symbolic representation of number in chimpanzees tetsuro...

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Symbolic representation of number in chimpanzeesTetsuro Matsuzawa

This paper aims to summarize the existing evidence for the

symbolic representation of number in chimpanzees.

Chimpanzees can represent, to some extent, both the cardinal

and the ordinal aspect of number. Through the medium of

Arabic numerals we compared working memory in humans and

chimpanzees using the same apparatus and following the same

procedure. Three young chimpanzees outperformed human

adults in memorizing briefly presented numerals. However, we

found that chimpanzees were less proficient at a variety of

other cognitive tasks including imitation, cross-modal

matching, symmetry of symbols and referents, and one-to-one

correspondence. In sum, chimpanzees do not possess human-

like capabilities for representation at an abstract level. The

present paper will discuss the constraints of the number

concept in chimpanzees, and illuminate some unique features

of human cognition.

Address

Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi

484-8506, Japan

Corresponding author: Matsuzawa, Tetsuro

([email protected])

Current Opinion in Neurobiology 2009, 19:92–98

This review comes from a themed issue on

Cognitive neuroscience

Edited by Michael Platt and Elizabeth Spelke

Available online 14th May 2009

0959-4388/$ – see front matter

# 2009 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.conb.2009.04.007

IntroductionUsing the Arabic numerals 0 through 9, the chimpanzee

Ai can represent both the cardinal and the ordinal aspect

of number to some extent [1�]. Similar skills have now

been partially confirmed in six other chimpanzees [2��,3].

A recent study has used numerical stimuli to demonstrate

an extraordinary memory capability in young chimpan-

zees [2��]. In contrast with the memory test, chimpanzees

show poor performance in many other cognitive tasks that

require some form of abstraction. The present paper will

address the following five topics. First, it describes the

logic and framework for the study of the number concept

in nonhuman animals. Second, it reviews the long-run-

ning Ai project, focusing in particular on studies dealing

with the symbolic representation of number. Third, it

describes the extraordinary memory capacity that young


chimpanzees possess for numerals. Fourth, it introduces

common characteristics of the difficulties experienced by

chimpanzees in various kinds of cognitive tasks. Finally,

it discusses the number concept within the larger context

of cognition, illuminating cognitive development in

chimpanzees and the unique features of human cognition.

The Ai project: psychophysical measurementand the underlying logicThe Ai project – encompassing a series of studies whose

principal subject has been a female chimpanzee named Ai

– began when Ai, at the age of 1.5 years, first touched an

experimental keyboard on April 15th 1978 [3–5]. The last

in a succession of ape-language projects launched in the

second half of the 20th century, the Ai-project was also

the forerunner of a new research paradigm called Com-

parative Cognitive Science (CCS) [6]. CCS is the com-

bined study of psychophysics and ape-language, using

computer-controlled apparatus. In its original form, CCS

aimed to compare perception, memory, and cognition in

humans with those of closely related species such as

chimpanzees. Crucially, such inter-species comparisons

rely on identical methods: subjects, irrespective of

species, use the same apparatus and follow the same

procedure during testing.

Psychophysics is the classic psychological study of

measuring human sensation, perception, memory, and

cognition in general. Psychophysics tries to unravel the

relationship between physical events and psychological

events. Psychophysical researchers have established

many laws, including, for example, Weber–Fechner’s

law and Steven’s power law. There exist well-established

methods for measuring the relationship between the

stimuli presented and the corresponding internal psycho-

logical states. Thus, psychophysics can be extended to

issues related to concept formation, such as the under-

standing of number.

The Ai project has two important features: the research

presents humans and chimpanzees with exactly the same

tasks so that their performance can be compared in detail,

and that the research undertakes that comparison by

using the methods of psychophysics. There is the syner-

gistic connection between these two features for the

enterprise of CCS. CCS aims to compare different species

at the level of cognitive mechanisms, and it is the great

virtue of psychophysical method that serves not only to

describe the performance of humans and nonhuman

animals but also to analyze that performance into its

component mechanisms. By adopting psychophysical

approach, you can go beyond questions of what trained

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Symbolic representation of number in chimpanzees Matsuzawa 93

chimpanzees can do and ask how chimpanzees and

humans do what they do: What cognitive capacities are

shared by the two species and what capacities distinguish

them.

