Cognition 131 (2014) 355366

Contents lists available at ScienceDirect

Cognition
journal homepage: www.elsevier.com/locate/COGNIT

Differential reliance of chimpanzees and humans on automatic

and deliberate control of motor actions
Takaaki Kaneko , Masaki Tomonaga
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan

a r t i c l e

i n f o

Article history:
Received 5 June 2013
Revised 4 February 2014
Accepted 12 February 2014
Available online 15 March 2014
Keywords:
Self-monitoring
Chimpanzees
Agency
Voluntary action
Imitation
Mirror system

a b s t r a c t
Humans are often unaware of how they control their limb motor movements. People pay
attention to their own motor movements only when their usual motor routines encounter
errors. Yet little is known about the extent to which voluntary actions rely on automatic
control and when automatic control shifts to deliberate control in nonhuman primates.
In this study, we demonstrate that chimpanzees and humans showed similar limb motor
adjustment in response to feedback error during reaching actions, whereas attentional allocation inferred from gaze behavior differed. We found that humans shifted attention to
their own motor kinematics as errors were induced in motor trajectory feedback regardless
of whether the errors actually disrupted their reaching their action goals. In contrast, chimpanzees shifted attention to motor execution only when errors actually interfered with
their achieving a planned action goal. These results indicate that the species differed in
their criteria for shifting from automatic to deliberate control of motor actions. It is widely
accepted that sophisticated motor repertoires have evolved in humans. Our results suggest
that the deliberate monitoring of ones own motor kinematics may have evolved in the
human lineage.
2014 Elsevier B.V. All rights reserved.

1. Introduction
To what extent do nonhuman primates intentionally
control their motor actions? This is an important question
for understanding the evolutionary origin of intentional
and deliberate control of motor actions. However, experimental studies comparing humans and nonhuman primates in this regard are scarce.
Humans automatically adjust their limb movements
according to the degree of discrepancy between the predicted results of actions and actual feedback, even when
they are unaware of the error (Fourneret & Jeannerod,
1998; Knoblich & Kircher, 2004; Musseler & Sutter,
2009). For example, when one moves a cursor to an icon
Corresponding author. Current Address: Department of Psychology,
Kyoto University, Yoshida-Honmachi, Kyoto 606-8501, Japan. Tel.: +81 75
753 2442.
E-mail address: kaneko.takaaki.22m@st.kyoto-u.ac.jp (T. Kaneko).
http://dx.doi.org/10.1016/j.cognition.2014.02.002
0010-0277/ 2014 Elsevier B.V. All rights reserved.

using a computer mouse, the contingency between mouse

movement and cursor action can often change due to conditions affecting the mouse (e.g., desk surface structure).
Motor corrections occur automatically and humans are
unaware of errors unless an error reaches a certain threshold. Several behavioral experiments have demonstrated
that primate species, including both humans and nonhumans, dedicate distinctive systems to conceptual representations of action goals and execution of actual motor
kinematics to achieve the goal (Glover, 2004; Nakayama,
Yamagata, Tanji, & Hoshi, 2008; Yamagata, Nakayama,
Tanji, & Hoshi, 2009). Humans perceptually represent simple goals of their actions, and the corresponding actual motor action is automatically activated (Mechsner, Kerzel,
Knoblich, & Prinz, 2001). Norman and Shallice (1986) argued that motor systems need to recruit attentional resources only when they face a novel and unpredictable
situation where routine solutions are not efcient.

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

On the other hand, accumulating evidence suggests that

perception of others actions is closely related to execution
of ones own actions. It has been proposed that perception
and understanding of others actions shares the same neural circuits with execution of ones own actions through
the mirror-neuron system (Kanakogi & Itakura, 2011;
Myowa-Yamakoshi, Kawakita, Okanda, & Takeshita, 2011;
Rizzolatti & Craighero, 2004; Sommerville, Woodward, &
Needham, 2005). Interestingly, mirror systems in humans
and non-human primates have one distinct difference.
The mirror system in humans is activated to observe
intransitive meaningless movements, in contrast to that
in non-human primates, which is activated only with
regard to others actions with an explicit action goal but
not to gross movements (Ferrari, Gallese, Rizzolatti, &
Fogassi, 2003; Rizzolatti & Craighero, 2004). Furthermore,
a growing body of research indicates differences in the
way humans and chimpanzees copy others actions. It is
well known that chimpanzees are capable of sophisticated
social learning (Tomasello, Davis-Dasilva, Camak, & Bard,
1987; Whiten, Custance, Gomez, Teixidor, & Bard, 1996;
Whiten et al., 1999). However, social learning by great
apes, including chimpanzees, is limited to emulation,
which is dened as reproducing the action-goal of an
observed action, and does not include imitation, which is
dened as copying the kinematic aspects of the action
(Call, 2001; Call, Carpenter, & Tomasello, 2005;
Myowa-Yamakoshi & Matsuzawa, 1999; MyowaYamakoshi & Matsuzawa, 2000; Nagell, Olguin, &
Tomasello, 1993; Tennie, Call, & Tomasello, 2006;
Tomasello et al., 1987). Many studies have emphasized
differences in how chimpanzees and humans perceive
others actions. Yet similarities and dissimilarities between
the two species in the execution and perception of ones
own actions have rarely been investigated (Kaneko &
Tomonaga, 2011; Kaneko & Tomonaga, 2012).
This species difference in copying action may reect
species differences in the execution of ones own actions.
Specically, it is possible that control of motor kinematics
in chimpanzees is highly dependent on the automatic
aspects of motor control, as chimpanzees, nd it difcult
to imitate a motor action without an explicit action goal
(Call, 2001; Myowa-Yamakoshi & Matsuzawa, 1999). This
view is also congruent with our previous study, which
showed that chimpanzees have a bias toward monitoring
goals when monitoring their own action, whereas humans
monitor kinematic information and goal representation
equally (Kaneko & Tomonaga, 2012). The monitoring of
own-action occurs hierarchically; that is, it entails an
automatic and implicit sensorimotor process and an explicit conceptual process. However, in that study, we could
not empirically determine to what extent implicit versus
explicit monitoring was involved.
In the present study, we investigated possible differences in reliance on automatic motor control between
the two species and examined when and to what extent
they paid attention to their own motor kinematics. We
hypothesized that humans and chimpanzees are comparable in conceptual representation of an action goal but may
differ in the extent and timing of the selective attention
that they allocate to controlling detailed motor kinematics

