JOURNAL O F NEUROPHYSIOLOGY
Vol. 67, No. 2, February 1992. Printed in U.S.A.
Automatic Control During Hand Reaching at Undetected
Two-Dimensional Target Displacements
CLAUDE PRABLANC AND OLIVIER MARTIN
Vision et Motricite, Institut National de la Sante et de la Recherche Medicale, Unite 94, F-69500 Bron; and Laboratoire
RESACT UFR-APS, Equipe Comportement Moteur, Universite Joseph Fourier BP53X, F-38041 Grenoble Cedex, France
SUMMARY AND CONCLUSIONS
1. The aim of this study was to demonstrate that goal-directed
pointing movements, executed at normal speed to a small visual
target, but without vision of the movement, do not rely on preprogrammed commands (open-loop process); by contrast these responses are under the control of a feedback loop, which compares
the ongoing response and the goal (or its internal representation).
When the location of this goal is changed at the onset of the movement, an automatic correction of the path occurs. Modification of
the goal was obtained by presenting a target in the peripheral visualfieldthat the subject had to look at and point at as quickly and
accurately as possible. When the orienting ocular saccade reached
its peak velocity, statistically corresponding to the hand movement onset, the target was suddenly shifted 10° in a random direction. This perturbation was undetected by the subject because of
the absence of perception during the saccade. For the compensation to occur, the initial orientation of the movement and also its
extent had to be modified. The results revealed 1) a nearly complete compensation of the movement path and a 66- to 80-ms
duration lengthening; 2) relatively short reaction times to the perturbations (from 145 to 174 ms, with effective reaction times even
40 ms shorter); 3) nearly identical spatiotemporal movement
characteristics to the perturbations, regardless of whether vision of
the hand was allowed, suggesting that corrections were subserved
by the same mechanisms.
2. The spatiotemporal characteristics of these unconscious corrections were similar to those observed in the classical double-step
experiments investigating the intentional modifications of ongoing movements and suggest that they might share some common
low-level mechanisms. That is, they could rely on visuokinesthetic
feedback loops, which compare the updated information provided
by the eye at the end of the saccade and the proprioceptive information of the end point effector (the fingertip here); they could
also rely on feed-forward processes detecting the discrepancy between an efference copy of the movement and the new goal; or
they could rely on a combination of those two main processes.
sponses that result from intentional corrections to a previously selected response.
Although the complexity of the sensorimotor systems has
led to controversial issues, there are two commonly well-accepted views on goal-directed actions. One assumes that the
initiation of a goal-directed movement depends essentially
on the selection of a preset group of muscles, where learning
or practice plays an essential role in tuning muscle activity.
The second considers that of the role of the visual feedback
provided by the simultaneous vision of the goal and of the
moving hmb. This feedback is believed to permit a correction of small errors of the ongoing motor program, provided the movement is not too fast. Since Woodworm
(1899), the role of visual feedback from the moving hmb
(called visual reafferences) in controlling the final accuracy
of an aimed response has been widely investigated (see
Georgopoulos et al. 1981; Keele 1981; Jeannerod 1988 for
review). Although, in the earliest studies the minimum delay for correcting a movement was evaluated at 500 ms, it
has been recently shown to go down to 200, or even to
100-150 ms, according to the level of predictability (Carlton 1981). In the present experiment visual reafferences
were also manipulated, but they exhibited such little influence that the paper will focus less on these aspects.
Double-step paradigm
At the experimental level, a fruitful! approach to the organization of a goal-directed movement has consisted in the
use of stimuli eliciting simple motor responses, associated
with a kinematic analysis, to infer some properties of the
motor systems involved. One way to investigate whether an
intended action results in a preset unmodifiable series of
commands is to observe to what extent a change in the prior
goal, during or after the motor response initiation, influences the temporal and spatial characteristics of the reINTRODUCTION
sponse. This type of paradigm, known as the double-step
The purpose of this paper is to elucidate some of the paradigm, was initially introduced in the study of the oculomechanisms responsible for the achievement of a correct motor system to gain insight into the rules of organization
motor response in the prehension space, such as pointing at of this "simple" motor system (Becker and Jurgens 1979;
a small visual target. The central idea is that a goal-directed Westheimer 1954; Wheeless et al. 1966). It was shown that,
movement that follows a path not entirely predetermined after the decision to execute a saccade to a target, there was
regardless of vision of the hand depends on automatic pro- no need to wait until completion of the previously initiated
cesses computing dynamic errors. As such, the response is response, before taking into account a new target as a goal.
modified in flight without even reaching the intentional Although the preceding double-step paradigms produced
level. This phenomenon, thought to be a very general prop- stimuli lying along the same horizontal line, which will be
erty of aimed motor responses, will be compared with the referred to as "one-dimension double step," further experinow well-documented studies on overlapping motor re- ments have used this paradigm with stimuli implying
0022-3077/92 $2.00 Copyright © 1992 The American Physiological Society
455
456
C. PRABLANC AND O. MARTIN
changes not only in the amplitude of the response but also
in its spatial orientation that will be referred to as a "two-dimensions double step." With the use of the latter one, van
Gisbergen et al. (1987) found curved saccades when the
second stimulus implied a large change of eye movement
orientation.
One of the early attempts, showing that parallel processing applied also in the hand motor control system, was performed in monkey using arm movements in the horizontal
plane (Georgopoulos et al. 1981). With the use of a two-dimensions double-step paradigm, they found reaction time
to the second stimulus similar to the normal reaction time
to the first stimulus (240 ms). The authors concluded that
the second stimulus had continual and effective access to
the process generating the aimed arm movement.
With a one-dimension double step, Megaw (1974)
showed in human, that if the second step was applied < 100
ms after the first one, it influenced the peak hand velocity.
With a two-dimensions double-step paradigm, Soechting
and Lacquaniti (1983) found electromyographic (EMG)
changes as low as 110 ms related to early modifications of
the trajectory. These latencies, although very low, were
equal to the normal latencies for a single-step trial, and thus
confirmed Georgopoulos et al.'s earlier findings (1981).
With the use of a one-dimension double-step design, Gielen
et al. (1984) similarly showed, with muscle activity, that
reaction time to the second step stimulus was even shorter
than the reaction time to a single-step stimulus. Recent experiments in man (Van Sonderen et al. 1988), with the use
of a paradigm similar to Georgopoulos et al.'s (1981),
showed early modifications in the initial spatial orientation
of the movement with a 200-ms reaction time to the second
step.
stimulus when it occurs. Although most double-step studies
have carefully considered the problem of prediction by introducing very few and randomly distributed perturbations, the problem of switching strategies cannot be
avoided; thus the modification of an ongoing motor response does not necessarily imply theflexibilityin the initial response but only shows the possibility of overlapping
responses. One may wonder whether the same fast corrections would be observed if the second step was made undetectable, and if the subject was uninformed of this doublestep stimulus. The idea followed by Goodale et al. (1986)
and Pelisson et al. (1986) was that, if such a mechanism
was observed, it would be very likely the same as that involved in corrections of an inaccurate initial response toward a stationary target. .
To show that the execution of a movement was likely to
be under the control of a gaze to hand guidance loop, independently from the visual reafference of the hand, they
imagined a one-dimension double-step paradigm, in which
perturbations would not be consciously detected by the
subject, by changing the target position during the orienting
saccade to it. The goal, by contrast with the above double
step, was unique. There was a full, although unconscious,
compensation for the perturbation without noticeable increase in duration. The major criticism to this procedure is
that the observed corrections may have been a "local" phenomenon related to the constant orientation of the movement, and only reflecting a limited capacity of the sensorimotor system to automatically modulate the amplitude of a
response.
Rationale
The present paper, through a feedback two-dimensions
double-step stimulus paradigm, intended to generalize the
findings from Goodale et al. (1986) by the introduction of
Synchronous undetected double-step feedback
undetectable perturbations implying complete changes in
By contrast with the above double-step studies in which hand movement path. It tried to extend the notion of autothe second step was applied a given delay after thefirstone, matic corrections from movement amplitude to both moveother studies have synchronized the second step with the ment amplitude and orientation, when undetected perturmovement onset to the first step, resulting in a first re- bations were introduced (see Fig. 1). The idea was that the
sponse initiated before any information on the second step previously observed corrections were not only modulations
was available. This feedback double-step stimulation tech- of the amplitude of the response, but that they were the sign
nique has been proved to be a very fruitfull technique in of a more general process in which, after its initiation, the
both eye and hand movements (Pelisson et al. 1986; Pra- unseen hand trajectory was driven by target visual informablanc and Jeannerod 1975). With the use of the same tech- tion when it began to deviate from its goal. An underlying
nique, Alstermark et al. (1990) found that cats could switch hypothesis was that the introduction of hand visual reafferthe orientation of an ongoing target-reaching forelimb ences would not modify drastically the corrective processes.
movement, within 83-118 ms after the second step. AnalyzThe main questions were as follows: 1) are on-line unining more complex movements in grasping objects in which tended corrections observed when not only the amplitude
location was perturbed at the onset of hand movement, of the movement is modified but also its spatial path (or
Paulignan et al. (1990) noticed early changes of the wrist orientation); 2) when the orientation of the second step is
acceleration as low as 100 ms after the hand movement such that it implies a curvature reversal of the original path,
onset. The results obtained in these feedback double-step can it be achieved on line when executing the response; 3)
experiments showed the same flexibility of the initial re- are corrections for changes in orientation more time consponse as for the classical double steps.
suming than those previously observed for changes in amIf there is a general agreement on the correction delays plitude only; 4) what is the earliest spatiotemporal cue indiobserved in all the above double-step experiments, it is that cating a departure of the perturbed paths from the unperthe delays deal with intentional modifications of the con- turbed paths; and finally, 5) what is the exact contribution
tents of motor commands during the early part of the re- of the external visual feedback loop (which compares the
sponse; they all assume an a priori knowledge of a two- whole hand-limb trajectory and target location) with restimuli sequence, with the instruction to react to the second spect to other possible internal loops?
