Behavioural Brain Research 172 (2006) 219–232
Research report
Visual search for moving and stationary items in chimpanzees
(Pan troglodytes) and humans (Homo sapiens)
Toyomi Matsuno ∗,1 , Masaki Tomonaga
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
Received 28 October 2005; received in revised form 2 May 2006; accepted 4 May 2006
Available online 21 June 2006
Abstract
Four visual search experiments were conducted using human and chimpanzee subjects to investigate attentional processing of movement, and
perceptual organization based on movement of items. In the first experiment, subjects performed visual searches for a moving target among
stationary items, and for a stationary target among moving items. Subjects of both species displayed an advantage in detecting the moving item
compared to the stationary one, suggesting the priority of movement in the attentional processing. A second experiment assessed the effect of the
coherent movement of items in the search for a stationary target. Facilitative effects of motion coherence were observed only in the performance
of human subjects. In the third and fourth experiments, the effect of coherent movement of the reference frame on the search for moving and
stationary targets was tested. Related target movements significantly influenced the search performance of both species. The results of the second,
third, and fourth experiments suggest that perceptual organization based on coherent movements is partially shared by chimpanzees and humans,
and is more highly developed in humans.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Chimpanzee; Perceptual organization; Search asymmetry; Coherent movement; Reference frame
1. Introduction
Detecting a moving item is highly important for animals
living in dynamically changing visual environments, and this
explains why our perceptual mechanisms are so well-developed
for that purpose. The visual search paradigm has frequently been
used to investigate visual attention mechanisms for processing
motion information [8,16,20,31,32]. For example, search asymmetry for motion was found in studies that tested human visual
search performance in two display conditions, one of which
consisted of a moving dot and stationary dots and the other
symmetrically designed with a stationary dot and moving dots
[37,54]. Results indicated that detecting a stationary item among
moving items is more difficult than detecting a moving item
among stationary items. Royden and colleagues explained these
findings according to feature integration theory [49], such that
“motion” is a basic feature in our visual system and “stasis” is
its absence.
∗
1
Corresponding author. Tel.: +81 568 63 0567; fax: +81 568 63 0550.
E-mail address: [email protected] (T. Matsuno).
JSPS Research Fellow.
0166-4328/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2006.05.004
When we think about detecting a target in a dynamic visual
field, perceptual organization is also an important consideration
because an item’s motion is often perceived in the global context
of the movement of other items. For example, our visual system
is sensitive to movement coherence [56]; coherently moving
items are more easily grouped [24]. Also, as is apparent in phenomena such as induced or relative motion, an object’s motion is
often perceived in relationship to the movements of other items.
This perceptual organization of moving items and its relation
to visual search performance has been investigated by several
researchers [9,23,55]. In studies using human subjects, motion
coherence of the search items was varied and effects on search
performance tested. These studies found that the effect of coherent motion was to perceptually group the items as an organized
surface, probably processed in the “preattentive” stage of human
visual perception [48], and that such perceptual grouping influenced the search for a moving target. Results of these studies
indicated a strong tendency for perceptual grouping or organizing of moving items in ways that affected later attentional
processing of the items.
In the field of comparative cognition, studies on visual
perception in non-human animals have been important in under-
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standing how non-human animals perceive their world, and to
manifest the evolutionary foundation of human visual processing [2,46]. Several learning experiments have shown similarities
between humans and chimpanzees, our closest evolutionary
relatives, in visual perception and attentional processing. For
example, chimpanzees showed comparable performance to
humans in characteristics of early vision, such as visual acuity
[30] and color and brightness perception [14]. In a series of visual
search experiments, Tomonaga [46] examined features such as
orientation, form, texture pattern, and shape-from-shading cues,
and demonstrated “pop out” and search asymmetry phenomena
in chimpanzees, similar to those in humans. Perception of
movement in visual search, however, has been less frequently
investigated in non-human animals, although information about
detection and attentional processing of moving items would
provide highly important ecological and evolutionary validity.
There has also been little investigation into how non-human
animals organize their visual perception of objects. Whereas
it is natural for humans to perceive the relationship between
items in a visual field [24], previous reports suggest that this
is not always true for non-primate animals [5,25,52], or even
non-human primates, such as chimpanzees [11,13].
The purpose of this study was two-fold. First, we sought
to reveal whether chimpanzees showed search asymmetry for
moving and stationary targets. The question was whether, like
humans, chimpanzees more rapidly detect a moving item than a
stationary item. In Experiment 1, we used a visual search task to
compare the performance of humans and chimpanzees in detecting a moving target among stationary distractors, and a stationary
target among moving distractors. This allowed us to measure the
most basic visual processing tendencies of chimpanzees.
Second, we examined the organization of visually perceived
discrete moving objects. Previous studies of perceptual organization in chimpanzees used stationary stimuli [12]; we attempted
to test the dynamic aspect of perceptual organization in nonhuman primates. In Experiment 2, a stationary item among
moving distractors was presented to the subjects under two
search conditions in which the uniformity of the movement of
the distractors was varied.
To further investigate perceptual organization, search performance for moving and stationary targets as in Experiment 1 was
evaluated in Experiment 3 (3a and 3b), with the addition of a
moving reference frame. These two experiments examined the
perceptual organization of discrete items in the context of related
movement.
2. General methods
2.1. Subjects
Five chimpanzees: Ai (27 years old, female), Akira (28 years old, male),
Mari (28 years old, female), Pendesa (27 years old, female), and Ayumu (3.5
years old, male), participated in the experiments. Ai and Akira participated in
Experiments 1, 3a, and 2 in that order. Mari, Pendesa, and Ayumu participated
in Experiment 3b.
The subjects were experienced in performing various perceptual-cognitive
tasks. At the time of the present study, Ai was experienced in matching-tosample-tasks, such as symbolic and identity matching tasks [1,27,29], and had
relatively little experience in visual search tasks [43,44]. Akira had been highly
trained in visual search tasks [42,45,47]. However, neither of these subjects had
prior experience of the task used in the present study. Mari and Pendesa also
had experience in performing discrimination tasks [1,27,41], and had learned
the visual search for a moving target task [28] in advance of this study. Ayumu
had little experience in computer-controlled tasks, but he had also learned the
visual search task that used a moving target among stationary discs [28].
The subjects lived with 10 other chimpanzees in an environmentally enriched
outdoor compound and attached indoor residences [33]. They were not deprived
of food at any time during the study. Care and use of the chimpanzees adhered to
The Guide for the Care and Use of Laboratory Primates of the Primate Research
Institute, Kyoto University, Japan.
In addition to the chimpanzees, human volunteers participated in the experiments. They were not informed about the purpose of the experiments. All were
right-handed and reported normal or corrected-to-normal visual acuity.