of their own actions. We compared the two species by

applying an equivalent behavioral task. The participants
manipulated a trackball device and moved a cursor to hit
a target shown on the computer display (Fig. 1a). The contingency between the trackball manipulation and the cursor action was stable in two-thirds of the trials. In the
remaining trials, the spatial mapping between the trackball
manipulation and the cursor action was distorted; thus,
the participants expectations for visual feedback of their
movements were inconsistent with the feedback received,
and they had to adjust their limb motor movements to the
novel mapping. The details of this distortion are described
later.
The extent to which motor control relies on automatic
operation can be inferred from the gaze behavior of participants (Fig. 2 and Supplemental Movies 1 and 2). While
performing a reaching action, humans generally continue
to xate on the goal (target location) of the reaching action,
and the action kinematics of their own limb (or cursor
trajectory) is observed only in their peripheral vision.
However, once contingency between ones own actions
and visual feedback is altered and the usual motor routines
do not work, then humans shift their gaze from the action
target to the action kinematic (Sailer, Flanagan, &
Johansson, 2005). Thus, by measuring gaze shifts from
the goal (target) to the action kinematic (cursor trajectory),
it is possible to infer when participants rely on overt attention to adjust a motor limb.
We introduced two types of distortion to alter the visual
feedback of participants actions and to induce an online
motor adjustment (Fig. 1b). One type of distortion disturbed the cursor motion and interfered with reaching
the goal (goal dissociation), and the other altered the motor
trajectory but had no effect on reaching the goal (goal
congruent). Under the goal-dissociation condition, cursor
action was rotated in a clockwise/counter-clockwise direction relative to the trackball manipulation. Thus, the cursor
could not reach the target unless the participants adjusted
their manipulation to the distorted spatial mapping. Under
the goal-congruent condition, cursor action was also
perturbed by angular rotation. However, the polarity of
rotation was gradually changed to the opposite direction
midway through the reaching action. This resulted in subjects not needing to adjust their manipulation to the distorted spatial mapping. Instead, to reach the target, they
needed to manipulate the trackball as if there were no
distortion. Thus, under this condition, distortion had no
effect on reaching the target (i.e., the goal of the action)
but still altered the action trajectory (see details in
Section 2). Under this condition, perceived cursor action
was dissociated from participants estimations of the
cursor action with respect to detailed spatiotemporal
parameters, although the cursor effectively reached the
planned action goal at the conceptual level. These distortion techniques were developed by Wolpert, Ghahramani,
and Jordan (1995).
In this experimental setting, we measured limb motor
adjustment in response to feedback errors and gaze shifts
as an indicator of when the feedback error triggered
participants overt attention to motor corrections as a
means of testing the possible difference between

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

(a)

(b)

Goal Dissociation

Goal Congruent

Altered
action

Start
Angular
rotation

Default
action

Stimulus
onset

(c)
P
P

Hit
D
L
Fig. 1. Schematic diagram of the behavioral task and design. (a) Task. The trial required the subject to hit three different locations of a target consecutively.
Here, only one target is shown for simplicity. (b) Test conditions. Two types of perturbations were used. The typical time course of angular rotation is shown
for each condition. (c) Schematic illustration of the goal-congruent distortion algorithm. The rectangle and circle represent the target and the cursor,
respectively. The dotted circle at left represents the initial location of the cursor. The dotted circle in the middle shows the invisible cursor (see Section 2 for
details).

(a)

(b)
2

4
6

7
3
1

(one male [Ayumu] and four females [Chloe, Cleo, Pal,

and Pan]; aged 1030 years). These chimpanzees have participated in various perceptual and cognitive studies
(Matsuzawa, 2003; Matsuzawa, Tomonaga, & Tanaka,
2006; Tomonaga, 2001). Seven female human participants
performed the experiment (aged 1927 years). The participants were undergraduate and graduate students, caregivers, and technicians who were unaware of the study
hypothesis. The care and use of animals complied with
the institutional ethical guidelines. The ethics committee
of the institution approved the human experiment.

Fig. 2. Automatic and deliberate control of action inferred from gaze

behavior. Examples of trials performed by chimpanzees with (b) and
without (a) distortion. Open green rectangles show the target location.
(Each target was shown successively but not simultaneously in an actual
trial). Solid lines represent cursor trajectory, and black arrows indicate
the direction of movement. Red crosses represent xation, and adjacent
numbers represent xation order. All xations were on the target in (a),
whereas there was some xation on cursor trajectory in (b). See also
Supplemental Movies 1 and 2. (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this
article.)

