J Neurophysiol 106: 1218 –1226, 2011.
First published June 8, 2011; doi:10.1152/jn.00278.2011.
Cross talk in implicit assignment of error information during bimanual
visuomotor learning
Shoko Kasuga and Daichi Nozaki
1
Division of Physical and Health Education, Graduate School of Education, The University of Tokyo, Bunkyo-ku; and 2The
Japan Society for the Promotion of Science, Tokyo, Japan
Submitted 29 March 2011; accepted in final form 3 June 2011
visual rotation; credit assignment; internal model
under a wide variety of
environments, the brain constructs a neural feedforward controller, known as an “internal model” (Bastian 2006; Kawato
1999; Wolpert et al. 1998). In this learning process, information regarding movement errors needs to be appropriately
assigned to the movement controller (in the present study, the
“movement controller” refers to both the inverse model and the
feedback controller comprised of the forward model). In contrast to unimanual movement, in which there is one-to-one
correspondence between the movement controller and the resultant movement error, the problem of “credit assignment”
(Berniker and Kording 2008; Chen-Harris et al. 2008; Kluzik
et al. 2008) is not trivial for bimanual movement (Diedrichsen
et al. 2004; Franz et al. 2001; Peters 1985), in which two
movement controllers for both hands can generate two distinct
movement errors (White and Diedrichsen 2010). Consider a
TO PERFORM A DESIRED MOVEMENT
Address for reprint requests and other correspondence: D. Nozaki, Graduate
School of Education, The Univ. of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo
113-0033, Japan (e-mail: [email protected]).
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task in which two cursors are controlled by moving handles
bimanually. Intuitively, if the subject explicitly knows which
cursor reflects which hand’s movement, it is likely that the
movement of each cursor will be appropriately assigned to the
actual movement controller of the hand. However, considering
a previous finding that implicit visuomotor learning can override even explicit strategy (Mazzoni and Krakauer 2006), such
appropriate assignment is not necessarily guaranteed. Furthermore, the existence of neuronal interference or cross talk in
movement planning and/or execution (Carson 2005; Heuer
1993; Marteniuk et al. 1984; Mechsner et al. 2001; Sherwood
1994; Swinnen and Wenderoth 2004) suggests that such cross
talk also exists in the process of credit assignment.
A recent study reports that when visual rotation is applied to
a cursor displayed at the middle position between both hands,
both hands exhibit adaptation at the subsequent trial, indicating
that the controllers of both hands refer to only one error
information (White and Diedrichsen 2010). However, in their
study, because of the redundant relationship between cursor
movement and hand movements, the participants’ natural reaction has been to move both hands to compensate for the
cursor movement. Furthermore, since the participants were
allowed to correct their movements during reaching, it is
possible that their natural response to online correction worked
as an explicit cue that could be used to teach the controllers
how they should adapt to the error.
Therefore, we investigated the credit-assignment problem
during bimanual movement more directly by gradually increasing the visual rotation such that the participants were unaware
of it (Kagerer et al. 1997; Michel et al. 2007; Saijo and Gomi
2010). The participants performed a symmetric, bimanual
movement, and apart from the study displaying a cursor at the
middle position of both hands (White and Diedrichsen 2010),
a single cursor moving with the right hand was displayed. We
found that although the participants explicitly knew that the
cursor reflected the movement of their right hand, the implicit
adaptation of their movement to the visual rotation occurred
not only for the right hand but also for the left hand, especially
when the cursor was presented just above the left hand.
Even when two cursors were presented for both of the hands,
the presence of such inherent cross talk in the credit assignment
could substantially influence the performance of the adaptation
to visual rotation during bimanual movement. Specifically, we
predicted that the adaptation was impaired when the rotational
directions imposed on both cursors were opposite compared
with when they were the same, because in the former case, the
movement correction of one hand to the relevant cursor should
be interfered with by the opposite directional error of the
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Kasuga S, Nozaki D. Cross talk in implicit assignment of error information during bimanual visuomotor learning. J Neurophysiol 106: 1218–
1226, 2011. First published June 8, 2011; doi:10.1152/jn.00278.2011.—
When a neural movement controller, called an “internal model,” is
adapted to a novel environment, the movement error needs to be
appropriately associated with the controller. However, their association is not necessarily guaranteed for bimanual movements in which
two controllers— one for each hand—result in two movement errors.
