ORIGINAL ARTICLE
Association of food location with biological cues in
the macaque monkey
Hidetoshi Ishibashi,1 Mari Kumashiro1 and Atsushi Iriki
Section of Cognitive Neurobiology, Tokyo Medical and Dental University, Tokyo, Japan(Received for publication on February 2, 2004)

Abstract. Many animal species including humans are endowed with the ability to use biological cues
and can extract information by observing other individuals. This study explored whether the macaquemonkey could use biological cue to ﬁnd a hidden target. When the experimenter hid food in one handand crossed and uncrossed hands quickly, the monkey had no difﬁculty in ﬁnding the food and correctly
reached for the baited hand. However, when the food was hidden in one of two cups and the cups were
shufﬂed, the monkey could correctly select the baited cup only at an equal level of luck. These results
indicate that the macaque monkey could associate the location of food with a biological cue better thana non-biological cue and keep it in memory when the target was unseen. (Keio J Med 53 (2): 98–102,June 2004)
Key words: animate, inanimate, monkey, object permanence

tomography study with human subjects examined thebrain activation upon observing objects being grasped
by an experimenter in an experimental condition, andobserving static scenes of the experimenter holding thesame objects in a control condition.3 Subtracting theactivation produced by the control condition from thatof the grasping condition yielded a portion of the STS
region of the brain, suggesting that activation of theSTS region was due to analysis of meaningful handmovement.
Macaque monkeys also have a neural system thathas been implicated in the ability of the perceptual
processing of the visual appearance of another individual’s face and body (reviewed by).4 The cerebral cortex
in the anterior section of the STS has neurons that
respond preferentially to movements of the hand, i.e.,such cells respond as monkeys view an investigator
making various types of hand movements.5 Only one
neuron thus far in the STS that responds to arm
movements has been found to distinguish between themovements of the left and right arms. The neuron
responded to movements of the left arm to the left but
did not respond to the right arm reaching in the same
direction (to the left).6 With regard to the neural representation of the hand movements, there is another

Introduction
For most animal species, the visual perception ofmotion is a particularly crucial source of sensory input.
The ability to pick out the motion of biological forms
from other types of motion in the natural environmentis essential to predict the actions of other individuals.
An animal’s survival depends on its ability to identify
the movements of prey, predators, and mates, and topredict their future actions, the consequences of which
differ radically and could in some cases be fatal. As
social animals, humans behave largely on the basisof their interpretations of and predictions about theactions of others. The superior perception in humans of
biological motion without interference from shape wasﬁrst reported by Johansson.1 He attached light sources
to an actor’s joints and recorded their movements ina dark environment. Naive participants, rapidly andeffortlessly, recognized the moving dots as a person
walking. A positron emission tomography study showed
activation of the brain regions in the intraparietal sulcus
and in the caudal part of the superior temporal sulcus(STS) when human subjects viewed a point light displayof the act of reaching towards a glass, picking it up, andbringing it to the mouth.2 Another positron emission

Reprint requests to: Dr. Hidetoshi Ishibashi, National Institute of Neuroscience, NCNP, Department of Animal Models for Human Disease,4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan
Present afﬁliation: 1National Institute of Neuroscience, NCNP, Department of Animal Models for Human Disease, Tokyo, Japan98

Keio J Med 2004; 53 (2): 98–10299(a)

Methods(b)

Procedure
To see whether the subject could make use of a biological or animate cue better than a non-biological orinanimate cue, we used human hands as the biologicalcue and plastic cups as the non-biological cue. Each test
session consisted of ten trials of the same condition
described below. Conditions were intermingled on asession by session basis, and the order was assigned
randomly. Where applicable, all choices, such as thestarting and ﬁnal hand, cup, or food position, and thenumber of times the hands were passed over eachother, were pre-determined randomly.

5025012>2
Times Crossing

012>2
Times Crossing

100
Percentage Persistent

We used a 5.7 kg male Japanese monkey (Macacafuscata). He was housed in an isolation cage and wasallowed water and monkey chow ad libitum. The Animal Care and Use Committee of Tokyo Medical andDental University approved this study, and all husbandry and experimental procedures were in accordance with the Guidelines for Animal Experimentation
at Tokyo Medical and Dental University.