2.2. Apparatus

chimpanzees and humans in their reliance on automatic

and deliberate control for online motor adjustment.

Stimuli were presented on a 17-in. LCD monitor (Gunze

AV10226N02W) at a 60-cm viewing distance. The participants manipulated a trackball device 12 cm in diameter
(Sanwa H55-0300-SET). Eye movements were measured
with an infrared remote eye tracker (Tobii TX300) at
300 Hz. Mean eye-movement and visual-angle tracking errors for each participant ranged from 0.45 to 0.60 for
chimpanzees and from 0.58 to 1.14 for humans. Details
of the eye-tracking method and apparatus are described
elsewhere (Kaneko, Sakai, Miyabe-Nishiwaki, & Tomonaga,
2013). A small piece of fruit was delivered to the chimpanzee participants using an automated universal feeder (Biomedica BUF-310) as a reward at the end of each trial.

2. Methods

2.3. Task

2.1. Participants

A schematic illustration of the experimental task is

shown in Fig. 1a. An open circle and cursor were presented
on the monitor at the start of a trial (trial initiation process). The participants were required to move the cursor

Five chimpanzees living at the Primate Research Institute, Kyoto University, Japan, took part in the experiment

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

to the open circle. They also needed to keep their heads in a

particular area where the eye tracker could stably measure
their gaze at the same time. The validity of head location
was indicated by the color of the open circle (blue or
red). The main part of the trial was initiated when these
two criteria were satised. Following this start process, a
cursor (white closed circle, 7.4 mm [0.7] in diameter)
and a target (green closed rectangle, 10.6  10.6 mm;
1  1) were presented on the monitor. The distance between the target and the cursor was 150 mm (15). The relative directions from the cursor to the target varied across
trials. Once the cursor hit the target, that target disappeared and reappeared at a different location. The participants had to move the cursor to hit the target at three
different locations. The experiment consisted of test trials
(cursor action was distorted) and baseline trials (no perturbation). In both trial types, the cursor action did not involve any perturbation during the trial initiation process.
2.4. Conditions
The spatial mapping between trackball manipulation
and cursor action was distorted during the test trials. The
test-trial parameters consisted of two within-subject factors, i.e., distortion type (goal dissociation and goal congruent) and distortion amplitude (6, 12, 24, and 46). Under the
goal-dissociation condition, cursor action was rotated in a
clockwise/counter-clockwise direction relative to trackball
manipulation. The amplitude of rotation was dened by
another experimental parameter, distortion amplitude. The
direction (clockwise/counter clockwise) of angular rotation
was pseudo-randomized across trials. Cursor location under the goal-congruent condition was determined by the
following calculation. Suppose there was an invisible virtual cursor, whose dependence on the trackball manipulation was the same as that during the baseline trial (i.e., no
perturbation). The invisible cursor provided two values
(see also Fig. 1c). One was the distance between the virtual
cursor and its start position along the axis between the
start position and the target (D). The second value was
the offset distance from the axis between the start position
and the target (P). The distorted visual feedback (location
of the visible cursor) was shown at the position where
the distance along the start-to-goal axis was D, and the offset distance relative to the start-to-goal axis was dP + P.
Distortion displacement dP was calculated using the following formula: dP = Amp  sin(D/L  p), where L is the
distance from the start to the goal (150 mm). Amp was adjusted so that the mean of the momentary angular rotation
(angular error between the trackball manipulation and the
cursor movement) was the same as that under the goal disassociation condition. Thus, the mean momentary angular
rotation under the goal congruent and dissociation conditions was the same. By applying these processes, the cursor
typically showed a curving action, as shown in Fig. 1b.
2.5. Procedure
Distortion type and amplitude were within-subject factors. The order of trial type was pseudo-randomized. The
chimpanzees performed 32 trials under each condition,

and the humans performed ve trials. The baseline trials,

where no perturbation occurred, were inserted in a pseudo-random order between the test trials. The ratio of the
test to the baseline was set to 1:2. Both humans and chimpanzees performed more than 62 habituation trials before
the test sessions. The habituation trial was equivalent to
the baseline trial.
The chimpanzees were already experienced in moving a
cursor to hit a target using a trackball device (Kaneko &
Tomonaga, 2011; Kaneko & Tomonaga, 2012); thus, no
training specic to this study was required. Here, we
briey describe the acquisition process of the trackball
use. The chimpanzees rst performed the aiming action
where the target was huge and the initial location of the
cursor was close to the target. In this condition, random
manipulation of the trackball resulted in a coincident hit.
As their manipulation skills improved, the target became
smaller, and the distance between the target and the cursor became longer. Through trial and error, the chimpanzees gradually learned to use the trackball. The
chimpanzees were also familiar with xing their head for
eye tracking before starting the trial. There was always a
trial initiation procedure before the main part of trial. During this phase, an open circle and cursor were presented,
and the participants were required to move the cursor to
the open circle. They also needed to keep their heads in a
particular area where the eye tracker could stably measure
their gaze at the same time. The appropriateness of head
location was indicated by the color of the open circle. Because a trial was not started until the head was stable
and at the proper location, the chimpanzees learned to
spontaneously move their heads to the predened position. The task was to hit the target with the cursor; thus,
we did not conduct further training specic to the current
experiment. Notably, our chimpanzees were nave to the
spatial perturbation used in this study (only Chloe had
experienced a few spatial distortion trials (see Experiment
3 in Kaneko & Tomonaga, 2011).
The human participants were verbally instructed to
move the cursor to the target by manipulating the trackball. The human participants learned the contingencies of
trackball manipulation and cursor action during habituation trials. They were also instructed to move their heads
to the proper location to start a trial and were told that
accurate head position was indicated by the color of the
open circle during the trial initiation procedure. They
were also informed that their eye movements would be
tracked. After the habituation trial nished, they performed test trials. They were instructed that the main
part of experiment was basically the same as the habituation trials, except with minor changes regarding experimental manipulation. Irrespective, please perform the
aiming task as efciently as possible. The participants
were not informed of the presence or the property of perturbation. This procedure and instruction minimized possible differences between human and chimpanzee
participants in their knowledge about the task structure.
Ad lib questioning of the human participants after the
experiment conrmed that all participants were unaware
of the specic purpose and hypothesis of the present
study.