2.2. Apparatus
Chimpanzees were tested in an experimental booth (approximately
1.8 m × 1.8 m × 2.0 m) with acrylic panels as walls on all four sides. Stimuli
were generated on a Pentium-based computer and displayed on 21-in and 22in CRT monitors (Totoku CV-213PJ for Ayumu and Mitsubishi TSD-221S for
the other subjects) equipped with capacitive and surface acoustic wave touch
screens. This monitor system served to present the stimuli, and was also the
input device for subject responses with accurate information for touch locations.
Monitor resolution was 1024 × 768 pixels with 8-bit color mode. The refresh
rate was 75 Hz and the display was synchronized with the vertical retrace of
the monitor. The positions of the moving stimuli were updated on every screen
retrace to give the impression of smooth motion. Subjects observed the monitor
at a viewing distance of about 40 cm without head restraint. The viewing distance
was roughly restricted by an acrylic panel, which was attached between the monitor and subjects to prevent the destruction of the monitor by the chimpanzees.
Stimulus luminance was measured using a colorimeter (Topcon, BM-7). A universal feeder (Biomedica, BUF-310) delivered small pieces of a food reward
(apples or raisins) into a food tray below the monitor.
Human subjects were tested with the identical apparatus in the experimental
booth. The only exception was that they were not rewarded with pieces of food.
They were required to observe the monitor from a distance of about 40 cm and
to respond with a finger touch as did chimpanzees.
3. Experiment 1: asymmetry in visual search for
moving and stationary targets
Experiment 1 tested visual search for moving and stationary
items. Targets and distractors were designed symmetrically in
two search display conditions (Fig. 1). In one condition, subjects
searched for a moving target among stationary items, and in the
other, they were required to detect a stationary target among
moving distractors.
3.1. Methods
3.1.1. Subjects
Two chimpanzees (Ai and Akira), and five undergraduate
students (three males and two females) ranging in age from 18
to 22 years (mean = 19.2 years), participated in Experiment 1.
3.1.2. Stimuli
The total screen area subtended 392 mm × 292 mm
(52.2◦ × 40.1◦ of visual angle at a viewing distance of 40 cm),
and the maximum display area (with 12-item display) was
230 mm × 172 mm (32.1◦ × 24.3◦ ), excluding the lower part
of the screen where a warning stimulus, which showed the
T. Matsuno, M. Tomonaga / Behavioural Brain Research 172 (2006) 219–232
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motion simultaneously after every migration of 12 mm (1.8◦ );
thus, the stimuli moved in phase. Each human subject confirmed that the moving items produced the impression of a
smooth continuous motion, and that they did not leave a persistently visible trail. Each item never passed beyond the cell,
and the minimum separation from an adjacent item was maintained at more than 28 mm (center-to-center). The laboratory
was dimly illuminated to prevent reflections on the computer
screen.
Fig. 1. Examples of search displays used in Experiment 1.
initiation of each trial, and a sample stimulus were presented.
Displays were comprised of 1, 4, 8, or 12 items (display-size
variable) including the target, and were presented continuously
until terminated by the subject’s response.
The stimuli were black discs (approximately 15 cd/m2 )
subtending about 12 mm × 12 mm (1.7◦ × 1.7◦ ) against a gray
background (approximately 30 cd/m2 ). They were randomly
distributed on an imaginary 4 × 3 square matrix with cell size
of 57 × 57 mm (8.2◦ × 8.2◦ ), subject to the constraint that each
cell contained no more than one item. The initial position of an
item in a cell was also randomly set within a 38 mm × 38 mm
(5.5◦ × 5.5◦ ) area centered in the cell, so that items never
formed orderly vertical or horizontal lines.
In the moving target condition, a display consisted of a
moving disc (target) and stationary discs. In the stationary
target condition, a display consisted of a stationary disc (target) and moving discs. The stimuli oscillated horizontally at
a velocity of 57 mm/s (8.2◦ /s). All moving items in a display
moved at the same velocity and reversed their direction of
3.1.3. Procedure
A delayed matching-to-sample (DMTS) task with multiple
alternatives [43] was used.1 Each trial was initiated by the simultaneous presentation of a warning stimulus (an empty black
square subtending 30 mm × 30 mm) located at the bottom right
of the screen, and a sample stimulus, which had the same movement state as the target, at the bottom center of the screen. The
warning and sample stimuli disappeared after they were sequentially touched. After 500 ms from when the sample was touched,
the search display was presented. The locations of the target and
distractors were randomly selected from the 12 cells in each
trial. A touch response to an item was defined as a detected
touch within an invisible rectangle (28 mm × 28 mm) around
the center of the item. The area moved with the movement of
the item. When subjects correctly touched the target, a chime
sounded, and for the chimpanzees, a food reward was delivered.
The choice of incorrect items was followed by a buzzer sound
and a 3-s timeout. The time interval between the presentation of
the search display and the touch of the item was recorded as the
response time.
Prior to the test sessions, the chimpanzees were trained on
the search task for moving and stationary targets in the display size 6 condition. A session consisted of 64 trials (32 trials
for each target condition). The criterion for learning was set
as >90% accuracy in three consecutive sessions for each target
condition. When performance reached the criterion in a target
condition, intensive training in the other condition was continued until reaching its criterion.
During the test phase, a session consisted of 104 trials in
which the display size varied among 1, 4, 8, and 12 items, with
26 trials for each display size. Display size 1 was used to collect
baseline chronometric information reflecting the processes of
stimulus detection, movement preparation, and movement execution. This also served maintain a high reward rate and sustain
the motivation of chimpanzees during test sessions. The first
eight trials (two trials for each display size) of a test session
1 In the initial phase of pilot training, one of the chimpanzee subjects, Ai, was
trained in an odd-item search paradigm [32], in which she was required to detect
the single moving or stationary target among five distractors without the sample
presented in advance of the search display. After 10 sessions of 32 trials for
each display condition of the training, Ai did not show any evidence of learning
and her motivation decreased to stop the task because of low reward rate. We
then introduced the delayed matching-to-sample (DMTS) task, with which the
subject had been familiar thorough long-term continuous training. The other
chimpanzee subject, Akira, started his training in the DMTS task with display
size 6, and succeeded in learning it.
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were treated as practice trials and were excluded from subsequent analyses. The other 24 trials of each display size were
intermixed randomly during the session. The position of the target was counterbalanced across the 24 trials. In a session, the
display condition was fixed, and the two conditions were alternately presented. Two consecutive sessions (one session for each
display condition) were counted as a test block.
Each chimpanzee subject participated in eight test blocks.
Accuracy and response time data from the last six blocks were
used for analyses. Ai began her test sessions with the condition
of a moving target, and Akira began with a stationary target.
Each human participant participated in a single test block (one
session for each display condition) with two practice sessions of
10 trials (one session for each display condition; display size 6).
A practice session was given to the subject just prior to the test
session of the display condition. Human subjects were verbally
instructed to correctly and quickly detect the target. Two of the
five subjects began their test with a moving target, and the other
three began with a stationary target.