Considering the implicit nature of the adaptation process, the movement error of one hand can be erroneously associated with the
controller of the other hand. Here, we investigated this credit-assignment problem in bimanual movement by having participants perform
bimanual, symmetric back-and-forth movements while displaying the
position of the right hand only with a cursor. In the training session,
the cursor position was gradually rotated clockwise, such that the
participants were unaware of the rotation. The movement of the right
hand gradually rotated counterclockwise as a consequence of adaptation. Although the participants knew that the cursor reflected the
movement of the right hand, such gradual adaptation was also observed for the invisible left hand, especially when the cursor was
presented on the left side of the display. Thus the movement error of
the right hand was implicitly assigned to the left-hand controller. Such
cross talk in credit assignment might influence motor adaptation
performance, even when two cursors are presented; the adaptation was
impaired when the rotations imposed on the cursors were opposite
compared with when they were in the same direction. These results
indicate the inherent presence of cross talk in the process of associating action with consequence in bimanual movement.
IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
irrelevant cursor associated with the other hand. Our additional
experiment confirmed this prediction, which further supported
the presence of inherent cross talk in the process by which
movement errors are associated with movement controllers
during bimanual movement.
MATERIALS AND METHODS
Participants
participating. The handedness of each participant was tested by the
Edinburgh Inventory (Oldfield 1971), and all were judged as righthanded (laterality quotient ⫽ 86.7 ⫾ 3.8).
Apparatus
The experiments were performed in a dark room. Participants sat in
front of a white horizontal screen at chest height, where a computer
screen (51 ⫻ 40 cm) was displayed using a projector (Fig. 1). Chair
height was adjusted such that the elbows and wrists did not touch the
working space or the upper horizontal plane. Participants were instructed to keep their head straight and face forward and to avoid
twisting their head and body. In each hand, they held a handle of a
custom-made manipulandum that could be moved in a horizontal
plane under the screen. The participants could not directly see the
handles and their hands. The vertical handle was attached to the end
of the two linked bars (length of each bar ⫽ 47.5 cm) whose angular
displacements were measured by potentiometers (Fig. 1A). The analog
outputs of the potentiometers were sampled at 1,000 Hz (PXI-1042,
National Instruments, Austin, TX) to display the positions of the
Fig. 1. Setup of experiments 1 and 2. A: schematic representation of the manipulandum. The device has 2 linked bars for each hand to measure the handle position.
The angular displacement of each bar was measured by potentiometers. B and C: in experiment 1, visual information of the right hand only (the visible hand;
the thick line) is displayed on a white horizontal screen just above the left (left panel) or right hand (right panel). Double circles indicate a target; gray circles
indicate a starting position; filled black circles indicate a cursor; and empty black circles indicate a handle. In the cursor rotation (CR) condition, a cursor is
presented at a given position by rotating the handle position around the starting position (B). The degree of rotation is gradually increased in the clockwise (CW)
direction. In the target rotation (TR) condition, the target position gradually shifted counterclockwise (CCW; C). D: in experiment 2, the visual information of
both hands is displayed. In the opposite rotation (OR) condition, the directions of visual rotation applied to the cursors of both hands are opposite (left panel).
In the same rotation (SR) condition, the directions of visual rotation are identical (right panel).
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A total of 26 subjects participated in this study and were randomly
assigned to one of two experimental groups. Each subject participated
in only one experiment. Ten participants (nine men and one woman;
aged 19 –31 years) participated in experiment 1; 16 participants (14
men and two women; aged 21–28 years) participated in experiment 2.
All participants had no cognitive or motor disorders and were naïve to
the purpose of the experiments. All experiments were approved by the
Ethical Committee of the Graduate School of Education, The University of Tokyo. All subjects provided written, informed consent before
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IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
handles by the cursors (blue and green for the left and right handles,
respectively; diameter, 0.5 cm) on the screen in real time by a program
written in LabVIEW 7.1 (National Instruments). The cursors were
presented on the screen above the actual or the shifted handle position.
Another computer was used for analog-to-digital conversion (200 Hz)
and stored the data for later analysis using the MATLAB data
acquisition toolbox (Mathworks, Natick, MA).
The experimental system also displayed starting position(s) and
target(s) using red circle(s) (diameter, 0.9 cm). A target was presented
for 2,000 ms every 5,000 ⫾ 500 ms directly ahead of the starting
position(s), whereas the starting position(s) were always visible. The
distance from a starting position to a target was 7 cm. The starting
positions of the left and right hands were separated by 32 cm.