T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

2.6. Analysis
As a measurement of limb motor adjustment in response to feedback errors, we dened the corrective movement as shown in Fig. 4a. The vector input of the
participants manipulation was divided into vertical and
horizontal components relative to the axis between the
target and the initial cursor location. At the baseline trial,
in which no distortion was imposed, the vertical component of the vector input was unnecessary but was induced
under the perturbation as a response to feedback error
during the test trial. Thus, we dened the total vertical
component as a corrective movement. Fixations were extracted from raw gaze-position data using a custom-made
xation lter based on Stampe (1993). A xation was
scored if the gaze remained stationary within a radius of
1 in visual angle for at least 50 ms. We calculated the
number of gaze shifts to the motor trajectory as an indicator of times when the feedback error triggered participants overt attention to motor corrections. Gaze shift
was dened as xation within a 1 visual angle from the
cursor location. We also recorded the movement time,
which was dened as time between the onset of stimulus
and hitting the target.
Statistical analyses were performed based on the functions of the statistical toolbox (ttest for t-test and anovan
for analysis of variance [ANOVA]) in MATLAB (R2011a).
Post hoc comparisons were conducted with Bonferroni correction. Alpha was set at .05 for all analyses, and the Bonferroni correction adjusted the alpha level as necessary.
Means of multiple trials for each subject were computed
for each behavioral measurement, and those values were
used as dependent variable in the statistical tests.
2.7. Expertise effect
We addressed possible artifactual effects of the difference in expertise between species. There were two types
of asymmetry between the two species in the degree of
expertise. The rst was experience with our experimental
device. The chimpanzee participants had previously performed several experiments using the current device, but
the humans had not. The second was the number of distortion trials the participants experienced. The chimpanzee
participants performed 32 trials per condition, and the humans performed only ve trials. Two controls were used
for these expertise asymmetries. First, we asked two
human participants (one female and one male; age, 27
28 years) to perform more than 1,200 aiming actions over
50 days (Fig. S1) until their movement performance became very stable. Additionally, the same two participants
performed 32 trials per condition, like the chimpanzees.
3. Results
The descriptive results of the participants overall
behavior are shown in Fig. 3. The results show that both
the chimpanzee and the human participants mainly xated
on the goal of the action and occasionally looked at cursor
trajectory during aiming. This trend was consistent across

359

species and from the baseline trial to the test trials involving distortion. The xation probability maps (color maps in
the rst row of Fig. 3) showed that there were roughly
three different color regions, i.e., gray, yellow, and green
areas, suggesting that the participants predominantly
looked at the target location (corresponding to the green
areas), irrespective of distortion type, and that they occasionally looked at the trajectory of the cursor (corresponding to the yellow areas). This trend is also evident in the
second row of Fig. 3, which shows the xation probability
as a function of the target and the start location axis. Target
location was the most frequent target of xation for both
humans and chimpanzees. The characteristics of the corrective movements were also similar between the species
(bottom row in Fig. 3). Corrective movements appeared
gradually as the cursor moved under both the goal-dissociation and goal-congruent conditions. Under the goal-dissociation condition, such corrective movements further
accumulated at the latter part of the trajectory. The polarity of corrective movement was reversed at the mid-point
of the trajectory during the goal-congruent condition. This
is because corrective movement was not required at all under this condition, and the corrective movements performed until the mid-part of the trajectory must be
compensated by movement in the opposite direction.
These patterns in the corrective movements appeared
comparable between species. In the latter analysis, we further analyzed the details of the corrective movement and
how the needs for these motor corrections induced gaze
direction toward the motor trajectory.
Both species effectively corrected their limb movements when distortion was applied (Fig. 5). The results
show that both species increased their corrective movements as distortion increased, irrespective of distortion
type. We performed a two-way ANOVA with distortion
type and distortion amplitude as xed factors and participant as a random factor for each species. The overall statistical results for corrective movement were comparable
between species. The ANOVAs showed signicant interactions
of
distortion
type  distortion
amplitude
(F(3, 12) = 58.7, p < .001, gp2 = .94 for chimpanzees;
F(3, 18) = 33.2, p < .001, gp2 = .85 for humans). Post hoc
comparisons of distortion type for each distortion amplitude with Bonferroni correction revealed that the corrective movements were the same between the distortion
types when the distortion amplitude was small
(t(4) = 1.8, p = .15, r = .67, for chimpanzees at 6;
t(6) = 1.6, p = .17, r = .54, t(6) = 1.6, p = .16, r = .55 for humans at 6 and 12, respectively) but were larger under
the goal-dissociation condition than the goal-congruent
condition when the distortion amplitudes were large
(t(4) = 3.1, p = .04, r = .84, t(4) = 6.1, p = .004, r = .95,
t(4) = 8.1, p = .001, r = .97 for chimpanzees at 12, 28, and
46, respectively; t(6) = 8.4, p = .0002, r = .96; t(6) = 7.2,
p = .0004, r = .95 for humans at 28 and 46, respectively).
The main effects of distortion type (F(1, 12) = 57.8,
p = .002, gp2 = .83 for chimpanzees; F(1, 18) = 68.4,
p < .001, gp2 = .79 for humans) and distortion amplitude
(F(3, 12) = 510.7, p < .001, gp2 = .99 for chimpanzees;
F(3, 18) = 130.6, p < .001, gp2 = .96 for humans) were also
signicant. These results show that both species increased

