J Neurophysiol 104: 949 –959, 2010.
First published June 10, 2010; doi:10.1152/jn.00025.2010.
Predicting Any Arm Movement Feedback to Induce Three-Dimensional
Illusory Movements in Humans
Chloé Thyrion and Jean-Pierre Roll
Laboratoire de Neurobiologie Humaine, Unité Mixte de Recherche 6149 du Centre National de la Recherche Scientifique, Université de
Provence, Marseille, France
Submitted 12 January 2010; accepted in final form 4 June 2010
INTRODUCTION
To access the muscle spindle proprioceptive feedback evoked by
movements in humans, the only method available so far is the
microneurographic method, whereby peripheral nerve activity
is recorded via microelectrodes in attending subjects (Vallbo
and Hagbarth 1968). This apparently simple, but actually quite
demanding method was recently used to record the muscle
spindle feedback triggered during not only differently oriented
straight-line movements but also more symbolic writing and
drawing movements (Bergenheim et al. 2000; Jones et al.
2001; Roll et al. 2000, 2004).
For many years, a large set of Ia proprioceptive afferent
patterns corresponding to movement trajectories with various
shapes, sizes, and velocities have been collected by our group
and archived in a sort of “neurosensory library.” Based on this
Address for reprint requests and other correspondence: C. Thyrion, Laboratoire de Neurobiologie Humaine, UMR 6149 du CNRS, Université de
Provence, Pôle 3C, Case B, 3 Place Victor Hugo, 13331 Marseille Cedex 03,
France (E-mail: [email protected]).
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body of data, the coding properties of muscle spindle primary
endings have been described (Bergenheim et al. 2000; Roll
et al. 2000). Primary endings present in a given muscle respond
to only a limited range of movement directions, covering about
180° and constituting the preferred sensory sector (PSS), and
their maximum firing rate occurs in a specific direction, the
preferred sensory direction (PSD) (Bergenheim et al. 2000). In
the PSS, as the movement direction moves farther away from
the PSD, the Ia afferent activity undergoes a cosine-shaped
decrease. Since the PSDs of the muscle spindle primary endings present in the same muscle are very similar (Bergenheim
et al. 2000), a muscle’s PSD can be defined by the mean PSD
of all these primary endings. All these data have been expressed in terms of the “population vector model,” initially
used to describe the activity of monkey motor cortical cells
(Georgopoulos et al. 1982). During a given movement trajectory, the mean instantaneous activity of the Ia afferent population present in a given muscle can be expressed in terms of
a “population vector.” The direction of this population vector is
the preferred sensory direction of the muscle and its amplitude
is proportional to the mean firing rate of the Ia afferent
population. Summing together all the population vectors gives
the instantaneous direction and velocity of an ongoing movement (Bergenheim et al. 2000; Jones et al. 2001; Roll et al.
2000, 2004).
This corpus of data was first used to develop a simple
propriomimetic method for determining the Ia afferent feedback originating from muscles during individual joint movements (Roll et al. 2009). This method consists in running the
process backward: i.e., starting with the tangential velocity
vectors describing the instantaneous movement direction and
velocity and calculating the population vectors corresponding
to the contribution of each Ia afferent population to the instantaneous coding of the ongoing movement. To generate these
simulated proprioceptive patterns, it suffices to feed a movement trajectory and the PSDs of the muscles involved into the
model. The model has proved to work efficiently, since the
simulated patterns resembled those recorded microneurographically when subjects were actually executing the movements (see Fig. 3 in Roll et al. 2009). These patterns were then
used to control a set of vibrators placed on the muscle tendons.
Since tendon vibration activates the primary endings of the
muscle spindle with a one-to-one ratio in the 1- to 100-Hz
frequency range (Burke et al. 1976; Roll and Vedel 1982; Roll
et al. 1989), it evokes illusory movements, the trajectories of
which were highly correlated with those used to compute the
patterns (Roll et al. 2009).
0022-3077/10 Copyright © 2010 The American Physiological Society
949
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Thyrion C, Roll J-P. Predicting any arm movement feedback to
induce three-dimensional illusory movements in humans. J Neurophysiol 104: 949 –959, 2010. First published June 10, 2010;
doi:10.1152/jn.00025.2010. Our sense of body posture and movement
is mainly mediated by densely packed populations of tiny mechanoreceptors present in the muscles. Signals triggered in muscle spindles
by our own actions contribute crucially to our consciousness of
positions and movements by continuously feeding and updating dynamic sensorimotor maps. Deciphering the coding rules whereby the
nervous system integrates this proprioceptive information perceptually could help to elucidate the mechanisms underlying kinesthesia.
The aim of the present study was to test the validity of a “propriomimetic method” of predicting the proprioceptive streams emitted by
each of the muscles involved in two- (2D) and three-dimensional (3D)
arm movements. This method was based on the functional properties
of muscle spindle populations previously recorded microneurographically in behaving humans. Ia afferent patterns mimicking those
evoked when the “arm–forearm” ensemble is drawing straight lines,
graphic symbols, and complex 3D figures were calculated. These
simulated patterns were then delivered to the main elbow and shoulder
muscle tendons of motionless volunteers via a set of vibrators. Results
show that the simulated proprioceptive patterns applied induced, in
passive subjects, illusory 2D and 3D arm movements, the trajectories
of which were very similar to the expected ones. These simulated
patterns can therefore be said to be a substitute for the Ia proprioceptive feedback evoked by any human arm movement and this method
can certainly be extended to other musculoskeletal ensembles. The
illusory movements induced when these proprioceptive patterns are
applied to muscle groups via sets of vibrators may provide useful tools
for sensorimotor rehabilitation purposes.