ON-LINE CONTROL OF HAND REACHING
457
FIG. 1. Experimental display. The subject sitting in front of the pointing table
had to point with his forefinger tip at visual targets that randomly appeared in his
right visual hemifield. Three types of targets were presented: 1) the unperturbed
single-step targets (PO) at 20, 30, and 40°
of eccentricity; 2) the perturbed doublestep targets (P—), in which the initial target location was changed during eye and
hand response movement toward a less eccentric one, targets noticed 20- (from 20
to 10°), 30- (from 30 to 20°), and 40(from 40 to 30°); and 3) the perturbed
double-step targets (P+), in which the
change of target location was to a more
eccentric one, targets noticed 20+ (from
20 to 30°), 30+ (from 30 to 40°), and
40+ (from 40 to 50°). The eye and hand
trajectories were respectively recorded by
an electrooculographic system and a Selspot infrared camera that detected the position of an infrared light-emitting diode
(LED) stuck on thefingertip.A fast light
electronic shutter (3-5 ms of response
time) was used to cut off all subject visual
reafferences from the limbs and body
(open-loop pointing) while maintaining
vision of the target. RP, resting position
(initial starting point of the hand); FP, visual fixation point; PT, peripheral pointing target.
METHODS
The general procedure was the same as in the Goodale et al.
experiment (1986), but used a two-dimensions double-step feedback, instead of a one-dimension double-step feedback. It was
carried out by introducing a perturbation of target location during
the orienting saccade to the target to which the subject had to
point. The horizontal table on which hand movements were performed was a 1.50-m-deep by 2.00-m-wide flat isotropic surface
without visual frame of reference. Underneath the table was a
matrix of red light-emitting diodes (LEDs) disposed along a 65cm-radius circle with angular deviations from center ranging from
0 to 10, 20, 40, and 50° on the right hemispace (Fig. 1). The
subject's head was at 40 cm above the center of this polar coordinate system. The initial starting point of the hand (resting position, RP) was in the subject's sagittal plane 30 cm behind the 0°
fixation point (FP). A chin and forehead rest allowed to position
subject's head. He/she was instructed to keep his head still when
orienting both his eyes and hand toward a peripheral target (PT).
Eye movements were monitored with an electrooculographic
(EOG) method with the use of disposable Ag-AgCl electrodes of
low impedance (100 i2) and disposed near the outer canthi of the
eyes, which gave the orientation of an equivalent cyclopean eye.
The subject's task was to look and point with his fingertip as
quickly and accurately as possible once a target was lit. The trial
sequence was the following: the room was initially illuminated,
the eyes were foveating FP while the finger was on RP, then FP
was turned off while a randomly selected PT was simultaneously
turned on, the subject having simultaneously to look and point at
PT. At peak velocity of his orienting saccade, an electronic shutter
cut off the illumination of the room in such a way that the only
point remaining visible was PT, the whole limb becoming instantaneously invisible. The instant of peak saccadic velocity, as will be
seen in the results, statistically corresponded, within some tenths
of a millisecond, to the onset of hand movement; thus visual reaf-
ferences from the hand movement were removed near the onset of
hand movement. The saccadic eye movement toward PT could
randomly have no effect on PT (single-step stimulus), or move PT
10° to the left (perturbation left noticed "P—") or to the right
(perturbation right noticed " P + " ) along the arc of circle of PTs
centered on the subject's head (see Fig. 2 A). After two s of presentation of a simple or composite PT, the stimulus went back on FP.
At the onset of the return hand movement toward FP, the room
was illuminated, allowing visual feedback from the hand, and thus
a perfect coincidence between the proprioceptive and the visual
cues for the next trial. For the return hand movement, the subject
was instructed to accurately move his fingertip on RP and his eyes
to FP.
The rationale for having different initial positions of the eyes
(FP) and the hand (RP) was to work roughly along the horizontal
meridian for the retina, and to show up changes in orientation for
the hand pointing; indeed, if the initial starting point for the hand
had been FP, we would have mostly seen changes in amplitude of
the movement, and very little ones in its orientation (see Fig. 1).
Recording techniques and control of real-time feedback
piloting of the experiments
The experiments were fully controlled on-line by a program run
on a PDP 11/73. To stabilize both EOG gain and drift, subjects
waited for 20 min before starting the experiments. However, as
drift could not be perfectly nullified, a special electronic device
produced a zeroing of the EOG offset at the time a peripheral
target appeared (Prablanc et al. 1978). Electronic Butterworth
derivative filters allowed to compute both velocity and acceleration. Once the velocity had reached a level twice over its maximum noise, the time of zero crossing of the acceleration (i.e., peak
velocity) was detected, and a logical pulse was sent to the com-
C. PRABLANC AND O. MARTIN
458
single step (PO)
/eye/^
^^Tiand
step 1
no perturbation -
double step"+" (P+)
step*
J
/^-
step 1
step 2
eye velocity hand vision -
eye latency
f
^
double step"-" (P-)
r ^ -
step 1
/
on
off
peak acceleration
/ \ peak velocity
hand
acceleration •
hand velocity •
peak deceleration
deceleration time
acceleration
I ime
j
i
target
hand latency ihand movement time:
n o . 2. A: spatiotemporal organization of eye and hand movement in the 3 different pointing conditions. First trace:
single-step stimulus (PO) in which the target jumps from the central position to a randomly determined stationary peripheral
position. Second and third trace: double-step stimulation in which the target jumps once more after the 1st step (step 1)
either to a more eccentric position [perturbation right (P+)] or to a less eccentric position [perturbation left (P—)]. Fourth
andfifthtrace: at the peak eye velocity, the vision of the hand was cut off(open loop), and the double-step stimulation was
applied simultaneously, corresponding also to the hand movement onset (see the 7th trace showing the kinematics of hand
tangential acceleration and tangential velocity). B: kinematic parameters of hand trajectory to perturbed and unperturbed
target. 0, initial hand position; 11, unperturbed hand trajectory (PO); t2, perturbed trajectory (P—); Tp, time ofperturbation;
Bl and B2, times of peak net acceleration of t1 and t2;BlGl and B2G2, peak net acceleration vectors at times Bl andB2;aA,
divergence angle between net acceleration vectors M1A1 and M2A2 of tl and t2; M1T1 and M2T2, tangential acceleration
vectors; aV, divergence angle between tangential velocity vectors Ml VI and M2V2 of tl and t2; CI and C2, time of peak net
deceleration of tl and t2; C1F1 and C2F2, net deceleration vector at times CI and C2; Dt, time interval for the analysis of
angular divergence between 2 vectors = 9 ms, and frequencyfilteringfor all hand parameters = 20 Hz.
puter. This pulse was used for an on-line feedback control of the
target stimuli and for the extinction of the working space by the
electronic shutter (3- to 5-ms response time). Because of the EOG
noise, the velocity and accelerations were filtered, and that filtering may have introduced delays of ~ 15-30 ms in the time detection of peak saccade velocity.
Eye movements were filtered with a low-pass Butterworth analog filter with a —12-db/octave cut-ofF frequency of 30 Hz before
being sampled through a 12-bit A / D converter. The x and y horizontal components of the hand pointing were recorded through a
small infrared-emitting diode 3 X 2 mm, stuck on the nail of the
fingertip and coupled with a Selspot II system. The Selspot camera, 2 m above the working surface, provided the coordinates of
the fingertip with an accuracy of ±2 mm. All the data regarding
eye and hand movements were collected at 333 Hz (every
3 ms).
An experimental session was composed of an equal number of
unperturbed targets [(PO); 20, 30, and 40°], perturbed targets left
[ ( P - ) ; 20-10, 30-20, and 40-30], and perturbed targets right
[ ( P + ) ; 20-30, 30-40, and 40-50], randomly distributed. The
probability of occurrence of any type of stimulation was equal to
one-ninth, and the sequence was randomized; however, when a
given type of stimulus had occurred twice consecutively, the third
occurrence of the same stimulus type was forbidden to prevent a
prediction efiect. Each type of stimulation was repeated five times
every session. Thus one session included 9 X 5 = 45 recorded
trials. The number of total trials within a session was higher because some trials could be rejected. The rejection was performed
on-line either by the experimenter (when he noticed artifacts) or
by the program itself, which used eye and hand latency criteria.
