor muscles. Several experimental paradigms have been used to investigate the mechanisms underlying this coordination (Dufoss6 et al. 1985). It was found that no anticipatory reduction in forearm flexor activity occurred when the unloading was preceded by a warning tone with a fixed interval. The characteristics of the voluntary movement in this coordination were investigated as follows. A 1 kg load was supported by the postural forearm with an electromagnet. The release of the load was triggered by the onset of various types of voluntary movements performed by the other arm. A simple distal loadreleasing voluntary movement, such as pressing a button with the thumb, did not elicit any anticipatory decrease in the postural forearm flexor activities (Dufoss6 et al. 1985); whereas an anticipatory decrease was observed when a I kg load was lifted with the voluntary forearm (Dufoss6 et al. 1987). The aim of the present study was thus to investigate the role of several factors that could be involved in the building up of the anticipatory postural control during a bimanual task. These factors were the mechanical parameters of the voluntary movement (force change and/or displacement), the intensity of the central command and the nature of the joint (proximal versus distal) involved in the voluntary action. The results show that the central command per se rather than the resulting physical parameters is the critical factor in this coordination. In addition, the central command of the muscles controlling the elbow joint are much more capable of in-
ducing an anticipatory action in the postural forearm than the central command of the muscles controlling distal finger joints. Methods Apparatus The method described in a previous paper (Dufoss6 et al. 1985) was adapted to the new situations. Right-handed subjects were seated on a hard-backed chair, equipped with a support to which the right arm could be fixed vertically just above the elbow. The instruction was given to maintain the right postural forearm horizontally, semi-prone during the whole session. This forearm carried a strain gauge equipped platform and a I kg load was hung onto the platform by means of an electromagnet. The load release triggered by the experimenter switching off the electromagnet at unpredictable times constituted the control situation (" Co"). In the other situations, the same perturbation was triggered by the onset of various elbow or finger movements or associated E M G bursts from the left voluntary moving arm. The load release was triggered in several ways: by electromyographic activity onset in the moving arm, by pressing a button switching off the electromagnet, by the increase in force or by the displacement resulting from the voluntary movement (see Results). In all cases, the movements of each forearm were developed in vertical parasagittal planes. The situations involving active elbow movements were as follows:
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Fig. 2. Imposed unloading: effect of repetition. The twenty trials in the first session where unloading was imposed were analyzed and summated in groups of 4 successive trials. The middle curves give the elbow angle before and after unloading (i kg). The vertical dashed line indicates the time of unloading. Note the decrease in the upward elbow rotation with repetition of the test. On the left, maximal amplitude (MA) and maximal
velocity (MV) are shown for each trial: the last column in each row corresponds to the mean maximal amplitude or velocity and standard deviation for the whole series of trials. Note the decrease in MA with repetition without any decrease in MV. On the right, integrated E M G of biceps. The unloading reflex increased in amplitude with repetition
- " F + D " : subjects were asked to raise a 1 kg load by about l0 centimeters from a steady platform. In this case, the force and displacement (F and D) reached significant values (Fig. 1 A). - " F + d " : subjects were asked to push their forearm upward using the distal head of the radius placed semi-prone against a fixed strain gauge equipped platform in order to produce a 1 kg force change. The main mechanical factor was the relatively large force change (F), whereas the displacement was small (d) (Fig. 1 B). - " f + D " : subjects were asked to rotate their left forearm upward by about 45 degrees without any external load. The main mechanical factor involved here was the displacement (D), whereas the force changed very little (f) (Fig. 1 C). - " f + d " : subjects were asked to push their arm upward using the distal head of the radius placed semi-prone in contact with a button in order to press the button. Both the force (f) and displacement (d) were small here (Fig. 1 D). Two situations involving active grip movements were tested. In both situations the active hand had to squeeze a force platform equipped with strain gauges and the thumb had to exert a force increase on the plattform against the palm of the hand. - " F + d " : the thumb exerted a force increase of I kg. - " f + d " : the thumb exerted a force increase of 100 g or less. The subjects were asked to make self-initiated fast movements. In all situations except for the control one, the onset and the time course of the perturbation were fully predictable by the subject. Translucid spectacles maintained the retinal illn-
mination at the normal ambient level but prevented the subjects from seeing their arms and the environment. At the end of each session, a bimanual unloading (" BI") was performed. In this situation, subjects were asked to quickly lift with their left active hand a I kg load initially supported by the platform fixed distally on the right postural forearm. This situation was used as a control representing the level of coordination reached during a natural bimanual task.