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

(a) Chimpanzees

Fixation propertion

(b) Humans

Fixation propertion
Fig. 3. Cursor action, hand manipulation, and gaze behavior. The three columns represent the baseline, goal-congruent, and goal-dissociation conditions,
respectively. The rst row shows cursor trajectory and xation probability. The solid line represents cursor trajectory, the left terminus is the start position,
and the right terminus is the target position. The yellowgreen color represents xation probability. The second and third rows represent xation
probability and corrective movements, respectively, as a function of the horizontal distance from the start position on the axis and the target. The dotted
vertical lines represent the start positions (left, 0 mm) and target locations (right, 150 mm). Data are given as the mean across participants. Shaded areas
represent 95% condence intervals. Results for the goal-congruent and goal-dissociation conditions were derived from the maximum degree of distortion,
which shows the most salient distortion effect on the participants behavior. Note that the direction of distortion and the directions from the start position
to the target varied across trials; thus, the results were realigned so that relative geometry was constant across trials. (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this article.)

their corrective movements as distortion increased, and

the amount of the corrective movement was higher under
the goal-dissociation than under the goal-congruent condition, particularly when the distortion amplitude was high.
This is reasonable, because the corrective movements were
necessary to reach the target during goal dissociation but
were completely unnecessary during the goal-congruent
condition. The overall results of motor corrections suggest
that the two species have similar sensitivity to feedback error in terms of limb motor adjustment.
We also measured the gaze-shifting responses from the
goal to the action kinematics during motor correction
(Fig. 6). Gaze-shifting responses increased in both species
as distortion increased; however, these trends differed

between chimpanzees and humans. We performed an ANOVA for each species with distortion type and distortion
amplitude as xed factors and participant as a random factor for each species. The ANOVAs showed a signicant
interaction of distortion type and distortion amplitude in
chimpanzees (F(3, 12) = 15.2, p < .001, gp2 = .79) but not
in humans (F(3, 18) = 0.17, p = .91, gp2 = .028). Post hoc
analyses of the simple main effects were conducted for
each distortion type for the chimpanzee results. The
chimpanzees increased their gaze-shifting response as
distortion increased under the goal-dissociation condition
(F(3, 12) = 10.96, p = .0009, gp2 = .73) but not under the
goal-congruent
condition
(F(3, 12) = 2.26,
p = .13,
gp2 = .36). The main effect of distortion amplitude was

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

Goal dissociation

(b)

Horizontal component
Vector input
Vertical component
=Corrective movement

Goal congruent

Chimpanzees

Humans

600

Corrective movement (mm)

Corrective movement (mm)

(a)

500
400
300
200
100
0
-100

12

28

600
500
400
300
200
100
0
-100

46

Distortion (degree)

12

28

46

Distortion (degree)

Fig. 4. Motor adjustment in response to feedback error. (a) Schematic illustration of the denition of corrective movements. (b) Mean corrective
movements across participants as a function of distortion amplitude. The gure shows values for each test condition subtracted from values for the baseline
condition. Error bars indicate standard errors. Dotted red lines represent the minimal corrective movements required for the goal-dissociation condition.
The minimal correction movement for the goal-congruent condition was zero regardless of distortion amplitude. (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this article.)

(a)

(b)

Goal dissociation

Chimpanzees

Altered action
Default action

2
1.5
1
0.5
0
-0.5

12

28

Humans

2.5

Number of gaze shifts (n)

Gaze shift

Number of gaze shifts (n)

2.5

46

Distortion (degree)

Goal congruent

2
1.5
1
0.5
0
-0.5

12

28

46

Distortion (degree)

Fig. 5. Overt attention to motor kinematics induced by feedback error. (a) Gaze shift was dened as xation within a 1 visual angle from the cursor
location. (b) Mean gaze shift across participants as a function of distortion amplitude. The gure shows the values for each test condition subtracted from
the values for the baseline condition. Error bars indicate standard errors.