Procedure
Experiment 1
Experiment 1 was designed to examine how visual errors are assigned
to the left- and right-hand movement controllers during bimanual movements when the error information of one hand was only provided
visually. In this experiment, the visual information of the right hand only
(i.e., the starting position, target, and cursor) was displayed on the screen
(Fig. 1B). The participants were instructed to simultaneously move
both hands straight ahead so that the cursor hit the target. They
explicitly knew that the movement of the cursor was associated
with the movement of the right hand. Since it was difficult to return
the invisible left hand to the starting position, a small tactile
projection was placed there to help the participants place the
invisible left hand.
Cursor rotation condition. The cursor rotation (CR) condition consisted of four different phases: baseline (15 trials), adaptation (135 trials),
unimanual catch trial (five trials), and washout (25 trials) (Fig. 2A).
During the adaptation phase, the degree of imposed visual rotation
gradually increased from 0° to 45° in a clockwise (CW) direction
(0.6°/trial) and fixed at 45° for the remaining 60 trials so that the
participants were not aware of the visual rotation. Such a gradual
increase in visual rotation was adopted to examine how the participants implicitly adapt their movements to the novel environment
(Kagerer et al. 1997; Michel et al. 2007; Saijo and Gomi 2010). In the
unimanual catch trial phase, to examine if the invisible left hand
actually adapts to the visual rotation, the after effect was measured
when the participants performed unimanual movement with the invisible left hand from the starting position toward a target located
directly ahead. In experiment 1, since every participant experienced
two trials within 1 day, the washout phase was placed at the end of the
trial of each condition to eliminate any remaining adaptation effect.
To investigate how the display location of visual information influences the performance of visuomotor learning, we set “left” and “right”
conditions, in which the starting and target positions and the cursor were
displayed above the left (CR-left) and right (CR-right) hands (Fig. 1B).
Target rotation condition. In the CR experiment, the visible right
hand should adapt to the visual rotation. The resultant change in the
direction of movement of the right hand can influence the direction of
movement of the invisible left hand. The target rotation (TR) condition
was conducted as a control experiment to examine this possible effect. In
this condition, the target location gradually shifted counterclockwise
(CCW) around the starting position from 0° to 45° every trial (Fig. 1C).
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Fig. 2. Protocols of experiments 1 and 2. A: experiment 1 consists of baseline
(15 trials), adaptation (135 trials), unimanual catch trial (5 trials), and washout
(25 trials) phases (180 trials in total). During the adaptation phase, the degree
of CR condition or TR condition gradually increased from 0° to 45° and was
fixed at 45° in the last 60 trials. B: experiment 2 consists of baseline (20 trials),
adaptation (70 trials), and washout (10 trials) phases (100 trials in total).
During the adaptation phase, the visual rotation imposed on the cursors
gradually increased from 0° to 30° and was fixed at 30° in the last 10 trials.
Otherwise, the experimental procedure was identical to that of the CR
condition. The participants were instructed to move the left hand straight
ahead regardless of the movement direction of the right hand.
Individuals participated in all four kinds of conditions (CR and TR
conditions ⫻ left and right conditions) over 2 days. Participants were
tested under both conditions for a given hand in 1 single day (i.e., CRand TR-left on the same day). The order of the conditions (CR vs. TR)
was reversed on the 1st and the 2nd day, and the order of the locations
was randomized for each participant.
Experiment 2
Experiment 2 was designed to examine whether the cross talk in the
error-information assignment was present, even when visual information was appropriately provided for both hands. In contrast to experiment 1, in which only one cursor was displayed, in experiment 2,
visual feedback (i.e., cursors) for both hands was provided (Fig. 1D).
There were two conditions (n ⫽ 8 for each condition): the opposite
rotation (OR) and same rotation (SR) conditions. In the OR condition,
the directions of visual rotation, applied to the cursors of both hands,
were opposite, whereas they were the same in the SR condition. The
rotation direction (CW or CCW) was counterbalanced for each condition. If the cross talk were present, the adaptation performance was
worse in the OR condition, because the left (or right)-hand movement
correction was negatively affected by the cursor of the right (or left)
hand in the opposite direction.
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The participants were instructed to move the cursor between the
starting position and the target by performing straight, fast, and
uncorrected out-and-back movements with a sharp reversal at the
target (peak velocity was ⬃250 mm/s). Before each trial, they needed
to place the cursor at the starting position and wait for the appearance
of a target. Prior to all experiments, the participants performed a
sufficient amount of bimanual movement practice (150 trials) under
normal visuomotor conditions.
IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
Each experiment comprised three phases (Fig. 2B): baseline (20 trials),
adaptation (70 trials), and washout (10 trials). In the adaptation phase, the
degree of visual rotations was gradually increased from 0° to 30°
(0.5°/trial) so that the participants were not aware that it was occurring.
