E lectroencephalogr aphy and clinical N europhy siology , 1991, 8 1 : 1 3 5 - 1 5 1

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© 1991 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/91/$03.50 ADONIS 0924980X9100067M

E L M O C O 89695

Changes in electromyographic responses to muscle stretch, related to the programming of movement parameters Michel Bonnet, Jean Requin and George E. Stelmach 2 Cognitive Neuroscience Unit, Laboratory of Functional Neurosciences, National Center for Scientific Research, Marseilles (France) (Accepted for publication: 15 June 1990)

Summary Three experiments are reported that used the advance information paradigm which consists of providing subjects with either no or partial information about an upcoming movement. Subjects moved handles to control the vertical displacements of C R T beams, to point to eight targets. The illumination of different combinations of these targets prior to movement execution provided advance information about which hand, movement direction, or movement extent would be required. Reaction time (RT), integrated E M G activity in the forearm extensor and flexor muscles, and MI, M2 and M3 components of the stretch reflex responses triggered in these muscles were analysed as a function of the precued movement parameter. Compared to the no-information condition, R T decreased in all precue conditions; however, the reduction was greater when direction than when hand was precued, and greater when hand than extent was precued. The E M G activity of forearm muscles increased during the preparatory period in all precue conditions, but generally did not differ a m o n g them. An overall facilitation of the stretch reflex components was observed in all precue conditions. This facilitation: (1) was greater for flexor than extensor muscles, (2) was similar regardless of the degree of extent precued, (3) differed for the M2 and M3 components depending on whether the responding hand precued was ipsilateral or contralateral. When the precued movement direction was considered, similar changes in the M3 component were found in extensor and flexor muscles. M3 was facilitated when the muscle was precued as an agonist and was inhibited when it was precued as an antagonist. Collectively these data provide support for a motor programming conception of movement organization. Key words: Stretch reflex; Electromyography; Motor programming; Reaction time; Precuing techniques; (Man)

Some of the experimental evidence for the motor program to be formed by a set of instructions that correspond to different movement parameters was provided, in the framework of an information-processing view of motor control, by the movement 'precuing' technique (cf., Rosenbaum 1980, 1983). In this technique the experimental arrangement requires pointing movements from a common starting position toward different spatially located targets. Before the movement, a preparatory signal (a precue) supplies the subject with partial information about one or several movement parameter(s), for instance movement direction, extent or force. As the central nervous system is able to use such partial information to program the corresponding movement parameter(s), the response latency will be shortened compared to conditions in which no advance movement information is given. This decrease in RT is

1 This research was supported by Research Grant No. 227/82 from Scientific Affairs Division, NATO. 2 Present address: Motor Behavior Laboratory, University of Wisconsin, 2000 Observatory Drive, Madison, WI, U.S.A.

Correspondence to." Michel Bonnet, C.N.R.S.-L.N.F. 1, 31 Chemin Joseph-Aiguier, 13402 Marseilles Cedex 9 (France).

interpreted as an index of the time it takes to specify the precued parameter, which may differ according to the movement parameter manipulated. Moreover, when RT decreases as a function of the number of precued parameters, it can be inferred whether the corresponding specification times are additive, i.e., the set of specification operations is serially processed. Moreover, when the RT shortening associated with the precuing of one movement parameter occurs only when another parameter is also simultaneously precued, it can be inferred that the serial specification process is ordered, the latter parameter having necessarily to be specified before the former. Since the first series of studies using the movement precuing technique (Goodman and Kelso 1980; Rosenbaum 1980), a number of experiments aimed at verifying the hypothesis of a parametric process of movement programming have provided converging data showing: (a) that each movement parameter (such as the limb to be moved, movement direction, movement extent, movement force or movement duration) can be independently specified, (b) that specification times differ as a function of the parameters considered. The same conclusions have been reached recently by Ghez and his collaborators (Favilla et al. 1989; Ghez et al. 1990) in the frame of the 'timed response' paradigm, thus ex-