Ai was the first chimpanzee who learned to discriminate

the 26 letters of the alphabet during tests of shape

perception and visual acuity [7]. She also mastered

additional visual symbols such as specially devised geo-

metric shapes (called lexigrams) and Japanese Kanji

characters signifying different colors, in the course of

experiments designed to examine her classification of

various colors [8].

Ever since the beginning of the Ai-project, my colleagues

and I have been focusing on the mathematical skills of

chimpanzees rather than on any form of bilateral com-

munication between humans and chimpanzees—the latter

having been the central theme of previous ape-language

studies. There were four reasons why we decided to

concentrate on issues related to number concepts.

First, the world of logico-mathematical skills was small.

Mathematical cognition is a part of human cognition in

general, but the number system is narrower and more

clearly and precisely defined in comparison to the lin-

guistic system. The number system includes the levels of

Integer that is a part of Real number, and that is a part of

Complex number. The scales of the number system

advance from Nominal to Ordinal, Interval, and Ratio

scales. Therefore, focusing on the Integer, for example,

we can examine both cardinal aspects (‘one, two, three,

four. . .’) and ordinal aspects (‘first, second, third,

fourth. . .’) of the number concept in chimpanzees. From

the perspective of future work, we can examine the

combination of numerical elements to create new mean-

ing: such as putting 1 and 0 together to create ‘10’ in the

decimal number system. Moreover, further questions

open up regarding numerical operations such as addition

and subtraction. These kinds of numerical manipulations

can be viewed as corresponding to the syntactical struc-

ture of the language system.

Our second reason for focusing on number concepts was

the accumulation of knowledge about mathematical

thinking in human subjects. Several important papers

had just been published about the child’s understanding

of number, including Gelman and Gallistel’s landmark

article [9]. These helped us to discern what we ought to

study in chimpanzees. Since then, further studies on

number concepts in humans have continued to shed light

on many relevant issues and promoted our understanding

of various aspects of numerical cognition (see reviews in

[10–13]) including its neural mechanisms [14,15].

Third, a handful of studies had reported on topics related

to the number concept in nonhuman animals, such as


enumeration, quantity discrimination, and sequential

responding. Today, much attention continues to be paid

to the concept of number in nonhuman animals [16,17].

Various researchers have published studies that they

described as tests of numerical competence in macaque

monkeys [18–20], cotton-top tamarin [21], elephant [22�],parrot [23], pigeons [24], even salamanders [25] and bees

[26�]. However, none of these compared the performance

of human and nonhuman subjects directly, using the

same methodology. Almost all the literature on nonhu-

man animals has focused on rudimentary forms of the

number concept. By contrast, the Ai-project’s series of

number concept studies stands out clearly for two reasons.

First, it focuses on the symbolic representation of number

using Arabic numerals. This symbolic representation

allowed us to conduct direct comparisons between

humans and chimpanzees. Second, we applied psycho-

physical measurements using a fully automated compu-

ter-controlled apparatus that completely excluded any

kind of social cueing.

The fourth reason why we decided to concentrate on

issues related to number concepts is the connection to the

psychophysical approach. Most domains of human cogni-

tion are not yet amenable to psychophysical analysis,

because the proper mathematical characterization of

the cognitive domain is not clear. Number, however, is

highly amenable to psychophysical analysis. Indeed, the

Weber–Fechner’s law of psychophysics holds in the

numerical domain.

Cardinal and ordinal aspects of number andintroducing zeroAi is the first chimpanzee who mastered the use of Arabic

numerals to represent numbers [4]. She learned both

cardinal and ordinal aspects of the number system. She

used the numerals to label real-life items, shown to her in

a display window, in terms of their numerosity. She also

became proficient at responding to Arabic numerals in

ascending order, selecting them from a touch-screen in

the correct sequence. When the numeral ‘0’ was intro-

duced, Ai mastered its use in both the cardinal and the

ordinal domains; however, the acquisition process and the

generalization tests in this case clearly highlighted the

constraints of the symbolic representation of number

acquired by the chimpanzee [1�]. Further detail on Ai’s

experience with numerals follows below.