Only trials with latencies > 150 ms and <500 ms were accepted
and subsequently stored. A further visual inspection allowed to
remove the few trials in which small blinks had produced erroneous perturbations before the saccadic eye movement.
Two basic experimental conditions were considered.
1) One was called "open-loop" condition, in which the illumination of the room, and thus the vision of the moving limb, disappeared systematically at the time-of-peak velocity of the orienting
saccade toward the initial stimulus. The visual feedback was suppressed throughout the pointing movement, the limb becoming
visible only when the target had jumped back to the central fixation point.
ON-LINE CONTROL OF HAND REACHING
2) the second one was called "closed-loop" condition, in which
the illumination of the room, and thus the visual feedback from
the moving limb, was permanently available, all other variables
being identical to the open-loop condition.
The choice of several target eccentricities intended to reduce or
cancel motor learning effect, even unconscious. The factorial design for the experiment and its three-way analysis of variance was
guided by the underlying hypothesis that corrections would not be
initiated on the basis of the hand visual reafferences, and that the
introduction of these latter ones would play a minor role; consequently, little interaction of the open- versus closed-loop factor
with the eccentricity or with the perturbation factors for most of
the kinematic parameters was expected.
Each of the open- and closed-loop conditions was blocked. Six
right-handed subjects, four males and two females, from 20 to 26
yr of age, ran the experiment; each subject was submitted to both
experimental conditions. Each session was repeated twice by randomizing the order of blocked open- or closed-loop conditions
across subjects. Thus there was a number of 2 (repeated sessions) X 2 (open/closed-loop conditions) X 6 (subjects) = 24
experimental sessions, each one including 9 types of stimulation X
5 repetitions, i.e., 1,080 trials. For each subject and condition, the
two (identical) sessions were grouped for the analysis, allowing to
average 10 repetitions for each type of stimulation; the 9 types of
stimulations corresponded to 3 target eccentricities X 3 jump orientations. For each measured parameter, a three-way analysis of
variance was performed ( 2 x 3 x 3 ) : vision availability (open vs.
closed loop) X target eccentricity (20, 30, and 40°) X jump orientation [(P-), (P0), (P+)]. Basically, the latencies, the global, and
the detailed spatiotemporal patterns of the responses were analyzed to detect the parameters that were influenced by the perturbations or by the presence of a visual feedback of the hand. Early
analyses on peak acceleration were mainly performed because of
recent studies mentioning very quick reactions to perturbations
on the peak acceleration itself and its rise time. Easily identifiable
spatial and temporal parameters such as peak acceleration, peak
velocity, peak deceleration, acceleration time, deceleration time,
hand movement duration, and accuracy in angular deviation as
well as in movement distance were computed to get landmarks on
the corrective processes. Mean and standard deviation for all parameters were computed.
Intrasubjects linear regressions among possibly coupled variables were performed for latency, accuracy, movement duration,
and velocity for both the eye and the hand, as both eye and hand
motor systems were involved in the target "catching" process.
Another reason for this correlation study was to see whether some
hand movement speed accuracy trade-off could be observed when
a perturbation was introduced, when the target eccentricity varied
and correlatively the movement distance, or when visual reafferences from the hand were either given or removed.
459
eration and of the acceleration component orthogonal to the tangential velocity; its angular orientation in space was shifted by
180°, when the peak tangential velocity was reached, as the tangential acceleration inverted its direction around that point.
The mechanisms responsible for the corrections to the ongoing
trajectory were further investigated by looking at the following: 1)
the relationship between accuracy of the initial saccade and peak
tangential velocity of the hand, to see whether a common signal
could drive the eye and the first part of the hand movement; 2) the
different kinds of final error: constant and variable error in orientation, absolute and distance error; 3) the correlation between time
available for correction and accuracy of the pointings, this available time being measured as the difference between the end of
hand pointing and the time at which perturbation occurs; 4) the
deceleratory period and its correlation with accuracy of the pointings, and 5) the speed-accuracy trade-off of the pointings in closed
loop for perturbed and unperturbed trials.
On Fig. 2, A and B, are represented the main analyzed parameters: eye latency, hand latency, hand movement duration, time-topeak acceleration (or acceleration rise time), peak acceleration,
time-to-peak velocity (or acceleration time), peak velocity, deceleration time, orientation of the net acceleration and tangential
velocity vectors in space, and their amplitude. These above parameters were computed automatically by an algorithm with the following thresholds: eye velocity = 20°/s, eye acceleration = 200°/
s2, hand velocity = 8 cm/s, and hand acceleration = 200 cm/s 2 .
The threshold values for hand onset movement were chosen to
statistically fit with the values obtained from another contact sensitive method, where the detection of the beginning and the end of
the movement was based on the electrical contact (or no contact)
of the hand on the surface on which the pointings were performed.
Position, velocity, and acceleration were averaged by synchronizing the traces at the onset of eye movement (for eye) and at the
onset of hand movement (for hand). Statistical analyses were performed to detect the earliest point where the trajectories to perturbed targets began to deviate from the trajectories to stationary
targets. For perturbations left (P—), and for each type of eccentricity (20, 30, and 40°), we took as a baseline the synchronized
curves obtained with the normal responses; then, the perturbed
left (P—) synchronized curves (eye and hand) were to align the
hand acceleration tangential profile on the corresponding hand
acceleration profile of the normal (P0) responses; then, by increasing steps of time every 9 ms, we tested according to a t test the
significant differences in angles between the net acceleration vectors of the normal (P0) responses and the net acceleration vectors
of the perturbed left (P—) responses. The same test was applied
both to the angles of the velocity vectors and to the instantaneous
distances between the two mean hand path curves. To prevent
meaningless detections of acceleration angles divergence, the test
began to be effective only after the time of peak amplitude acceleration. The velocity angles were also tested after the time of peak
amplitude acceleration. As for perturbations left, the perturbed
Computational methods
right (P+) synchronized curves were shifted to align the tangential
The x and y hand position werefilteredwith a zero phase finite hand acceleration profile on the corresponding profile of the norimpulse response (FIR) filter with the use of 24 coefficients with a mal (P0) responses; however, because in this latter case most of
frequency cut-offset at 20 Hz. For the eye position the same type the initial paths were common to unperturbed and perturbed right
of filter was used but with a frequency cut-off set at 30 Hz; this responses the index of the earliest change of the responses used,
choice being a compromise between the real power spectrum of a instead of being a vector orientation in space, was the time at
normal saccade (Bahill et al. 1981) and the noise present in the which 1) the amplitudes of the net acceleration amplitude, 2) the
EOG method. The eye or hand velocity was computed from the tangential velocity amplitude, and 3) the instantaneous distances
filtered position signal by a least-square second-order polynomial between paths were diverging. The threshold for significant divermethod with the use of a window of ±3 points. The same method gence was chosen at P < 0.05.
was then applied for the acceleration computation from the hand
For both types of perturbations, the reaction time to the perturvelocity x et x; it was also repeated for the tangential velocity, the bation was estimated as the difference between the time of divernet acceleration, their respective angular orientation in space, and gence minus the time of peak saccadic eye velocity (corresponding
the tangential acceleration, colinear with the tangential velocity. to the time of occurrence of the perturbation). The processing
The net acceleration was the vectorial sum of the tangential accel- delay of the perturbation, or effective reaction time, was, in fact,
460
C. PRABLANC AND O. MARTIN
likely to be lower than the above reaction time; indeed, during the
saccade the retinal signals are blurred and omitted (Campbell and
Wurtz 1978; Dodge 1900; Matin et al. 1972), which results in a
reupdating of retinal signals only toward the end of the saccade
(Prablanc et al. 1978), when the eye velocity decreases under
100 ° / s (corresponding approximately to 40 ms after the peak saccadic velocity for a 30° eccentricity target). If this instant is taken
as the time at which the perturbation becomes available for visual
processing mechanisms, the processing delay that is the effective
reaction time is 40 ms shorter (in the following, reaction time will
refer to its physical determination, whereas effective reaction time
or processing delay will refer to the reaction time minus the 40 ms
of the saccadic omission when the perturbation cannot yet be
processed).
The reaction time measures (on the basis of acceleration vectors, velocity vectors, and paths distance) were averaged over subjects, perturbations (P—, P+), and eccentricities (20, 30, and
40°); this operation was performed separately for the open- and
closed-loop conditions.
RESULTS
Qualitative observations
After the end of all sessions, subjects were questioned
about their sensations during the experiments. No subject
reported any detection of the double-step stimuli, even in
the 10% cases in which the second step stimulus was erroneously triggered by EOG signal artifacts, like blinks or jaw
muscle contraction. However, on very few trials, some subjects had the sensation of both being inaccurate, and of an
unintentional correction of their movement.