Data Analysis
Quantification of Adaptation
In experiment 1, to quantify the degree of adaptation to the visual
rotation and the effect of TR, we calculated the mean movement
direction of the last 60 trials of the adaptation phase, in which the
amount of cursor or TR reached a constant angle (45°). We also
calculated the correlation coefficient of the trial-by-trial changes in the
movement directions between both hands to determine the similarity
of the trial-by-trial movement corrections between them. Positive and
negative correlations indicate that the movement directions of the
hands are modified in the same or opposite direction in the extrinsic
space, respectively. In the unimanual catch trial phase, only the
movement direction of the first of five trials in a row was calculated
and compared between conditions.
In experiment 2, the average movement direction of the last 10
trials in the adaptation phase was calculated to quantify the degree of
adaptation. The correlation coefficient of the trial-by-trial changes in
the movement directions between both hands was also obtained to
determine the similarity of the trial-by-trial movement correction.
Statistics
Data values are expressed as means ⫾ SE, calculated using data
from all participants. Repeated-measures ANOVA as well as paired
and unpaired t-tests were performed to detect significant differences in
the movement direction between hands, conditions, experimental
types, and phases in each experiment. We also used a two-way
factorial ANOVA to test the interaction between the positions of the
visual information displayed (i.e., left vs. right) and the CR vs. TR
condition. Regarding the values of the correlation coefficients, we
calculated Fisher’s z-scores and used them to compare different
conditions by repeated-measures ANOVA. If a significant difference
was detected by ANOVA, a post hoc Bonferroni test was used for
multiple comparisons. The significance threshold was set at P ⬍ 0.05.
RESULTS
Experiment 1: Adaptation to Visual Rotation
of a Single Cursor
Correlation of the Trial-by-Trial Changes with Respect to
the Movement Directions of Both Hands
The correlation coefficient between the trial-by-trial changes in
the movement directions of both hands during the adaptation
phase was positive only in the CR-left condition (r ⫽ 0.15 ⫾ 0.06;
Fig. 5A), indicating that the movement direction was corrected in
the same direction for both hands. The correlation coefficient was
negative in the other conditions (CR-right, r ⫽ ⫺0.15 ⫾ 0.07;
TR-left, r ⫽ ⫺0.12 ⫾ 0.04; TR-right, r ⫽ ⫺0.12 ⫾ 0.03; Fig. 5A).
There was a significant main effect of experimental types [F(3,36) ⫽
7.24, P ⬍ 0.001]. Furthermore, the post hoc test indicated that
there was a significant difference between the CR-left and
other three conditions (P ⬍ 0.01; Fig. 5A).
Unimanual Catch Trials
None of the participants noticed the presence of the visual
rotation due to the gradual increase. The averaged times to the
peak velocity from the trial onset were 310.1 ⫾ 14.3 ms (left
hand) and 325.7 ⫾ 24.1 ms (right hand). The averaged peak
J Neurophysiol • VOL
velocities were 256.6 ⫾ 5.6 mm/s (left hand) and 232.9 ⫾ 11.7
mm/s (right hand). In experiment 1, the participants performed
two sessions within 1 day, but the influence was negligible,
because the movement direction of the baseline phases was not
statistically different between sessions, thanks to the washout
phase performed at the end of each session.
Predictably, the movement direction of the visible right hand
gradually rotated in the CCW direction and reached a plateau
to compensate for the imposed CW visual rotation of the cursor
in both the CR-left and CR-right conditions (Fig. 3). The
average values of the last 60 trials of the adaptation phase were
significantly different from zero [CR-left, 33.1 ⫾ 1.4°, t(9) ⫽
23.7, P ⬍ 0.01; CR-right, 34.5 ⫾ 1.1°, t(9) ⫽ 30.3, P ⬍ 0.01];
however, they were not significantly different between the
CR-right and CR-left conditions.
On the other hand, although the movement direction of the
left hand did not change in the CR-right condition, it gradually
shifted CCW with increasing the CW visual rotation imposed
on the cursor of the visible right hand in the CR-left condition
(Fig. 3). The average value in the last 60 trials of CR was not
significantly different from zero in the CR-right condition
[⫺0.9 ⫾ 3.2°, t(9) ⫽ 0.29, P ⫽ 0.78]; however, that in the
CR-left condition was significantly greater than zero [14.1 ⫾
3.0°, t(9) ⫽ 4.7, P ⬍ 0.01; Fig. 4].