Recordings, and data analysis Bipolar surface electrode recordings were obtained from the brachio-radialis, the biceps and the triceps of the postural arm and from one convenient muscle of the voluntary arm involved in the task being performed, i.e. biceps or brachio-radialis in the case of elbow movements and adductor pollicis in the case of thumb movements. The E M G were amplified, filtered (80 Hz-10 KHz band pass), rectified and integrated with a 10 ms time constant (leaky integrator). On each trial, the force and angular elbow displacement signals on both sides were recorded and digitalized (4 or 5 ms bin width) along with the muscle E M G signals. The signals in each series were averaged (n ~ 20), the unloading onset being used as the reference time. As far as the postural forearm E M G changes are concerned, only the results on the elbow flexors are given here, since the spontaneous and reflex activity of the triceps was usually null. Changes in the postural forearm position were quantified by means of two indexes: the maximal angular amplitude (MA)
340 and the maximal angular velocity (MV) of the upward movement of the right postural forearm. Both indexes, computed within 600 ms of the perturbation onset, were expressed in percentages of the values obtained during the control (" C o " ) situation. In fact, the maximal amplitude was usually reached within 250 and 300 ms (see Fig. 2), and maximal velocity occurred within 100 ms after the onset of unloading. As the interval between the onset of unloading and the mechanical changes resulting from a spinal reflex action would have been equal to at least 100 ms (see Discussion), any reduction in the maximal velocity attained within the first 100 ms was taken to reflect changes in the E M G activity of the muscles involved in the forearm postural maintenance prior to the perturbation onset. In the imposed control situation, the initial part of the upward movement of the postural forearm was related to the flexor muscle force which was initially set at an appropriate reference value for maintaining the forearm horizontal. After the brisk unloading, this force suddenly exceeded the elbow torque exerted on the forearm by gravity and causes a forced upward movement. In the case of active planned bimanual unloading (" BI" situation), a decrease in the E M G flexor activity was found to anticipate the unloading of the postural forearm in such a way that the actual muscle force almost never exceeded the torque forearm gravity. Consequently, not only was the amplitude index markedly reduced but so was the related velocity index, which could drop to near zero. The values of these two indexes and the elbow angular position curves corresponding to each situation were compared with those of the control situation " C o ". The intervals between perturbations were randomly selected between 10 and 15 seconds. Comparisons were also made with the bimanual situation " B I " , keeping in mind the fact that in this bimanual situation the perturbation was conspicuously slower than that due to the magnet release. A session usually included 12-15 series. Each series consisted of 20 to 24 trials on the same situation. Intertrial intervals were randomly distributed between 10 and 15 s. Successive series were separated by rest periods of about 10 min. The same situation was usually studied in successive series. However, every two series, a control situation series of 10 trials was inserted in order to make sure that the experimental conditions and the state of the subject (the degree of fatigue, for example) were constant. A whole session usually lasted 24h.
Results
Unloading triggered by the experimenter ( ""Co ", Fig. 2) In this control situation, the release of the load supported by the postural forearm was triggered when the experimenter switched off the electromagnet. This release was followed by an upward movement of the forearm which reached a maximum after some 250 ms and then decreased to a stable value at about 400 ms, which was higher than the initial position, without any marked oscillation. When the task was performed by a naive subject, the effect of unloading on the postural forearm position changed during the first few trials before reaching a stable lower value. In the example shown in Fig. 2, the data have averaged in
groups of four successive trials during the first series of 20 trials. It can be noted that the forearm rotation in the first group of trials was higher than in the subsequent ones. The average of the integrated E M G of the biceps demonstrates that with repetition of the test, an increasing unloading reflex occured, affecting both the intensity and the duration of the deactivation. In addition, the late activation after the pause was often reduced. These results suggest that the subjects in some way learned to predict the forthcoming perturbation by setting the reflex circuit at a more efficient level. The diagram showing the amplitude index for each trial in a sequential order confirm the changes observed in averaged groups of 4 trials. The value of the velocity index in the individual trials was quite constant, on the contrary, which indicates that no anticipatory change in the E M G of the forearm flexors took place.