Cardinal number training began when Ai was about five

years old. She had already learnt to use lexigrams corre-

sponding to object and color names. Ai mastered the skill

of naming 1 through 6, in addition to the naming of 14

objects and 11 colors. Although the ‘word order’ of

describing a particular sample (such as ‘five red tooth-

brushes’) was free, she spontaneously adopted a favored

sequence, assigning the object and color names first and

then naming the number last. This rule of describing the


94 Cognitive neuroscience

number in the final position was preserved in the case of

new objects and new colors. It was preserved even when

the number of objects was limited to just one. In a sense,

the chimpanzee spontaneously developed her own ‘gram-

mar’ to describe the world [4].

Patterns in the ease with which Ai acquired object, color,

and numerical labels provide an interesting contrast.

During the initial phase of learning to use visual symbols

to label corresponding objects, Ai experienced consider-

able difficulties: the first two objects required a long

period of training. However, once past this early hurdle,

learning to name a third object became easier, and the

fourth easier yet. The same pattern was evident in the

case of color naming [8]. This suggests that the chim-

panzee ‘learned to learn’ in terms of objects and color

naming. On the contrary, no comparable improvement

was observed in the case of numerical naming: The

sessions required to reach the learning criterion did not

decrease as the numerals 3, 4, 5, and 6 were successively

introduced.

After becoming proficient at the numerical naming of real

life objects, Ai learned to label white dots projected onto a

touch-screen monitor [27,28]. Her range of numerosities

and associated labels was also extended, up to nine.

Transferring the task on to a fully automated, computer-

ized system further allowed us to measure precisely Ai’s

response latencies in numerical naming. We found that the

response latency remained constant up to about five dots;

thereafter we saw a gradual increase in the time taken to

label progressively larger sets. At a look, this tendency

reminded us of the two phases of numerical labeling in the

case of human subjects, subitizing and counting. However,

Ai’s response latency reached its maximum at eight dots,

rather than the largest of the sets, at nine. In fact, this

tendency was clear throughout the process of acquisition:

The latency was always at maximum at n � 1 dots, when

the largest set being tested was of size n. This strongly

suggests that instead of counting the dots one by one, the

chimpanzee seemed to be performing analog magnitude

estimation of the number of dots. Such magnitude esti-

mation of quantity is well documented not only in chim-

panzees [29] but also in other animals [18]. Of course, Ai’s

performance does not necessarily imply that chimpanzees

cannot count; it simply proves that it is not a straightforward

task to teach them to solve problems by counting items one

by one.

In addition to the cardinal aspect of number, we also

trained Ai in the ordinal domain. First she learned to

select Arabic numerals from 1 to 9 on a touch-screen, in

ascending order [30]. After initial training with consecu-

tive items, we introduced sequences of nonadjacent

numerals—these tests revealed both a positional and a

symbolic distance effect in Ai’s performance. The pos-

itional effect means that Ai’s latency to select the first


item in a sequence was short when this item was a small

number; she took longer to decide on the first item when

this was large. The symbolic distance effect describes the

finding that latency decreases when two numerals being

compared are far apart (in terms of their position in the

sequence); the task becomes more difficult when the

numerals are close. In sum, Ai (as well as other chimpan-

zees we subsequently trained) clearly mastered the

sequencing of numerals along the ordinal scale [30,31].

In a follow-up study, we attempted to add the number 0 to

Ai’s repertoire, training her in the meaning of ‘zero’ first in

the cardinal and then in the ordinal domain [1�]. She was

initially required to use the numeral 0 to describe the

absence of dots in the display frame. After she had learned

to use zero in this cardinal setting, we introduced the

numeral 0 in the ordinal sequence task. She did not

spontaneously place the numeral 0 before 1; there was,

thus, no immediate transfer of the meaning of zero from

the cardinal to the ordinal domain. However, once again,

these negative data do not imply that chimpanzees cannot

possess the concept of zero—in fact, Ai eventually suc-

ceeded in mastering both the cardinal and the ordinal

meaning of the numeral. Nevertheless, whether chim-

panzees are capable of bilateral transfer between cardinal

and ordinal domains of number remains an open question.