The two-dimensional spatial paths (projection of the
movement on the plane of pointings) exhibited a general
curved shape for the unperturbed trials, the curvature of
which increased with the eccentricity of the target; the
closed-loop paths were, however, more curved (although
not significantly) than the open-loop paths. The perturbations right (P+) induced paths that had the same general
pattern as those of the unperturbed trials, but with an increased curvature toward the end of the movement. The
paths corresponding to the perturbations left ( P - ) underwent an inversion of curvature; the less eccentric the target
the earher the inversion occurred. On the average, corrections were nearly complete (Fig. 3), whatever the sign of
the perturbation (P—) or ( P + ) , the eccentricity (20, 30,
40°), or the nature of the visual loop (open or closed loop).
Quantitative results
Table 1 shows the mean and standard deviation for most
of the analyzed movement parameters, and Table 2 summarizes the results of the three-way analysis of variance with
double interaction only. A general overview shows that the
vision (or no vision) of the hand had little influence except
on the pointing error.
EYE LATENCY. The latency did not significantly depend on
the eccentricity (from an overall 266-269 ms for targets
ranging from 20 to 40°). Although it varied from 255 ms in
open loop to 280 ms in closed loop, the open- versus closedloop pointing condition did not reach significance. Neither
was it sensitive to the perturbation (269 ms in the perturbed
conditions against 264 ms in the nonperturbed one), indicating that subjects did not predict the occurrence of a perturbation as it occurred after saccade onset. None of the
interactions for the eye latency were significant.
TIME TO PERTURBATION (OR TIME-TO-PEAK EYE VELOCITY).
This time, equal to the eye saccadic latency plus the acceleration time of the saccade, corresponded to the instant of the
perturbation. Saccades were fairly fast and had little variability, thus time was equal to the eye latency plus a 31-ms
saccadic acceleration time in open loop and a 32-ms in
closed loop. It exhibited exactly the same sensitivity as the
eye latency to the analysis of variance.
HAND LATENCY. The hand latency did not significantly depend on the initial target eccentricity (ranging from an
overall 296 to 293 ms); it was independent of the occurrence of a perturbation; as for the eye latency, it varied
slightly but not significantly with the type of visuomotor
loop, closed-loop latencies being 22 ms longer than openloop latencies, thus exhibiting the same behavior as eye latencies.
It did not depend on
the nature of the visuomotor loop, but depended on the
eccentricity of the initial target. The perturbations left ( P - )
produced a mean shortening of the saccade of 1.9° whereas
the perturbations right (P+) produced a mean lengthening
of~1.8°.
AMPLITUDE OF THE INITIAL SACCADE.
The duration of the initial saccade
was typically dependent on eccentricity, ranging from 83 to
109 ms on the average when target eccentricity varied from
20 to 40°. It was also slightly affected by the perturbation in
open-loop condition (P < 0.05) with a maximum variation
of 2 ms. As expected, it did not depend on the open- or
closed-loop condition. None ofthe interactions were significant.
SACCADIC DURATION.
The components of the acceleration (amplitude and angle) are illustrated in Table 1 and
Fig. 6 for subject AP.
Amplitude. At the early beginning of the trajectory, the
net acceleration and the tangential acceleration had the
same amplitude. None of the factors had any significance
on the amplitude of the net peak hand acceleration.
Angle of the net peak acceleration. The only strong factor
influencing the angle of the peak hand acceleration was the
eccentricity, as expected, the mean angles varying from 32
to 51° for target eccentricity, varying from 20 to 40°. The
acceleration angles and the visual angles of the targets do
not coincide as the hand is starting from a point 27 cm
ahead of the eye, as can be seen on Fig. 1. None of the other
factors reached the level of significance.
Time-to-peak acceleration. This is the image of the rising
time of the net force at the end of the tip. None of the
factors influenced the time-to-peak acceleration. Its mean
value was 63 ms.
To summarize, the global spatiotemporal pattern of net
peak acceleration was independent of the perturbations. Its
rise time and amplitude were constant, and its orientation
in space depended only on the initial orientation of the
targets.
PEAK HAND ACCELERATION.
bUU Y(mm)
: closed loop
: open loop
20
30
400
300
it,
1
200
100
0
/
/
•
x(mm)
•
•
100
•
•
200
..
1
300
1
- J
400
1
M -
500
0
100
200
300
400
500
0
100
200
300
400
500
3000
2000
1000
0
-1000
ra -2000
0 200 400 600 800 1000 1200
0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200
FIG. 3. Mean hand trajectories and corresponding synchronized tangential accelerations to different unperturbed and
perturbed targets in closed-loop (thick line) and open-loop conditions (thin line). First, 2nd, and 3rd columns group,
respectively, data of 20, 30, and 40° centered targets, laid out in rows, for trajectory and net acceleration of unperturbed
targets (rows 1 and 2), trajectories and tangential acceleration of perturbed ( P - ) and perturbed (P+) targets (rows 3, 4, and
5). Subject AP;n= 10.
461
462
C. PRABLANC AND O. MARTIN
TABLE 1.
Movement parameters in closed- and open-loop condition
Target Perturbation, deg
Target Eccentricity, deg
Closed loop
Time to perturbation, ms
Hand latency, ms
Hand duration, ms
Time-to-peak acceleration, ms
Peak acceleration amplitude,
cm/s 2
Angle peak acceleration vector,
deg
Acceleration time, ms
Peak velocity amplitude, cm/s
Time-to-peak deceleration, ms
Deceleration time, ms
Absolute error, mm
Distribution error re hand, mm
Angular error re hand, deg
Angular error re head, deg
Open loop
Time to perturbation, ms
Hand latency, ms
Hand duration, ms
Time-to-peak acceleration, ms
Peak acceleration amplitude,
cm/s 2
Angle peak acceleration vector,
deg
Acceleration time, ms
Peak velocity amplitude, cm/s
Time-to-peak deceleration, ms
Deceleration time, ms
Absolute error, mm
Distribution error re hand, mm
Angular error re hand, deg
Angular error re head, deg
P0
P20-
297
305
499
60
± 28
± 43
+ 53
±9
40-
30-
309
303
480
62
±
±
±
±
41
47
43
11
327
312
476
72
±31
± 41
±51
± 17
P+
20
30
40
317 ± 3 6
403 ± 38
66 ± 16
312 ± 4 2
408 + 52
61 ± 10
303 ± 37
444 ± 58
6 9 + 15
20+
308
297
467
61
1,786 ± 384
1,925 ± 6 1 8
2,025 ± 620
1,876 + 463
1,915 ± 5 7 8
1,959 ± 6 1 2
33 ± 11
155 ± 12
146 ± 18
241 ± 2 6
343 ± 49
9.2 + 4.5
1.9 ± 3 . 2
1.1 ± 0 . 9
0.6 + 0.5
42 ± 10
166 ± 18
169 ± 2 7
246 ± 38
313 ± 31
7.6 ± 1.6
3.8 ± 3 . 8
0.2 + 0.6
0.2 ± 0.2
53 ± 11
174 + 32
191 ± 2 9
250 ± 44
302 ± 47
10.7 ± 1.0
5.8 ± 4 . 7
0.1 ± 0 . 9
0.3 ± 0.4
35 ± 9
169 ± 15
168 ± 17
272 ± 34
233 ± 28
11.9 ± 1.8
9.1 ± 4 . 8
0.5 ± 0.6
0.5 ± 0.2
42 ± 9
177 ± 2 8
177 ± 2 5
303 ± 5 1
231 ± 3 2
14.4 ± 2.4
10.7 ± 2.4
0.0 ± 0.7
0.4 ± 0.3
53 ± 9
184 ± 2 9
187 ± 2 9
321 ± 7 2
261 ± 3 8
13.2 ± 2 . 5
8.5 ± 2.5
- 0 . 2 ± 1.0
0.3 ± 0.7
35
174
168
311
294
13.8
6.7
-0.6
-0.1
275
278
501
58
289
282
479
58
296
277
477
67
301 + 50
406 ± 60
57 + 5
284 ± 49
413 + 30
64 ± 14
286 ± 48
430 ± 42
69 ± 16
286
280
456
56
± 41
+ 52
+61
+ 8
± 53
± 56
± 56
±10
±
±
±
±
46
54
56
17
± 36
± 35
± 58
±8
2,043 + 662
30+
313 ± 4 3
294 + 41
516 ± 53
6 4 + 16
40+
317
300
554
70
+
+
±
±
43
42
55
14
1,996 ± 5 5 4
2,081 + 706
+ 10
±27
± 18
±40
± 50
±5.6
± 7.0
± 1.3
±0.7
44 ± 11
179 ± 30
177 ± 2 3
322 + 57
338 + 53
17.1+4.9
6.9 + 8.5
- 1 . 2 + 0.7
-0.5 + 0.5
51+9
184 + 28
189 ± 2 6
349 ± 66
370 + 47
18.4 ±5.5
7.6 ± 7.9
- 1 . 3 + 0.7
-0.5 ± 0.4
± 43
± 46
±71
±8
291+68
277 + 66
491 + 6 9
61 + 6
298
283
517
65
± 48
+ 52
±84
± 16
1,643 + 401
1,840 ± 4 1 3
1,915 ± 5 6 7
1,769 ± 2 9 1
1,767 ± 4 7 5
1,880 ± 4 0 7
1,849 + 635
1,817 + 487
1,883 ± 669
33 + 8
161 + 2 0
143+ 17
251 + 3 6
340 + 53
17.8 + 6.6
4.7 ± 5.8
2.4 ± 1.4
1.3 ± 0 . 8
39 ± 10
165 ± 13
163 ± 17
252 ± 34
314 ± 4 5
15.6 ± 2 . 8
8.3 ± 4.4
0.6 ± 1.0
0.6 ± 0.6
48 ± 8
178 ± 2 8
183 ± 2 9
276 ± 45
299 ± 41
16.1 ± 3 . 6
7.2 ± 5.5
-0.5 ± 1.2
0.0 ± 0.8
33 ± 8
176 ± 17
161 ± 2 6
291 ± 52
228 ± 56
15.5 ± 4 . 9
9.0 ± 4.6
0.5 ± 1.3
0.5 ± 0.7
41 ± 7
188 ± 17
174 ± 20
309 ± 38
225 ± 21
17.9 ± 5.0
7.9 ± 8.0
-1.1 ± 1.7
- 0 . 3 ± 1.2
49 ± 7
194 + 20
190 ± 2 5
324 + 45
236 ± 28
23.4 ± 4 . 9
9.7 ± 6.5
- 1 . 9 ± 1.1
- 0 . 8 ± 0.8
32 ± 8
194 ± 3 3
169 + 28
324 ± 52
262 ± 69
24.5 ± 6.6
14.6 ± 5.3
- 1 . 4 ± 1.9
- 0 . 3 ± 1.3
40 ± 7
189 ± 19
179 ± 2 7
327 ± 50
302 ± 67
25.7 ± 7 . 7
7.6 ± 6.0
- 2 . 6 + 1.5
- 1 . 3 ± 1.2
48 ± 7
194 + 23
191 ± 3 1
352 ± 60
323 ± 75
30.7 ± 9.9
3.2 ± 7.0
-3.2 ± 1.5
-2.0 ± 1.1
Values are means ± SD; n = 60. P- and P+, perturbed responses; P0, unperturbed responses.