signicant for both chimpanzees (F(3, 12) = 7.98, p = .003,

gp2 = .67) and humans (F(3, 18) = 16.6, p < .001, gp2 = .73),
whereas distortion type was not signicant in either chimpanzees (F(1, 12) = 5.64, p = .076, gp2 = .32) or humans
(F(1, 18) = 0.09, p = .77, gp2 = .0058). These results show
that humans increased their gaze-shift responses as distortion increased, regardless of whether the distortion affected only the momentary spatiotemporal parameters or
actually interfered with achieving the nal goal of the action. In contrast, in chimpanzees, overt attention shifted
to motor kinematics only when the distortion actually
interfered with the chimpanzee reaching the action goal.
Additionally, we analyzed the movement time for the
aiming action. If the pattern of overall movement times
were the same as the pattern of gaze shifts, this could create difculty when interpreting species differences in gaze
pattern. However, the results showed that overall patterns
of time spent to hit the target were comparable between

species (Fig. 6), and differed from that of gaze shifts. Both
species increased movement time as distortion amplitude
increased (F(3, 12) = 112.8, p < .001, gp2 = .97 for chimpanzees; F(3, 18) = 72.8, p < .001, gp2 = .92 for humans). The
degree of incentive was larger under the goal-dissociation
than under the goal-congruent condition, which is evident
in the signicant interaction between distortion type and
distortion amplitude (F(3, 12) = 66.2, p < .001, gp2 = .94 for
chimpanzees; F(3, 18) = 7.10, p = .002, gp2 = .54 for humans). A post hoc analysis showed that movement time
was not different between distortion types (t(4) = 1.07,
p = .34, r = .48, t(4) = 1.29, p = .27, r = .54 , t(4) = 3.38,
p = .028, r = .86 for chimpanzees; t(6) = 1.55, p = .17,
r = .53 , t(6) = .29, p = .78, r = .12 , t(6) = .85, p = .43, r = .33
for humans at 6, 12, and 28 respectively), except that
for the largest distortion amplitude. Under the largest distortion, the movement time was longer under the goal-dissociation than under the goal-congruent condition

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

Goal dissociation

Chimpanzees

Humans
2500

Movement time (ms)

Movement time (ms)

2500

1750

1000

250

-500

Goal congruent

12

28

46

1750

1000

250

-500

Distortion (degree)

12

28

46

Distortion (degree)

Fig. 6. Movement time under perturbation. Mean movement time across participants as a function of distortion amplitude. The gure shows the values for
each test condition subtracted from the values for the baseline condition. Error bars indicate standard errors.

(t(4) = 8.96, p < .001, r = .98 for chimpanzees; t(6) = 2.55,

p = .044, r = .72 for humans), although this effect was not
statistically signicant after the Bonferroni correction in
humans. Close inspection of the data revealed that there
was one exceptional participant who showed longer movement time for the goal-congruent condition than that for
the goal-dissociation condition, and removing this participant made the result signicant even after the Bonferroni
correction (t(5) = 4.04, p = .099, r = .88). Notably, this subject was similar to the other human participants in gazeshift pattern. The main effect of distortion type was significant in chimpanzees (F(1, 12) = 93.7, p < .001, gp2 = .89)
but not in humans (F(1, 18) = 3.25, p = .12, gp2 = .15). However, it is problematic to interpret the absence or presence
of a main effect in ANOVA when there is a signicant interaction (Tabachnick & Fidell, 2001). The important point
here is the presence of a signicant main interaction in
both species. An increasing trend was observed as distortion amplitude increased in both species, and its effect
was higher under the goal-dissociation than under the
goal-congruent condition at the largest distortion amplitude. This overall movement time was not the same as
the gaze shift pattern and could not account for the species
differences in gaze pattern.

3.1. Expertise effect

We controlled for the asymmetry of task expertise between species. The results for the human participants
who were experts at trackball manipulation and performed
the same number of test trials as chimpanzees were comparable to those for novice participants (Fig. S2). We conducted a two-way ANOVA on distortion type and
distortion amplitude for each participant, combining the
128 consecutive trials into a single block and treating the
mean value for each block as a dependent variable. The
ANOVAs showed a signicant main effect of distortion
amplitude (F(3, 15) = 34.1, p < .0001, gp2 = .87 for participant T; F(3, ) = 11.3, p = .0004, gp2 = .69 for participant F).
Importantly, no signicant two-way interaction was
observed between distortion type and amplitude

(F(3, 15) = 2.0, p = .16, gp2 = .28 for participant T;

F(3, 15) = 2.1, p = .14, gp2 = .29 for participant F). The main
effect of distortion type was also non-signicant
(F(1, 15) = 0.7, p = .40, gp2 = .05 for participant T;
F(1, 15) = 2.0, p = .18, gp2 = .12 for participant F). These statistical results were qualitatively the same as those for the
human participants who did not have extensive experience
with this experiment. Thus, expertise with the trackball
device or with the perturbation did not explain the species
difference in the allocation of attention during online motor adjustment.