In the TR conditions (TR-right and TR-left), the mean
movement direction during the last 60 trials of the TR phase
was significantly smaller than that of the baseline phase [TRleft, ⫺8.9 ⫾ 2.9°, t(9) ⫽ 3.1, P ⬍ 0.05; TR-right, ⫺8.8 ⫾ 2.5°,
t(9) ⫽ 3.5, P ⬍ 0.01; Fig. 4]. This indicates that the movement
direction of the invisible left hand gradually changed in the
direction (CW) opposite of the visible right hand (Fig. 3).
The two-way factorial ANOVA also showed a significant
interaction between the position of the visual information (left
vs. right) and the CR and TR conditions [F(1,36) ⫽ 6.80, P ⬍
0.05]. A post hoc test showed that there was a significant
difference between visual positions only for the CR condition
[F(1,36) ⫽ 13.3, P ⬍ 0.01], indicating that the change in the
movement direction of the left hand after adaptation of the
right hand to the visual rotation was influenced by the position
of the visual information displayed only for the CR condition.
In the movement direction in the first unimanual catch trial,
we observed a significant positive after effect (i.e., in the CCW
direction) for the CR-left condition [10.3 ⫾ 2.8°, t(9) ⫽ 3.6,
P ⬍ 0.01] but not for the CR-right condition [2.1 ⫾ 2.6°, t(9) ⫽
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The position data of the handle were low-pass filtered with a
zero-lag fourth-order Butterworth filter (cutoff frequency, 5 Hz).
Then, the velocity of the handle was calculated by differentiating the
position data with a three-point central difference equation. We
obtained the position at which the outward velocity peaked. Movement direction was defined as the angle from a line connecting the
starting position and the target to a line connecting the starting
position and the position where the peak velocity was observed; CCW
and CW directions were defined to take positive and negative value of
the direction, respectively. The averaged value of the movement
direction in the baseline phase was calculated; this value was subtracted from the data in the other phase for subsequent analyses. We
also evaluated the movement direction at a fixed time (200 ms) after
the movement onset, but the results did not differ. Thus we demonstrated only the data evaluated at the peak velocity.
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Fig. 3. A: trial-by-trial changes in movement direction. Each dot represents the movement direction of the left (red) and right (blue) hands averaged across participants. The dashed black lines
represent the angle of visuomotor rotation applied
to a CR condition or the angle of a rotation of a
TR position. The positive value refers to the CCW
movement for hands and the CW rotation for the
cursor and target. B: an average hand path of the
baseline phase (from the 1st to the 15th trial;
dashed lines) and the last 60 trials of the adaptation phase (from the 91st to the 150th trial; solid
lines) in experiment 1. The directional shift was
observed in the CCW (CR-left) and CW directions
(TR-left and TR-right). The seemingly CCW rotation of the left hand in the baseline trials (especially in the TR-right condition) was due to the
fact that some participants tended to move the
invisible left hand CCW in the baseline trials.
0.80, P ⫽ 0.45]. On the other hand, a significant negative after
effect (i.e., in the CW direction) was observed for both the
TR-left [⫺4.3 ⫾ 1.0°, t(9) ⫽ 4.3, P ⬍ 0.01] and TR-right
conditions [⫺4.3 ⫾ 1.7°, t(9) ⫽ 2.6, P ⬍ 0.05; Fig. 5B].
Experiment 2: Adaptation to Visual Rotation Applied
to Both Hands
In experiment 2, the averaged times to the peak velocity from
the trial onset were 295 ⫾ 30.6 ms (left hand) and 300.5 ⫾ 30.0
ms (right hand), and the averaged peak velocities were 255.3 ⫾
20.0 mm/s (left hand) and 248.3 ⫾ 18.4 mm/s (right hand).
J Neurophysiol • VOL
Figure 6 shows the changes in the movement direction in
experiment 2. The rate of the changes appeared to be slower in
the OR condition than in the SR condition (Fig. 6A). The average
movement directions of the last 10 trials in the OR condition were
17.4 ⫾ 2.0° and 20.0 ⫾ 0.7° for the left and right hands,
respectively. On the other hand, the average movement directions
in the SR condition were 24.0 ⫾ 1.6° and 24.0 ⫾ 1.0° for the left
and right hands, respectively (Fig. 6B). These changes in movement direction were significantly different between the two conditions for both hands [left hand, t(30) ⫽ 9.9, P ⬍ 0.01; right hand,
t(30) ⫽ 7.9, P ⬍ 0.01, Fig. 6B].