Unloading triggered by elbow joint control Unloading triggered by the subject lifting a ! kg weight ( " F + D " , Fig. 3). The load release was triggered on the right side at the very beginning of the active movement in two different ways: when unloading by the voluntary hand reached a threshold value of 200 g and at the onset of the biceps E M G burst in the moving arm, in a situation where the voluntary forearm was initially resting on a horizontal support. On the whole, the postural changes were similar, whichever way the load release was triggered. The amplitude index of the forearm upward rotation usually reached a minimum after 2-3 series of 20 trials, depending on the subjects; it reached between 68 and 25% of the control values. The velocity index also showed a reduction and reached 92 to 50% of the control values. Since a reduction in the velocity index is related to E M G changes prior to the perturbation (see Methods), it can be concluded that the reduced forearm rotation was due to at least some anticipatory decrease in postural flexor activity. Actually, the E M G traces in Fig. 3 show that a reduction in the brachio-radialis activity of the postural arm occurred prior to the onset of unloading. The onset of this reduction was more or less time locked with the onset of the biceps activity in the voluntary arm, as previously observed in the case of bimanual coordination " B I " (Hugon et al. 1982). In addition, a second wave of deactivation was observed, which corresponds to the latency of the unloading reflex. Finally, the " F + D "
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LOAD LIFTING
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Unloading triggered by the subject exerting an isometric force of i kg ("F+d", Fig. 4). The subjects were first trained to actively exert with their forearm an upward force of I kg against a strain gauge equipped platform fixed above the wrist. They were instructed to rapidly reach the required force level but not to maintain it. The subjects were informed about their performances by the experimenter. Two situations were compared: first, the load release was triggered when the upward force increased beyond 200 g; and secondly, the load release was triggered by the biceps E M G burst in the voluntary arm initially resting on a horizontal support.
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forearm triggered by load lifting with the active forearm. On the left, summation of 20 trials. The unloading onset is indicated by a vertical dashed line. The lifting of the weight by the active arm can be seen on the first force trace, whereas the unloading of the postural arm can be seen on the second force trace. The upward forearm rotation on the third trace is less than half of that observed under control situation. The rectified integrated E M G of the postural arm bracbio-radialis decreased before the onset of unloading, whereas a second phase with reduced activity corresponding to the unloading reflex was observed after the onset of unloading. The last E M G trace, corresponding to the biceps of the active arm, shows the activation occurring prior to load lifting with that arm. On the right, maximal amplitude and velocity of the forearm rotation in individual trials. First row: imposed unloading (CO). Second row: third load lifting series with the right hand triggering the release of the postural forearm load. Third row: bimanual load lifting (BI). Note the reduction in both maximal amplitude and velocity indicating an anticipatory control of the postural forearm flexors. Rectified and integrated E M G activity: 0, at rest; 1, forearm horizontal and loaded with 1 kg
Under these nearly isometric conditions, all the subjects showed a reduction in the maximal velocity of forearm rotation, which indicates the existence of an anticipatory control of the flexors of the postural forearm. The coordination was progressively organized and stabilized within 40-60 trials. The minimal values of the amplitude and velocity indexes were obtained after 2-3 series of 20 trials and ranged from 67 % to 43 % of the control values in the case of the amplitude index and from 86% to 62% in that of the velocity index. The associated reduction in the amplitude and velocity curves indicates that an anticipatory control was exerted on the postural forearm (Fig. 4, right). This was confirmed by the E M G recordings. A reduction in the forearm flexor activity was observed prior to the onset of the burst from the
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Unloading triggered by the subject performing a 45 ~ upward rotation ( " f + D", Fig. 5). The subjects were instructed to make a upward rotation of about 45 ~. In this series, the left forearm was not lifting a load. The unloading of the postural forearm was triggered either by the onset of the rotation of the active forearm or by the onset of the biceps E M G activity of that arm. In the second case, the left forearm was initially set at rest on a support. The upward rotation of the contralateral postural forearm due to the unloading always showed a drop in both the amplitude and velocity indexes which after 2-3 series of trials ranged from 56% to 47% in the case of the amplitude and from 87% to 76% in that of the velocity, as compared to the " C O " situation (Fig. 5). A clearcut anticipatory reduction in the flexor
activity of the postural forearm was found to be time locked to the onset of E M G activation in the voluntary arm as in all the other cases of actually triggered unloading.