TABLE 2.
Summary of3-way analysis of variance
Sources of Variation
Movement Parameters*
Eye latency
Saccadic duration
Hand latency to 1st stimulus
Hand movement duration
PHTV
Amplitude of PHTV
Acceleration time
Deceleration time
Time from onset to peak deceleration
PHNA
Amplitude of PHNA
Angle of PHNA
Time to PHNA
Absolute error
Distance error
Angular error re hand
Angular error re head
LXP
t
+
*
t
*
*
+
+
*
LXE
PXE
f
t
*
+
t
+
*
+
t
L, closed loop/open loop; P, target perturbation; E, target eccentricity; aX b, interaction; —, not significant; PHTV, peak hand tangential velocity;
PHNA, peak hand net acceleration. * Vision vs. no vision of the hand X target eccentricity X direction of the perturbation; n = 60. f-Ps 0.05. %P< 0.001.
§P<0.01.
ON-LINE CONTROL OF HAND REACHING
As for the acceleration,
the components of the velocity (amplitude and angle) are
illustrated in Fig. 6 for one subject.
Amplitude. The open- or closed-loop factor did not play
any role, but the two eccentricity and perturbation factors
were highly significant. With unperturbed responses the
peak velocity ranged from 164 to 188 cm/ s for target eccentricities from 20 to 40° of visual angle. Separate comparisons showed that perturbations left (P—) significantly decreased peak velocity (166 cm/s) with respect to unperturbed targets (PO) (176 cm/s; P < 0.001), whereas
perturbations right (P+) did not significantly increase it
(179 cm/ s). There was a reliable interaction between eccentricity and perturbation (P < 0.008), the tangential velocity
of (P—) responses increasing for 40° eccentricity and decreasing for 20° eccentricity.
PEAK HAND TANGENTIAL VELOCITY.
The acceleration time measured
from hand movement onset to peak velocity did not depend on the open- or closed-loop condition. It was slightly
dependent on the eccentricity (P < 0.05), with a variation
from 172 to 189 ms for unperturbed responses at 20 and
40° targets. It was highly dependent on the perturbation
factor. For (P0) responses this time was 181 ms, whereas it
was 167 ms for (P—) and 186 ms for (P+) responses,
pooled over eccentricity and open/closed loop. None of the
interactions between factors reached any level of significance. The significant decrease (P < 0.006) of time-to-peak
velocity for (P—) compared with (P0) was an indication
ACCELERATION TIME.
463
that, around 167 ms after the hand movement onset, the
( P - ) perturbation was taken into account. For the (P+)
perturbation the time-to-peak velocity was not significantly
different from the (P0) one (5 ms difference).
DECELERATION TIME. It was measured as the duration from
the peak hand velocity to the end of the movement. The
vision of the hand had no systematic effect on the deceleration time: as shown in Table 1, the open- and closed-loop
deceleration times of (P—) responses were similar and also
observable in a typical subject's response (see Fig. 3); on
the other hand, Table 1 shows that (P+) perturbation responses resulted in a nonsignificant 38 ms additional time
for deceleration under closed loop, also observable in Fig. 3.
The strongest factor influencing deceleration time was the
perturbation that increased it from 236 ms for the (P0)
responses to —319 ms for the (P—) and (P+) responses.
The eccentricity factor was just below the level of significance (P < 0.06), but there was a strong perturbation X
eccentricity interaction (P < 0.001). It resulted mainly
from a marked change at 20° eccentricity, observed as well
in closed-loop as in open-loop condition, with an increased
deceleration time (341 ms) for (P—) and a decreased deceleration time (278 ms) for (P+), with respect to the other 30
and 40° eccentricities.
TIME-TO-PEAK DECELERATION. It was defined as the duration from the onset of the movement to the peak deceleration of the hand. It was independent from the open/closedloop condition. It depended slightly on the eccentricity
FIG. 4. A-D: relationship between mean absolute error (A; in mm), mean distance error (B; in mm), mean angular error
re hand (C; in deg), mean angular error re head (D; in deg), and the different types of unperturbed and perturbed responses
in closed-loop (•) and open-loop (o) conditions. Vertical lines indicate standard deviation; n = 60 (6 subjects X 10
repetitions).
C. PRABLANC AND O. MARTIN
464
(P < 0.03) and heavily on the perturbation (P < 0.001)
without any significant interaction between eccentricity
and perturbation. Comparing the pooled unperturbed
(P0), perturbed left ( P - ) , and perturbed right (P+) responses, we obtained, respectively, 303, 253, and 331 ms.
The absolute error was the distance between the pointing position at the time of impact and the
final target position. As illustrated in Fig. A A, it was found
to depend on the open/closed-loop condition and on the
perturbation factor, and slightly on the eccentricity. The
overall error in open loop was 21 mm, whereas it dropped
to 13 mm in closed-loop condition. The perturbations (P—)
and (P+) gave overall errors of 13 and 22 mm, respectively,
against an error of 16 mm for the unperturbed (P0) responses. The perturbed and unperturbed overall accuracy
for 20, 30, and 40° initial target eccentricity was 16,16, and
19 mm, respectively.
ABSOLUTE ERROR.
DISTANCE ERROR. From Fig. 2B, it can be seen that if RP is
the resting starting hand position, PT2 the target final position, and HP the position of the hand pointing when it hits
the surface, the distance error can be defined as the difference between the length of the segments (RP — HP) and
(RP - PT2), positive values being noticed as overshoots in
depth and negative values as undershoots. Distance error
did not depend on eccentricity, nor on open/closed-loop
condition, as shown in Fig. AB, but slightly depended on
perturbation factor (P < 0.05); the overall distance errors
for perturbation ( P - ) , (P0), and (P+) were, respectively,
5.3, 9, and 7.8 mm. An interaction between eccentricity
and perturbation was observed (P < 0.05).
ANGULAR ERROR REFERENCED IN A HAND COORDINATE
SYSTEM. The angular error was defined in Fig. 2B as the
angle between vector 1 (RP - HP) and vector 2 (RP PT2). Positive errors corresponded to overshoots, whereas
negative errors corresponded to undershoots. The open/
closed-loop condition did not influence the angular error,
but the perturbation and the eccentricity significantly did
(see Fig. AC). The overall angular errors for perturbation
left ( P - ) , for (P0), and for (P+) were, respectively 0.7,
-0.4, and -1.7°. The overall angular error for 20, 30, and
40° of eccentricity were, respectively, 0.4, -0.7, and — 1.1°.
There was loop X eccentricity and loop X perturbation interactions (P < 0.05 and P < 0.001, respectively) clearly
shown in Fig. AC.
ANGULAR ERROR REFERENCED IN A EYE (OR HEAD) COORDINATE SYSTEM. If EP is the projection of the cyclopean eye
on the hand pointing plane, then the angular error of the
pointing can be defined as the angle between the vectors
(EP - HP) and (EP - PT2). The sign notations are the
same as for the above defined error. Like angular error re
hand, the angular error re head was only significantly influenced by the perturbation and the eccentricity (Fig.