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IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
Correlation of the Trial-by-Trial Changes in the Movement
Directions of Both Hands
If the motor learning system refers to only one of the cursors in
a given trial because of the limited amount of attention we have,
movement of both of the hands should be corrected according to
a common cursor’s movement error; consequently, they should be
corrected in the same direction. Thus we can expect that the
trial-by-trial correction in a movement direction should be positively correlated between the hands for both the OR and SR
conditions, as was observed in experiment 1 (Fig. 5A). However,
the correlation coefficient between the trial-by-trial changes in
both hands’ movement direction during the adaptation phase
averaged across participants was r ⫽ ⫺0.07 ⫾ 0.12, which is not
significantly different from zero [t(7) ⫽ 0.58, P ⫽ 0.58; Fig. 6C].
In addition, a significantly positive correlation coefficient was
observed in only two participants in the SR condition, indicating
that the movement direction is not corrected in the same direction
for both hands in most cases. In the OR condition, none of the
participants exhibited significant positive correlation coefficients.
Rather, the average across participants was significantly negative
[r ⫽ ⫺0.25 ⫾ 0.07, t(7) ⫽ 3.9, P ⬍ 0.01; Fig. 6C]. Again, this
indicates that they did not refer to only one of the cursors.
DISCUSSION
Previous studies demonstrate the existence of neural cross talk
in the motor planning and execution during bimanual movements
(Carson 2005; Heuer 1993; Marteniuk et al. 1984; Mechsner et al.
2001; Sherwood 1994; Swinnen and Wenderoth 2004). For example, cortical neural cross talk exists at a higher level of motor
control through interhemispheric interaction via the corpus callosum (Eliassen et al. 2000; Franz et al. 1996; Kennerley et al.
2002). Bilateral brain activity related to the maintenance of unstable bimanual rhythmic movements is reported in the dorsal
premotor cortex, a supplementary motor area (Meyer-Lindenberg
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et al. 2002), and primary motor cortex (Maki et al. 2008).
Furthermore, the transition phase from unstable to stable in a
bimanual, rhythmic finger-tapping task is also reported to be
accompanied with activity in various brain areas, including the
ventral premotor cortex though the corpus callosum (Aramaki et
al. 2006), indicating the existence of the interhemispheric interaction during bimanual movements. Neural cross talk also exists
at a lower level through the ipsilateral corticospinal tract (Cattaert
et al. 1999; Kagerer et al. 2003), where motor signals are sent to
the effector from both contralateral- and ipsilateral-descending
corticofugal fibers. These intersecting interactions of neural pathways are thought to cause involuntary, bimanual interactions, such
as mirror movements (Carson 2005).
We hypothesize that such cross talk during bimanual movement exists not only at the level of motor planning and motor
execution but also at the level of motor learning. To test this
hypothesis, we examined how left-hand movement was corrected during symmetric bimanual movements when visual
information of only the right hand was provided (experiment
1). We also investigated that such implicit cross talk, if any,
can influence the performance of motor learning, even when
two cursors are displayed (experiment 2).
Single Visual Movement Errors are Implicitly Assigned to
the Controllers of Both Hands
In the CR-left condition, in which the visual information
was displayed just above the left hand, we observed a
directional shift in hand movement along with the visual
rotation both for the visible right hand and invisible left
hand (Fig. 3), despite the fact that participants explicitly
knew that the movement of the cursor was associated with
their right hand alone. Considering that the participants were
unaware of the presence of visual rotation in the adaptation
phase, this result suggests that the unnoticeable movement
error in the right hand is implicitly used to correct the motor
output of the left hand. The significant, positive correlation in
the trial-by-trial correction of the movement directions (Fig.
5A) also supports this idea.
In contrast, no such cross talk in the motor learning process was
observed when the visual information was displayed just above
the right hand (i.e., the CR-right condition). Such lateral bias
suggests that the degree of error assignment is influenced by the
position of the visual information in the workspace. We assumed
that the degree of visual error assignment is related to the credit of
visual information; that is, if visual information is on the left side,
the left-hand controller tends to put more credit on it. One possible
reason for this might be ascribed to the response characteristics of
multisensory neurons. These neurons receive both proprioceptive
and visual inputs; their response is positively correlated to the
distance between the body part and visual stimulus (Bremmer et
al. 2001; Duhamel et al. 1998; Fogassi et al. 1999; Graziano et al.
1994; Rizzolatti et al. 1998). If such neurons are involved in
visuomotor learning, greater distances between proprioception
and visual information in the CR-right condition would decrease
the visuomotor learning performance of the left hand.