Unloading triggered by the subject pressing a button with the wirst ( " f +d"). In order to determine whether the force exerted by the voluntary movement played an important part in the organization of anticipatory deactivation of the postural forearm flexors when it involved the elbow joint, which is one of the joints utilized during natural load lifting movements, we compared the results obtained with a slight isometric forearm movement (pressing a button with the wrist) with those obtained with a 1 kg isometric contraction. The "voluntary" forearm rested on a support and a switch was placed in contact with the skin of the wrist. The subjects had to perform a slight elbow rotation and an upward torque in order to press the switch. Four naive subjects were tested, each during four sessions of 20 trials involving pressing a button at the wrist level through an elbow flexor contraction. With these subjects the velocity index was
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Velocity only moderately reduced and amounted to between 98% and 72% of the control values. These data indicate that the amplitude of the force control exerted through the elbow flexors on the voluntary side was responsible to some extent for the anticipatory postural command on the other side, because only with a large isometric force did all the subjects show an anticipatory deactivation of the postural forearm flexors.
Unloading triggered by voluntary grip movements ('~f+ d" and "F+ d") In a previous study (Dufoss6 et al. 1985), no anticipatory action on the postural forearm flexors was observed, even after several hundred trials in which a weak isometric movement was exerted by the thumb pressing a button. In order to investigate the contribution of the joint to be controlled (distal versus proximal) to the occurrence of an anticipa-
tory deactivation of the postural forearm flexors, two naive subjects were instructed to develop isometric force by adduction of the thumb on a strain gauge platform, either with a low force of less than 100 g ( " f + d " ) or with a force of I kg ( " F + d"). The load release was triggered by the E M G activation of the thumb adductor muscle. Only a slight change in the maximal amplitude of the postural forearm rotation was observed in the first naive subject, when the force exerted by the thumb was weak. In the second naive subject, the amplitude index dropped to 77% of the control value. However, in both subjects the velocity index remained at 97% or more of the control values. This indicates that no anticipatory reduction in the flexor activity of the postural arm occurred. This was confirmed by the analysis of the E M G traces and agrees with the previous results. The same subjects were then asked to exert a force of 1 kg with their thumb, by squeezing the
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same platform. Surprisingly, after 3 series, only the amplitude index decreased, whereas the velocity index remained unchanged and no anticipatory reduction was observed in the postural forearm flexors. With two other subjects which underwent repeated sessions with various paradigms for two years, the results obtained were quite different. With one of these subjects, when only a slight grip force was exerted, a reduction in the postural arm elbow rotation was observed (amplitude index of 72%) together with a slight reduction in the maxim u m velocity (velocity index of 89%) whereas more pronounced effects on the amplitude (58%) and velocity (81%) indexes were observed with a I kg grip force exerted by the thumb. With the second subject, both weak and strong isometric grip forces reduced the forearm rotation (amplitude index of 58% during weak grip force and 40% during I kg grip force) and the maximal velocity (velocity index of 86% in the case of weak and 69 % in that of I kg grip force). This suggests that in naive subjects, distal isometric actions are not appropriate for organizing co-ordination between posture and movement, even when the subjects are exerting a 1 kg grip force. Only subjects with a long training could build up a coordination with thumb movements, mainly with a 1 kg force exerted by the thumb (one subject) and with both weak and large (1 kg) forces (second subject).