The number of correct responses and median response times
for correct trials were collected for each display size in a session. During test sessions, averaged accuracy and mean median
(MMdn) response time of display sizes 4–12 were analyzed
using two-way analysis of variance (ANOVA; display condition × display size); repeated measures were blocks for chimpanzees and subjects for humans. The search slope of the
response times in the test sessions was also analyzed using twotailed t-tests.
cess was biased to favor stationary items. This may be partly
because she had previously worked only on tasks with stationary stimuli (such as matching tasks using Arabic numerals with
stationary dots, color patches, and geometric figures), and this
was the first time she was to select moving items as correct
answers.
3.2.2. Test phase: response time
The response time data for display sizes 4–12 in the test
phase are presented in Fig. 2. Searching for a stationary item
3.2. Results
3.2.1. Training phase
In the display size 6 training phase, Akira took longer to
meet the criterion in a stationary target condition than a moving
target condition (8 sessions for a moving target condition; 23
sessions for a stationary target condition). He performed much
more accurately in a moving target condition (mean percentage
correct = 77.3, S.E. = 8.05) than in a stationary target condition
(mean percentage correct = 9.38, S.E. = 2.83) in the first eight
sessions, t(7) = 6.34, p < 0.01. This suggests that moving targets
were more salient among stationary distractors than stationary
targets among moving distractors for Akira. Correct response
times were not significantly different between conditions (a
moving target, MMdn = 1167 ms, S.E. = 97; a stationary target,
MMdn = 1649 ms, S.E. = 281), partly because of large variance
caused by very few correct trials in a stationary target condition.
In contrast, Ai reached the learning criterion more rapidly
in a stationary target condition (29 sessions for a moving
target condition; 21 sessions for a stationary target condition). However, Ai was slower to correctly detect a stationary target (MMdn = 1181 ms, S.E. = 22) than a moving target
(MMdn = 939 ms, S.E. = 27) in the first 21 sessions, t(20) = 6.82,
p < 0.01, despite no significant difference in accuracy between
the two conditions (stationary target, mean percentage correct = 82.1, S.E. = 2.9; moving target, mean percentage correct = 78.4, S.E. = 1.9), t(20) = 1.37. These results suggest that
detecting a moving target was easier, but that Ai’s selection pro-
Fig. 2. Mean median response times in Experiment 1. Each graph presents the
response time × display size functions for the two display conditions. Filled
squares represent the moving target conditions; open circles represent the stationary target conditions; error bars are ±1 S.E.
T. Matsuno, M. Tomonaga / Behavioural Brain Research 172 (2006) 219–232
among moving items was markedly more difficult than finding a
moving target among stationary items for both chimpanzees and
humans. There was, however, a remarkable discrepancy between
chimpanzees and humans. Response time differences between
display conditions increased as a function of the display size
for chimpanzees, but stayed relatively constant for human performance. The main effect of display condition was significant
both in chimpanzees, F(1, 5) = 48.88 for Ai and 88.1 for Akira,
p < 0.01, and humans, F(1, 4) = 193.42, p < 0.01. The main effect
of display size was significant for Ai, F(2, 10) = 6.20, p < 0.01,
and humans, F(2, 8) = 4.90, p < 0.05, but not for Akira, F(2,
10) = 0.43. There was a significant interaction of display condition and display size for the chimpanzees, F(2, 10) = 5.86 for Ai
and 10.90 for Akira, p < 0.01, but not for the human subjects, F(2,
8) = 3.10, indicating that the simple main effect of display condition was significantly modified by display size for chimpanzees.
Response times were not significantly different between display
conditions in display size 4, F(1, 15) = 3.48 for Ai and 1.45 for
Akira, but were significantly different in display sizes 8 and 12,
F(1, 15) = 14.16 and 44.11 for Ai; F(1, 15) = 34.92 and 61.86
for Akira, p < 0.01.
Search slopes in the detection of a stationary target (mean
search rate = 70.11 ms/item, S.E. = 22.07, for Ai, 42.80 ms/item,
17.01, for Akira) were higher than those in the detection of a
moving target (mean search rate = −0.85 ms/item, S.E. = 2.47
for Ai, −72.09 ms/item, 24.70 for Akira) in chimpanzees,
t(5) = 3.03 for Ai, p < 0.05, and 4.14 for Akira, p < 0.01, but they
were not significantly different between conditions in humans
(stationary target, mean search rate = 7.78 ms/item, S.E. = 3.24;
moving target, 0.64 ms/item, 0.84), t(4) = 1.91, p > 0.10.
3.2.3. Test phase: accuracy
Chimpanzees performed much more accurately than due to
chance in the test sessions, and the mean percentage correct
showed similar patterns to response time (Table 1). For Ai,
there were no significant main effects of display condition,
F(1, 5) = 0.13, or display size, F(2, 10) = 1.03, but the interaction was significant, F(2, 10) = 7.20, p < 0.05. The simple main
effects analysis revealed that performance in a stationary target
condition was significantly more accurate than performance in
a moving target condition for display size 4, F(1, 15) = 5.84,
p < 0.05, and that the tendency was reversed for display size
Table 1
Mean percentage of correct responses with the standard error for each subject
and each condition in Experiment 1
Display size
Ai
% Correct
Akira
S.E.
% Correct
S.E.
Motion
4
8
12
78.5
84.0
95.8
4.5
5.0
2.2
86.1
91.0
88.9
2.3
1.3
3.5
Stasis
4
8
12
96.5
92.4
73.6
1.7
1.3
10.2
72.2
89.6
87.5
3.7
3.2
2.8
223
12, F(1, 15) = 8.81, p < 0.01. For Akira, the main effect of display condition was significant, F(1, 5) = 7.50, p < 0.05, reflecting
more accurate performance in a moving target condition than in
a stationary target condition. The main effect of display size was
also significant, F(2, 10) = 16.32, p < 0.01, indicating less accurate performance in display size 4 than in display sizes 8 and
12 (post-hoc comparisons using Ryan’s method, p < 0.05). The
interaction was not significant, F(2, 10) = 2.78.
Human subjects exhibited almost perfect performance (mean
percentage correct = 99.3), so their accuracy was not analyzed
for statistical significance because of possible ceiling effects.
3.3. Discussion
Both chimpanzees and humans demonstrated asymmetrical
search performance; it was more difficult to find a stationary item
among moving distractors than a moving target among stationary stimuli. These results are consistent with previous studies
on human search performance that showed a clear advantage of
detecting a moving target [37,54], and imply that chimpanzees
and humans share the same mechanism of visual attention that
processes motion. These results are compatible with evolutionary theories because the ability to rapidly shift visual attention
to moving items may have a major survival value for visually
dependent species like chimpanzees and humans.
