S . Calvin-Figuiere et al. Brain Research 881 2000 128 –138
131
Fig. 2. Motor responses during tendon vibration at 80 Hz on the wrist flexor muscles. The recordings show from bottom to top: The surface EMGs of the Abductor pollicis longus muscle APL emg and of the Extensor carpi radialis muscles ECR emg. The integrated EMGs of the same muscle groups ECR
int. emg; APL int. emg. ECR motor unit discharge ECR MU, its instantaneous frequency curve Inst. Freq., and its fitted curve. APL motor unit discharge APL MU, its instantaneous frequency curve Inst. Freq., and its fitted curve. The slope of the phase of frequency increase was calculated
between the vertical dotted lines 1 and 2.
calculated for all the trials was R 50.97. The slope S of
3. Results
the best fit line is taken to represent the rate of initial increase in frequency. Since some motor units did not
3.1. Relations between the characteristics of the respond in all trials, the conventions we used were that, in
movement illusions and the parameters of the motor this case, the mean maximal frequency and the velocity of
responses the initial increase in frequency were 0, the latency was 21
s. These values were chosen so as not to change the We performed 58 experiments. Motor responses could
variance of the sample. be recorded from the ECR muscles all 58 times, and 45
For each muscle, the six parameters EMG latency and times from the APL muscle, because recording from this
amplitude, motor unit response rate, latency, frequency and muscle was not always possible. We recorded discharges
velocity of increase in frequency were subjected to from 89 motor units from the ECR and 25 from the APL.
separate one-way analyses of variance ANOVA with Analysis of the recordings from the digitizing table
repeated measures and a trend analysis ANOVA factor: showed that illusions evoked by vibration applied on the
direction of illusory movement, with three modalities: flexor muscle tendons were wrist extensions direction
21
extension, abduction and oblique. Vector directions were 20.3863.58, velocity 1.3861.00 m.s , while illusions
compared using the V-test [1], and their modulli were evoked by vibration applied on the adductor muscle
compared using a paired t-test. tendons were wrist abductions direction 82.6
867.818,
21
All values given in the results are mean 6S.D.
velocity 1.51 60.96 m.s . Combined vibration of both
132 S
muscle groups induced an illusory sensation of movement The global results are illustrated in Fig. 3, and the
of the hand, whose direction was intermediate between results of the ANOVAs are given in Table 1.
wrist extension and abduction direction 37.5 8613.18,
AVRs in ECR muscles appeared with the shortest
21
velocity 0.85 60.43 m.s .
latencies and reached the highest amplitudes during illus- In all three vibration conditions, the Extensor carpi
ory sensations of wrist extension and during intermediate radialis and Abductor pollicis longus muscles were both
kinesthetic illusions Fig. 3A and B. AVRs in the APL activated, but with different patterns.
muscle appeared with the shortest latencies and reached Indeed, vibrating one muscle group or covibrating the
the highest amplitudes during illusory sensations of wrist two muscle groups induced motor responses that were
abduction and during intermediate kinesthetic illusions clearly related to the direction of the illusory movement
Fig. 3A and B. perceived because they developed specifically in the
muscles that would have driven the movement had it been 3.2. Recruitment and discharge patterns of motor units
performed. More precisely, vibration of the flexor muscles evoked
To further analyze the organization of the motor re- an illusory sensation of wrist extension together with the
sponses, we recorded the discharges of 89 motor units strongest AVR in the ECR muscles and the smallest in the
from the Extensor carpi radialis muscles and of 25 motor APL muscle, while adductor vibration evoked an illusory
units from the Abductor pollicis longus muscle. Each sensation of wrist abduction together with the strongest
condition of vibration flexor, adductor, both was applied AVR in the APL muscle and the smallest in the ECR
five times. For each trial, three parameters were used to muscles. Combined vibration of both muscle groups
describe the activity of the motor unit: its response latency, induced an illusory sensation of movement of the hand,
its mean maximal frequency and the velocity of the initial whose direction was intermediate between wrist extension
increase in frequency. For each motor unit, every parame- and abduction. In this case, the motor responses evoked in
ter was averaged over the five trials in each condition. the two muscles did not differ.