950
C. THYRION AND J.-P. ROLL
Since most of our everyday movements involve several
joints and occupy three-dimensional (3D) space, the aim of the
present study was to map the muscle spindle “proprioceptive
landscape” evoked by complex multisegmental movements.
An anatomical model was first developed for the “arm–forearm” ensemble to calculate the muscles’ PSDs. Based on these
muscle PSDs, specific afferent patterns mimicking those
evoked during the performance of drawing movements describing differently oriented straight lines, graphic symbols,
and complex 3D figures were then computed. These afferent
patterns were then delivered via a set of vibrators placed on the
subjects’ elbow and shoulder muscle tendons to evoke illusory
movements, the perceived trajectories of which were compared
with the trajectories of the movements initially used to compute the proprioceptive patterns.
Experimental setup
Experiments were carried out on healthy volunteers (experiment 1:
five males and six females aged between 24 and 64 yr, mean age: 36.9
yr; experiment 2: seven females and two males aged between 21 and
62 yr, mean age: 35.7 yr; experiment 3: four males and four females
aged between 23 and 63 yr, mean age: 37.4 yr). All the subjects
experienced kinesthetic illusions in response to muscle tendon vibration. About half of these subjects were naive university students and
the others were colleagues from research laboratories who were
variably familiar with the vibration procedure. All the participants
gave their informed consent as required by the Helsinki declaration.
This study was approved by the local ethics committee (CCPPRB,
Marseille I).
The participants were comfortably seated in an armchair with their
right forearm and the palmar aspect of their right hand resting on an
adjustable support. In the first and second experiments, their right
hand was holding a pencil, the tip of which was fixed to a digitizing
tablet by means of a small suction pad. During vibratory stimulation,
subjects were instructed to relax, close their eyes, and focus on the
perception of the illusory movement trajectory described by the
pencil tip (experiments 1 and 2) or the tip of their index finger
(experiment 3).
In the first and second experiments, four electromagnetic vibrators
(Vibralgic model, IKAR Cie) were applied perpendicularly to the
tendons of four right elbow and shoulder muscles (biceps brachii,
Calculating the vibration patterns
To calculate the proprioceptive patterns subsequently used to control the sets of vibrators, the only parameters that had to be defined
were the preferred sensory directions (PSDs) characterizing each
muscle involved in the movement and the two-dimensional (2D) or
3D movement trajectories.
Computation of PSDs. The PSD of each muscle was taken as the
movement direction that lengthened the muscle the most. To determine the elbow and shoulder muscles’ PSDs, an anatomical computer
model for the “arm–forearm ensemble” was specially developed.
This model focuses on the elbow (1 degree of freedom [df]) and
shoulder (2 df) joints and takes into account the relative arm and forearm lengths, which were previously measured in ten subjects and averaged (mean arm length ⫽ 31.1 cm; mean forearm ⫹ hand length ⫽
43.7 cm). The initial state of the model was determined by the posture
adopted by the subjects during the whole experiment (elbow angle:
␣ ⫽ 105°, shoulder angle: ␦ ⫽ 150° in the horizontal plane and ␪ ⫽
90° in the vertical plane; see Fig. 2A). The model computed the
changes in the joint angles ␣, ␤, ␦, ␥, and ␪ occurring while the
fingertip was moving along a straight line in all the directions in 3D
space in 2° steps (Fig. 2). In this model, the muscle lengths were
approximated by considering them to be proportional to the joint
angles. The PSD of each of the muscles was then defined as the
movement direction that evoked the largest corresponding joint angle.
Figure 2 also shows how the joint angles varied with the fingertip
movement directions (Fig. 2B) and gives the resulting PSDs obtained
with each of the six main elbow and shoulder muscle groups involved
(Fig. 2C).
Movement trajectories. It was then necessary to specify the movement trajectories during which the proprioceptive feedback would be
computed. In the first and third experiments, which involved differ-
A
B
Vibration frequency
Time
FIG. 1. General experimental design. A: during vibration periods, the subject’s right forearm was resting on a support and the hand was holding a pencil. In
experiments 1 and 2, 4 vibrators were applied perpendicularly to the following right elbow and shoulder muscle tendons: the biceps brachii, triceps brachii,
pectoralis major, and posterior deltoid muscle tendons. In experiment 3, 2 additional vibrators were applied perpendicularly to the shoulder adductors tendons:
the latissimus dorsi, pectoralis minor and major tendons, and the common deltoid tendon. B, top: trajectories used to compute the vibration patterns corresponding
to the 2-dimensional (2D) inward spiral (note that the arrow gives the rotation direction) and the letter “b.” Bottom: the corresponding simulated patterns, i.e.,
the vibration frequency applied as a function of time to each of the 4 muscles involved (from top to bottom: biceps brachii, triceps brachii, pectoralis major, and
posterior deltoid).
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METHODS
triceps brachii, pectoralis major, and posterior deltoid). The vibrator
heads were specially designed to fit the tendon morphology (length:
3–10 cm; diameter: 0.6 cm). In the third experiment, two other
vibrators were added at shoulder level: they were applied perpendicularly to the common tendon of the deltoid muscle and the tendons of
the shoulder adductors, i.e., the latissimus dorsi and pectoralis minor
and major muscles (Ling Dynamic System Type 101) (Fig. 1A).
In all three experiments, the vibration patterns were delivered via
two multichannel electronic devices connected to high-power amplifiers (pulse duration: 5 ms, regardless of the vibration frequency;
amplitude: 0.25 mm peak-to-peak; Rematic). The vibration frequency
(1–100 Hz) was controlled by a software program (LabVIEW 6i).