4. Discussion
We examined the difference between chimpanzees and
humans in their reliance on automatic motor control and
investigated when and to what extent they shifted their
attention from the goal to their own motor kinematics.
We found that the two species were similar with respect
to online motor correction in response to feedback error,
whereas the attentional allocation for that motor adjustment differed. Humans were sensitive to both goal and trajectory information about gaze shift, whereas chimpanzees
were mainly sensitive to goal information. Our results suggest that chimpanzees have a more parsimonious cognitive
system in that they relied on an automatic process for online motor adjustment as long as they were able to reach
the planned action goal. The motor system recruited their
deliberate attention only when they could not reach the
goal. In contrast, humans appeared to have more complex
criteria for shifting to deliberate control of their action and
exerted excess attentional monitoring over their own motor kinematics.
One may argue that because the chimpanzees were
interested only in the food reward and thus lacked motivation to move the cursor precisely to hit the target, they did
not pay attention to the detailed motor kinematics required to reach the target. However, this is unlikely, because the chimpanzees showed a certain amount of
corrective movement under the goal-congruent condition.
No corrective movement was necessary to obtain a reward

T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

under this condition, and yet the chimpanzees modied

their limb motor movement. If they were interested only
in getting rewards, the chimpanzees would not have
shown corrective movements under this condition. Thus,
a lack of motivation to control the cursor precisely is unlikely to explain the species difference in the allocation of
attention. Furthermore, we conrmed that the time required to hit the target could not explain the species differences. We also ruled out the possibility of expertise effects.
The overall results of expert human participants were the
same as those for human participants who did not undergo
extensive training. These results eliminate the possibility
that the difference in gaze pattern derived from expertise.
In our previous study, we investigated the relative contributions of kinematic information and goal representations to self-monitoring in chimpanzees and humans
(Kaneko & Tomonaga, 2012). Both species performed aiming actions whereby participants moved a cursor to hit targets. Additionally, a distractor cursor was presented
simultaneously, and participants discriminated a cursor
under their control from a cursor not under their control.
The results showed that chimpanzees found it difcult to
determine whether they were controlling the distractor
when it moved toward the same target as the one the participant intended to hit, even though the distractors kinematics and the participants actions were dissociated.
These results suggest that goal representation, rather than
motor kinematics, is the primary source of information for
self-monitoring in chimpanzees. However, the monitoring
process for the outcome of ones own action occurs hierarchically; that is, sensorimotor processing occurs at a lower
level, and conceptual representation of action goals occurs
at a higher level. It is hard to believe that chimpanzees are
insensitive to their own motor kinematics with respect to
sensorimotor control. In our previous study, we hypothesized that the species difference we observed reected a
difference in the extent to which implicit motor information can reach explicit recognition. However, we were unable to determine to what extent automatic/implicit and
more explicit aspects of monitoring were involved in that
task. The present study directly supports our hypothesis.
We found that both species showed similar sensitivity to
altered visual feedback in terms of limb motor adjustment.
However, we observed a clear difference in how the two
species allocated their overt attention to these motor
adjustments. In chimpanzees, unlike in humans, the feedback error that occurred at the motor kinematics level
was insufcient to trigger overt attention to it. Overall,
our results support the view that chimpanzees and humans differ in the extent to which implicit kinematic motor information reaches explicit recognition (Kaneko &
Tomonaga, 2012).
Our results indicate that the species difference in copying actions is due not only to the difference in the recognition/encoding of others actions but also to the difference
in the execution of ones own actions. Many studies have
revealed that great apes tend to copy the goal, but not
the kinematic aspects, of others actions, whereas human
show a bias toward copying the kinematics of actions (Call,
2001; Call et al., 2005; Myowa-Yamakoshi & Matsuzawa,
1999; Myowa-Yamakoshi & Matsuzawa, 2000; Nagell

363

et al., 1993; Tennie et al., 2006; Tomasello et al., 1987).

Our results suggest that chimpanzees control of motor
kinematics is highly dependent on the automatic aspects
of motor control, making it difcult for chimpanzees to
imitate a motor action in the absence of an explicit action
goal. Thus, the extent to which species differ in the encoding/recognition of others actions remains unclear because
most studies have not differentiated between the observational and executional aspects of copying actions and have
focused exclusively on the recognition aspect. On the one
hand, there is growing evidence in support of the directmatching hypothesis, which holds that the same neural
circuits are involved in perceiving and understanding others actions and in executing ones own actions (Rizzolatti
& Craighero, 2004; Rizzolatti, Fogassi, & Gallese, 2001).
For example, Kanakogi and Itakura (2011) showed a developmental correspondence between the ability to recognize
the action of others and the ability to execute the same action in early infancy. Following this theory, it can be argued
that the ability to deliberately control ones own motor
kinematics and the ability to both explicitly and implicitly
encode the detailed motor kinematics of others actions
may be related, from an evolutionary perspective.
A growing number of studies in recent years have identied neural differences between humans and other primates, including chimpanzees, which seems consistent with
our view. Hecht et al. (2012) discussed connectivity differences in the mirror system among chimpanzees, macaques, and humans. They found that only humans possess
a dense connection between the superior parietal cortex
and temporal cortex on diffusion tensor imaging, which
may support spatial attention to the kinematics of motor
action. Additionally, functional imaging studies suggest
that the human brain may process actions at a higher level
of kinematic/motion detail. Non-human primates have
more frontal activation than do humans during the observation/execution of grasping movements (Hecht et al.,
2013; Nelissen, Luppino, Vanduffel, Rizzolatti, & Orban,
2005), suggesting that non-human primates represent
incoming visual information using higher-order cognitive
operations (Denys et al., 2004) involving coding the abstract goal rather than the detailed motor kinematics. Furthermore, humans show parietal cortex responses to
observed actions that are lacking in macaques, suggesting
that humans process observed actions at a higher level of
movement detail (Peeters et al., 2009; Vanduffel et al.,
2002).
Our present ndings raise the question of why humans
evolved the ability to monitor redundant motor kinematics
with deliberate attention to detail. The execution and
adjustment of motor kinematics entails implicit processing
and is generally beyond ones deliberate intentional control (Mechsner et al., 2001; Norman & Shallice, 1986;
Pisella et al., 2000). Automatic control of a motor action
enables us to perform motor movement smoothly and
quickly and also allows us to save cognitive resources such
as attention (Liu, Chua, & Enns, 2008). Furthermore,
excessive attention to ones own motor kinematics interferes with performance of the motor repertoire of familiar
routines (Beilock, Carr, MacMahon, & Starkes, 2002; Gray,
2004). Primate species evolved distinct neural architecture