Acquisition of the feedforward postural control (Figs. 6, 7) When a new experimental situation was tested for the first time with a given subject, no anticipatory adjustment of the forearm position was observed at the beginning and it usually took from 40 to 60 trials to reach the maximal anticipation. Figure 6 illustrates the acquisition of feedforward postural control in a given subject when the situation was an isometric force of 1 kg exerted by the wrist through an elbow flexor contraction (situation " F + d"). This figure shows that during the first series a decrease in both amplitude and velocity indexes developed with repetition of the trials. During the second series, this improvement was initially lost, but the decrease developed again quickly up to a limit. The next question investigated concerned the adaptation of the feedforward postural control in an experimental situation where the coordination had already reached a stable level. For this purpose two subjects were trained to lift a 1 kg weight and
ACQUISITION OF THE COORDINATION
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the lifting triggered the release of the load on the postural forearm. Once the coordination had reached a stable level (see Fig. 7, 1 kg), the subject was instructed to lift a weight of 2 kg. It was observed that the maximal amplitude and velocity remained at the same level right from the very first trial of the series with the new load. This was also the case when the subject lifted a 0.5 kg load. The feedforward postural control remained the same despite the fact that a different force command was exerted by the subject's " v o l u n t a r y " arm. Discussion
In a bimanual load lifting task, the voluntary movement of one arm was associated with an anticipatory control of the position of the load-bearing forearm, which minimized the position change re-
345 ACQUISITION
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Maximal Velocity Fig. 7. Effect of lifting various weights on the feedforward postural control. The subject was asked to lift a I kg weight with the left hand. When the decrease in maximal amplitude and maximal velocity of the postural elbow rotation had became stabilized with a 1 kg series, the subject was asked to lift a 2 kg weight. Right from the first trials, the maximal amplitude and velocity were the same as with a 1 kg weight. The same occurred right from the first trials with a 0.5 kg weight. CO: control situation (imposed unloading), BI: weight lifted with the left hand in a normal bimanual situation
suiting from the perturbation. The present experimental series was designed to investigate the mechanisms underlying the acquisition of this coordination. It was demonstrated that two types of mechanisms are responsible for maintaining the postural forearm position when a disturbance is caused by a voluntary movement: a feedback postural correction and an anticipatory feedforward postural adjustment.
Feedbackpostural adjustment The feedback postural correction results from the unloading reflex previously described by Angel
et al. (1965) and Struppler et al. (1973). A change in this reflex characterized by an increase in the amplitude and duration of the silent period and a decrease in the amplitude of the late activation was observed. This type of change occurs under several experimental conditions which allow the possibility of predicting the load release, such as those involving repetition of the unloading test during the control situation (Fig. 2), the presence of a warning tone prior to unloading (Dufoss6 et al. 1985), the load release being triggered by thumb pressure on a button, or even the thumb pressure against a platform with a 1 kg grip force. The improved reflex action might be related to a presetting of the reflex gain which occurs in any situation where prediction of some of the parameters of the perturbation is possible. Some previous examples of the presetting of the monosynaptic reflex gain depending on predictable events have been reported in the literature. Let us mention the blocking of Ia afferents during gait (Dietz et al. 1985) or the presetting of the monosynaptic reflexes in both agonist and antagonist muscles of the wrist prior to the reception of a falling ball (Lacquaniti et al. 1987, 1989).
Feedforwardpostural adjustment A second type of change providing a more efficient stabilization of the forearm position occurs when the perturbation due to unloading results from certain types of voluntary movements performed by the subject himself. In these situations, the reduction of the maximal velocity attained during the first J00 ms after onset of unloading cannot be explained by a change in the reflex action because the neural latency (2540 ms) and the additional mechanical requirements for the release of the muscle fiber contraction can take 80-100 ms after the unloading onset. It indicates rather that the state of muscle contraction has changed before or very soon after the unloading onset. The precise contribution of the flexor deactivation to the forearm stabilization cannot be estimated in the present series because analysis was made on averages based on 20 trials and the contributions of indivudual trials could not be evaluated. In addition to the action of the whole set of elbow flexors, the contribution of elbow extensors should be taken into account in some cases where muscle fatigue was present. What then are the parameters of the voluntary movement involved in the acquisition of the" anticipatory" control of the postural forearm position ?