136 tending the early data observed in step-tracking tasks (see Semjen 1984, for review). However, divergent data were found when the timing, serial vs. parallel processing, as well as the order, fixed or not, of programming operations were considered (Bonnet et al. 1982; Zelaznik et al. 1982; Larish and Frekany 1985; Zelaznik and Hahn 1985; Stelmach et al. 1986; Bonnet and MacKay 1989; Lrpine et al. 1989; Riehle and Requin 1989; Ghez et al. 1990). Neurophysiological studies on the functional role played by neural structures in motor control also have provided some evidence that different neuronal networks are responsible for programming different movement parameters. This conclusion is mainly supported by data which show that changes in neural structure activity result from a selective manipulation of advance information provided about a movement parameter. Especially, prior instruction about the direction of a forthcoming movement has been found to change the neuronal activity of the primary motor cortex (Tanji and Evarts 1976; Evarts 1984; Georgopoulos et al. 1989; Riehle and Requin 1989), premotor cortex (Wise et al. 1983; Wise and Mauritz 1985; Georgopoulos et al. 1986; Riehle and Requin 1989), and supplementary motor area (SMA; Tanji et al. 1980; Tanji and Kurata 1982), without any - - or slight - - related change in either the activity (Lecas et al. 1986; Riehle and Requin 1989) or reactivity (Requin et al. 1977) of spinal motor structures. In contrast, the neural process involved in the programming of movement extent and force is not so well known. Nevertheless, some data collected from single-cell recording in monkey (Riehle and Requin 1989), event-related cerebral potentials in monkey (Hashimoto et al. 1980) and in man (Kutas and Donchin 1977, 1980; Becker and Kristeva 1980; Bonnet and MacKay 1989), as well as from reflex studies (Bonnet et al. 1981) converge to suggest that the pathways that connect motor cortical areas to spinal motor structures are involved in programming movement extent and force. However, the extended functional overlap of the neural structures involved in the programming of kinematic and dynamic movement parameters makes it difficult to argue for a serial and, afortiori, hierarchical organization of these neural mechanisms. The limited size of the data set implicating neural pathways is, in large part, due to the fact that different animals, motor tasks, designs and methods have been used to study processes associated with motor programruing. However, a promising method for accessing changes in the activity of spinal and supraspinal motor structures in animal as well as in man is based on the recording of E M G responses to muscle stretch (cf., Marsden et al. 1978; Bonnet and Requin 1982; Wiesendanger and Miles 1982). In short, the 3 successive components, M1, M2 and M3 (Tatton et al. 1975) of the E M G response pattern can be viewed as resulting

M. BONNET ET AL. from the activation of 3 hierarchically organized reflex loops that include segmental spinal pathways (cf., Bonnet et al. 1981), cortical pathways (Tatton et al. 1983; Cheney and Fetz 1984) and cerebellar pathways (Milner-Brown et al. 1975; Strick 1983). The rationale underlying the present set of experiments was to combine the muscle stretch and the movement precuing techniques to examine differential changes in E M G response components during the preparation period of an RT task when various movement parameters (hand involved, movement direction and movement extent) were precued. Previous studies have shown that M1 could be selectively related to the dynamic parameters of an intended movement (Bonnet et al. 1981), while the late E M G component, especially M3, could be preferentially modified when movement direction was precued (Bonnet and Requin 1982; Bonnet 1983).

General methods

Experimental plan Subjects sat at a table directly in front of a C R T (60 cm away) and grasped two handles which were horizontally disposed on a table (see Fig. 1). The wrist and elbow rested upon stands and their positions were fixed. When the subjects moved either handle vertically, by rotating the hand around the wrist axis, they independently controlled, by means of a potentiometer attached to the handle axis, the vertical position of CRT beams. These beams, 1 mm in diameter, which were horizon-

Fig. 1. Schema of the experimentalplan showing the hand position on the handles, precue display, CRT beams and the feedback screen on which the trial number and RT were displayed after each trial. The insert shows how the forearm muscles were stretched by the pneumatic hammers (A and B) and how musclepreactivationwas achieved by the loading system(C).

L O N G - L O O P REFLEXES A N D M O T O R P R O G R A M M I N G

tally separated from each other by 1 cm, served as target pointers located within a vertical slot, 10 cm high and 2 cm wide, cut out of a display panel dissimulating the C R T screen. By rotating one handle to displace the C R T beam, subjects thus performed indirect pointing movements. Eight red electrohiminescent diodes (LEDs), which served as precues, imperative and target signals for pointing movements, were vertically disposed on this display panel on either side of the slot, according to the combination of 3 binary spatial dimensions (in terms of L E D location). These dimensions were side (left vs. right) in reference to the mid-sagittal plane, vertical location (above vs. below), and distance (proximal vs. distal) in reference to the mid-horizontal plane. In terms of parameters of the monoarticular hand movement to reach target, the corresponding dimensions, were the active hand (left vs. right), the direction (extension vs. flexion), and the extent (long vs. short). The starting position of the C R T beams was indicated by a green L E D located on each side of the slot on the mid-horizontal plane. The proximal and distal LEDs were located at 20 m m and 40 mm, respectively and, in terms of angular vision, at 2 ° and 4 °, respectively, from the mid-horizontal plane. The angular displacement of each handle to move the corresponding C R T beam toward the LEDs was 9.5 ° for the proximal LEDs, and 18 ° for the distal ones. The accuracy requirement for pointing movements (i.e., the range within which the C R T beam was considered as correctly located on the target) was 1.5 ° for proximal targets and 2 ° for distal targets.