Search asymmetry itself was observed both in chimpanzees
and humans, but the degree of asymmetry was much greater in
chimpanzees. In humans, the rates to detect moving and stationary targets were almost the same, with little or no increment in
response times as a function of display size. In fact, the search
slopes showed an efficient level (<10 ms/item) [57] under both
conditions in humans. The search for a moving target was performed as efficiently by the chimpanzees as the humans, and
there was no deterioration in performance with an increment
in the number of distractors. Performance was facilitated with
larger display sizes, suggesting that a moving target “popped
out” among dense and uniform background items in the perceptual analysis of chimpanzees, as it did for humans [2,42].
The search for a stationary item, however, was not as efficient
in chimpanzees, and the difference in performance among display conditions was much greater with larger display sizes. This
difference in the performance of chimpanzees and humans may
reflect species differences in visual processing.
Even in humans, the search for a stationary target is not
always performed efficiently. Royden et al. [37] investigated
visual search performance for a stationary item under three
motion conditions. In the Uniform motion condition, all display items moved in phase as in the present experiment; in
the other two conditions, the Random and Brownian motion
conditions, the items moved out of phase to randomly selected
directions. They found that response times in the Uniform condition were only slightly or not at all affected by display size,
which is consistent with the results of the present study, whereas
response times in the other two conditions increased as a function of increased display size, consistent with the results for our
chimpanzee subjects. They suggested that perceptually grouping uniformly moving distractors, or an induced motion effect
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caused by their uniformity, would make it easier to detect a stationary target. The discrepancy in search performance between
the two species we tested could thus be explained by differences
in perceiving uniformly moving distractors. Humans could take
advantage of distractor uniformity to efficiently detect a target,
but this would be more difficult for chimpanzees.
The effect of uniform or coherent motion on visual search
performance has been investigated in humans [9,23,55], but no
such studies have been conducted in chimpanzees. Therefore,
we addressed this issue in Experiment 2.
stationary target search prior to Experiment 3a, in which the
search performances for moving and stationary targets were
compared as in Experiment 1.
Each human subject performed one test block (one session for
each display condition) with two practice sessions of 10 trials.
The order of the tested conditions was counterbalanced between
subjects.
Accuracy and response time were analyzed using two-way
ANOVA (display condition × display size) as in Experiment 1.
Search slopes were also analyzed using one-tailed t-tests.
4. Experiment 2: visual search for a stationary target
among uniformly or randomly moving distractors
4.2. Results
We conducted a search for a stationary target among moving
distractors task under two conditions. One condition was the
same as in Experiment 1, where all distractors moved in phase.
In the other condition, the distractors moved out of phase. If the
uniform motion of the distractors facilitates search performance,
visual search in the former condition, i.e., when the distractors
moved in phase, would be easier.
4.1. Methods
4.1.1. Subjects
The same chimpanzees from Experiment 1 participated in
Experiment 2. Newly recruited four graduate and undergraduate
student subjects (one male and three females) ranging in age
from 18 to 24 years (mean = 20.8 years) also participated in the
experiment.
4.1.2. Stimuli
The stimuli used in Experiment 2 were the same as in Experiment 1 except as reported here. In the Uniform condition, the
distractors oscillated horizontally in phase. Movements of the
stimuli were the same as those in Experiment 1 except for the
oscillation amplitude (18 mm, 2.6◦ ) and display size (1, 3, 7, and
11). The oscillation amplitude was enlarged in order to allow
more variations of oscillation phase in Random condition and
to make the difference between two conditions more apparent.
In the Random condition, half of the distractors moved horizontally and the others moved vertically. In addition, the oscillation
phases of all distractors varied randomly, so that the movement
of distractors appeared disorganized. The amplitudes of the vertical and horizontal oscillations were the same as those of the
horizontal oscillations in the Uniform condition.
4.1.3. Procedure
A test session consisted of 104 trials (26 trials for each display
size), in which the display condition (Uniform or Random) was
fixed. Each chimpanzee participated in eight test blocks (eight
sessions for each display condition), and the last six blocks were
used for analyses. Ai started her test sessions with the Random
condition and Akira started his with the Uniform condition.
The test sessions were presented to the chimpanzees without
any additional training or practice. Experiment 2 was conducted
after Experiment 3a to avoid the additional sessions biased for a
4.2.1. Response time
Both chimpanzees showed monotonically increasing
response time as a function of display size in both the Uniform
and Random conditions (Fig. 3). In the performance of both
chimpanzees, only the main effect of display size was significant, F(2, 10) = 57.31 for Ai and 10.77 for Akira, p < 0.01,
suggesting that searching for a stationary target was inefficient
under both display conditions for chimpanzees. In contrast,
human response times in the Uniform condition were relatively
constant compared to those in the Random condition. Two-way
ANOVA revealed significant main effects for display condition,
F(1, 3) = 12.86, p < 0.05, display size, F(2, 6) = 10.41, p < 0.05,
and their interaction, F(2, 6) = 6.03, p < 0.05. Post-hoc analyses
revealed simple main effects of the display condition for display
sizes 7 and 11, F(1, 9) = 12.37 and 16.38, respectively, p < 0.01,
but not for display size 3, F(1, 9) = 0.04.
Analyses of search slopes also revealed a discrepancy between chimpanzees and humans. Humans showed
steeper search slopes in the Random condition (mean search
rate = 12.22 ms/item, S.E. = 1.17) than in the Uniform condition (mean search rate = 4.20 ms/item, S.E. = 2.59), t(3) = 2.78,
p < 0.05, as reported in a previous study [37]. In contrast, search
slopes of chimpanzees were not significantly different between
the Uniform condition (mean search rate = 40.36 ms/item,
S.E. = 3.42, for Ai and 51.07 ms/item, 16.21, for Akira)
and the Random condition (mean search rate = 55.59 ms/item,
S.E. = 9.85, for Ai and 48.56 ms/item, 12.68, for Akira),
t(5) = 1.64 for Ai and 0.26 for Akira, p > 0.10.
4.2.2. Accuracy
Chimpanzees maintained a very high level of performance
throughout the sessions (Table 2), partly because the target was
fixed to a stationary item during testing. Only the main effect
of the display size in Akira’s performance was significant, F(2,
10) = 7.60, p < 0.01, consistent with the results for response time.
Human subjects exhibited almost perfect performance
(M = 98.8). The data were not analyzed further.
4.3. Discussion
The results of Experiment 2 supported the hypothesis that
the different tendencies in human and chimpanzee performance
revealed in Experiment 1 were partly due to the uniformity of
the moving distractors. The results of human performance were
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225
Table 2
Mean percentage of correct responses with the standard error for each subject
and each condition in Experiment 2
Display size
Fig. 3. Mean median response times in Experiment 2. Each graph presents the
response time × display size functions for the two display conditions. Open
circles represent the conditions of uniformly moving distractors; filled lozenges
represent the conditions of randomly moving distractors; error bars are ±1 S.E.
consistent with the study by Royden et al. [37], showing shorter
response times and more efficient search rates in the Uniform
than in the Random condition. This advantage for the Uniform
condition suggests that human subjects perceptually organize a
group of distractors depending on the uniformity of their motion.