For the populations of motor units of the two muscles, Figure 2 shows an example of motor response to
Fig. 4 presents the variations of response latency A, mean vibration of the flexor muscle group tendons, while the
maximal frequency B, and initial velocity of frequency subject reported a sensation of wrist extension. EMG
increase C, in relation to the direction of the illusory activity develops in the Extensor carpi radialis muscles
movement. sooner and reaches a higher amplitude than in the Abduc-
In the two muscles, all three parameters depend on the tor pollicis longus muscle. The motor unit in the Extensor
vibration condition and were therefore related to the carpi radialis muscles is recruited with a shorter latency
direction of the illusory movement. and fires with a higher frequency than the motor unit in the
On average, motor units in the Extensor carpi radialis Abductor pollicis longus muscle.
muscles were activated with the shortest latencies when the
Fig. 3. Surface EMG amplitude and latency during motor responses corresponding to three directions of illusory movements of the hand. Grand averages over 58 experiments for ECR and 45 for APL. Error bars are standard deviations. ECR, Extensor carpi radialis muscles. APL, Abductor pollicis longus
muscle.
S . Calvin-Figuiere et al. Brain Research 881 2000 128 –138
133 Table 1
Comparisons of the latencies and amplitudes of the motor responses in the Extensor carpi radialis ECR, n 558 and in the Abductor pollicis longus APL,
a
n 545 muscles during illusions of wrist extension, abduction, or intermediate movement
Parameters ANOVA
Paired comparisons Main effect
Ext. vs. Obl. Ext. vs. Abd.
Obl. vs. Abd. Latency ECR
F2–114 55,04
F1–57 50.19
F1–57 57.65
F1–57 54.26
P ,0.01
N.S. P
,0.01 P
,0.05 Latency APL
F2–88 512.03
F1–44 512.32
F1–44 521.05
F1–44 51.35
P ,0.0001
P ,0.025
P ,0.0001
N.S. EMG ECR
F2–114 55.28
F1–57 50.19
F1–57 56.80
F1–57 57.24
P ,0.01
N.S. P
,0.01 P
,0.01 EMG APL
F2–88 54.86
F1–44 54.76
F1–44 57.81
F1–44 50.68
P ,0.05
P ,0.05
P ,0.01
N.S. Ext., extension; Abd., abduction; Obl., oblique.
a
ANOVAs: for each parameter, one-way repeated measures analyses of variance factor: direction of illusory movement, modalities: extension, abduction, oblique.
perceived illusory movement was a wrist extension and On the contrary, motor units in the Abductor pollicis
with the longest ones when the perceived movement was a longus muscle were activated with the shortest latencies
wrist abduction. Similarly, both the mean maximal fre- when the perceived movement was a wrist abduction and
quency and the initial velocity of frequency increase were with the longest ones when the perceived movement was a
highest during illusory sensations of wrist extension and wrist extension. Similarly, the mean maximal frequency
lowest during illusory sensations of wrist abduction. When and the initial velocity of frequency increase were highest
the direction of the perceived movement was intermediate during illusory sensations of wrist abduction and lowest
between wrist extension and abduction, the latencies, mean during illusory sensations of wrist extension. During
maximal frequencies, and initial velocities of frequency illusory movements intermediate between wrist extension
increase were also intermediate. These results are statisti- and abduction, the values of the motor units latencies,
cally significant Table 2. mean maximal frequencies and initial velocities of fre-
Fig. 4. Motor unit discharge parameters during motor responses corresponding to three directions of illusory movements of the hand. Grand averages over 89 motor units for ECR 25 for APL. Error bars are standard deviations. ECR, Extensor carpi radialis muscles; APL, Abductor pollicis longus muscle.