AD). The overall angular errors, pooled over eccentricity,
for perturbations ( P - ) , (P0), and (P+) were, respectively,
0.5, 0.1, and -0.7°. As the perturbation produced a 10°
target jump, it means that, in the worst case [the one of the
perturbation (P+)], the residual error, compared with the
unperturbed control condition, was an undercorrection of
0.1 + 0.7 = 0.8°, i.e., <10%. Thus the angular compensation to the perturbation was nearly complete. The overall
angular errors, pooled over perturbed and unperturbed
trials, for 20, 30, and 40° of eccentricity were, respectively,
0.4, -0.2, and -0.5°. There was an interaction between
loop and target eccentricity (P < 0.01) that clearly appears
in Fig. AD.
Hand movement duration
significantly depended on the target eccentricity (P <
0.01): for stationary targets ranging from 20 to 40° it varied
from 406 to 430 ms in open loop, whereas it varied from
403 to 444 ms in closed-loop condition. It depended very
slightly but not significantly on the status of the visuomotor
loop (see Table 1 and Fig. 5). It did not depend globally on
the vision of the hand. For perturbations ( P - ) and for eccentricities varying from 20 to 40°, the corresponding durations varied from 501 to 477 ms in open loop, and from 499
to 476 ms in closed-loop condition, being totally insensitive
to the visual reafferences of the hand. For perturbations
(P+), with initial targets ranging from 20 to 40°, the durations in open-loop condition varied from 456 to 517 ms,
whereas in closed-loop condition they varied from 467 to
554 ms.
HAND MOVEMENT DURATION.
650
•
600-
c
o
CLOSED LOOP
O OPEN LOOP
550-
'•s
•D
500-
<»6
4—'
C
O
OO
FIG. 5. Mean hand movement duration vs. eccentricity for the different types of unperturbed
and perturbed targets in closed-loop (•) and
open-loop (o) conditions. Vertical lines indicate
standard deviation; n = 60.
CD 450
J
400
73
C 350
CO
300 J
20-
30-
©
40-
20
30
40
20+
30+
40+
CLOSED LOOP
OPEN LOOP
Hand movement duration (msec)
FIG. 6. Comparative variation of tangential velocity, amplitude, and net acceleration amplitude {top 4 frames), and
corresponding comparative divergence of tangential velocity vector angles and net acceleration vector angles {bottom 4
frames), for pointing movements directed to targets at 30, 30-, and 30+, in closed-loop {leftframes) and open-loop (right
frames) conditions. Net acceleration vector angle has been rectified of 180° after instant of peak tangential velocity. Note the
similarity of the open- and closed-loop responses up to the peak velocity. Subject AP; n = 10.
465
C. PRABLANC AND O. MARTIN
466
TABLE 3.
Reaction time to target perturbations
Open Loop
Closed Loop
P-/P0
P+/P0
Target
20°
30°
40°
Overall
D
D
162 ± 17
163+ 14
160 ± 20
162 ± 16*
177
176
208
187
± 17
± 19
± 24
±48*
273
259
307
280
± 25
± 44
± 16
± 42f
P-/P0
268 ± 40
263 ± 32
315 ±73
284 ± 53f
P+/P0
D
303 ± 39
314 ±33
369 ± 56
295 ± 80f
145 ± 36
146 ± 47
174 ± 18
155 ±36*
171 ±33
175 ±28
195 ±29
180 ±30*
264 ± 42
279 ± 21
295 ± 28
279 ± 32f
D
203 ± 36
318 ± 31
301 ± 67
274 ± 76f
303 ± 50
347 ± 69
373 ± 45
341 ± 60f
Values are means ± SD and are represented in milliseconds; n = 10 for each subject. A, signficant variation of acceleration vector angle; V, velocity
vector angle; D, paths distance. *Phase detection; fAmplitude detection.
The other strong factor influencing hand movement duration was the occurrence of a perturbation (P < 0.001), the
mean duration (pooled over eccentricity and open/closed
loop) for unperturbed responses (P0) was 417 ms, whereas
it was 485 ms for ( P - ) and 500 ms for (P+); thus the
perturbation lengthened by ~ 78 ms the movement duration.
There was a strong interaction between target eccentricity and perturbation (P < 0.01), but not with open- versus
closed-loop condition, which appears very clearly in Fig. 5.
A perturbation ( P - ) gave a decreasing duration with increasing target eccentricity, whereas a perturbation (P+)
gave an increasing duration with increasing target eccentricity, this phenomenon being true as well for the open as for
the closed loop. The observation of Fig. 3 explains this phenomenon: the qualitative structure of the spatial path of
(P+) responses was roughly the same as for (P0) responses,
whereas it differed largely for ( P - ) responses, with an inversion of the radius of curvature, this phenomenon being
accentuated for ( P - ) at small eccentricities (large dissimilarities) and for (P+) at large eccentricities (large similarities).
INTRASUBJECT CORRELATIONS BETWEEN THE MAIN DIFFERENT
KINEMATIC PARAMETERS. Peak acceleration versus time-
to-peak acceleration showed no correlation (0.07 < r2 <
0.21), nor peak acceleration versus time to perturbation
(0.08 < r2 < 0.17), independent of the vision of the hand or
of the perturbation.
The accuracy parameters [absolute error, distance error,
and angular errors (re head and re hand)] versus movement duration, deceleration time, peak velocity amplitude,
and time from perturbation to movement end, were uncorrelated (r 2 ranging from 0.07 to 0.29), indicating a total
absence of speed accuracy trade-off. This lack of correlation
was the same whether vision of the hand was available or
not, and whether perturbation appeared or not.
REACTION TIME OF THE SENSORIMOTOR SYSTEM TO THE
PERTURBATION. This reaction time has been defined in
METHODS as the time elapsed between the onset of the per-
turbation and the earliest detectable signs of the corrections. It was measured from both the angle of the acceleration vector, the angle of the tangential velocity vector, and
the segment distance between the perturbed and the unperturbed family of curves (see Fig. 6 and Table 3). There was
no difference between open- and closed-loop reaction
times, whatever the method (acceleration, velocity, or distance) used to compute them.
For ( P - ) the reaction time was, on the average, 65 ms
shorter on the basis of velocity detection rather than on
distance detection, and 25 ms shorter on the basis of acceleration detection rather than velocity detection. The results
showed mean reaction time (pooled over 20, 30, and 40°)
measured on the basis ofthe divergence between the acceleration vector angles, which were 155 ms for the open-loop
condition and 162 ms for the closed-loop condition (180
and 187 ms, respectively, when based on velocity vector
angles). This result is consistent with the (P—) time-topeak velocity (167 ms) obtained from the analysis of variance, which was significantly different from the corresponding 181 ms of the (P0) time-to-peak velocity. Thus, at
very close times (from ~ 155 to 175 ms), all series of kinematic parameters (the angle of the net acceleration vector,
the tangential velocity vector angle, and its amplitude) began to deviate from those of the normal responses. As mentioned above, the measured reaction time was an overevaluation of the processing delay, as the retinal information is
known to be unavailable until near the end of the saccade.
As the average "blind" deceleration time of a saccade is
~40 ms for a 30° eccentric target, the effective reaction
time (or processing delay) to the perturbations ( P - ) steps
down to ~ 115 ms in open-loop condition (and 142 ms in
closed-loop condition).
If the perturbations (P+) are now considered, the reaction time, based on velocity divergence and averaged over
open- and closed-loop conditions, was ~279 ms (318 ms
when based on curve distance), which is much higher than
the reaction time to the perturbations ( P - ) .
The hand movement durations analyzed above have
shown averaged measures of 417 ms for (P0), 485 ms for
( P - ) , and 500 ms for (P+). If the duration is normalized
for the (theoretical) path length from the starting point to
the final target position, its value becomes 485 + 12 = 497
ms for ( P - ) and 500 - 17 = 483 ms for (P+), the normalization procedure being based on a linear interpolation of
the duration versus movement amplitude; thus the normalized increase in movement duration corresponding to a
perturbed response is in the range of 66-80 ms.
DISCUSSION
The most striking finding of this experiment was the generalization of the on-line mechanisms of control in aimed
movements, in a very automatic way, previously described
by Goodale et al. (1986) and Pelisson et al. (1986). In the
Goodale et al.'s experiment, the undetected perturbation
was such that the necessary corrections resulted, at the level
of the end point fingertip effector, as a modification of the
ON-LINE CONTROL OF HAND REACHING
movement amplitude (lengthening or shortening according
to the type of perturbation), but not of its general orientation. In the present experiment, with the use of the same
paradigm, the perturbation mainly involved a modification
of the orientation of the movement and also, although to a
lesser extent, of its amplitude.
The other main observation concerns the comparison between the present experiment of corrections to undetected
perturbations, and the classical double-step experiments of
corrections to clearly identified distinct targets: a considerable similarity appears for all the observed shortest reaction
times and the path changes (Paulignan et al. 1990; Soechting and Lacquaniti 1983; Van Sonderen et al. 1988). However, there are some discrepancies on a few details of the
kinematics: for instance, in Paulignan et al. (1990), a
change as early as on the peak acceleration amplitude was
detected, whereas we did not observe any variation on this
kinematic parameter, neither in its amplitude nor in its orientation. However, their task involved less steep movements, with a peak acceleration at ~100 ms after movement onset, whereas it occurred much earlier (~60 ms) in
our experiment; therefore the reaction times that they noticed are still compatible with the lowest 115-ms effective
reaction times that we got.