However, before these results can be ascribed to the cross
talk in the motor learning process for certain, we need to
consider other possibilities that explain the results of the
present study. One of the possibilities is the influence of
right-hand movement. Since the movement direction of the
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Fig. 4. Average movement directions of the left and right hands during the last
60 trials of the adaptation phase in experiment 1. Positive values indicate CCW
direction. In all conditions, the movement direction of the right hand shifted
CCW, indicating that the adaptation occurred to compensate for the imposed
CW visual rotation. The movement direction of the left hand shifted CCW only
in the CR-left condition; CW shifts were observed in the TR-left and TR-right
conditions. Asterisks indicate significant directional shifts (*P ⬍ 0.05; **P ⬍
0.01). Error bars indicate ⫾ 1 SE.
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IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
right hand gradually shifted with motor learning, such changes
in movement direction could mechanically or neurally contribute to directional shift in left-hand movement. However, this is
unlikely for the following two reasons. First, the directional shift
was observed only in the CR-left condition. Second, in the TR
conditions, the changes in the movement direction of the right
hand induced the directional shift of the left-hand movement in
the opposite direction (Fig. 3), rather than in the same direction, as
observed in the CR-left condition. Such shifts toward the opposite
direction can be partly explained by a preference for mirrorsymmetric movements in bimanual movement when we perform
movements with both hands simultaneously (Franz et al. 1996;
Kelso 1984; Kelso et al. 1979; Lee et al. 2002; Swinnen et al.
1997; Swinnen and Wenderoth 2004).
Another possibility is that participants tried to maintain a
constant distance between both hands, leading to the directional shift in left-hand movement. However, this explanation
cannot explain why the shift was observed only in the CR-left
condition. Furthermore, we observed significant after effects in
the unimanual catch trials, indicating that directional changes
in left-hand movement are not caused by the participants’
intention to keep the distance between both hands constant but
rather, by the adaptation of the left hand. The amount of after
effect (10.3 ⫾ 2.8°) was significantly [t(9) ⫽ 2.12, P ⬍ 0.05]
smaller than that of the adaptation phase (14.1 ⫾ 3.0°). This result
was consistent with the partial motor learning transfer observed
from bimanual to unimanual movement in previous studies (Nozaki et al. 2006), although almost full transfer was reported in
visumotor rotation between unimanual and bimanual movements
(Wang et al. 2010; Wang and Sainburg 2009).
Directional Shift of Left-Hand Movement
in the TR Condition
In the previous section, the shift in the movement direction of
the left hand in the TR condition was explained by the preference
of mirror-symmetric bimanual movement. Here, we provide the
alternative possibility that this shift can be explained by cross talk
in the credit-assignment processes. In the TR condition, the
J Neurophysiol • VOL
movement of the right-hand cursor was gradually rotated CCW,
according to the target position shift. If the movement of the
cursor is implicitly assigned to the movement controller of the left
hand, even in the TR condition, a discrepancy might arise between
the controller’s prediction (i.e., movement straight ahead) and the
cursor’s movement (i.e., CCW movement); this prediction error
could correct the CW movement direction of the left hand. This
idea is corroborated by the results of the TR condition (Figs. 3 and
4), although it could not perfectly explain why the CW shift of the
left hand was not greater for the TR-left condition.
Cross Talk Exists Even When Two Cursors are Displayed
Experiment 2 examined the presence of implicit cross talk
when cursors for each hand were displayed. In the OR condition,
in which two cursors were rotated in opposite directions, the
directions of errors between the left and right hands are opposite.
Therefore, the cross talk, if it exists, should result in conflict in
motor adaptation between the two controllers. In contrast, in the
SR condition, such conflicting influence might be much smaller,
because movement corrections in the same direction are needed.
The results are consistent with the prediction when the presence of
cross talk is assumed (Fig. 6, A and B). Similar results are reported
by a recent study (Wang et al. 2010) using sudden visual rotation.
In that study, the authors ascribe the impairment of visuomotor
learning to the greater demands of visual information processing
required for the opposite visual rotation. Our proposed cross-talk
hypothesis provides a more concrete understanding of what the
greater demand indicates. Our cross-talk scheme could also explain a recent finding by Casadio et al. (2010) that the adaptation
to two opposite force fields to both of the arms was worse than the
adaptation to the same force fields, because the adaptation to the
opposite force fields necessarily accompanied the opposite directional visual error.
Although a study (Diedrichsen et al. 2004) reported that the
participants did not find it difficult to pay attention to the two
cursors when manipulating them with both hands, one might
still consider that limited attention could cause the motor
learning system to refer to only one of the cursors in a given
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Fig. 5. A: average correlation coefficients of the
trial-by-trial shift of movement direction between
hands during the adaptation phase in experiment 1.