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Role of movement parameters The first sets of factors which might take part in the acquisition of the feedforward postural control investigated here are the mechanical parameters of the movement such as the force, the displacement or a combination of both the force and the displacement involved in lifting a weight. The experimental data obtained with elbow flexion movements indicated that each of the experimental paradigms resulted in an anticipatory control of the postural forearm, which reached a maximal value after 2 to 3 series of 20 trials. The anticipatory deactivation of the postural forearm flexors was more or less time locked with the activation of the forearm flexors of the "active" arm, as during a natural load lifting task. The anticipatory action on the position of the postural forearm remained, however, less effective than that obtained with a natural bimanual load lifting task. This may be attributable to the fact that the perturbation resulting from the load release under the artificial bimanual conditions in the present series was much more sudden than in the natural load lifting task and could less easily be compensated for in advance by flexor deactivation.
Role of the central command A second major aspect thus emerged, that is the central control per se exerted on the motoneuronal pool of the active arm. This control is responsible for the acquisition of the feedforward adjustment of the postural forearm whatever the mechanical result in terms of movement parameters, i.e. force, displacement or a combination of both. In a similar task, Forget and Lamarre (1986) reached a similar conclusion since they reported that the anticipatory effects observed in a bimanual load lifting task did not depend on the direction of the "active" movement: the same degree of coordination was obtained with an active elbow flexion as with an active elbow extension or even with a leg movement. The prevalent role of the central command as a means of controlling the associated adjustment of posture has also been observed in an experimental series on the standing cat, where a controlateral forelimb movement elicited by intracortical microstimulation and the associated postural adjustments involving the other limbs were found to be controlled in a feedforward manner, the intensity of the postural adjustment being graded in proportion to the intensity of the cortical stimulation (see Gahery and Massion 1981). The following general
Control of Posture
Control of Movement
i III Gain and Gate Control Execution of Posture
Execution of Movement
1 POSTURE
MOVEMENT
Fig. 8. Central organization of the coordination. In this schema, two levels of control are considered for both movement and posture. The striped line from the upper level indicates the open loop control postural maintenance. The continuous line from the upper level corresponds to the phasic command of movement. The collateral joining the "execution" level of posture is responsible for the phasic anticipatory control of the postural muscles. On this collateral pathway, a gate and gain control takes place
functional scheme has then been proposed (Fig. 8). The parameters of the descending volley controlling the active side might be responsible for the associated anticipatory adjustment of the posture via internal collaterals acting on the appropriate postural networks. Is this scheme applicable to the load lifting task? It is worth mentioning in support of this interpretation that the coordination between the load lifting arm and the postural arm observed in a split brain patient was comparable to what occurs in normal subjects (Massion et al. 1989). The phasic anticipatory postural control, which is time locked with the movement control, could not be initiated by a direct action from one motor cortex to the other. In addition, in the natural load lifting task, the intensity of the feedforward control is related to the load to be lifted and thereby to the intensity of the central command for movement. The scheme is of course a highly simplified, however, because the links between an active movement and a postural adjustment are not inborn, at least in the case of a bimanual task, but result from learning. This means that the intensity of the postural adjustment associated with a given active movement can vary with time. One can
347 Table 1. Values of amplitude (A) and velocity (V) index (mean +_ SD) for the subjects tested in each experimental situation and for the 3d series of 20 trials. * Subjects who had underwent training sessions for the different paradigms for two years
1 2 3 4 5 6 7 8
1 2 3 4
1 2 3
Elbow (F + D)
Elbow (f+ d)
A
V
A
V
33+_12 29_+11 68+_12 39+_10 64_+14 63_+18 39+_13 25_+13
61+_13 50_+11 92+_12 64_+1/ 77_+ 9 78+-15 55+_/4 61_+18
70_+ 8 57_+14 68+_16 55_+13
98_+ 7 84+_ 8 72+_10 82_+20
1 2 3 4
Elbow (F+d)
Grip (f+d)
A
V
A
67-+16 44-+15 59+ 8 43+-12
86-+11 72+_13 79_+ 7 62_+11
1 2 3* 4*
91+_10 77_+ 8 58_+ 5 72+- 9
V 97_+10 100+_ 9 86_+10 89+_ 8
Elbow (f+ D)
Grip (F + d)
A
V
A
55_+16 47+_16 56-1-12
87_+14 76_+ 9 84_+ 5
1 2 3* 4*
98+13 70+ 7 40_+ 9 58+_14
V 102_+10 95+ 9 69_+13 81_+11
therefore hypothesize that a gate and gain control may operate in the internal collateral circuit between the pathways involved in the active movement and the circuit responsible for the phasic postural adjustment. Does the coordination between voluntary movement of one forearm and the feedforward postural adjustment of the other forearm obey the same scheme of organization in our artificial situations? Unlike the natural load lifting task where the voluntary movement to be performed depends on the load to be lifted, the present experimental situations gave rise to the same postural perturbation whatever the intensity of the voluntary movement. Therefore, it might be expected that under this artificial situation, the central command would trigger the same feedforward postural control, whatever the intensity of the movement control. This is what was actually observed, once learning of the coordination had been completed. The feedforward control of the postural forearm remained unchanged whatever the weight lifted by the voluntary arm. The intensity of the central
command nevertheless plays a role during the acquisition of the task. The coordination set up after a few series of weak elbow movements was either absent or not as marked as with movements executed with larger force changes or displacement (see Table 1).