7550250(c)100Percentage Persistent

All experiments used for Fig. 1 were conducted in anexperimental room outside of the room in which thehousing cage was kept. The subject was well acclimatedto the experimental room, sitting in a primate chair, andshowed no hesitation to extend his arms to get foodfrom the experimenter. We set the table to the height ofthe monkey’s waist. An additional test was conductedin a corridor. The subject was allowed to sit on the ﬂoor
until the experimenter started the test. The test wasconducted as in the experimental room except thattable was not used in this test. Pictures used in Fig. 2
were taken under this test condition.

750Subject

Experimental setup

100

Percentage Correct

type of neurons called mirror neurons. Mirror neurons,
found in the premotor cortex,7–8 and the parietal cortex,9 become active when the subject moves their handor mouth and when the subject sees someone else doing
the same movement. Their activities do not depend on
which hand the performer has used for that action. It
is not well known, however, how well the macaquemonkey can take advantage of biological or animatecue and make use of them in its behavior, and whether
the monkey could use the information on which hand of
the performer is used. This study was thus designed tofocus on these aspects.

75502500255075100
Percentage Correct

Fig. 1 Successful Use of Biological Cue. (a) The correct rate in eachcondition. It is higher when the food was hidden in the experimenter’s
hands than in the cups. (b) The percentage of the persistent trial. (c)The correlation between the correctness and the persistency. Filled
circles: hands condition. Shaded circles: cups-hands condition. Opencircles: cups condition.

Straight hands condition: an experimenter showed
the subject both hands on one of which was placed apiece of food in the full view of the subject, closed bothhands, and extended both hands toward the subject.
Hands crossed once condition: an experimenter placed apiece of food on one hand, closed both hands, crossed
arms once, and extended both hands toward the subject. Hands crossed twice condition: similar to the pre-

100

Ishibashi H, et al: Biological cue utilization in monkeyFig. 2 Monkey’s Typical Behaviour in the Choice Test. (a) Non-conﬁdent reaching after cup shufﬂing. After observing the shufﬂing of thecups, the monkey stood up and tried to look into the cups. (b) Conﬁdent reaching after hand shufﬂing. After observing the shufﬂing of thehands, the monkey reached out to the baited hand without standing.

vious condition except that the experimenter returned
the crossed arms to their original location. Shufﬂed
hands condition: the same as in the previous condition
except that the experimenter crossed and uncrossed
their arms twice or more. The ﬁnal status, whether theywould be crossed or not, was pre-determined randomly.
In all conditions where the food was held in the experimenter’s hand, the subject solved the task by correctly
selecting the hand which held the food at the beginningof the trial.
Straight cups condition: an experimenter placed apiece of food on a table in the full view of the subject,placed a green cup and a red cup upside down to coverand hide the food, released cups, withdrew both hands
for about 10 cm. The experimenter, then, moved thecups, each cup with one hand, toward the subject. Cups
crossed once condition: an experimenter placed cups
to hide the food on the table, moved them around toexchange their locations, released the cups, uncrossed
arms, and pushed both cups toward the subject. Cups
crossed twice condition: the same as in the previous
condition except that the exchange of the cup locations
was made twice. Shufﬂed Cups condition: the same asin the previous condition except that the cup locations
were exchanged 3 or more times. In these conditions,the locations of the experimenter’s hands when presented did not give any cue and the subject solved thetask by correctly selecting the cup which covered thefood at the beginning of the trial.

Straight cups-hands condition: an experimenter
placed a piece of food in one of two cups that wereplaced on the table in the full view of the subject,picked up the cups, and moved the cups straight toward
the subject. Cups-hands crossed once condition: thesame as in the previous condition except that after
picking up the cups the experimenter crossed arms andmoved the crossed arms toward the subject. Cups-hands
crossed twice condition: the same as in previous condition except that the experimenter uncrossed arms
before moving the cups to the subject. Shufﬂed Cupshands condition: the same as in the previous condition
except that the experimenter crossed and uncrossed
arms 3 or more time before extending them to the subject. In these conditions, the subject solved the task bycorrectly selecting either which hand held or which cup
contained the food at the beginning of the trial.
For all shufﬂe conditions, the experimenter quickly
moved hands and arms to prevent the subject fromfollowing the motion. The times taken to hold the foodin the hand, to hide the food with the cup, and in thepresentation of the hands, cups, or cups with hands
were approximately matched across the corresponding
conditions, i.e., 1.5 sec for straight, 2 sec for crossed
once, 2.5 sec for crossed twice, and 4 sec for the shufﬂed
condition.
Analysis
The trials in which the subject did not reach out tothe hands or cups were omitted from the analysis. We