There was a significant difference in the correlation
coefficient between the CR-left and the other 3 conditions (P ⬍ 0.01). B: average movement directions
of the first trial of the unimanual catch trial phase.
Positive values indicate CCW direction. A significant
CCW shift was observed only for the CR-left condition (P ⬍ 0.01) and significant CW shifts for the
TR-left (P ⬍ 0.01) and TR-right conditions (P ⬍
0.05). Asterisks indicate significant directional shifts
(*P ⬍ 0.05; **P ⬍ 0.01). Error bars indicate ⫾ 1 SE.
IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
1225
trial. Furthermore, we did not constrain their eye movements,
which would disperse their attention. However, without taking
the effect of cross talk into account, such partial reference of
visual error cannot explain the difference in motor learning
performance between the OR and SR conditions (Fig. 6, A and
B); although it might retard motor learning, as long as the
credit assignment is appropriate, the degree of retardation
should have been identical between these two conditions.
We also doubt that such partial reference itself is the case. If
this were true, the trial-by-trial correction in movement direction should have been correlated between both hands, because
the controllers referred to the visual error information of only
one hand. However, the results are inconsistent with the prediction (Fig. 6C), indicating that the visual-error information of
both hands simultaneously influences the motor learning of the
movement controllers of both hands.
Possible Neuronal Mechanism of Cross Talk in Bimanual
Motor Learning
Previous studies indicate that several brain areas are involved in
adaptation to visual rotation during reaching movements, such as
the primary cortex (Paz et al. 2003), cerebellum (Imamizu et al.
2000; Smith and Shadmehr 2005), posterior parietal cortex, and
premotor cortex (Krakauer et al. 2004). Some of these areas are
known to have bilateral, receptive field-like neurons in the BrodJ Neurophysiol • VOL
mann’s Area 5 (BA5) (Iwamura 2000). Bilateral activation has
been found in error information processing in response to visual
rotation during reaching movements in the BA5 (Diedrichsen et
al. 2005) and cerebellum (Diedrichsen et al. 2005; Imamizu et al.
2000). These findings suggest the possibility that some neurons
are commonly used to process the information of both arms’
movement errors and/or that the error-information processing is
not specific to the arms, which might promote a cross-talk effect
in bilateral visuomotor learning.
In summary, similar to the presence of cross talk in motor
planning and execution during bimanual movement, the present
study reveals that there is an implicit cross talk in credit-assignment processes in visuomotor learning. The cross talk is inevitable, despite explicit knowledge about the association of the movement controller and the resultant visual information.
Is such cross talk just a byproduct, or does it play any functional
role in bimanual movement control? White and Diedrichsen
(2010) recently demonstrated that when a visual rotation is applied to a cursor displayed at the middle position of both hands,
both hands exhibit adaptation at the subsequent trial; this indicates
that the controllers of both hands refer to only one visual error
information. Such flexible construction of the reference to error
information would require both hands’ movement controllers to
possess a mechanism that considers what the other hand is doing.
Then, the implicit cross-talk effect found in this study might
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Fig. 6. A: trial-by-trial changes in average movement direction in experiment 2 (left panel, OR
condition; right panel, SR condition). Dashed
black lines indicate the imposed visual rotations.
Each dot indicates the movement directions for
the left (red) and right (blue) hands. The imposed rotation and the compensatory rotation of
the movement direction are represented by positive values, regardless of the direction of rotation. B: average magnitude of movement during
the last 10 trials of the adaptation phase. There
was a significant difference between the OR and
SR conditions (P ⬍ 0.01). C: average correlation coefficient of the trial-by-trial shift in movement directions between hands during the adaptation phase. There was a significant negative
correlation regarding the OR condition (P ⬍
0.01); the correlation for the SR condition was not
significantly different from 0 (P ⫽ 0.58). Asterisks
indicate significant correlations (**P ⬍ 0.01).
Error bars indicate ⫾ 1 SE.
1226
IMPLICIT CROSS TALK IN BIMANUAL VISUOMOTOR LEARNING PROCESS
reflect the foundation of the flexible construction of visual error
information. Our recent study also demonstrates that such interference between the controllers of both hands may play an
important role in constructing and switching among internal
models, depending on the kinematics of the opposite hand (Yokoi
et al. 2011). Future studies are needed to elucidate the possible
functional role of the interference.
ACKNOWLEDGMENTS
S. Kasuga is a Research Fellow of the Japan Society for the Promotion of
Science. The authors thank Yoshiharu Yamamoto, Gentaro Taga, and the
members of the Nozaki lab for their helpful comments.
GRANTS
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
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