Muscle stretch device and EMG recording Pneumatic hammers, located under the table (cf., schemata inserted in Fig. 1), were used for stretching either forearm flexors or forearm extensors of either arm. Each handle was extended under the table by a plate which was vertical when the subject maintained the C R T beam at the starting position on the display panel. Two pneumatic hammers were disposed facing the two sides of this plate in such a location that, when inactivated, they did not restrict the handle rotation necessary to reach the targets. When activated, each pneumatic hammer, according to its location, displaced the plate and moved the handle either upward or downward. By either extending or flexing the hand, the forearm flexors or extensors were thus stretched. The handle displacement resulting from the mechanical tap was about 15 o and was reached after 40 msec with a mean speed of 375°/sec. Since the triggering of late E M G responses requires the stretched muscle to be slightly activated, each handle plate was loaded (about 0.6 N / m ) by using a pulley system (either forward or backward), in such a way that the maintenance of the C R T beam at the starting position involved a slight

137

activation of either the forearm flexor or extensor muscles. Pairs of surface Ag-AgCl electrodes, 8 m m in diameter, were fixed 2 cm apart, 5 cm from the elbow joint, bilaterally, on the inside of the forearm upon the flexor carpi radialis and on the outside of the forearm upon the extensor digitorum communis. E M G activity was continuously monitored, amplified, filtered (lowfrequency cut-off 10 Hz, high-frequency cut-off 3000 Hz), full-wave rectified, digitized on-line with a sampling rate of 1000 Hz and collected, together with the digitized handle-potentiometer signal, on magnetic tape for further off-line analysis.

Procedure The subject's task was to move, as quickly as possible, one of the C R T beams from the starting position to one of the red LEDs when illuminated as a target. Prior to the performance of the pointing task, the illumination of a set of LEDs was used as a precue to supply the subject with advance information about one movement parameter, the other parameters remaining unspecified until the imperative signal occurred. That was realized by using different patterns of 4 LEDs (cf., Fig. 2). When the active hand was precued, either the 4 LEDs on the left side or the 4 LEDs on the right side of the display panel were illuminated. When movement direction was precued, either the 4 LEDs of the upper part or the 4 LEDs of the lower part of the display panel were illuminated. When movement extent was precued, either the 4 distal LEDs or the 4 proximal LEDs, by reference to the starting position, were illuminated. Fur-

PRECUE

ion Q'~'~'ee'°e

U°~ J . . J °

T AI~G E T

DISPLAY

Fig. 2. Sketch of how the different movement parameters (direction, hand and extent) were precued on the target display. Note that the subjects had to perform a 4-choice RT in all the precuing conditions and an 8-choice RT in the no precuing, control condition.

138 ther, a control condition, in which no information was provided about movement parameters, was formed by the illumination of the 8 LEDs. This control condition formed the reference sample in order to evaluate the effects of partial advance information upon RT, background E M G activity and the components of the stretch reflex. The detailed timing of a trial was as follows: a trial started when the subject adjusted both C R T beams at the central rest position. A correct adjustment was signalled by a tone of 100 msec, the onset of which started a waiting period. After 1.5 sec, this period ended with the presentation of the precue for 1 sec. When LED(s) were turned on, a preparatory period of either 1.5 or 2.0 sec duration started; across trials the duration of the preparatory period was random, each with a probability of 0.5. It ended with the illumination, as an imperative and target signal, of one of the LEDs previously illuminated as the precue. The subject was required to move the beam as quickly as possible towards the target, stop it within the target range and maintain it there for 100 msec. Reaction time, i.e., the time between when the L E D was activated as the imperative signal and when the C R T beam left the central rest position, was immediately displayed for 4 sec, together with the number of trials already performed, on a screen just above the CRT. After each trial, the subject was thus informed not only about the RT but also whether an error (i.e., anticipatory response, movement of the contralateral hand, movement in the wrong direction) had occurred. In such a case, the number of trials was not incremented, but the subject was not informed about the type of error made. The disappearance of feedback information indicated to the subjects that they must initiate the next trial.

Experimental design Each trial resulted from the combination of advance information (N = 4), preparatory period duration (N = 2), and imperative signal (N = 8). These 64 possible combinations formed a series of 64 trials which were randomly ordered by using a computer program of sampling without replacement. If an error occurred, the trial was not accepted and was repeated at a later time.