In contrast, the chimpanzees did not demonstrate such an advantage; performances in both conditions were the same, with a clear
increment in response time as a function of display size, comparable to human performance in the Random condition. This
suggests that chimpanzees did not have the significant advantage of perceptual grouping by uniform motion, nor could they
Ai
Akira
% Correct
S.E.
% Correct
S.E.
Uniform
3
7
11
98.6
97.2
93.8
1.4
1.4
3.8
93.1
97.9
92.4
1.8
1.4
2.0
Random
3
7
11
94.4
97.2
95.1
4.8
1.8
2.7
91.7
97.9
93.8
1.1
1.4
0.9
globally process motion coherence in this task, although the relatively large drop seen in response time for the Uniform condition
for Ai at display size 11 implied a similar but weaker tendency.
Previous studies using stationary stimuli also report restricted
perceptual organization in chimpanzees compared to humans.
Studies by Fagot and Tomonaga [13] on the perception of the
Kanizsa illusory figure found that chimpanzees were more sensitive than humans to the separation between four Pacman-shaped
elements within a display, and that the illusory effect disappeared
only for the chimpanzees when the distance between the visual
elements was enlarged. Fagot and Tomonaga [12] also studied global and local processing in chimpanzees using geometric
figures comprised of smaller geometric elements and found that
when the density of the elements was sparse, chimpanzee performance shifted to local precedence, while humans consistently
exhibited global precedence.
Chimpanzees can, however, perceptually organize visual
objects in a display; when the separation between elements was
not so large, chimpanzees could perceptually organize the visual
elements and perceive the illusory square [13]. This was also the
case for the advantage of global processing [17,18]. Given these
results, it is possible that chimpanzees differ from humans only
in the degree with which they can perceptually organize visual
elements.
We reasoned that, if the visual stimuli are easier to organize
perceptually, the chimpanzees should take advantage of the perceptual grouping of moving items in their search performance.
Thus, in the next experiments, we further investigated the influence of perceptual organization on the visual search for moving
and stationary targets.
5. Experiment 3a: asymmetry reversal with frame
motion
To further investigate the ability of chimpanzees to perceptually organize coherently moving items in the visual field, we
tested the effect of movement of the reference frame on the
search for moving and stationary targets. In addition to using
tests similar to those in Experiment 1 (visual search for a moving or a stationary target with a stationary reference frame), we
introduced two new display conditions; these required searching
for a moving or a stationary target among distractors within a
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synchronously moving reference frame. The mutual coherence
due to proximity or inclusiveness between the moving items and
the reference frame used in this experiment was expected to be
stronger than the coherence that was present in the relationship
of the discrete discs in Experiment 2.
Strong coherence of the reference frame with the target items
could influence the perception of the relative movements of the
target items. Human subjects reported that they perceived the
coherent movement of discs with the reference frame as if the
discs were settled on the surface of the moving reference frame.
If chimpanzees also perceived the relative state of the target in a
similar fashion, the influence of the movement of the reference
frame on detecting moving and stationary targets would be different because the interaction of the reference frame and target
could change the relative position of the target to its opposite
direction. If chimpanzee perception was dissimilar from that of
humans, the movement of the reference frame would not influence search performance or the influence would be constant
(merely disturbing), rather than provide relative and positional
information.
5.1. Methods
5.1.1. Subjects
The same chimpanzees from Experiments 1 and 2 participated in Experiment 3a. Six graduate and undergraduate student
subjects (one male and five females) ranging in age from 19 to
26 years (mean = 22.8 years) also participated in Experiment 3.
One of these had previously participated in Experiment 1, and
the other five were newly recruited.
5.1.2. Stimuli
In Experiment 3a, a reference frame was added to the display
used in Experiment 1 (Fig. 4). The frame appeared as a gray
square area (approximately 30 cd/m2 ) with black lines (the same
color as the background) of 2-mm (0.3◦ ) width on the borders of
cells of 55 mm × 55 mm (7.9◦ × 7.9◦ ). The frame was presented
against an intense black background (approximately 0 cd/m2 ).
Black discs (approximately 15 cd/m2 ) were presented on gray
cell areas in the same manner as in Experiment 1.
The movement of the stimuli and frame was a horizontal
oscillation at a velocity of 57 mm/s (8.2◦ /s) and a swing of 12 mm
(1.7◦ ). All moving items, including the frame, in a display moved
in phase. No item passed over the cell confined by black lines.
Minimum separation from the adjacent item was maintained at
more than 28 mm (center-to-center). Display size varied among
1, 4, 8, and 12 items.
Four display conditions (moving frame or stationary
frame × moving target or stationary target) were tested. When
we focused on the relativity of target motion to the reference frame, the moving frame–moving target and stationary
frame–stationary target conditions were equivalent.
5.1.3. Procedure
As in Experiments 1 and 2, a DMTS procedure was employed.
A sample stimulus was presented on the center of the gray square
subtending 42 mm × 42 mm (6.0◦ × 6.0◦ ), which served as the
Fig. 4. Examples of search displays in the moving reference conditions used in
Experiment 2. Moving discs and the reference frame are moving in phase. The
arrows depict the oscillation of each element.
reference frame of the sample stimulus at the bottom center of
the screen. The square moved in the same way as the reference
frame. The reference frame and sample stimulus were presented
simultaneously. The sample stimulus and square disappeared
when touched. After a 500-ms interval, a test target and distractors were presented in the reference frame.
A session consisted of 104 trials (26 trials for each display
size) for each display condition. The first eight trials (two trials
for each display size) were treated as practice trials. Four display
conditions were tested in four consecutive sessions (one block),
and the order within each block was randomly determined.
Each chimpanzee was presented with eight test blocks (eight
sessions for each display condition). Accuracy and response
times from the last six blocks (six sessions for each) were used
for analyses. The Experiment 3a test sessions were presented
to the chimpanzees just after the Experiment 1 test sessions,
with no additional training sessions. Each human participant
T. Matsuno, M. Tomonaga / Behavioural Brain Research 172 (2006) 219–232
was presented with a test block (1 session for each) and 4 practice sessions of 10 trials (1 session for each display condition;
display size 6) immediately prior to the test sessions of the
corresponding display condition. Averaged accuracy and mean
median response time for display sizes 4–12 were analyzed using
three-way ANOVA (reference frame condition × target condition × display size). Search slopes were analyzed using two-way
ANOVA (reference frame condition × target condition).