Working memory of numerals in chimpanzeesPeople’s general view of the chimpanzee mind is that it is

inferior to that of humans [32]. My colleagues and I

showed for the first time that young chimpanzees have

an extraordinary working memory capacity for numerical

recollection [33,2��]. Their performance was better than

that of human adults tested on the same apparatus fol-

lowing the same procedure.

The subjects of this study were six chimpanzees, three

mother–offspring pairs, including Ai. We started training

the three young chimpanzees at the age of four years; the

two mothers who were also naı̈ve to the task received the

same training in parallel. All of them succeeded in learn-

ing the sequence of Arabic numerals from 1 to 9, using a

touch-screen monitor connected to a computer. A mem-

ory task called ‘masking task’ was then introduced, at

around the time when the young chimps reached five

years of age. In this task, after touching the first numeral,

all other numerals were replaced by white squares. The

subjects had to remember which numeral had appeared in

which location, and then touch the squares in the correct

ascending order. Ayumu, one of the three young chim-

panzees, can memorize the nine numerals in 0.67 s. His

performance is much faster and more accurate than

human adults (Figure 1).

We next invented a novel variation of the memory test,

the so-called ‘limited-hold memory task’ [2��]. In this

task, after touching the initial white circle that served as



Figure 1

Chimpanzee Ayumu, at the age of 5.5 years, performs the masking task in which the subject has to remember which numeral appeared in which

location of the monitor. The latency to touch the first numeral was 0.67 s. The young chimpanzees can memorize the nine numerals much faster and

more accurate than human adults [2��].

the start key to each trial, the numerals appeared only for

a certain limited duration, and were then automatically

replaced by white squares. We tested both chimpanzee

subjects (Ai and her son Ayumu) and human subjects on

three different hold duration conditions: 650, 430, and

210 ms.

The number of numerals was limited to five. In human

subjects and Ai, the percentage of correct trials decreased


as a function of hold duration. However, from the very

first session, Ayumu’s performance remained at almost

the same level irrespective of hold duration, and showed

no decrement. Ayumu outperformed all of the human

subjects in both speed and accuracy. Our most recent

(unpublished) data show that Ayumu can remember eight

numerals shown for only 210 ms with an accuracy of 80%.

Such memory performance has never been obtained in

human subjects, even after intensive training. Seeing is



believing: Please enter the keywords ‘chimpanzee mem-

ory’ in YouTube.com’s search engine, and watch the 10-

min video clip entitled ‘Ayumu’ that we have uploaded.

Not only Ayumu but also the other two young chimpan-

zees we tested showed the same extraordinary memory

capability [2��]. Young chimpanzees thus appear to have

an extraordinary working memory capacity for numerical

recollection—better than that of human adults. The

results may be reminiscent of the phenomenon known

as ‘eidetic imagery’ or the feats of so-called ‘idiot savants’.

Such abilities are known to be present in some human

children among thousands, with the ability generally

declining with age.

A recent study presented the first examination of eye

tracking in chimpanzees by a computer-based automatic

detection system [34�]. The eye movements of chimpan-

zees as they viewed naturalistic pictures were recorded.

The results were compared with those of humans in the

same apparatus following the same procedure. Although

the two species shared many common features such as

looking at faces and eyes, chimpanzees shifted the fix-

ation location more quickly and more broadly than

humans. The chimpanzees are good at quickly grasping

the pattern as a whole.

Cognitive tasks that present particulardifficulties for chimpanzeesDuring my past three decades with the chimpanzees [35],

it became clear that some cognitive tasks easy for humans

were not so easy for chimpanzees. For example, although

infant chimpanzees show neonatal imitation of facial

gestures just like humans, this does not develop into

generalized imitation [36]. Chimpanzees can master

the ‘Do this!’ game to some extent. Although they can

imitate actions toward objects, it is difficult for them to

imitate actions toward their own bodies, and even more

difficult to imitate simple actions without objects [37].