In the Goodale et al. (1986) and Pelisson et al. (1986)
experiments, a target jump in amplitude only was used, and
the authors did not find any difference in movement duration for nonperturbed and perturbed responses of the same
final amplitude, despite that the perturbation was fully
corrected. These authors suggested that, as perturbed and
unperturbed responses had both a bell-shaped profile, the
modifications of trajectory might have been very early,
without noticeable changes on the velocity and acceleration
traces. In the present experiment the normalized movement duration (corresponding to a same movement amplitude) exhibited a slight increase [an average of 80 ms for the
perturbations left ( P - ) and 66 ms for the perturbations
right (P+)]. This increase in duration compared with
Goodale et al.'s experiment could represent an additional
time to take into account a more time-consuming process
for a change in orientation than for a change in distance
only, as already suggested in reaction time and isometric
force control experiments (Bonnet et al. 1982; Favilla et al.
1990; Ghez et al. 1990). Further insight into these corrections came from the simultaneous analysis of the amplitude
and the orientation of the fingertip acceleration vector. It
allowed the detection of the earliest changes in force or
torque, which are closely locked in time to the nervous
command; they were observed, on the average, 15 5-162 ms
(open and closed loop) after the perturbation. Another
converging result came from the hand peak tangential velocity, for which amplitude and rise time (165-168 ms for
open and closed loop on the average) were significantly
altered. As illustrated on the xy trajectories in Fig. 4, the
perturbations (P—), which involved an inversion of the
curvature, seemed to be corrected much earlier than the
perturbations (P+), which kept roughly the same curvature. Two alternative explanations to this difference in observed reaction times to the perturbations right and left
could be suggested: either the (P+) and (P—) real reaction
times are of the same order of magnitude [but it is difficult
467
to statistically detect minor early changes in the (P+) perturbations], or the reaction time is determined mainly by
the "pressure" of the spatial constraints, which are high for
the ( P - ) and low for the (P+) perturbations, and the real
reaction times are effectively different. However, on the
other hand, both left ( P - ) and right (P+) perturbations
produced similar increases in movement durations, with
similar mean errors on the final target.
In the (blocked) closed-loop condition, although perturbations remained undetected, the subject may have had,
however, the sensation of an inaccurate movement initiation, as he/she saw both his hand and the target permanently; this could have possibly given rise to a task-dependent strategy such as reducing the speed of the movement
immediately after the onset of the movement. Such was not
the case with the perturbations left ( P - ) , as movement durations did not differ from those of the open-loop responses;
for the perturbations right (P+), the closed-loop durations
increased with respect to the open-loop durations by ~20
ms, and increasingly with target eccentricity, although both
phenomenon did not reach the level of significance. Another block-dependent strategy could have been also to increase the delay between hand and eye latencies to take
advantage of this delay to process the visual error; if the
closed-loop condition increased the hand latency, it did the
same for the eye, keeping intact the delay between both.
None of those two possible strategies seemed to be used. In
fact, the only significant effect of the presence of the visual
reafferences from the hand movement was a slight increase
of curvature on the average path and a decrease of the
pointings scatter, i.e., a reduction of the variability of the
responses. From the above results, corrections appear not
to be achieved by fundamentally different mechanisms, regardless of whether vision is available. They seem to be
implemented like if thefingertipwas attracted by the target,
onto which the gaze is anchored, mainly without the help of
visual reafferences.
In addition, the observation of a similar reaction time to
the perturbation, for open- and closed-loop conditions, favors the hypothesis of a main internal feedback loop (comparing the spatial representation of the target location with
the hand trajectory, derived either centrally from an efference copy and/or peripherally from a kinesthetic signal).
Such a conception of an internal servosystem has been previously developed for eye-head orienting systems (Guitton
and Voile 1987, Guitton et al. 1990; Laurutis and Robinson 1986; Pelisson et al. 1988), for speech production
(Abbs and Gracco 1984), and for multijoint hand motor
control (Prablanc and Pelisson 1990). This view has received an electrophysiological confirmation in cat's gaze
orienting (Munoz and Guitton 1985; Munoz et al. 1989,
1991): the instantaneous motor error has been found to be
topographically encoded by neuronal populations in the
superior colliculus during the few 100-200 ms of a goal-directed saccade. This motor error, present in lower structures, is a very elaborated vectorial variable that results
from the difference between the target location and the sum
of the angular eye vector within the orbit and the angular
head vector with reference to the trunk. Under normal circumstances, and before an orienting saccade to a target, the
motor error is built from the retinal error signal itself; but
468
C. PRABLANC AND O. MARTIN
immediately after the initiation of the saccade, the retinal
error is omitted. This retinal signal is therefore uninterpretable during most of the saccade; however, even in the absence of retinal feedback, the representation of motor error
is continued in the superior colliculus. Considering the analogy between target capture by either gaze or hand, the gaze
motor error, which is the angular error between the line of
gaze and the line to the target, is functionally the equivalent
of the distance between the fingertip and the target in our
experiment. Although the neural substrate for a motor
error signal in hand reaching has not yet been found, the
present experiment suggests this top down organization to
be a general feature of the motor control systems, in which
the controlled variables, even at low levels, are finalized
global variables such as gaze error vectors or fingertip error
vectors, and in which intermediate variables such as eye
position within the orbit, or joint angles, torques and muscle forces are devoted to meet the goal of the end-point
effector.
The modifications to the perturbed trajectories ( P - ) involving deep structural changes are an indirect argument
suggesting that the execution structures are not only capable of small amplitude adjustments, as in Pelisson et al.'s
(1986) experiments, but of a very high flexibility in the
reorganization of multijoint muscles synergies. It would
also suggest that those joint muscles synergies are located
more downstream than thought in the classical conceptions
of preprogramming. However, our results do not exclude
such a global organization at the very beginning of the
movement; indeed, although pointing within the prehension space at a target in the near peripheral visual field requires some a priori knowledge of a very raw sequence of
flexion-extension patterns on shoulder and elbow, the present experiment suggests that, once this process is initiated,
the exact tuning of muscle activity is not mediated hierarchically and that low-level processes could be responsible for
the optimization of multijoint trade-offs. The likelihood of
such a view is supported by the above-mentioned electrophysiological findings from Munoz et al. (1991), who
showed that eye-head movement trade-offs during fast
gaze-orienting responses were mediated by low-level feedback loops.
decision to switch the location of the goal. It could be that
once a decision to execute a given type of motor response
has been initiated, the necessary amendments to cope with
the goal are automatically implemented at lower levels, in
which the previously defined goal could act like an attractor, for instance in our case by "pulling" the general movement of the end-point effector (the finger) toward the target. This view is not fundamentally different from the reference trajectory hypothesis (Bizzi et al. 1984), itself derived
from the final equilibrium point hypothesis (Fel'dman
1966); it would also support the even more general notion
of motor equivalence (Abbs and Gracco 1984), proposing
that a given goal may be carried out by several ways whenever a given limitation of the system prevents the execution
of the response according to the initial plan. However, because of the undetectable feature of the perturbation, the
most interesting suggestion from this experiment is that it
would have revealed a natural correcting mechanism acting
in normal conditions, when the initiation of the response is
inaccurate. This suggestion is supported by experiments of
single-step stimulation (Prablanc et al. 1986), which
showed that turning the target off, at the onset of the movement but after its perfect foveation, decreased the accuracy
of the open-loop pointings, compared with the situation in
which the target remains lit all throughout the movement.
All these observations indicate that the vision of the target
alone exerts some corrective action on the ongoing response. In the present experiment, in which the displacement of the target was 10°, even the responses without visual feedback (open loop) compensated >90% of the perturbation; it might be that the discrepancy between the
intended path and the actual position of the target, although detected at a nonperceptual level, results in a raw
feed-forward action changing the orientation of the initial
path. Nevertheless, the relative accuracy of the corrections
associated with a variability similar to that of the unperturbed responses would rather be an argument for a kinesthetic feedback processing of the corrections, would they be
initiated by a feed-forward process. However, these arguments are indirect, and to have more decisive evidence for
feedback versus efferent control, it would be necessary to
carry out the same kind of experiments on deafferented
animals, or with patients having a loss of kinesthetic feedback with little motor damage.