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T. Kaneko, M. Tomonaga / Cognition 131 (2014) 355366

for planning abstract action goals and converting them into

actual motor actions (Hoshi & Tanji, 2007; Tanji & Hoshi,
2008) and for online motor control of the actual motor execution (Desmurget & Grafton, 2000). Thus, it is an optimal
and adaptive strategy not to pay attention to the execution
and control of motor kinematics, as the usual motor routines are sufcient to achieve the goal of an ongoing action.
Therefore, it is rather peculiar that human participants focused overt attention on motor kinematics when feedback
errors occurred in the spatiotemporal parameters of actions that could have been managed automatically.
The advantage of extensive attention to motor kinematics may be that humans can thereby develop a novel motor
repertoire, particularly via imitation. If the imitator readily
appreciates the goal of others actions, then emulation is a
sufcient strategy to reproduce others motor actions.
However, if the goal of others actions is obscure, then
the imitator needs to pay attention to the spatiotemporal
characteristics of others actions. As the direct-matching
hypothesis states (Kanakogi & Itakura, 2011; Rizzolatti &
Craighero, 2004; Rizzolatti et al., 2001), the recognition of
others action goals seems to partially depend on the neural mechanism for the execution of ones own actions,
which, in turn, means that to understand the goals underlying others actions, one should already have acquired the
skill to perform the same goal-directed action. Therefore,
imitation of detailed motor kinematics, rather than simple
reproduction of others goal actions, may be necessary to
truly expand the novel repertoire of goal-directed behaviors. In fact, human infants copy others actions even when
they have an alternative, more efcient behavioral strategy
to achieve the same goal (Gergely, Bekkering, & Kiraly,
2002; Jones, 2009; Nielsen, 2006). Human infants have a
stronger bias for imitation than for mere reproduction of
a goal. This tendency has been proposed to be an adaptive
strategy for cultural transmission of complex action repertoires. Furthermore, the advantage of extensive attention
to motor kinematics is not limited to imitation but in a
more general context. Theoretical and experimental studies have indicated that humans pay more attention to action kinematics when they are learning novel motor
actions (Curran & Keele, 1993; Nissen & Bullemer, 1987;
Norman & Shallice, 1986; Sailer et al., 2005; Taylor &
Thoroughman, 2007; Willingham, 1998). Thus, extensive
attentional monitoring of ones own kinematics could be
advantageous to the acquisition of a variety of motor
repertoires during the course of ontogenic development.
Our results showed chimpanzees were insensitive to
motor kinematics at the explicit level. However, our results
do not necessarily mean that they never monitor kinematics explicitly. It may be better to consider the species difference as a matter of extent. Horner and Whiten (2005)
showed that chimpanzees have the ability to copy motor
kinematics during social learning in a particular situation
when goal emulation is not available and when copying a
motor action is the only way to solve the problem. However, chimpanzees immediately switch to copying only
goals once the situation allows. These authors suggested
that chimpanzees share the ability to attend to and copy
action-specic methods with humans to some extent, but

that chimpanzees have a bias toward goal-copying,

whereas humans have a bias toward method-copying
(which has been called over-imitation). Thus, it seems
possible that chimpanzees may be capable of deliberately
monitoring their own kinematics but that they may exercise this ability only under very limited circumstances,
whereas humans may have a relatively stronger bias toward kinematic monitoring. The opposite is also true,
namely that not all kinematic errors reach explicit recognition in humans. Metcalfe and Greene (2007) asked human
participants to perform an aiming action where a hidden
force helped participants achieve their goal (compensating
for their errors). Participants felt better control when task
performance was experimentally manipulated so that it
appeared they achieved the task goal more efciently than
was actually the case. This result suggests that the detection of errors at the kinematic level may be masked by
the monitoring process at a more abstract level. It requires
further research to understand how error detection at an
implicit level reaches explicit recognition and to understand how the two levels of processing interact.
As a nal note, we found that the species differed in
their reliance on automatic motor control and the attentional monitoring of their own motor kinematics. It is
widely accepted that sophisticated motor repertoires have
evolved in humans (Courtine et al., 2007; Heffner &
Masterton, 1975; Heffner & Masterton, 1983; Nakajima,
Maier, Kirkwood, & Lemon, 2000). Our results suggest that
the deliberate attention to ones own motor kinematics
may have also evolved in the human lineage in response
to the demand for expanding the variety of ones novel
motor repertoires during the course of ontogenic
development.
Acknowledgments
We thank Drs. Tomoko Imura and Christoph D. Dahl for
useful discussion. We also acknowledge the continuous
support of Dr. Tetsuro Matsuzawa. This project was nancially supported by JSPS-MEXT Grants-in-Aid for Scientic
Research (212668, 16002001, 19300091, 20002001 and
23220006) and the Global COE Program (A06, D07).
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.cognition.2014.02.002.
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