HUMAN PROPRIOCEPTIVE MOTION FEEDBACK
A
951
B
FIG. 2. Calculating muscles’ preferred sensory directions (PSDs). A: anatomical model for the “arm–forearm ensemble”: the subjects’ posture determined the
initial state of the model: ␣ ⫽ 105°, ␦ ⫽ 150°, and ␪ ⫽ 90°. The fingertip moved along straight lines in all directions, in 2° steps (to simplify the graphic
representation, only 12 directions are illustrated here). B: the changes in the joint angles ␣, ␤, ␦, and ␥ are represented as a function of the fingertip movement
direction. The maximum value of the function gave the fingertip direction that evoked the largest joint angle, i.e., the PSD of each muscle involved. C: the
anatomical model covering the whole 3-dimensional (3D) space gives the preferred sensory directions of the 6 muscles involved: the biceps brachii (75° in the
xy plane; 90° in the zy plane), triceps brachii (xy: 255°; zy: 90°), pectoralis major (xy: 286°; zy: 90°), posterior deltoid (xy: 102°; zy: 90°), shoulder adductors
(xy: 180°; zy: 19°), and deltoid (xy: 180°; zy: 162°) muscles.
ently oriented straight-line movements and more complex 3D spiral
movements, the trajectories were generated by a computer on the basis
of the mathematical functions giving bell-shaped velocity profiles to
straight-line movements and constant velocity and curvature to 3D
spiral movements. In the second experiment, the writing and drawing
trajectories were previously actively traced by an experimenter on a
digitizing tablet to ensure that the trajectories would be natural, i.e.,
that they would obey the so-called two thirds power law, relating the
movement velocity to the trajectory curvature (Viviani and Stucchi
1992). Trajectories were then filtered (using a Hanning filter with a
half-window of 0.05 s) to smooth out the signals recorded.
Proprioceptive afferent pattern simulation. The afferent patterns
were calculated using an extended version of a method based on the
“population vector model.” This method generates frequency patterns
very similar to those recorded microneurographically during actual
movements (see Fig. 3 in Roll et al. 2009). More specifically, the
tangential velocity vectors of each trajectory (i.e., the vectors describing the instantaneous direction and velocity of the trajectory) were
determined every 200 ms and projected orthogonally onto the previously determined PSD of each muscle to obtain the “population
vector,” giving the Ia afferent feedback originating from the muscle
under consideration. In other words, with each muscle, the mean
instantaneous firing frequency was determined in terms of the cosine
of the angle formed by the tangential velocity vector and the muscle’s
PSD and was taken to be proportional to the instantaneous movement
velocity. In practice, at each time point, the mean firing frequency of
the afferent population from each muscle (F) was expressed as the
J Neurophysiol • VOL
scalar product of the tangential velocity vector (V) and the muscle
PSD (P), using the formulas
→
→
F ⫽ V ⴱ P ⫽ xV ⴱ xP ⫹ yV ⴱ yP
and
→
→
F ⫽ V ⴱ P ⫽ xV ⴱ xP ⫹ yV ⴱ yP ⫹ zV ⴱ zP
This method of computation simulates the direction-dependent cosine
variations in the Ia afferent firing activity. Last, the proprioceptive
streams originating from each muscle were normalized with respect to
the maximum total firing rate obtained across muscles, which was set
to be equal to 100 Hz. Interestingly, the frequency patterns simulated
here in each muscle were almost proportional to the muscle stretching
velocity (Table 1).
Experimental procedure
Experiment 1: inducing straight-line illusory multijoint movements
(2D). The simulated vibratory patterns applied were expected to evoke
straight-line illusory movements oriented in the four directions of a
horizontal Cartesian frame centered on each subject’s fingertip (0, 90,
180, and 270°). These directions were selected to prevent the occurrence of any “oblique effects” (Appelle 1972), given that the perception of diagonal stimuli has been reported to be less accurate than that
of horizontal and vertical ones (Gentaz and Hatwell 1995; M Bergenheim, JC Gilhodes, and J-P Roll, unpublished observations). However, subjects were told that the illusory trajectories could be oriented
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C
952
TABLE
C. THYRION AND J.-P. ROLL
1. Correlation coefficients between simulated frequency patterns and muscle stretch velocity
Muscle
a
b
e
3
6
8
□
⌬
Œ
Biceps b.
Triceps b.
Pectoralis m.
P. deltoid
Mean
0.95
0.99
0.96
0.73
0.95
0.93
0.91
0.83
0.99
0.94
0.96
0.94
0.77
0.71
0.88
0.84
0.87
0.59
0.36
0.72
0.95
0.90
0.96
0.96
0.95
0.92
0.98
0.85
0.91
0.93
0.93
0.84
0.82
0.84
0.87
0.92
0.99
0.71
0.98
0.96
0.96
0.95
0.94
0.93
0.95
Mean
0.97
0.96
0.98
0.92
0.96
0.94
0.96
0.89
0.91
0.93
The anatomical model presented in Fig. 2 was also used to compute the velocity profiles of the joint angle variations, whereas the fingertip was describing
the various 2D writing and drawing trajectories studied in experiment 2. The velocity profiles derived from the changes in the values of of ␣, ␤, ␦, and ␥ defined
in Fig. 2A were assumed to reflect the stretch velocity of the corresponding muscle, i.e., the biceps brachii, triceps brachii, pectoralis major, and posterior deltoid.
Correlation coefficients were then computed between the frequency modulations computed for each muscle and the corresponding muscle stretching velocity.
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Data analysis
Experiment 1. Circular statistical analyses (Batschelet 1981) were
performed on the illusory movement directions indicated by all the
subjects in all the conditions tested. The Watson–Williams test was
used to compare the mean movement directions perceived in the four
experimental conditions. The V test was also used to determine
whether any clusters occurred around the expected orientations, depending on the vibratory patterns applied.