Cross-modal matching is also a challenging task for chim-

panzees. They require intensive training to master

matching auditory stimuli to corresponding visual stimuli

[38]. Similar difficulties can be observed in symbolic

matching-to-sample tasks. Very little evidence exists

regarding the symmetry of symbols and their referents.

Let us consider a symbolic matching-to-sample task in

which a referent needs to be matched to the correspond-

ing symbol. For example, the color ‘red’ must be matched

to the symbol ‘red’, and the color ‘green’ to the symbol

‘green’. After intensive training on the task, chimpanzees

can become proficient at selecting the correct symbol in

response to being presented with a specific color. In turn,

you can now test the reverse scenario: showing a symbol

first and then providing two choice alternatives, the color

‘red’ pitted against the color ‘green’. Chimpanzees,

trained only on color-to-symbol matching, find it difficult


to match the symbol to the corresponding color. This kind

of bi-directional correspondence between symbols and

referents is referred to as ‘symmetry’. Symmetry is almost

automatically established in the early phase of human

language development. However, this is not the case in

chimpanzees, who do not transfer spontaneously but need

further intensive training [39].

Let us return to the issue of number. In true counting

behavior, one-to-one correspondence should provide

the essential basis for further establishment of the

number concept. Imagine that you place five cups

upside down in front of a chimpanzee, and then provide

her with small wooden blocks. Using a gesture, you

then ask the chimpanzee to put the wooden blocks on

top of the cups. It is extremely difficult for the chim-

panzee to place the wooden blocks – which can be seen

as representing ‘counters’ – on the cups one by one. She

will more probably stack the blocks on top of one

another, the chimpanzees’ preferred way of manipulat-

ing objects in such situations. Of course, chimpanzees

may learn to solve this particular task, however, it will

not automatically generalize to variations thereof. One-

to-one correspondence looks easy to us, but it is not so

for the chimpanzees.

Human infants assume stable supine posture from right

after birth [40�]. This enhances face-to-face visual com-

munication, vocal exchange, as well as bimanual object

manipulation since the hands are freed from having to

cling to the mother. By contrast, chimpanzee infants

continuously cling to their mothers at least throughout

the first three months of life. It is the stable supine

posture, not bipedal locomotion, that makes human hands

free and provides important clues to the complexity of our

object manipulation, a precursor of tool use. When we

analyze the development of object manipulation in chim-

panzees using standard tests involving wooden blocks,

nesting cups, and so forth, we see interesting differences

between the two species in terms of action grammar [41].

Only one of the three infant chimpanzees we studied

started to stack blocks spontaneously—she did so at a

little less than three years of age, much later than human

infants [42]. The other two never stacked blocks, despite

having had extensive experience of watching their

mothers’ stacking behavior. No chimpanzees, not even

Ai, succeeded in making a copy of a simple three-block

structure, such as a ‘bridge’ or ‘arch’ in which two blocks

are placed side by side a short distance apart and a third is

placed on top of both [43�]. Chimpanzees can manipulate

blocks into one-dimensional structures, in a vertical or

horizontal alignment. However, they find two-dimen-

sional structures difficult, and three-dimensional con-

struction more difficult still. These kinds of

hierarchical constraints are seen throughout all examples

of object manipulation by chimpanzees both in the

laboratory and in the wild [44–47].



Conclusions: a trade-off theory of memoryand symbolic representationWhy do chimpanzees have a better memory than humans

for immediately capturing visual stimuli? Why do chim-

panzees have difficulties representing things at an

abstract level? The existing data can be interpreted

according to an evolutionary trade-off hypothesis [40�].The common ancestor of humans and chimpanzees five to

six million years ago may have possessed an extraordinary

memory capability. At a certain point in evolution,

because of limitations on brain capacity, the human brain

may have acquired new functions in parallel with losing

others—such as acquiring language while losing visuo-

spatial temporal storage ability.