134 S
Table 2 Comparisons of the latencies of activation, mean maximal frequencies mean max. freq., and velocities of frequency increase VFI of the motor units in
the Extensor carpi radialis ECR, n 589 and in the Abductor pollicis longus APL, n525 muscles during illusions of wrist extension, abduction, or
a
intermediate movement Parameters
ANOVA Main effect
Trend Paired comparisons
Ext. vs. Obl. Ext. vs. Abd.
Obl. vs. Abd. Latency ECR
F2–176 521.96
F1–88 510.75
F1–88 510.74
F1–88 537
F1–88 513.34
P ,0.00001
P ,0.005
P ,0.005
P ,0.0001
P ,0.001
Latency APL F2–48
534.31 F1–24
53.01 F1–24
53.01 F1–24
566.48 F1–24
528.95 P
,0.00001 N.S.
N.S. P
,0.0001 P
,0.0001 Mean max. freq.
F2–176 525.66
F1–88 58.51
F1–88 58.51
F1–88 542.29
F1–88 519.33
ECR P
,0.00001 P
,0.005 P
,0.001 P
,0.0001 P
,0.0001 Mean max. freq.
F2–48 538.52
F1–24 51.42
F1–24 52.3
F1–24 589.71
F1–24 534.38
APL P
,0.00001 N.S.
N.S. P
,0.0001 P
,0.0001 VFI
F2–176 510.31
F1–88 55.2
F1–88 55.2
F1–88 516.61
F1–88 56.44
ECR P
,0.0001 P
,0.05 P
50.025 P
,0.0005 P
,0.025 VFI
F2–48 515.25
F1–24 50.21
F1–24 50.21
F1–24 517.23
F1–24 516.36
APL P
,0.00001 N.S.
N.S. P
,0.0005 P
,0.0005 Ext., extension; Abd., abduction; Obl., oblique.
a
ANOVAs: for each parameter one-way repeated measures analyses of variance factor: direction of illusory movement, modalities: extension, abduction, oblique.
quency increase did not differ from their values during 65 during illusions of wrist abduction F
526.63,
2 – 48
illusory wrist extensions Table 2. P
,0.00001. The trend analysis showed that the relations between
Motor units were thus preferentially activated during each of the three parameters and the direction of the
illusory sensations corresponding to movements that would illusory movement were statistically linear in the Extensor
be driven by their bearing muscles. To further analyze the carpi radialis muscles, but not in the Abductor pollicis
difference between motor units that responded in all longus muscle Table 2. This means that the activation of
conditions and those that did not, we looked whether they the Extensor carpi radialis muscles was linearly spread
could be divided into two groups depending on their fast or over the angular range studied, i.e., from extension to
slow nature. To this end, we measured the contraction abduction, whereas the Abductor pollicis longus muscle
times of 41 motor units from the ECR muscles. had a much narrower range of activation.