To estimate the overall vividness of the illusory movements, a mean
subjective score was calculated and the rate of occurrence of each
category of subjective score (1, 2, or 3) was determined.
Experiments 2 and 3. In these two experiments, the illusory trajectories copied on the digitizing tablet (experiment 2) or recorded with
the motion analysis system (experiment 3) were first repositioned with
a common starting point. The average shape of each movement was
then determined from all the trajectories. The illusory trajectories
copied by the subjects were then compared with the expected trajectories (those used to compute the patterns of stimulation) by calculating the correlation coefficients of the {x, y} or {x, y, z} coordinates.
In the case of the 3D trajectories, the mean spatial directions of the
illusory movements’ copies were also compared with the expected
ones by computing the vectors giving the general orientation of the
annulospiral trajectories. Last, the criterion used in experiment 2 to
determine whether the participants recognized the illusory movements
was whether they were able to accurately name the symbol formed by
each movement trajectory.
RESULTS
When delivered via a set of vibrators applied to the elbow
and shoulder muscles, the simulated proprioceptive patterns
induced illusory sensations of complex 2D or 3D movements
in all the subjects. The trajectories perceived and drawn by the
subjects formed straight lines, letters, numbers, and geometrical figures in the horizontal plane and 3D figures resembling
annulospirals, the long axis of which was differently oriented,
depending on the vibration pattern used. Moreover, in the great
majority of participants, these illusory movements looked quite
natural in terms of their subjective spatial and kinematic
characteristics, except that the velocity was slower than that of
usual writing and drawing movements and the size was slightly
larger.
Vibration-induced two-joint straight-line illusory
movements (2D)
In all the subjects, propriomimetic vibratory patterns applied
to specific elbow and shoulder muscles induced illusory movements oriented in the cardinal directions (i.e., north, 0°; east,
90°; west, 270°; and south, 180°) on the horizontal plane. The
movements were clearly perceived and continuous: each sub-
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in any direction in the horizontal plane. Each vibratory sequence was
applied three times and the subjects were asked to open their eyes and
quickly look at their hand after each sequence to enable them to
visually recalibrate their actual hand position. After the three stimulations, subjects were asked to define as exactly as possible the
direction of the illusory trajectories they had just perceived, in
minutes, using a picture of a clock face divided into 2.5-min (i.e., 15°)
segments placed under their hand. They were also requested to rate the
vividness of the illusory movements on the following psychophysical
scale adapted from Sheehan (1967).
The illusory sensation of movement evoked by the stimulation was:
● Perfectly clear and precise, like a real perception: score ⫽ 3
● Moderately clear and precise: score ⫽ 2
● Vague and not precise: score ⫽ 1
Each of the four conditions (0, 90, 180, and 270°) was repeated three
times during the experiment, giving three qualitative assessments, and
the order of the various trials was randomized.
Experiment 2: inducing illusory multijoint writing and drawing
movements (2D). The vibratory patterns were expected to induce
illusory movements forming three letters (a, b, and e), three numbers
(3, 6, and 8), and four geometric shapes (a square, a triangle, a circle,
and an inward 2D spiral). As an example, Fig. 1B gives two different
movement trajectories and the corresponding mean afferent patterns
computed by the model. At each trial, the subjects were previously
informed about the general category of movement liable to be perceived—i.e., letters, numbers, or geometrical shapes—and each vibration sequence was applied successively three times. The participants were asked to first name the movement trajectory they had just
perceived and then to draw it with their contralateral hand on a
digitizing tablet, paying special attention to the shape, velocity, and
size of the illusory trajectory. The movement trajectories drawn by the
participants were then sampled at 200 Hz and stored for further
analysis. Each trial was repeated three times during the experiment,
resulting in three drawings per vibratory pattern tested, and the order
of the trials was randomized.
Experiment 3: inducing 3D illusory movements. The simulated
afferent patterns delivered by the set of vibrators were expected to
induce two kinds of illusory movements with 3D annulospiral trajectories: upward-oriented counterclockwise annulospiral and forwardoriented clockwise annulospiral movements. Each vibration sequence
was repeated three times and the subjects were then asked to copy the
trajectory they had just perceived with their contralateral hand, paying
special attention to its shape, general spatial orientation, size, and the
velocity of the movement. A 3D motion analysis system (Codamotion, Charnwood Dynamics) was used to record the movement trajectories copied by the subjects. For this purpose, an active marker was
placed on the tip of each subject’s contralateral index finger and the
trajectories perceived and copied by the subjects were sampled at a
frequency of 200 Hz and stored for further analysis. Each trial was
repeated twice during the experiment, giving two recordings of each
illusory movement, and the order of the trials was randomized.
HUMAN PROPRIOCEPTIVE MOTION FEEDBACK
953
FIG.
3. Individual and mean orientations of the straight-line illusory movements perceived. Black arrows give the illusory trajectories’ expected orientations in the 4 experimental conditions (north: 0°; east: 90°; south: 180°; and
west: 270°), whereas colored arrows give the mean orientations of the corresponding perceived illusory trajectories (blue arrow: 3°; purple arrow: 79°;
gray arrow: 149°; green arrow: 264°). Each of the 4 directions was tested 3
times during the experiment. To illustrate the variability of the direction of the
illusory movements, thin gray lines give the movement orientations perceived
by the 11 subjects in the 3 trials run in each experimental condition. Thin
colored lines give the interindividual variability: in each experimental condition, each of the lines was computed by averaging the movement orientations
perceived by one subject in the 3 trials.
ject’s fingertip followed a straight line oriented in a specific
direction, depending on the vibration pattern used. In some
subjects, kinesthetic posteffects occurred in the direction opposite to that of the previous illusion. The subjects’ qualitative
assessments, which were rated on a subjective scale (Sheehan
1967), show how lifelike these illusory sensations of movements were (mean score ⫽ 2.5/3). Overall, the subjects perceived the illusory movements “as clearly and precisely as a
real perception” in about 60% of the trials. The remaining
TABLE
Vibration-induced illusory two-joint writing and drawing
movements (2D)
When used to control the sets of vibrators placed on the
elbow and shoulder muscle tendons, the complex vibratory
patterns based on actual writing and drawing trajectories
evoked illusory sensations of arm endpoint displacement (corresponding in this case to the displacement of the pencil tip).