Humans may have developed unique cognitive capa-

bilities such as symbolic representation or the ability to

handle abstract concepts. Imagine that you witness a

creature that passes quickly in front of you. You notice

that body is covered in brown hairs, and the creature has

a white streak on its forehead and a black spot on its

right front leg. This, in a sense, is one useful way of

dealing with stimuli that you encounter. However,

there might be a different way to view the world. On

the basis of the various features you observed, you may

summarize this detailed information and label the

creature as a ‘horse’. This kind of representation may

be efficient because it can save you having to memorize

details, allow you to generalize the experience to similar

encounters in future, and share the information with

others. In the case of the number concept, there is

adaptive value in being able to report the number of

enemies, count the number of allies, and communicate

about the number of potential prey.

Communication is likely to have been more important

than immediate memory in the social life of early homi-

nids. Humans are creatures who can learn from the

experiences of others. The trade-off theory has support

from not only a phylogenetic but also an ontogenetic

perspective. In humans, youngsters often outperform

adults on certain memory tasks. In the course of cognitive

development, human children may acquire linguistic

skills while losing a chimpanzee-like photographic mem-

ory [40�]. This may be due to the time lag of myelination

of neuronal axons in each part of the brain. It is known

that the association cortex responsible for complex

representation and linguistic skills develops more slowly

than other primary areas. Further study on the mind–brain relationship will illuminate this kind of trade-off

across phylogeny and ontogeny. In sum, the present

paper summarized the potentials and constraints of sym-

bolic representation of number in chimpanzees, as

revealed through the medium of Arabic numerals and

through comparative studies using humans undergoing

identical test procedures. In conclusion, the number

concept in terms of symbolic representation is uniquely


human, and comparable levels of abstraction have yet to

be demonstrated in the rest of the animal kingdom—

even in our closest evolutionary neighbor, the chimpan-

zee.

AcknowledgementsThe present study was supported by grants from the Ministry of Education,Science, and Culture in Japan (#12002009, #16002001, #20002001), andJapan Society for the Promotion of Science (gCOE-A06, gCOE-D07, ITP-HOPE). Thanks are due to the staff of the Primate Research Institute,Kyoto University, and to keepers and veterinarians who took care of thechimpanzees at the institute. I thank Dora Biro for her help given in thecourse of revising the manuscript.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest�� of outstanding interest

1.�

Biro D, Matsuzawa T: Use of numerical symbols by thechimpanzee (Pan troglodytes): cardinals, ordinals, and theintroduction of zero. Anim Cogn 2001, 4:193-199.

An adult female chimpanzee with previous training in the use of Arabicnumerals 1–9 was introduced to the meaning of ‘‘zero’’ in the context ofthree different numerical tasks. The first two were cardinal tasks ofproductive use of numerals and receptive use of numerals. The thirdtask addressed the ordinal meaning of the same symbols. The subjectmastered the recognition of the meaning of zero on all three tasks.However, the level of abstraction was incomplete in comparison tohumans.

2.��

Inoue S, Matsuzawa T: Working memory of numerals inchimpanzees. Curr Biol 2007, 17:R1004-R1006.

The authors showed for the first time that young chimpanzees have anextraordinary working memory capability for numerical recollection. Itwas better than that of human adults tested on the same apparatusfollowing the same procedure.

3. Matsuzawa T, Tomonaga M, Tanaka M (Eds): CognitiveDevelopment in Chimpanzees. Springer; 2006.

4. Matsuzawa T: Use of numbers in a chimpanzee. Nature 1985,315:57-59.

5. Matsuzawa T: The Ai project: hisotorical and ecologicalcontexts. Anim Cogn 2003, 6:199-211.

6. Matsuzawa T (Ed): Primate Origins of Human Cognition andBehavior. Springer; 2001.

7. Matsuzawa T: Form perception and visual acuity in achimpanzee. Folia Primatol 1990, 55:24-32.

8. Matsuno T, Kawai N, Matsuzawa T: Color classification bychimpanzees (Pan troglodytes) in a matching to sample task.Behav Brain Res 2004, 148:157-165.