5.2. Results
5.2.1. Response time
The response time for display sizes 4–12 revealed the effects
of the reference frame movement (Fig. 5). Akira and the human
subjects exhibited a reversal of their ease in detecting the moving
and stationary targets with the addition of a moving reference
frame. On the other hand, Ai did not display that tendency,
although the degree of search asymmetry was slightly smaller.
There were significant effects of frame condition and target condition, F(1, 5) = 9.59 and 10.02, p < 0.05, for Akira’s
performance. The two-way interactions were also significant, F(1, 5) = 215.41 for frame × target; F(2, 10) = 11.50
for frame × display size; F(2, 10) = 44.46 for target × display
size, p < 0.01, while the three-way interaction was not, F(2,
227
10) = 0.52. Post-hoc analyses revealed simple main effects of target condition in both the stationary and moving reference frame
conditions, F(1, 10) = 69.45 and 5.98 respectively, p < 0.01,
which indicates that detecting a moving target was significantly
easier than detecting a stationary one when the display included
stationary frames, but that the inverse was easier with moving
frames.
Similar effects of frame motion were also observed in
humans. The main effect of reference frame condition, F(1,
5) = 11.13, p < 0.05, the interaction of reference frame and target
conditions, F(1, 5) = 24.67, p < 0.01, and the three-way interaction were all significant, F(2, 10) = 9.57, p < 0.01. Post-hoc analyses revealed simple-simple main effects of the target condition
for reference frame condition and display size, F(1, 30) = 6.41,
10.75, 12.09, 12.89, 29.55, and 38.47 for stationary framedisplay sizes 4, 8, and 12, and moving frame-display sizes 4, 8,
and 12, respectively, p < 0.05, consistent with the search asymmetry reversal in Akira’s performance.
Ai did not demonstrate reversed search asymmetry. The
three-way ANOVA revealed main effects for reference frame
condition, F(1, 5) = 183.76, p < 0.01, target condition, F(1,
5) = 178.07, p < 0.01, and display size, F(2, 10) = 35.27, p < 0.01,
and the interaction of target condition and display size, F(2,
10) = 23.28, p < 0.01. The other interactions, including refer-
Fig. 5. Mean median response times in Experiment 3a. The three graphs on the left present the response time × display size functions for the stationary reference
frame conditions, and the three graphs on the right present the moving reference frame conditions. Filled squares represent the moving target conditions; open circles
represent the stationary target conditions; error bars are ±1 S.E.
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ence frame and target conditions, were not significant, F(1,
5) = 4.74 for reference frame × target, F(2, 10) = 0.92 for reference frame × display size; F(2, 10) = 0.96 for reference
frame × target × display size. The simple main effects analysis
of target condition revealed that Ai took much longer to detect
a stationary target than a moving target in all display size conditions, F(1, 15) = 18.50, 72.91, and 175.78 for display sizes 4,
8, and 12, respectively, p < 0.01.
Search slopes did not show a common tendency among
subjects. Ai had steeper search slopes in the detection of
a stationary target (stationary reference frame condition,
mean search rate = 46.42 ms/item, S.E. = 4.80; moving reference frame condition, 41.90 ms/item, 4.37) than in the detection
of a moving target (stationary frame condition, mean search
rate = 3.42 ms/item, S.E. = 1.89; moving reference frame condition, −2.07 ms/item, 5.31) irrespective of the movement of
the reference frame, showing only a significant main effect
of target condition, F(1, 5) = 70.58, p < 0.01. Akira had higher
search slopes in the stationary target condition (stationary reference frame condition, mean search rate = 142.09 ms/item,
S.E. = 17.94; moving reference frame condition, 41.53 ms/item,
12.75) than in the moving target condition (stationary reference
frame condition, mean search rate = −0.52 ms/item, S.E. = 4.35;
moving reference frame condition, −113.31 ms/item, 19.22),
and higher search slopes in the stationary reference frame condition than in moving reference frame condition, showing significant main effects for both conditions, F(1, 5) = 41.39 and
146.27 for target and reference frame conditions, respectively,
p < 0.01. The search slopes of humans showed a significant difference between the detection of a moving target (mean search
rate = 2.09 ms/item, S.E. = 1.03) and a stationary target (mean
search rate = 10.16 ms/item, S.E. = 5.29) only in the moving reference frame condition, showing a significant interaction of
the two conditions, F(1, 5) = 13.861, p < 0.05, and significant
simple main effects of target condition for the moving reference frame condition, F(1, 10) = 10.01, p < 0.05. The difference
was not significant in the stationary reference frame condition
(moving target, mean search rate = −2.46 ms/item, S.E. = 1.68;
stationary target, 6.66 ms/item, 2.99), F(1, 10) = 1.32, as in
Experiment 1.
5.2.2. Accuracy
Human subjects exhibited almost perfect performance
(M = 98.7). Chimpanzee performance varied, however, according to the display conditions (Fig. 6).
Akira’s accuracy showed a main effect of display size,
F(2, 10) = 7.20, p < 0.05, and significant interactions for reference frame × target, F(1, 5) = 153.62, p < 0.01, reference
frame × display size, F(2, 10) = 12.52, p < 0.01, and target × display size, F(2, 10) = 10.74, p < 0.01. The simple main
effects of target condition were significant in both the stationary
and moving reference frame conditions, F(1, 10) = 28.95 and
21.56, respectively, p < 0.01, indicating more errors detecting
a stationary target than a moving target with a stationary reference frame, and fewer errors in detecting a stationary target
with a moving reference frame. These results were consistent
with those of response time.
Fig. 6. Mean percentage of correct responses for each subject and each condition
in Experiment 3a. The leftmost six bars represent the stationary reference frame
conditions, and the others represent the moving reference frame conditions. The
leftmost three of the six bars represent the moving target conditions, and the
right three of the six bars represent the stationary target conditions. Each bar is
for a different display size (DS) condition. Error bars are ±1 S.E.
Ai’s accuracy showed a main effect of reference frame condition, F(1, 5) = 32.11, p < 0.01, and significant interactions for
reference frame and target conditions, F(1, 5) = 9.14, p < 0.05,
and target condition and display size, F(2, 10) = 6.47, p < 0.05.
While there were no simple main effects of the target condition
with a stationary reference frame, F(1, 10) = 0.30, there were
effects of a moving reference frame, F(1, 10) = 10.24, p < 0.01,
indicating greater accuracy in detecting a stationary target than
a moving target with a moving reference frame, consistent with
the accuracy of Akira’s performance.
5.3. Discussion
The search performance of humans and the chimpanzee,
Akira, showed the same search asymmetry reversal tendency.