M. BONNET ET AL. was thus necessary to take into account possible changes in the level of muscle preactivation in the analysis of the relationships between the components of the E M G response to muscle stretch and precue information provided about the parameters of the forthcoming movement. Two sources of change in E M G activity could be expected. The first was related to the maintenance of the hand at the starting position. Changes in the force exerted for squeezing the handle could result in changes in the coactivation level of forearm antagonist muscles, including the muscle to be stretched. The second was related to the possible change in the muscle activation level that resulted from the precue conditions themselves, as it has been suggested that changes in preparation could be reflected in spontaneous E M G activity (Requin and Paillard 1971; Brunia and Vingerhoets 1980). The aim of this first experiment was, thus, to analyse changes in the E M G activity of the wrist extensor and flexor muscles during the preparatory period when advance information about the hand to be involved, the direction and the extent of a forthcoming pointing movement was manipulated.

Method Subjects Thirteen subjects, 9 right-handed and 4 left-handed, 1 female and 12 males, between the ages of 16 and 26 years, participated in exchange for 30 F F / h . They were not informed about the purpose of the experiment.

Experimental plan Apparatus, procedure and E M G recording techniques were as described in the General Methods section, but the pneumatic devices for muscle stretching were not used.

Experimental design Each subject performed the task during 2 successive daily sessions. Each session comprised 2 series of 64 trials. The first series of the first session was considered a training period during which RT, movement time (MT) - - i.e., the time between when the C R T beam left the central rest position and when it was stabilized on the illuminated target - - and E M G data were not analysed.

Experiment I

EMG data analysis Muscle preactivation is a prerequisite to record the 3 components of the E M G reflex response to muscle stretch. However, the size of each of these 3 components of the stretch reflex response has been found to depend upon the initial level of muscular activation (Akazawa et al. 1983; Bedingham and Tatton 1984). It

Digitized E M G activity of the riglat wrist flexor and extensor muscles during the second series of the first session was integrated during the last 0.5 sec of the preparatory period. To evaluate changes in the activation level of the same muscles on the two sides, the E M G activity of both wrist flexor muscles was in-

139

L O N G - L O O P REFLEXES A N D M O T O R P R O G R A M M I N G TABLE I Reaction times and movement times in the different precueing conditions. Movement parameter Extent

Hand

Direction

- -

Not precued

RT MT RT MT

Precued

m

m

Large

Short

M

Right

Left

M

Up

Down

M

318 218 318 250

336 210 317 225

327 214 317 238

330 204 314 229

324 224 317 225

327 214 315 227

326 197 306 203

329 232 304 235

327 214 305 219

tegrated during the same period, in both series of the second session. For every 64 trial series, each muscle and each subject, changes in E M G activity were expressed in terms of standardized ( Z ) scores. After calculation of the mean (M) and standard deviation (S.D.) of samples of integrated E M G activity recorded during the control condition, the mean integrated E M G activity (x) recorded in each precuing condition was converted into the Z score ( Z --- (x - M)/S.D.). Thus, changes in E M G activity were expressed in standard deviation units in reference to the control condition, allowing averaging over series and subjects. Results Reaction times and movement times

Reaction times and MTs in the different precuing conditions are shown in Table I. These data were submitted to ANOVAs. When compared to control condition, RTs were significantly shorter when the hand to be activated ( F RIGHT

(1, 12) = 13.70, P < 0.01), movement direction ( F (1, 1 2 ) = 137.95, P < 0 . 0 0 1 ) , or movement extent ( F (1, 12) = 20.27, P < 0.001) was precued. Moreover, RTs were significantly shorter ( F (1, 12) = 10.95, P < 0.01) when movement direction was precued compared to when the hand to be activated was precued, but did not significantly differ ( F (1, 1 2 ) = 0 . 3 1 ) between conditions where either the hand to be activated or movement extent was precued. In control condition, a significant difference in RT was found for only movement extent, RTs being longer for movements of short extent than for movements of large extent ( F (1, 1 2 ) = 31.44, P < 0.001). This difference in RT between extent values disappeared when extent was precued ( F (1, 1 2 ) = 0.32), which resulted from the fact that the effect of the precue was significant when the short extent ( F (1, 12) = 48.14, P < 0.001) but not when the long extent was precued. Movement times were longer when extent was precued compared to control condition ( F (1, 1 2 ) = 4.79, P < 0.05). They differed according to the movement parameter precued, being longer when extent rather RIGHT

FLEXOR

FLEXOR

z 40

I-1

R

R

m

n

_

I-I

ext

flex

E

short left

large

40

0

right

ext

flex

NM E RIGHT

large

shorl left

R

t---z

H EXTENSOR

D

right

E LEFT

H

D

FLEXOR

Fig. 3. Amplitude ( Z score) of the E M G activity during the last 500 msec of the 2 sec preparatory period as a function of advance information. Left part: E M G activity of the antagonistic muscles of the right forearm when the flexor muscles were preactivated (first session, series 2). Right part: E M G activity of the homologous flexor muscles of both forearms (second session, both series). Averaged data for 13 subjects (E, extent; H, hand; D, direction).