These perceived trajectories, which all subjects drew by hand
on the digitizing tablet, clearly resembled the outlines of
various letters, numbers, and geometrical figures, depending on
the vibration pattern used. They varied in shape and size
between subjects. All the illusory trajectories drawn by the
subjects are given in Fig. 4, along with the mean trajectory of
each writing or drawing movement. These mean shapes were
very similar to the expected ones, i.e., those originally used to
compute the proprioceptive patterns applied.
To analyze whether the illusory trajectories (the subjects’
drawings) matched the expected ones, correlation analyses
were carried out on the x and y coordinates of each type of
trajectory. High levels of correlation were found to exist
between the experimentally induced and expected illusory
2. Circular statistical analyses on the straight-line illusory movements
A
1
¡
2
¢
Expected orientation
Mean orientation
SD
v
u
P value
0°
3.26°
31.59°
0.858
6.967
⬍0.001
90°
78.53°
15.91°
0.943
7.661
⬍0.001
180°
149.19°
42.39°
0.653
5.307
⬍0.001
270°
263.72°
12.681°
0.97
7.88
⬍0.001
B
1 vs. ¡
1 vs. 2
1 vs. ¢
¡ vs. 2
¡ vs. ¢
2 vs. ¢
F (Watson–Williams test)
P value
143.71
⬍0.001
215.08
⬍0.001
265.22
⬍0.001
79.05
⬍0.001
1952.3
⬍0.001
206.77
⬍0.001
A, left to right: Columns 1– 4 correspond to the four differently oriented straight-line movements tested, which are described by arrows: 0°-oriented illusory
trajectory (1), 90°-oriented illusory trajectory (¡), 180°-oriented illusory trajectory (2), 270°-oriented illusory trajectory (¢). Top to bottom: illusory
trajectories’ expected orientations; mean orientations computed from the illusory trajectory orientations indicated by all the subjects; circular SD values;
corresponding V-test values (v, u) and associated P values. B: comparisons between the mean directions of the illusory trajectories in the various experimental
conditions: statistical values (Watson–Williams F tests) and the corresponding P values.
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movements were rated “moderately clear and precise” (31.8%)
or “vague and imprecise” (8.3%).
The individual and mean orientations of the trajectories
perceived in all four experimental conditions are shown in Fig. 3.
The directions of the illusory trajectories indicated by the
subjects showed a significant tendency (V test, P ⬍ 0.001) to
cluster around the expected trajectory directions (see Table 2A). In
addition, depending on the vibratory pattern used, the mean
directions of the four spatially oriented illusory movements
differed significantly (Watson–Williams test, P ⬍ 0.001; see
Table 2B). When delivered via the sets of vibrators, each
proprioceptive pattern therefore evoked a highly specific illusory trajectory in terms of its orientation.
All in all, this model therefore seems to provide an efficient
means of mimicking the Ia proprioceptive feedback evoked
during the execution of differently oriented straight-line movements involving the simultaneous stretching of the elbow and
shoulder muscles, since these proprioceptive patterns evoked
the expected appropriately oriented movements when they
were used as vibratory stimuli.
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C. THYRION AND J.-P. ROLL
FIG. 4. Illusory vibration-induced writing and drawing
movements. Dark gray lines give the trajectories used to compute the vibration patterns in the case of 3 letters (a, b, and e),
3 numbers (3, 6, and 8), and 4 geometrical shapes (square,
triangle, circle, and 2D-inward spiral). Thin gray lines give the
individual trajectories perceived and copied by each subject and
the average shape is given by a bold superimposed outline.
Vibration-induced illusory two-joint annulospiral
movements (3D)
The proprioceptive vibratory patterns computed from complex 3D trajectories and applied to various elbow and shoulder
muscles induced the expected illusory movements (Fig. 5). The
perceived trajectories actively copied by the subjects and
recorded using a 3D motion analysis system closely resembled
the two original differently oriented annulospiral movements
used to compute the proprioceptive patterns (Fig. 5B). High
levels of correlation were found to exist between these expected 3D trajectories and the corresponding mean illusory
trajectories (Table 3B). However, some differences in shape,
size, and general orientation were observed, depending on the
subjects. Figure 5C shows in addition that the mean orientations of the annulospirals were very similar to the expected
ones (see also Table 3B).
In short, these results show that our “propriomimetic method”
can be used to simulate the Ia proprioceptive feedback evoked by
2D or 3D arm movements, as shown by the fact that when
delivered by specific sets of vibrators, these proprioceptive patterns elicited the expected illusory movements, the trajectory of
which is virtually described by the arm endpoint.
TABLE
DISCUSSION
When subjected to propriomimetic vibratory patterns, the subjects were mostly convinced that the illusory movements had
actually occurred: they were generally perceived as resulting from
“internal forces” and therefore seemed to be very similar to
voluntary actions, although they were not generated intentionally
(Roll et al. 1996; Thyrion and Roll 2009). In all subjects, the
proprioceptive patterns delivered by the sets of vibrators
placed at elbow and shoulder levels evoked illusory arm
endpoint displacements driven by the arm–forearm ensemble. Depending on the pattern used and the muscles vibrated,
the trajectories perceived corresponded to either differently
oriented straight lines, letters, numbers, or geometrical figures in the horizontal plane or complex 3D figures, which
were highly correlated with those initially used to compute
the proprioceptive patterns.