Role of distal versus proximal joints The next question about the proposed scheme for the coordinating mechanisms concerns the role of the joint controlled by the voluntary movement. Previous experiments (Dufoss6 et al. 1985) indicated that not every active movement was able to give rise to an anticipatory postural adjustment. When the load release was obtained by pressing a button with the thumb, no anticipatory deactivation of the postural forearm flexors was observed, even after several hundreds of trials. Pressing a button is a movement involving a weak force and a weak displacement. It was therefore suggested that a weak central command was not able to carry out the coordination and that a threshold in terms of the number of descending impulses per unit of time must exist. However, these previous results can be reinterpreted in another way. In the new experimental series using a grip task on a force platform, both weak (100 g or less) and strong (around 1 kg) grips were tested and it was observed in naive subjects that neither weak nor strong grip resulted in a coordinated feedforward postural action. The coordination was thus found to depend not only on the central control parameters acting on specific muscles but also on the joint on which these muscles act: movements of the more proximal joints are more efficient than those of the more distal joints, such as those involved in the grip task. This might be due to the fact that the proximal joints are more often utilized in load lifting tasks than the distal ones, which are more specialized in grip tasks, and also to the fact that the combination of elbow movement and load release on the postural forearm used under our experimental conditions was more similar to natural conditions. Konorski (1967) has claimed that new associations which are similar to natural conditions are always easier to acquire that those which are unlike natural conditions. In conclusion, the central messages reaching the motoneuronal pool seem to be the main factor responsible for the coordination between movement and posture in a load lifting task. This coordination results from a short term learning. In ad-
348
dition, the joint controlled by the muscles is an important factor, since coordination can be more efficiently achieved when proximal rather than distal joints are involved. Acknowledgements. The authors wish to thank R. Massarino for his help in the design of the experimental set-up and R. Aurenty for her help in the preparation of this manuscript. English revision by Dr. Jessica Blanc.
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Gahery Y, Massion J (1981) Coordination between posture and movement. Tins 4:159-202 Forget R, Lamarre Y (1986) Central control of anticipatory postural adjustment asociated with active unloading. Neurosci Lett Suppl 26 : $275 Hugon M, Massion J, Wiesendanger M (1982) Anticipatory postural changes induced by active unloading and comparison with passive unloading in man. Pflfigers Arch 393:292296 Konorski J (1967) Integrative activity of the brain: an interdisciplinary approach. The University of Chicago Press, Chicago Lacquaniti F, Maioli C (1987) Anticipatory and reflex coactivation of antagonist muscles in catching. Brain Res 406:373378 Lacquaniti F, Maioli C (1989) The role of preparation in tuning anticipatory and reflex responses during catching. J Neurosci (in press) Massion J, Viallet F, Massarino R, Khalil R (1989) Supplementary motor area region is involved in the coordination between movement and posture. CR Acad Sci (Paris) 308:417 423 Struppler A, Burg D, Erbel F (1973) The unloading reflex under normal and pathological conditions in man. In: Desmedt JE (ed) New developments in electromyography and clinical neurophysiology, Vol 3. Karger, Basel, pp 603-617 Received August 8, 1988 / Accepted March 16, 1989