Of these 41 motor units, 28 ‘non directional’ units responded for all three directions of illusory movement,
3.3. Vibration-induced activation of motor units related whereas 13 ‘directional’ units responded only during
to their slow or fast type illusions of wrist extension and or of intermediate direc-
tion. As shown in Fig. 5, the distributions of motor unit Since each condition of vibration flexor, adductor, both
contraction times of the two groups did not line up; their was applied five times, there were a total of 445 trials for
means differed significantly t 54.83, P,0.025. They
each vibration condition for ECR motor units and 125 were 45
610 ms and 3267 ms for the ‘non directional’ and trials for APL motor units. Not all motor units responded
the ‘directional’ units respectively, which means that the in all conditions, nor did they always respond in every trial
‘non directional’ units could be classified as slow motor for a given condition. We therefore calculated the total
units, and the ‘directional’ units as fast motor units. percentage of motor unit responses in each muscle for each
condition of vibration. 3.4. Vectorial description of kinesthetic and motor
The percentages of motor unit responses in the two responses
muscles depended on the condition of vibration Fig. 4D, and were thus related to the direction of the illusory
Kinesthetic illusions were represented as vectors, using movement perceived. Indeed, the rate of response for ECR
the model proposed by Roll and Gilhodes [23]. According- motor units was 77 during kinesthetic illusions of wrist
ly, the direction of the vector was that of the perceived extension, 65 during illusions of intermediate movement
movement, and its modulus was the mean velocity of the and 45 during illusions of wrist abduction F
5 perceived illusory movement. The Cartesian coordinates of
2 – 176
21.25, P ,0.00001. The rate of response for APL motor
the end point of each vector were calculated. units was 15 during kinesthetic illusions of wrist exten-
Using these coordinates, the mean vectors representing sion, 29 during illusions of intermediate movement, and
the mean illusory wrist extension, abduction, and inter-
S . Calvin-Figuiere et al. Brain Research 881 2000 128 –138
135
representing illusory sensations in the intermediate direc- tion was compared. The directions of the experimental
vector and of the theoretical vector were compared using a V-test [1], whereas their moduli were compared using a
paired t-test. There was no statistical difference between the directions and amplitudes of the two vectors U
56.49, P
,0.0001; t50.034, N.S.. The AVRs recorded simultaneously with the illusory
sensations of movement were also represented as vectors. Since the electromyographic activities recorded in the two
muscles during AVRs were related to the direction of the illusory sensations of movement, we chose to use the EMG
recorded from the two muscles as the Cartesian coordi- nates of the end points of the vectors. The EMG recorded
from the ECR was taken to be the abscissa x, and the EMG recorded from the APL the ordinate y. One can
then switch from Cartesian coordinates to Polar coordi-
]]
2 2
nates using
the formulas:
modulus 5 x 1 y , and
œ
y ]
direction 5 Arctg .
x As for the kinesthetic illusions, we calculated the mean
Fig. 5. Distributions of the contraction times of ‘non directional motor
vector in each direction. The intermediate vector did not
units’ A and ‘directional motor units’ B of the Extensor carpi radialis
appear to correspond to the sum vector of the extension
muscles.
and abduction vectors Fig. 6B. Indeed, although the direction of the oblique vector did not differ from that of
the sum vector U 59.71, P,0.0001, their moduli dif-
mediate movement were calculated. Fig. 6A shows that fered statistically t
57.56, P,0.05. Since the length of illusory wrist extension and illusory wrist abduction could
the oblique vector appeared to correspond to the average of be represented by orthogonal vectors. The sum vector of
the extension and abduction vectors, we calculated this these two orthogonal vectors was calculated and taken as
average vector and compared their moduli. There was no the theoretical vector to which the experimental vector
difference t 51.89, N.S., and since the direction of an
Fig. 6. Vector representation of the perceptual and motor effects induced by tendon vibration of two wrist muscles. A Vector representation of the illusory sensations of movements. Each arrow represents the mean vector in one direction. The black vector represents the movement illusions during flexor
vibration, the gray vector represents the movement illusions during adductor vibration, and the black and gray vector represents the movement illusions during combined vibration. The dotted black and gray vector is the sum of the extension and abduction vectors. B Vector representation of the motor
responses recorded in the Extensor carpi radialis ECR and Abductor pollicis longus APL. Each arrow represents the mean vector in one direction. The black vector represents the motor responses during flexor vibration, the gray vector represents the motor responses during adductor vibration, and the black
and gray vector represents the motor responses during combined vibration. The dotted black and gray vector is the mean of the extension and abduction vectors.
136 S
average vector is the same as that of the corresponding However, the Extensor carpi radialis muscles are larger.
sum vector, the intermediate vector corresponded to an It is less likely that other muscle activities could be picked
averaging of the extension and abduction vectors. up by the same surface electrodes. Herrmann and Flanders
showed that in the Biceps brachii and deltoid muscles, motor units had best directions that changed gradually with
4. Discussion location in the muscle [14]. They proposed that central