Predicting the proprioceptive feedback evoked by any
arm movement
The propriomimetic method tested here was designed to
approximate the Ia afferent patterns evoked by any movement
performed by the arm–forearm ensemble in 2D or 3D space. In
our previous study (Roll et al. 2009), the rules used to calculate
the Ia afferent feedback were directly based on physiological
data recorded from humans during individual joint movements
3. Correlation coefficients between expected and illusory movement trajectories
A
Coordinate
a
b
e
3
6
8
□
⌬
Œ
x
y
0.90
0.97
0.51
0.77
0.66
0.85
0.92
0.96
0.80
0.88
0.84
0.96
0.93
0.99
0.98
0.99
0.97
0.98
Upward Counterclockwise Annulospiral
B
Trajectories correlation
Orientation vector
Theoretical values
Mean values
Circular SD values
x
0.99
0
⫺0.2
Mean
0.92
0.95
0.89
0.95
Forward Clockwise Annulospiral
y
z
x
y
z
0.98
0.93
0.99
0.99
0.98
0
0.19
31.62°
1
0.96
0
0.05
1
1
35.27°
0
0
A: Correlation coefficients of the x and y coordinates describing the expected writing and drawing trajectories and the mean shape of each illusory movement,
based on the illusory trajectories copied by all the subjects. B, top line: Correlation coefficients of the x, y, and z coordinates describing the expected and mean
upward and forward annulospirals. Three bottom lines: Theoretical coordinates of the vectors defining the expected general orientations of the annulospiral
trajectories; coordinates of the mean vectors based on all the subjects’ drawings; and the corresponding circular SD values.
J Neurophysiol • VOL
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trajectories (rx ⫽ 0.89; ry ⫽ 0.95, Table 3A). In addition, the
symbols formed by the various illusory trajectories were correctly named by the subjects in 80% of the trials.
HUMAN PROPRIOCEPTIVE MOTION FEEDBACK
A
C
B
Vibration frequency
955
100 Hz
0
Time
0
FIG. 5. Illusory vibration-induced annulospiral movements. A: vibratory patterns used to induce the upward counterclockwise annulospiral illusory movement
(top) and the forward clockwise annulospiral illusory movement (bottom): the vibration frequency applied to each muscle is given as a function of time. B: dark
gray lines give the expected upward (top) and forward (bottom) annulospiral trajectories. Bold black lines give the mean trajectories based on all the subjects’
copies of the illusory trajectories. C: dashed gray lines give the expected general orientations of the illusory annulospiral movements. Thin gray lines give the
interindividual variability: each line gives the general orientation of the trajectory perceived by one subject and the mean orientation vector based on all the
subjects’ recordings is superimposed (black vector).
(Bergenheim et al. 2000; Jones et al. 2001). These rules obeyed
a “population model” in which each muscle spindle ensemble
present in a given muscle makes an instantaneous contribution
to the coding of the direction and velocity of the ongoing
movement (Jones et al. 2001; Roll et al. 2000, 2004, 2009;
Verschueren et al. 1998). The present propriomimetic method
was based on these previous neurosensory data and the results
obtained, which show that the simulated patterns accurately
mimicked the Ia firing patterns evoked by passive arm movements, confirm that the “population vector model” previously
used to describe the Ia afferent feedback associated with
individual joint movements is also applicable to the case of
multijoint 3D movements. It will certainly also be possible to
use this method to mimic the proprioceptive feedback evoked
by movements performed with other musculoskeletal systems.
It might therefore be possible to extend the scope of this
method to include most human actions.
However, extending the propriomimetic method to multisegment movements and 3D space required making considerable
changes. First, the match between a muscle’s PSD and that of
the illusion perceived when this muscle is vibrated (Bergenheim et al. 2000) no longer exists in the case of multisegment
movements and even more so when they occur in 3D space.
The muscle’s PSD, an essential parameter defined as the
movement direction that lengthens the muscle the most, was
therefore computed in a Cartesian frame centered on the
position of the endpoint, by taking the biomechanical characteristics of the musculoskeletal ensemble executing the movement (the limb segment lengths, the number of joints, and the
degrees of freedom) into account. Interestingly, the cosineJ Neurophysiol • VOL
shaped decrease in the Ia firing rate observed on both sides of
the PSD actually reflects the direction-dependent decrease in
the muscle stretching rate and the Ia firing rate modeled is thus
almost proportional to the muscle stretching velocity. Under
our experimental conditions, the Ia firing patterns associated
with the muscle stretching velocity sufficed to induce predictable illusory trajectory perceptions. However, in many previous studies on cats, monkeys, and humans, recordings performed during ramp and hold stretching, sinusoidal stretching,
and normal locomotion have shown that the Ia and II afferents
clearly respond to changes with time in both the length and the
velocity parameters (e.g., Poppele and Kennedy 1974;
Prochazka and Gorassini 1998). The use of velocity alone in
the present study was thus a simplification, especially compared with one of our previous reports in which length plus
velocity were used to drive the vibration frequency (Gilhodes
et al. 1993). It is quite surprising that the subjects in the present
study perceived the illusory movements as accurately as they
had in the previous study. This suggests that in the two studies
the sensory inputs evoked by tendon vibration are permanently
decoded by the CNS in terms of both movement velocity and
displaced spatial position. Finally, it is worth noting that the
specificity of our method is the introduction of a major parameter in the modeling procedure: the instantaneous movement
orientation.