140

than when direction was precued ( F (1, 1 2 ) = 12.42, P < 0.01). Moreover, MTs differed as a function of direction values, MTs being longer for a flexion than for an extension movement ( F (1, 12) = 13.98, P < 0.01).

EMG activity during the preparatory period Mean changes in the integrated E M G activity of the right forearm flexor and extensor muscles are shown in the left part of Fig. 3. Mean changes in the integrated E M G activity of both forearm flexor muscles are shown in the right part of Fig. 3. Averaged data for the 13 subjects were separately examined for movement parameter values in the 3 precuing conditions and were expressed as average differences from the E M G activity recorded during the control condition. No significant change in E M G activity was found when considering forearm flexor muscles, which were both involved in the maintaining of the hand starting position. In contrast, when considering right forearm extensor muscles that were antagonistic to these muscles involved in resisting against load, a significant increase in E M G activity was found when the flexion movement was specified in advance ( F (1, 12) = 9.45, P < 0.01).

Discussion" Changes observed in RT according to the different precuing conditions generally agree with data previously found with the movement precuing technique (cf., Rosenbaum 1980; Bonnet et al. 1982; Larish and Frekany 1985; Lrpine et al. 1989). First, providing advance information about any movement parameter significantly shortened RT. Second, the RT shortening differed according to the precue movement parameters, being substantially larger for direction than for the other parameters. However, conclusions which can be drawn from the finding about the time for specifying movement parameter are of limited value, as the amount of 'difference' between parameter values cannot be evaluated on a scale common to the 3 movement parameters (cf., Lrpine et al. 1989). Third, differences in RT between parameter values, which were found for movement extent only when this parameter remained to be specified, disappeared when movement extent was specified in advance. As mentioned elsewhere (Requin 1985; Lrpine et al. 1989), this finding is a strong argument for a preprocessing conception of preparation, i.e., that the precued parameter is programmed before the imperative signal occurs. Except in one precuing condition and for one muscle, no statistically significant change in E M G activity was observed during the preparatory period. Note that this lack of change in E M G activity between when a movement parameter was precued and when no information was provided agrees with experimental findings that

M. BONNET ET AL.

have previously shown only a general increase in E M G activity associated with preparation (Requin and Paillard 1970; Brunia and Vingerhoets 1980). Moreover, these results are in agreement with studies conducted on monkeys with single-cell recording techniques, which showed that changes in the neuronal activity of motor cortical areas associated with various preparatory conditions did not result in any change in E M G activity of the muscles involved (cf., Wise et al. 1983; Lecas et al. 1986; Riehle and Requin 1989). Considering our results and those of others together, it can be concluded that the specification of spatial movement parameters does not result in any activation of spinal motoneurones prior to movement onset. The only exception to this interpretation, i.e., the increase observed in the E M G activity of the forearm extensor muscles when they had to perform a precued flexion movement, is difficult to explain. It cannot be interpreted as an increase in the coactivation level of both forearm muscle groups since no simultaneous increase in the E M G activity of the flexor muscle was found. However, this difference in antagonistic muscle E M G activity was compatible with the maintenance of a fixed hand position. This suggests that the equilibrium of the mechanical forces that this maintenance implied was insured by the involvement of muscles, the activity of which was not recorded.

Experiment II The purpose of this second experiment was to analyse the changes in the 3 components of the E M G response to a muscle stretch triggered during the preparatory period, as a function of advance information provided to the subject. Although the experimental device was suitable for the triggering and recording of E M G responses to muscle stretch in flexor and extensor muscles of both forearms, several reasons led us to focus the investigation upon only one muscle. First, it was obviously not possible to stretch antagonistic muscles simultaneously. Second, changing the stretch reflex from one to another antagonistic muscle across trials would also have been very difficult to accomplish due to the loading system used to 'pretense' the muscles. Such an alternation would have changed the biomechanical conditions of the pointing task within a series of trials. Moreover, a simultaneous stretch of two (either the same or different) muscles of both forearms was also excluded in order to avoid possible interactions between ipsilateral and contralateral reflex responses from a bilateral stretch. Consequently, this second experiment focussed upon changes in the components of the E M G response to stretch in the right forearm flexor muscles only.

LONG-LOOP REFLEXES AND MOTOR PROGRAMMING

141 series. These mean latency values were then used to determine 3 successive and contiguous time-windows during which the 3 M1, M2 and M3 c o m p o n e n t s were integrated for each trial. The mean values of these time windows were from 15 to 30 msec for the M1 c o m p o nent, f r o m 30 to 45 msec for the M2 c o m p o n e n t and from 45 to 60 msec for the M3 c o m p o n e n t (cf., Fig. 4), with between-subjects differences less than 5 msec for M1 and 10 msec for M2 and M3. Like the b a c k g r o u n d E M G activity in Experiment I, the magnitude of each of the 3 E M G response c o m p o nents to muscle stretch in each precue condition was expressed as a Z score with reference to the control condition. These data were then averaged over series, sessions and subjects and submitted to statistical analysis.