9. Gelman R, Gallistel CR: The Child’s Understanding of Number.Harvard University Press; 1978.

10. Butterworth B: The Mathematical Brain. Macmillan; 1993.

11. Spelke ES, Breinlinger K, Macomber J, Jacobson K: Origins ofknowledge. Psychol Rev 1992, 99:605-632.

12. Dehaene S: The Number Sense: How the Mind CreatesMathematics Oxford University Press; 1997.

13. Feigenson L, Carey S, Hauser M: The representationsunderlying infants’ choice of more: object files versus analogmagnitudes. Psychol Sci 2002, 13:150-156.

14. Dehaene S, Spelke E, Pinel S, Stanescu R, Tsivkin S: Sources ofmathematical thinking: behavioral and brain-imagingevidence. Science 1999, 284:970-974.

15. Nieder A, Freedman DJ, Miller EK: Representation of thequantity of visual items in the primate prefrontal cortex.Science 2002, 297:1708-1711.



16. Dehaene S, Dehaene-Lambertz G, Cohen L: Abstractrepresentations of numbers in the animal and human brain.Trends in Neurosci 1998, 21:355-361.

17. Boysen ST, Hallberg KI: Primate numerical competence:contributions toward understanding nonhuman cognition.Cogn Sci 2000, 24:423-443.

18. Brannon EM, Terrace HS: Ordering of the numerosities 1 to 9 bymonkeys. Science 1998, 282:746-749.

19. Hauser MD, Carey S, Hauser LB: Spontaneous numberrepresentation in semi-free-ranging rhesus monkeys. Proc RSoc Lond B 2000, 267:829-833.

20. Cantlon JF, Brannon EM: Basic math in monkeys and collegestudents. PLoS Biol 2007, 5:e328.

21. Hauser MD, Tsao F, Garcia P, Spelke ES: Evolutionaryfoundations of number: spontaneous representation ofnumerical magnitudes by cotton-top. Proc R Soc Lond B 2003,270:1441-1446.

22.�

Irie-Sugimoto N, Kobayashi T, Sato T, Hasegawa T: Relativequantity judgment by Asian elephants (Elephas maximus).Anim Cogn 2009, 12:193-199.

This study investigated whether Asian elephants can make relativequantity judgment, a dichotomous judgment of unequal quantitiesordered in magnitude. Elephants were simultaneously or sequentiallyshown two baskets with differing quantities of bait (up to six items).The elephants succeeded in choosing the larger one. The elephants didnot exhibit disparity or magnitude effects.

23. Pepperberg IM, Gordon JD: Number comprehension by a greyparrot (Psittacus erithacus), including a zero-like concept. JComp Psychol 2005, 119:197-209.

24. Brannon EM, Wusthoff CJ, Gallistel CR, Gibbon J: Numericalsubtraction in the pigeon: evidence for a linear subjectivenumber scale. Psychol Sci 2001, 12:238-243.

25. Uller C, Jaeger R, Guidry G, Martin C: Salamanders (Plethodoncinereus) go for more: rudiments of number in an amphibian.Anim Cogn 2003, 6:105-112.

26.�

Gross HJ, Pahl M, Si A, Zhu H, Tautz J, Zhang S: Number-basedvisual generalisation in the honeybee. PLoS ONE 2009, 4:e4263.

Using a y-maze, the authors found that bees not only can differentiatebetween patterns containing two and three elements but also can use thisprior knowledge to differentiate three from four, without any additionaltraining. This is the first report of number-based visual generalization byan invertebrate.

27. Murofushi K: Numerical matching behavior by a chimpanzee(Pan troglodytes): subitizing and analogue magnitudeestimation. Jpn Psychol Res 1997, 39:140-153.

28. Tomonaga M, Matsuzawa T: Enumeration of briefly presenteditems by the chimpanzee (Pan troglodytes) and humans (Homosapiens). Anim Learn Behav 2002, 30:143-157.

29. Tomonaga M: Relative numerosity discrimination bychimpanzees (Pan troglodytes): evidence for approximatenumerical representations. Anim Cogn 2008, 11:43-57.