Conclusions
This study has shown the generalization of an automatic
When observing the tiny differences of response with and
on-line control of complex movements involving several without visual reafferences from the hand, it clearly appears
joints in a pointing task, regulating not only the extent of that both processes rely on a single baseline mechanism
the movement but also the orientation of its spatial path. (efferent and/or afferent) attracting the hand toward the
The modification of the initial path did not require the target, with additional slight modifications because of the
conscious detection of the perturbation. The perturbation vision of the moving hand. It seems that strategies play a
randomly introduced during the middle of the orienting little role, as visual reafferences from the hand induce very
saccade statistically corresponded to the onset of the hand little and unsignificant changes in the latencies, nor in the
movement. However, the latency of the earliest corrections other kinematic parameters up to the peak velocity. The
(or effective reaction time) was approximately the same as incidence of visual reafferences from the hand appears only
in experiments in which the possible occurrence of a pertur- during the deceleration phase (lengthened on the overall by
bation was a priori known, and indeed detected by the sub- 21 ms); it is associated with a decrease of the pointing error
jects, i.e., ~ 155 ms after its occurrence ( ~ 115 ms after the of 3 mm only, with respect to the condition in which visual
retinal image became interpretable, as the perturbation oc- reafferences are absent.
curred during the saccadic flight). Thus intentional and
Whatever the processes involved in this type of experinonintentional changes to an ongoing movement could ment, they show that error-correcting mechanisms of an
share common corrective mechanisms, except perhaps the ongoing even complex motor response are effective inde-
ON-LINE CONTROL OF HAND REACHING
pendently of a conscious detection of the error. However,
the similarity of the reaction time to the perturbation, with
intentional amendments to perturbations of the same type,
suggests that both could share some common lower stages.
We are very grateful to M. Jeannerod and D. Pelisson for useful comments. We thank M. Soulier for typing the manuscript and P. Giroud for
illustrations.
This study was supported by a Grant BRAIN SCI 0029C from the Commission of the European Community.
Address for reprint requests: C. Prablanc, Vision et Motricite, INSERM
Unite 94, 16 avenue du doyen Lepine, F-69500 Bron, France.
Received 4 March 1991; accepted in final form 23 October 1991.
469
visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature Lond. 320: 748-750, 1986.
GUITTON, D., M U N O Z , D. P., AND GALLIANA, L. Gaze control in the cat:
studies and modelling of the coupling between orienting eye and head
movements in different behavioural tasks. J. Neurophysiol. 64: 509531, 1990.
GUITTON, D. AND VOLLE, M. Gaze control in human: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. / . Neurophysiol. 58: 427-459, 1987.
JEANNEROD, M. The Neural and Behavioural Organization of Goal-Directed Movements. Oxford, UK: Clarendon, 1988.
KEELE, S. W. Behavioral analysis of movement. In: Handbook of Physiology. The Nervous System. Motor Control. Washington, DC: Am. Physiol. Soc, 1981, sect. 1, vol. II, p. 1391-1414.
LAURUTIS, V. P. AND ROBINSON, D. A. The vestibulo-ocular reflex during
human saccadic eye movements. J. Physiol. Lond. 373: 209-233, 1986.
MATIN, E., CLYMER, A. B., AND MATIN, L. Metacontrast and saccadic
ABBS, J. H. AND GRACCO, V. L. Control of complex gesture: oro-facial
muscle responses to load perturbations of lip during speech. / . Neurophysiol. 51:705-723, 1984.
suppression. Science Wash. DC 178: 170-181, 1972.
MEGAW, E. D. Possible modification to a rapid ongoing programmed manual response. Brain Res. 71: 425-441, 1974.
MUNOZ, D. P. AND GUITTON, D. Tecto spinal neurons in the cat have
discharges coding gaze position errors. Brain Res. 341: 184-188, 1985.
ALSTERMARK, B., GORSKA, T., LUNDBERG, A., AND PETTERSON, L. G.
MUNOZ, D. P., GUITTON, D., AND PELISSON, D. Gaze control in the head-
Integration in descending motor pathways controlling the forelimb in
cat. 16. Visually guided switching of target reaching. Exp. Brain Res. 80:
1-11, 1990.
free cat. II. Spatio-temporal variations in the discharge of superior colliculus output neurons. Soc. Neurosci. Abstr. 15: 807, 1989.
REFERENCES
BAHILL, A. T., ROCKENBROUGH, R. A., AND TROOST, B. T. Variability
and development of a normative data base for saccadic eye movements.
Invest. Ophthalmol. Visual Sci. 21: 116-125, 1981.
BECKER, W. AND JURGENS, R. An analysis of the saccadic system by
means of double-step stimuli. Vision Res. 19:967-983, 1979.
Bizzi, E., ACCORNEO, N., CHAPPLE, W., AND HOGAN, N. Posture control
and trajectory formation during arm movement. / . Neurosci. 4: 27382744, 1984.
M U N O Z , D. P., PELISSON, D., AND G U I T T O N , D. Movement of neural
activity on superior colliculus motor map during gaze shifts. Science
Wash. DC. 251: 1358-1360, 1991.
PAULIGNAN, Y., M A C KENZIE, C , MARTENIUK, R., AND JEANNEROD, M.
The coupling of arm and finger movements during prehension. Exp.
Brain Res. 79: 431-435, 1990.
PELISSON, D., PRABLANC, C , GOODALE, M. A., AND JEANNEROD, M.
and extent in motor programming. Bull Psychon. Sci. 19: 31-34, 1982.
Visual control of reaching movements without vision of the limb. II.
Evidence for a fast unconscious process correcting the trajectory of the
hand to the final position of a target step. Exp. Brain Res. 62: 303-311,
1986.
CAMPBELL, F. W. AND WURTZ, R. H. Saccadic omission: why we do not
PELISSON, D., PRABLANC, C , URQUIZAR, C Vestibuloocular reflex inhi-
see a grey-out during a saccadic movement? Vision Res. 18: 1297-1303,
1978.
CARLTON, L. G. Processing visual feedback information for movement
control. / . Exp. Psychol. 1: 1019-1030, 1981.
DODGE, R. Visual perception during eye movement. Psychol. Rev. 7:454465, 1900.
bition and gaze saccade control characteristics during eye-head orientation in human. / . Neurophysiol. 59: 997-1013, 1988.
BONNET, M., REQUIN, J., AND STELMACH, G. E. Specification of direction
FA VILLA, M., G O R D O N , J., HENING, W., AND G H E Z , C. Trajectory control
in targeted force impulses. VII. Independent setting of amplitude and
direction in response preparation. Exp. Brain Res. 79: 530-538, 1990.
FEL'DMAN, A. G. Functional tuning of the nervous system during control
of movement of a steady posture. II. Controllable parameters of the
muscle. Biophysics 11: 566-578, 1966.
GEORGOPOULOS, A. P., KALASKA, J. F., AND MASSEY, J. T. Spatial trajec-
tories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. / . Neurophysiol. 46: 725-743,
1981.
GHEZ, C , HENING, W., AND FAVILLA, M. Parallel interaction channels in
the initiation specification of motor responses. In: Attention and Performance. XIII. Motor Representation and Control, edited by M. Jeannerod. Hillsdale, NJ: Erlbaum, 1990, p. 265-293.
PRABLANC, C , ECHALLIER, J. F., AND MASSE, D. Error correcting mecha-
nisms in large saccades. Vision Res. 18: 557-560, 1978.
PRABLANC, C. AND JEANNEROD, M. Corrective saccades dependence on
retinal reafferent signals. Vision Res. 15:465-469, 1975.
PRABLANC, C. AND PELISSON, D. Gaze saccade orienting and hand pointing are locked to their goal by quick internal loops. In: Attention and
Performance. XIII. Motor Representation and Control, edited by M.
Jeannerod. Hillsdale, NJ: Erlbaum, 1990, p. 653-676.
PRABLANC, C , PELISSON, D., AND GOODALE, M. A. Visual control of
reaching movements without vision of the limb. I. Role of retinal feedback of target position in guiding the hand. Exp. Brain Res. 62: 2 9 3 302, 1986.
SOECHTING, J. F. AND LACQUANITI, F. Modification of trajectory of a
pointing movement in response to a change in target location. / . Neurophysiol. 49: 548-564, 1983.
VAN SONDEREN, J. F., DENIER VAN DER G O N , J. J., AND GIELEN, C. C. A.
J. J. Modification of muscle activation patterns during fast goal-directed
arm movements. J. Mot. Behav. 16: 2-19, 1984.
M. Conditions determining early modification of motor programmes in
responses to changes in target location. Exp. Brain Res. 71: 320-328,
1988.
WESTHEIMER, G. Eye movement responses to a horizontally moving visual stimulus. Arch. Ophthalmol. 52: 932-941, 1954.
VAN GISBERGEN, J. A. M., VAN OPSTAL, A. J., AND ROEBROEK, J. G. H.
WHEELESS, L., J R . , BOYNTON, R., AND COHEN, G. Eye movement re-
GIELEN, C. C. A. M., VAN DER HEUVEL, P. J., AND DENIER VAN DER G O N ,
Stimuli-induced midflight modification of saccade trajectories. In: Eye
Movements: From Physiology to Cognition, edited by J. K. O'Reagan
and A. Levy-Schoen. Amsterdam: Elsevier, 1987, p. 27-36.
GOODALE, M. A., PELISSON, D., AND PRABLANC, C. Large adjustments in
sponses to step and pulse step stimuli. / . Opt. Soc. Am. 56: 956-960,
1966.
WOODWORTH, R. S. The accuracy of voluntary movements. Psychol. Rev.
Monogr. Suppl. 3: 1899.