With a moving reference frame, Akira displayed obvious facilitation in searching for a stationary target and difficulty searching for a moving target. These results suggest the possibility
that chimpanzees can perceive relativity of motion in a search
display. In contrast to human performance, which showed a relatively inefficient search rate in the detection of a moving target
with a moving reference frame, Akira was quicker to respond,
T. Matsuno, M. Tomonaga / Behavioural Brain Research 172 (2006) 219–232
resulting in a negative search slope, and was more accurate with
larger display sizes in the moving frame–moving target condition. We speculate that the multiple stationary discs served as
a reference point, and helped in detecting an incongruent item
within the moving reference frame. Given the stronger human
ability to perceptually organize coherent movements, as shown
in Experiment 2, humans could not ignore the coherent movement of the reference frame, an effect that would be robust even
with larger display sizes.
Although Ai’s response time and search slope did not show
evidence of asymmetry reversal, her accuracy was compatible
with the response time performance of Akira and the human
subjects. Ai’s speed-accuracy trade-off would logically affect
her response speed.
6. Experiment 3b: asymmetry reversal with frame
motion; an additional experiment
In Experiment 3a, one of the two chimpanzees did not show a
clear tendency to use the coherently moving reference frame in
perceptual organization. For further investigation of the nature
of chimpanzees’ visual search in a dynamic display, three other
chimpanzees were introduced as subjects. Prior to this experiment, they had already learned to detect a moving target among
stationary distractors [28], but were unfamiliar with the opposite task, that of detecting a stationary target among moving
distractors, as well as a moving reference frame. In this additional experiment, we tested how they performed in such novel
situations.
6.1. Methods
229
stimulus and the 500 ms interval, a search display (stimuli and
the reference frame) was presented.
The chimpanzees were tested in Experiment 3b with no
advance training or practice. In a 60-trial session, the display
condition was fixed, and the four different display conditions
were tested in four consecutive sessions (one block). The order
of the four sessions was randomly determined. Each chimpanzee
was tested in five blocks (five sessions for each display condition). Accuracy was analyzed, but because subjects showed no
correct responses in some sessions, correct response time was
not analyzed.
6.2. Results
The accuracy data from Experiment 3b are presented in Fig. 7.
The marked effect of reference frame movement was apparent
in the stationary target conditions, in which the chimpanzees
made many mistakes with the stationary reference frame, but
were very successful with the coherently moving frame. Twoway ANOVA of reference frame and target conditions found
that all main effects and the interaction were significant, Ayumu:
F(1, 4) = 26.01, 512.87, and 33.01 for reference frame condition,
target condition, and their interaction, respectively, p < 0.01;
Mari: F(1, 4) = 22.04, 41.36, and 31.38, p < 0.01; Pendesa:
F(1, 4) = 10.10, 92.80, and 35.03, p < 0.05. Post-hoc analyses
revealed simple main effects of reference frame for the stationary
target condition, F(1, 8) = 59.03, 50.60, and 39.50 for Ayumu,
Mari, and Pendesa, respectively, p < 0.01, showing an advantage
of a moving reference frame in the search for a stationary target.
The simple main effects of reference frame in the moving target
condition were significant only for Mari, F(1, 8) = 8.34, p < 0.05.
6.1.1. Subjects
Three chimpanzees, Mari, Pendesa, and Ayumu, participated
in Experiment 3b. Immediately prior to this experiment, they participated in visual search experiments [28], and learned to detect
a moving disc target in three conditions in which the target was
defined by movement state (distractors were stationary discs),
form (distractors were moving cross marks), or a conjunction of
the features (distractors were moving cross marks and stationary
discs). The first condition was almost the same as the stationary
frame–moving target condition in this study. The three subjects
had no experience detecting a stationary item among moving
items. Pendesa had experienced other visual search tasks that
tested discrimination of the perceptual depth of the stimuli [19];
the other two new subjects had no other previous visual search
training.
6.1.2. Stimuli
Stimuli and display conditions were the same as in Experiment 3a except for display size, which was fixed to size 6
throughout the sessions.
6.1.3. Procedure
A visual search task was presented to the subjects. The procedure was almost the same as in Experiment 3a, although sample
presentation was omitted. After the termination of the warning
Fig. 7. Mean percentage of correct responses for each subject and each condition
in Experiment 3b. The six bars on the left represent the stationary reference frame
conditions, and the others represent the moving reference frame conditions. The
leftmost three of the six bars represent the moving target conditions, and the
right three of the six bars represent the stationary target conditions. Each bar is
for a different subject. Error bars are ±1 S.E. A dashed line indicates the chance
level (16.6% correct); an open circle indicates the first-session performance of
each subject.
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These results were not caused by rapid learning to detect
specific targets in the course of the test sessions, as they were
apparent even in the first sessions (circles in Fig. 7 indicate
first-session performance). All subjects exhibited the tendency
revealed in the averaged accuracies, although both improvement and deterioration were observed in several conditions as
the sessions continued. We suggest that the relatively good performance in the moving frame–stationary target and moving
frame–moving target conditions, which were novel for the subjects, was the result of generalization from the prior tasks that
required detecting a moving disc on a neutral gray background.
6.3. Discussion
Success in detecting a stationary target depended on the
movement of the reference frame. Although subjects had no
prior experience detecting a stationary target and, in fact, their
performance in the stationary frame–stationary target condition
was below chance levels (16.7%), they were able to successfully
detect targets in the moving frame–stationary target condition.
In the same way, success in detecting a moving target was significantly influenced by the movement of the reference frame
for one subject, Mari. These results suggest that subjects more
readily perceive the “motion” of an absolutely stationary target under the influence of the moving reference frame, although
relatively good performance in the moving target-moving frame
condition suggests that such relative perception did not lead to a
complete perceptual reversal of the movement states. Absolutely
stationary discs may serve as a reference point, as discussed in
Experiment 3a. In summary, these results further support the
view that chimpanzees partially share with humans the ability
to perceive an object in relation to other objects in the visual
field.
7. General discussion
This study investigated visual search in chimpanzees and in
humans for moving and stationary targets. The main findings
in this series of experiments were as follows: (1) chimpanzees
exhibited search asymmetry for moving and stationary items as
did humans; however, a qualitative difference between chimpanzees and humans was observed in the degree of asymmetry.
While humans found it fairly easy to search for a stationary target among moving distractors, chimpanzees found it difficult.
(2) Coherent motion of the distractors facilitated detection of a
stationary target in humans, but not in chimpanzees. (3) Relative movement states of the stimuli, which were altered by the
movement of the reference frame, similarly influenced search
performance in chimpanzees and humans. These results can
be discussed from two perspectives: attentional processing of
motion and perceptual organization.
First, this study provides further evidence of search asymmetry in chimpanzees, and supports shared attentional mechanisms
between chimpanzees and humans. In Experiment 1, detecting
a stationary item among moving items was more difficult than
detecting a moving item among stationary items for both chimpanzees and humans. According to previous studies in humans
[37,50,51], this would suggest that “motion” is a basic feature
in the visual system of both species, and the presence of that
basic feature is more easily detected than its absence. Rosenholtz [38,39] has offered a different account of search asymmetries using a simple saliency model. According to the model,
asymmetrical search performance between the conditions can
be explained by differences in discriminability of the target
from distractors in the represented feature space of velocity
and motion direction. In chimpanzees, Tomonaga [46] replicated search asymmetry using stationary figures, and confirmed
that the conditions causing search asymmetry are similar for
humans and chimpanzees. This study demonstrates that attentional processing of the moving items is common, and supports
the view that chimpanzees and humans share the attentional tendency to asymmetrically process the visual features depending
on the general presence and absence of features or represented
saliency.