30. Tomonaga M, Matsuzawa T: Sequential responding to Arabicnumerals with wild cards by the chimpanzee (Pantroglodytes). Anim Cogn 2000, 3:1-11.

31. Biro D, Matsuzawa T: Numerical ordering in a chimpanzee (Pantroglodytes): planning, executing, and monitoring. J CompPsychol 1999, 113:178-185.

32. Premack D: Human and animal cognition: continuity anddiscontinuity. Proc Natl Acad Sci U S A 2007, 104:13861-13867.


33. Kawai N, Matsuzawa T: Numerical memory span in achimpanzee. Nature 2000, 403:39-40.

34.�

Kano F, Tomonaga M: How chimpanzees look at pictures: acomparative eye-tracking study. Proc R Soc B 2009 doi:10.1098/rspb.2008.1811.

The authors present the first examination of eye tracking in chimpan-zees. The eye movements of chimpanzees as they viewed naturalisticpictures were recorded. The results were compared with those fromhumans. Although the two species shared many common features,chimpanzees shifted the fixation location more quickly and morebroadly than humans.

35. Matsuzawa T: Q and A Tetsuro Matsuzawa. Curr Biol 2009,19:R310-R312.

36. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T:Imitation in neonatal chimpanzees (Pan troglodytes). Dev Sci2004, 7:437-442.

37. Myowa-Yamakoshi M, Matsuzawa T: Factors influencingimitation of manipulatory actions in chimpanzees. J CompPsychol 1999, 113:128-136.

38. Hashiya K, Kojima S: Acquisition of auditory-visual intermodalmatching-to-sample by a chimpanzee (Pan troglodytes):comparison with visual-visual intramodal matching.Anim Cogn 2001, 4:231-239.

39. Kojima T: Generalization between productive use andreceptive discrimination of names in an artificial visuallanguage by a chimpanzee. Int J Primatol 1984, 5:161-182.

40.�

Matsuzawa T: Comparative cognitive development. Dev Sci2007, 10:97-103.

Human infants right after the birth take the stable supine posture. Thisenhances the face-to-face visual communication, vocal exchange, andalso the bimanual object manipulation because the hands are free fromclinging to the mothers. The paper pointed out the significance of stablesupine posture as the important clue for hominid evolution.

41. Hayashi M: A new notation system of object manipulation inthe nesting-cup task for chimpanzees and humans.Cortex 2007, 43:308-318.

42. Hayashi M, Matsuzawa T: Cognitive development in objectmanipulation by infant chimpanzees. Anim Cogn 2003,6:225-233.

43.�

Poti P, Hayashi M, Matsuzawa T: Spatial construction skills ofchimpanzees (Pan troglodytes) and young human children(Homo sapiens sapiens). Dev Sci 2009 doi: 10.1111/j.1467-7687.2008.00797.x. Published online.

The authors have assessed spatial construction skills in chimpanzees andyoung children with a block modeling task. Chimpanzees do not developin the direction of constructing in two dimensions as human children dostarting from the age of 30 months. The pattern of development ofconstruction skills indicates that spatial analysis and spatial representa-tion are partially different in the two species.

44. Matsuzawa T: Chimpanzee intelligence in nature and incaptivity: isomorphism of symbol use and tool use. In GreatApe Societies. Edited by McGrew W, Marchant L, Nishida T.Cambridge University Press; 1996:196-209.

45. Poti P: Chimpanzees’ constructional praxis (Pan paniscus, Pantroglodytes). Primates 2005, 46:103-113.

46. Hayashi M: Stacking of blocks in chimpanzees. Anim Cogn2007, 10:89-103.

47. Crast J, Fragaszy D, Hayashi M, Matsuzawa T: Dynamic in-handmovements in adult and young juvenile chimpanzees.J Phys Anthropol 2009, 138:274-285.


http://dx.doi.org/10.1098/rspb.2008.1811

http://dx.doi.org/10.1098/rspb.2008.1811

http://dx.doi.org/10.1111/j.1467-7687.2008.00797.x

http://dx.doi.org/10.1111/j.1467-7687.2008.00797.x

symbolic representation of number in chimpanzees tetsuro...

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