Method Subjects Eleven subjects, 9 right-handed and 2 left-handed, 1 female and 10 males, between the ages of 16 and 26 years, participated in exchange for 30 F F / h . T h e y were not informed about the purpose of the experiment, but all of them previously participated in Experiment I.

Experimental plan Apparatus, procedure and E M G recording techniques were exactly the same as described in the General Methods section. However, a pneumatic h a m m e r that stretched the right forearm flexor muscles was used.

Experimental design Results

Each subject performed the task during 2 successive daily sessions, each comprising 2 series of 64 trials. The pneumatic h a m m e r device was activated 1.5 sec after the end of precue presentation only during the 32 trials in which the duration of the preparatory period was 2 sec, so that the stretch was unpredictable.

Reaction times and movement times Reaction times and MTs in the different precuing conditions are shown in Table II. It can be seen that when c o m p a r e d to the RTs observed in control condition, RTs were significantly shorter when either the h a n d to be moved ( F (1, 10) = 14.96, P < 0.01), movement direction ( F (1, 10) = 59.74, P < 0.001) or movement extent ( F (1, 10) = 29.02, P < 0.001) was precued. Moreover, RTs were significantly shorter ( F (1, 1 0 ) = 5.83, P < 0.05) when movement direction than when the hand to be moved was precued, but did not significantly differ ( F (1, 10) = 0.03) between conditions where either the h a n d to be moved or movement extent was precued.

Analysis of the stretch reflex components The output of the potentiometer providing the angular position of the right handle and the E M G activity of the right forearm flexor muscle were continuously recorded on magnetic tape. Off-line analysis consisted, first, in determining for each trial the onset of handle movement. This time was then used to measure the mean latency of the 3 response c o m p o n e n t s to stretch from the E M G samples of the first 5 trials of each

a

b

right

up

2

:

,d

i

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~

:

1

i

Ji.

wrist flexors

J2mv t

t o

5o

! foo m s e c

slre~.. •5

SeC

wristfposition I lO? I

Fig. 4. Left part: sample of the handle angular displacements (a) and EMG activity in the forearm extensor (b) and flexor (c) muscles, recorded during a trial in which a short, right, down (i.e., flexion) response (1) was performed by the subject. The stretch reflex was evoked in the preactivated extensor (2) 500 msec before the response signal (RS). Note the silent period of the antagonist muscle (3) during the voluntary response. Right part: EMG activity of the right forearm flexor muscles averaged over 10 stretch reflex responses in condition of no advance information. Data for 2 subjects (white and hatched areas, respectively) are superimposed. Note that the M1 and M2 components are apparent for both subjects, but that the M3 component is apparent for only 1 subject.

M. B O N N E T ET AL.

142 T A B L E II Reaction times and movement times in the different precuing conditions. Movement parameter Extent

Not precued

RT MT RT MT

Precued

Hand

Large

Short

M

Right

Left

M

Up

Down

333 213 321 248

333 220 309 215

333 217 315 232

333 209 314 224

333 224 313 227

333 217 314 226

329 212 302 217

337 221 301 211

In control condition, no significant differences in RT between movement parameter values were found. In the precue conditions, a difference in RT between parameter values appeared for movement extent only ( F (1, 10) = 6.04, P < 0.05). This resulted from the fact that the precue produced a significantly shorter RT ( F (1, 10) = 69.60, P < 0.001), but only when a short extent was precued. Movement time was significantly longer when extent was precued compared to when direction was precued ( F (1, 1 0 ) = 7.55, P < 0.05). A similar effect was also observed when extent and no informations were compared ( F (1, 1 0 ) = 6.91, P < 0.05). These differences followed expected values as longer movements were found to produce larger movement times than shorter movements ( F (1, 10) = 5.09, P < 0.05).

Mean changes in the magnitude of the 3 M1, M2 and M3 components of the E M G response to muscle stretch recorded in the different precue conditions are shown in Fig. 5. When movement extent was precued, differential changes in the amplitude of the. 3 components were

RIGHT large

3. E

e

=..