From an ecological standpoint, this rapid processing of movement against a stationary background is environmentally adaptive, and thus, important from the perspective of the evolution of
our visual processing systems. Given its importance, this rapid
attentional processing would not be a particular feature of the
two species, but rather would be a general feature in visually
dependent animals. Physiological studies have shown highly
sensitive motion detectors in a variety of species, such as monkeys, birds, and even insects [15], although behavioral evidences
comparing their attentional processing is relatively scarce. We
need further comparative studies of other species, both distant
and close to humans, to investigate the phylogeny and the evolution of attentional processing.
Second, the present study focused on how chimpanzees perceptually organize moving items. As Gestalt psychologists have
indicated [24], coherent motion is a strong determinant of perceptual grouping for humans. Previous studies with human subjects reported that such perceptual organization is helpful for
effective visual search performance in a dynamic visual field
[31,37,55]. The results of the present experiments indicate that
chimpanzees have a weaker ability than humans to perceptually
group items in their visual field. In Experiment 2, chimpanzees
failed to eliminate the unit of coherently moving items to efficiently search for a stationary target, and appeared to process
the items one by one, as they did for the non-coherently moving
items. In contrast, humans took advantage of the uniformity of
the moving items to improve their search rate. This difference
would not have been caused by simple differences in visual resolution, because one of the subject (Ai) showed almost the same
visual acuity as that of humans in a previous study [30], and
chimpanzees detected moving target as efficiently as humans in
this study. Previous studies reported that even macaque monkeys
and pigeons, which are more remotely related to humans than
chimpanzees, can discriminate coherent motion from random
motion as a result of intensive training [3,4,7]. Therefore, what
was difficult for chimpanzees would not have been the detection
of motion coherence but the process of perceptual organization
to put the moving items into one group based on the perceived
coherence and/or to reject them as a unit in search. To efficiently
detect a stationary target among coherently moving distractors,
T. Matsuno, M. Tomonaga / Behavioural Brain Research 172 (2006) 219–232
we would need two dissociated stages, i.e., the unitization of
spatially separated discs (grouping) and the inhibition of the
unit. In the task presented here, the answer to which stage was
difficult for chimpanzees was not evident.
In Experiment 3, chimpanzees showed evidence of an ability
to perceptually organize the coherently moving discs and the
reference frame. One plausible explanation for the difference
in the results of Experiments 2 and 3 may be the proximity of
the organized objects. The items to be organized were presented
discretely and scattered within a display in Experiment 2, but the
discs and reference frame were very proximal in Experiment 3.
In the latter case, the items appeared to be placed on the surface
of the reference frame; such a strong proximity and association
between objects may have compensated for the weaker grouping ability of chimpanzees [12]. Another possible explanation
may be a difference in the predominant way in which the phenomena were perceived, which could be as coherently moving
grouped items in Experiment 2, and items influenced by relative or induced motion in Experiment 3. The movement of the
reference frame could also have altered the perceived relative
movements of the discs. Such relative motion could be perceived
by chimpanzees and influence their performance, even though
they could not perceptually group the discs with the reference
frame.
These results revealed certain aspects of how chimpanzees
use perception to organize moving visual elements, and
addressed some of the differences in perceptual organization
between chimpanzees and humans. Most previous studies on
perceptual organization in non-human animals focused on
stationary aspects, such as global/local processing of visual
elements and perceptual grouping based on the proximity
of elements [5,11,25]. Given the dynamic environment in
which organisms live, however, we should accumulate more
evidence about the dynamic aspects of the perceptual process in
non-human animals, such as the perception of relative motion,
perceptual grouping of moving objects, and recognition of an
object constructed by interactively moving elements [21,35].
The question regarding the neural basis explaining our behavioral data that showed similarities and differences between the
species is difficult to address for two reasons. First, it is still
unclear which neural mechanisms or cortical areas underlie
search asymmetry and perceptual organization. In search asymmetry, bottom–up processes that originate in early visual areas
were suggested to explain the phenomenon in a neural model
study [26], but no physiological surveys have clarified this postulate. Several studies have claimed that types of perceptual
grouping are correlated with neural activity in the primary visual
cortex [40] or the synchronous neural activity [10], but a general mechanism explaining perceptual grouping as a whole has
not been elucidated [34]. Second, our knowledge on the brain
functions of chimpanzees is limited. Visual systems in primate
species exhibit common properties depending on homologies in
the visual cortex [53]. Several studies, however, have reported
the qualitative differences in human brain [6], even in the early
visual stream [36], in addition to volumetric differences from
those of other primate species, including chimpanzees. It is difficult to discuss the correlation between such differences in brain
231
microstructure and those in perception, partly because of the lack
of functional studies on the chimpanzees brain that connect brain
activity and behavior. We should look for future development of
non-invasive neuroimaging devices and techniques applicable
to chimpanzees. Cumulative efforts to collect behavioral evidence would also be helpful for such comparative research on
the evolution of neural systems.
In summary, this study demonstrated not only the similarities
in the attentional processing of moving objects, but also apparent
differences between chimpanzees and humans in the perceptual organization of moving items. Presumably, humans have
refined their visual perception abilities from the stage of sensitivity to visual objects to the stage in which spatially discrete
items are relationally perceived in their visual context. Although
it would be premature to discuss the evolutionary relevance of
such a refinement with these few evidences, such an advantage
in humans perceptual organization may be related to the large
cognitive capacity of humans to recognize variable things at
one time, as well as the complex relationships among them.
Further experimental studies that extensively compare visual
properties between humans and non-human primates will be
helpful in understanding the evolution of visual perception and
cognition.
Acknowledgements
This study was financially supported by Grants-in-Aid
for Scientific Research (12002009, 16002001, 13610086 and
16300084) and for the 21st Century COE Program (D2) from
the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and also supported by Research Fellowship
(16/1060) from the Japan Society for the Promotion of Science
for Young Scientists. We would like to express my thanks to Dr.
M. Tanaka and Dr. T. Matsuzawa of Kyoto University for their
helpful supports and instructions, to Mr. S. Nagumo and Dr. A.
Izumi of Kyoto University for their technical advices, to Ms.
T. Imura of Kyoto University for her suggestions on this study,
and to anonymous reviewers for their helpful comments. We are
also grateful to all the staffs at the Primate Research Institute
of Kyoto University who work with the chimpanzees for their
management of the health of the subjects.
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