The situation is much more complex in the case of active
movements, during which the Ia firing rate may also reflect
the influence of the fusimotor drive (e.g., Dimitriou and
Edin 2008a; for reviews, see Hulliger 1984; Prochazka
1996) and the amount of tendon strain exerted (Dimitriou
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100 Hz
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C. THYRION AND J.-P. ROLL
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of the same movement when it is returned to the subjects via
muscle tendon vibration, even when the frequency range
used resembles that of the natural Ia spiking that occurs in
humans (Albert et al. 2006). The kinesthetic illusions induced result from the central processing of the proprioceptive messages triggered by the vibration, which simulate the
natural inputs evoked by the simultaneous and/or successive
muscle stretching occurring during a given movement. In
addition, since the subjects’ posture remains unchanged
throughout the vibration periods, the CNS might continuously update the perceived hand position on the basis of the
ongoing Ia proprioceptive inputs.
However, in experiments of this kind, the question inevitably arises as to whether the participants were actually replicating the illusory movements evoked by vibratory stimulation. In
a study in which similar symbolic illusory movements were
induced, Albert et al. (2006) established that the subjects
copied the illusory trajectory they perceived rather than producing their own usual handwriting. This was particularly
obvious in the case of the number “8”: the expected and
reproduced trajectories both started with an upward movement
to the left, whereas a significant proportion of the subjects
usually write this number starting with a downward movement
to the left (Albert et al. 2006; Fig. 3C). In addition, the
correlation coefficients between the vectors describing the
symbols copied and the subjects’ usual handwriting trajectories
were distinctly lower than those calculated between the expected and reproduced trajectories. In the present study, an
additional control experiment confirmed that the subjects
were accurately reporting the illusions they had felt: three
volunteers were subjected to vibratory patterns intended to
induce 2D spiral trajectories, without being informed about
the direction of the rotation or whether the spirals were
inward or outward ones. As shown in Fig. 6, none of these
subjects made any mistakes in this experiment, which confirms that they were actually reporting the illusory trajectory
they had perceived and not a “standard” spiral movement
they might have had in mind.
Since our “propriomimetic” method of simulation can be
used to induce the illusion that a motionless body segment is
moving and to specify the parameters of the forthcoming
illusory movement, this method should provide a useful tool
for rehabilitation purposes. Imaging studies performed during
vibration-induced illusory movements have indeed clearly
shown that a perceptuomotor transform occurs at the cortical
level (Calvin-Figuière et al. 1999, 2000), which strongly activates the corresponding motor areas (Casini et al. 2006; Duclos
et al. 2007; Hagura et al. 2009; Naito et al. 1999; Romaiguère
et al. 2003). Appropriately patterned vibrations could therefore
be used to maintain the activity of sensorimotor cortical network in the absence of any actual movement. Clinical studies
have reported, for example, that a vibratory treatment applied
during limb immobilization improved the patients’ movement
amplitude after the cast had been removed (Neiger et al. 1986)
and preserved the extent and functional properties of the
sensorimotor cortical network involved (Roll R 2010). It has
also been reported that hand mobility was clearly improved in
algodystrophic patients in response to vibratory treatment (Gay
et al. 2007).
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and Edin 2008b; Fukanaga et al. 2001; Griffith 1991;
Kawakami et al. 2002). Other types of feedback, such as the
force feedback originating from the Golgi tendon organs,
are also obviously involved in the performance of active
tasks (Jami 1992; Proske 2005). In addition, when movements are performed under active conditions, one cannot
rule out the possible contribution of information originating
from the motor command itself, the so-called efferent copy,
which is known to contribute to the perception of voluntary
movements (Desmurget et al. 2009; Jaeger et al. 1979;
McCloskey 1981): this information itself may also generate
visual field displacements (Teuber 1972) or body movement
sensations (Gandevia et al. 2006), even when proprioceptive
feedback is available (Smith et al. 2009), as occurs in the
case of the voluntary command of paralyzed muscles. Although all this information is necessarily processed by the
CNS during active movements, the present model was specifically developed on the basis of the muscle spindle activity recorded during passively imposed movements and it
has proved to work efficiently under our experimental conditions, where the subjects were both passive and motionless
(i.e., presumably in the absence of fusimotor drive). Interestingly, the present results are to be linked with those
obtained using models based on spindle recordings carried
out on freely moving animals, which accurately predicted
the Ia afferent feedback, taking only the changes in muscle
length into account (Prochazka and Gorassini 1998). When
these models were used to simulate active behavior, the
predictions could be slightly improved by adding small
electromyographic signal components to mimic the fusimotor activity.
The fact that Ia proprioceptive feedback alone evoked
such complex illusory movements supports the now widely
recognized idea that muscle spindles contribute importantly
to kinesthesia (Cordo 1990; Gandevia 1996; Gandevia and
Burke 1992; Proske and Gandevia 2009; Roll et al. 1996).
However, we cannot rule out the contribution of other
sensory modalities, especially the tactile modality (Aimonetti et al. 2007; Burke et al. 1988; Edin 2004), since simple
illusory movements can also be evoked by stimulating cutaneous afferents by stretching the skin (Collins and
Prochazka 1996; Collins et al. 2005). Under the present
experimental conditions, the activation of the skin receptors
located just under the vibration probes might have reinforced the illusions of movement perceived. However, the
contribution of skin receptors to the illusion can be assumed
to be relatively modest, since powerful illusory movements
can be evoked directly by stretching exposed tendons in
humans (McCloskey et al. 1983) and anesthetizing the skin
under the vibrator heads does not significantly affect the
vibration-induced illusory movement (Roll 1981).