.80

.40

-.2:

short

333 217 302 214

found ( F (2, 2 0 ) = 3.37, P < 0.05): both M2 and M3 components significantly increased, while M1 component did not change. However, these increases did not significantly differ, according to the precued extent (short vs. large), for M2 ( F (1, 10) < 1), as well as for M3 ( r (1, 10) < 1). When the active hand was precued, differential changes in the amplitude of the 3 components were found ( F (2, 20) = 3.23, P < 0.05). The M3 component significantly increased, becoming larger (but not significantly) when the ipsilateral than when the contralateral hand was precued, while an increase of the M2 component was found, being significant only when the contralateral hand had to perform the movement. Consequently, the increase of the M3 component was significantly larger than the increase of the M2 component ( F (1, 10), = 5.81, P < 0.05) when the ipsilateral hand had to perform the movement, while M2 and M3 did not significantly differ when the contralateral hand was precued. When movement direction was precued, differential changes in the amplitude of the 3 components were found ( F (2, 20) = 4.83, P < 0.05). The M3 component

E M G response components to muscle stretch

"0

Direction

FOREARM left

right

FLEXOR

M3]

ext

flex

_J H

D

Fig. 5. Amplitude ( Z score) of the 3 components (M1, M2, M3) of the stretch reflex E M G response evoked in the right forearm flexor muscles as a function of advance information (E, extent; H, hand; D, direction). Averaged data for 11 subjects.

LONG-LOOP REFLEXES AND MOTOR PROGRAMMING significantly increased, while both M1 and M2 components did not significantly change. However, these differential changes depended upon the movement direction value (extension vs. flexion) that was precued ( F (2, 20) -- 4.31, P < 0.05) and were observed only when a flexion was performed ( F (2, 20) = 5.94, P < 0.01), i.e., when the stretched muscle was agonist in movement performance. They resulted from an increase of the M3 component only ( F (1, 10) = 4.79, P < 0.05), that significantly differed from changes in the M1 component ( F (1, 10) = 8.00, P < 0.05), but failed to reach statistical significance when compared to changes in the M2 component ( F (1, 10) = 3.55, P < 0.10). Discussion

The changes observed in R T according to precue conditions were very similar to those found in Experiment I and, therefore, are interpreted in a similar manner. However, it must be noted that in contrast with Experiment I, RT for extent values did not differ when extent was not precued but differed when extent was precued. In both experiments, the changes observed in RT may result from the same source, i.e., that the precue reduced RT for a short extent only. Such a differential effect of the precue upon extent values has been previously observed (Bonnet et al. 1982). Alternatively, the observed R T difference m a y relate to the difference in accuracy requirements of the pointing tasks in which the target w i d t h / t a r g e t distance ratio was not adjusted for the Fitts' (1954) index of difficulty. Similarly, as already reported in Experiment I, small changes in M T were found according to precue conditions. This suggests that some trade-off function between programming and execution processes may have intervened and prevented us from drawing more specific inferences from the RT data about programming processes. The latencies observed for the 3 E M G components, which look shorter than those generally reported in the literature (but, see Marsden et al. 1981; Gerilovski et al. 1987), mainly result from the differences in the mechanical properties of the apparatus used for stretching muscles and in the methods for measuring latencies. Most authors used a torque motor which produces a ramp displacement whose m a x i m u m speed is reached progressively. One can ~stimate (see, for instance, Lee and Tatton 1982) at about 10 msec the delay between the electrical impulse delivered to the torque motor - which served as time origin - - and the first significant displacement of the handle. In contrast, the pneumatic hammer we used resulted in a very sharp mechanical impulse. Moreover, latencies are measured from the rotation onset of a potentiometer located on the wrist axis which, because of the biomechanical properties of the wrist-hand linkage, is probably delayed by about 10

143 msec after the onset of the muscular stretch. If one thus considers that latencies are slightly overestimated with the torque motor device and slightly underestimated with the pneumatic hammer device, our data are quite compatible with those reported in the literature. These differences in the stretching technique also explain why we always observed a relatively large M1 component - very similar to the monosynaptic reflex triggered by a tendon tap - - which is often small and sometimes absent when a torque motor is used. Compared to conditions in which no advance information was provided, changes in the magnitude of the E M G response components to muscle stretch show that the excitability of the reflex loops, especially those responsible for M2 and M3, often increased during the precue conditions. However, this finding may be of limited value because it is not possible to separate the effects of the number of response alternatives from the effects of precue information. This methodological issue has been discussed elsewhere ( G o o d m a n and Kelso 1980; Larish ad Frekany 1985; L6pine et al. 1989). Since our goal was primarily to examine whether advance information caused differential preparation, we shall focus our discussion on the changes observed within each precue condition which will allow us to examine the differences in the 3 response components for each precued parameter. In the process, we take into account that the observed differences were superimposed upon an overall excitability increase of reflex loops. Considering conditions in which movement extent was precued, the facilitation of M2 and M3 components did not differ according to extent values. Therefore, they did not reflect the changes observed in performance speed, i.e., that only the precuing of a short extent significantly reduced RT. In other words, it was not possible to interpret these data in relation to processes selectively responsible for programming movement extent. On the other hand, the fact that the overall increase of the E M G response components to muscle stretch was not observed for M1, but was identical for both late components suggests that the neural structures responsible for this facilitation are common to the reflex loop involved in producing M2 and M3 respectively, that is, the motor cortical areas. For the precue conditions in which the involved hand was p r o g r a m m e d in advance, the main finding was that M2 and M3 did not differ when the stretched muscle was contralateral to the hand involved in movement, but differed (M3 being larger than M2) when the stretched muscle was ipsilateral to the hand involved in the intended movement. The observed asymmetry can be related to interhemispheric differences, as documented by Kutas and Donchin (1977, 1980) and Gratton et al. (1988) for slow cortical potentials which develop during foreperiods associated with hand move-

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ments. However, it should be noted that the slight asymmetry found in M2 and M3 magnitudes resulted from simultaneous changes in M2, larger when the stretched muscle was contralateral than when it was ipsilateral to the involved hand, and in M3, larger when the stretched muscle was ipsilateral than when it was contralateral to the involved hand. This prevents us from inferring which neural pathways are responsible for EMG response components, because the lateralized part of the preparatory activation could equally result from functional asymmetry of neural structures involved in M2 as well as in M3 reflex pathways. The data further revealed that for the conditions in which movement direction was precued, the M3 component was primarily dependent upon the precued direction value. When the stretched muscle was precued as being agonistic in movement performance, a large facilitation of M3 was observed, which was considerably reduced when the stretched muscle was precued as being antagonistic. These data are in full agreement with those previously collected in an experiment in which the direction of hand movements executed in the horizontal plane was manipulated (Bonnet 1983; Requin et al. 1984). The functional meaning of these changes in the M3 component can be viewed as a possible tuning process adapting the gain of the corresponding reflex loop, according to the role to be played by the muscle: when the latter has to be activated, a gain increase would make the reflex loop more able to assist movement execution (MacKay et al. 1983). In contrast, the relaxation of an antagonistic muscle would be facilitated by a decrease in the reflex loop gain in that muscle.

M. B O N N E T ET AL.

Method Subjects Ten subjects, 7 right-handed and 3 left-handed, 1 female and 9 males, between the ages of 18 and 26 years, participated in exchange for 30 F f / h . They were not informed about the purpose of the experiment, but 7 of them participated in Experiments I, II, or both.

Experimental plan Apparatus, procedure and E M G recording techniques were exactly the same as described in the General Methods section, but the pneumatic hammer stretched the right wrist extensor muscle.

Experimental design Each subject performed the task during one session which comprised 3 series of 64 trials. In the first series, only the E M G activity of both wrist extensor muscles during the last 0.5 sec of the preparatory period was recorded. In the two following series, only the stretch reflex of the right extensor digitorum communis, triggered 1.5 sec after the presentation of the precue during trials with a 2 sec preparatory period, was recorded.

Data analysis Analyses of RT, MT, E M G activity and stretch reflex components were identical to those described in the two previous experiments.

Results Reaction times and movement times

Experiment III The purpose of this experiment was similar to that of Experiment II. Essentially, we wanted to analyse changes in the components of the E M G response to stretch as a function of advance information. In this experiment, the EMG response to muscle stretch was examined in the right wrist extensor muscle. However, to ensure greater inference from our data a change in the analysis protocol was made. In the first experiment the only significant alteration in background E M G activity according to precue conditions was found in the right wrist extensor muscle, even though the subjects performed a hand flexion movement. This finding concerned us so we attempted to examine E M G response components in a condition where there was no simultaneous change in E M G background activity. Thus E M G activity changes of both wrist extensor muscles during the preparatory period and the E M G response components changes in the right extensor muscle were analysed in different series of trials.

Reaction times and MTs in the different precue conditions are shown in Table III. When compared to RTs observed in the control condition, RTs were significantly shorter when either the hand to be activated ( F (1, 9) = 33.71, P < 0.001) or movement direction ( F (1, 9 ) = 66.54, P < 0.001) was precued. However, RTs in conditions where movement extent was precued were not, although shortened, significantly different from RTs in condition where no movement parameter was precued ( F (1, 9) = 3.97, P < 0.10). Whereas RTs did not significantly differ ( F (1, 9) = 3.15, P < 0.10) between conditions where either the hand to be activated or movement direction was precued, RTs when movement extent was precued were significantly longer ( F (1, 9) = 8.35, P < 0.05) than RTs when movement direction was precued, but did not significantly differ ( F (1, 9) = 3.61, P < 0.10) from RTs when the hand to be activated was precued. In control condition, a significant difference in RTs between movement parameter values was found for movement extent, RTs being longer for movements of short extent than of large extent ( F (1, 9) = 7.52, P