Among the advantages of this model is the fact that it can
be used to supply motionless subjects’ proprioceptive channels with well-patterned afferent information via muscle
tendon vibration, which is a well-known and highly reliable
method (Burke et al. 1976; Goodwin et al. 1972; Roll and
Vedel 1982; Roll et al. 1989). Illusory movements were
recently evoked in subjects by applying muscle tendon
vibration patterns exactly copying natural Ia afferent frequency modulations. The results showed that the Ia afferent
feedback evoked by a given movement induces the illusion
HUMAN PROPRIOCEPTIVE MOTION FEEDBACK
Center in clockwise
initial
S1
Center out clockwise
average
S2
S3
initial
S1
average
S2
S3
average
S2
S3
Center out counterclockwise
initial
S1
average
S2
S3
FIG. 6. Altering the vibration pattern affects the parameters of the illusory
trajectories. Black lines give the initial trajectories used to compute the
vibration patterns in the case of 4 different spirals (2 different directions of
rotation, clockwise or counterclockwise, and inward or outward trajectories).
Each trial was repeated twice during the experiment: thin gray lines give the 2
individual trajectories perceived and copied by each subject (S1, S2, and S3)
and the corresponding average shape, computed from all these trajectories, is
given in dark gray. The arrows indicate the direction of rotation of the inward
and outward spirals.
Does the illusory endpoint trajectory result from the
perceptual integration of the proprioceptive feedback
originating from all the muscles involved?
Back in 1947, Bernstein defined the “motor equivalence
principle,” according to which motor invariants are involved in
the performance of writing tasks, since the shape of a graphic
sign remains almost unchanged, irrespective of which effector
is used to trace it (e.g., hand, shoulder, or foot). This principle
may basically support the idea that movements might be
represented in terms of limb endpoint trajectories.
Studies based on the use of vibratory stimulation have
yielded convincing evidence in favor of this idea by showing
that the afferent streams arising concomitantly or successively
from the muscles surrounding a given joint are completely
integrated, giving rise to a single kinesthetic percept referred to
the limb endpoint. It was established, for example, that two
illusory hand movements evoked simultaneously in orthogonal
directions combine to form a single percept consisting in an
oblique trajectory (Roll et al. 1996). Likewise, applying appropriate multivibration patterns to the wrist muscles elicited a
single illusion that the hand was drawing a unique graphic
J Neurophysiol • VOL
symbol (Albert et al. 2006; Roll et al. 1996, 2009; Thyrion and
Roll 2009). These findings certainly mean that the multiple
proprioceptive messages evoked by performing a movement
are not integrated in terms of perceptual cues about muscle
lengths or joint angles, but in terms of the dynamic displacement of the limb segment’s endpoint. Afferent feedback from
all the muscles involved is therefore integrated by the CNS to
form the only behaviorally relevant cue (i.e., the perceived
endpoint trajectory), since all the muscles involved ultimately
contribute to achieving a single motor goal and its perceptual
representation. The idea that all these proprioceptive messages
may specify the ongoing displacement of the segment tip is
also supported by psychophysical data obtained during forearm
position matching tasks, in which the errors were consistently
smaller when the subjects were requested to match their limb
orientation (Soechting 1982) or arm-tip position (Fuentes and
Bastian 2010) than when they had to match their joint angles.
The idea that the CNS may require information about the
ongoing trajectory of the limb endpoint rather than other
biomechanical parameters such as the muscle lengthening or
joint angle variations is also consistent with previous neurophysiological data obtained in animal experiments. Unitary
recordings from the dorsal root ganglia of anesthetized cats
showed that the Ia firing rate tends to be highly correlated with
the endpoint position measured in polar coordinate terms
relative to the hip (Stein et al. 2004). Another study on walking
cats has also suggested that movement representations may be
more accurate when they are based on endpoint coordinates
rather than joint coordinates (Weber et al. 2006, 2007). In
addition, recordings of second-order proprioceptive cat dorsal
spinocerebellar neuron activity (Bosco and Poppele 1993,
1997; Bosco et al. 2000) showed the existence of a linear
relationship between the segment-tip position and the singlecell firing rate, which persisted in about half of the neurons
after the endpoint position had been decoupled from the limb
geometry using mechanical constraints. Likewise, unitary recordings on the primary sensory cortex of behaving monkeys
showed that the cortical neurons were broadly tuned to the
movement direction and hand position (Prud’homme and
Kalaska 1994; Tillery et al. 1996). Data on the motor aspects
have also suggested that the activity of motor cortical neuronal
populations predicts the kinematics of the limb endpoint (Georgopoulos et al. 1982; Kakei et al. 1999; Schwartz 1994).
Based on all these data, the most noteworthy feature of the
present model seems to be the fact that processing the Ia
afferent feedback using population vector model principles
makes it possible to transform local sensory information reflecting muscle lengthening into a more functional endpoint
trajectory representation.
In conclusion, our propriomimetic method can be said to be
fairly natural, since it was based on the muscle spindle afferent
activity recorded in humans. The simulated patterns used here,
which can be said to be substitutes for the Ia proprioceptive
feedback evoked by any human arm movement, could certainly
be extended to other musculoskeletal ensembles. The fact that
these simulated proprioceptive patterns can be used to induce
motor illusions in motionless humans suggests that they may
provide a valuable tool for motor rehabilitation and learning
purposes.
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Center in counterclockwise
initial
S1
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C. THYRION AND J.-P. ROLL
ACKNOWLEDGMENTS
We thank N. Kinderstuth for the biomechanical modeling and Dr. Jessica
Blanc for revising the English manuscript.
GRANTS
This research was supported by grants from Agence Nationale de la
Recherche and Association Française de Lutte contre les Myopathies.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
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