Keio J Med 2004; 53 (2): 98–102

calculated the persistent rate as the rate of the trials inwhich the subject responded to the same side as in theprevious trial. We used this parameter as a measure of
the subject’s status, whether he would be attempting
to solve or giving up the trial. Since monkeys typically
respond successively to the same side regardless of thestimulus if they cannot use any cues to solve the choicetask, we expect high rate of persistency under suchconditions.
Results
The response in each trial did not seem to differ
among the conditions. In some trials throughout allconditions, the subject looked somewhere else duringthe trial and did not reach out to the hands or cups,
especially when the correct rate was low. In othertrials, the subject kept looking at the experimenter orcups, although he did not seem to gaze at a particulartarget.
In all hand conditions where the food was hidden in
the experimenter’s hands, the monkey chose the baitedhand consistently. The correct rate was higher than theequal chance level, i.e. 50%, even when hands were
shufﬂed (90%, 36/40) (Fig. 1a). Consistent with thegood performance, the rate of trials showing persistent
response was near the chance level (Fig. 1b). In thestraight-cups condition, the monkey quickly reached forthe cup from the ﬁrst trial, and the correct rate was 82%(49/60) that was higher than the chance level, indicatingthat the monkey was not afraid of the cups and that heknew that hidden food should lie under the cup placed
over the food pellet at the beginning of each trial.
However, the correct rate dropped as the number of thecup relocations increased: 69% (97/140) when crossed
once, 54% (27/50) when crossed twice, and 50% (25/50)
when shufﬂed. Consistent with the deterioration inperformance, the persistent response increased. In cuphand conditions, the performance was in between thehand condition and cup condition.
Across all conditions, the percentage of the persistency trial was inversely correlated with the correct rate
(Fig. 1c), suggesting that the subject chose the sameside as in the previous trial when he did not know whichhand or cup was baited, and thus strengthens the conclusion that the monkey could correctly choose whichhand was baited but could not make a correct choice
when the food was hidden in the cup.
Making use of biological cues was observed also inthe condition where the monkey could choose under amore natural test condition. The monkey stood up as
if he were trying to see the inside of the cups in thecups condition (Fig. 2a) but remained sitting in thehand condition (Fig. 2b) and reached out for the baitedhand.

101

Discussion
In the cups-hands conditions, the subject could solve
the task by retrieving the memory of either which hand
had held or which cup had contained the food in thebeginning of the trial. Contrary to our expectation thatthe performance would be better than hands alone andcups alone conditions, it was worse than hands alone
conditions. Two simple possible mechanisms are thathands hidden by the cups gave less visual information
than hands alone, and that cups interfered the information of hands as a cue. Another mechanism, and one
we think quite probable, is that the scene of the actor’sholding food in the palm has more biological and perceptual meaning than the scene of the actor’s placing
food into the cup – the monkey could no longer associate the food location with the hand in the latter
case, since the human and monkey neural systems areendowed with processing meaningful motion, e.g., someneurons in the STS respond when the subject observes
an actor’s hand manipulating an object but not whenobserving a hand and an object moving but spatiallyseparate.5
The experimenter quickly moved hands and arms inall shufﬂe conditions to prevent the subject from following the motion. There still is a possibility that under
the shufﬂe conditions the subject could visually follow
the motion of the hand better than that of the cup. Although we could not estimate the relative contributionof the memory and visual motion following, it could not
be solely attributed to the latter factor since the performance differed between the biological hands condition and the non-biological cups condition even in thestraight conditions. Thus, there must be at least some
contribution from the nature of monkeys to associate
the food location with the right or left hand and to keep
the association in memory.
When the subject’s attention was diverted somewhere else during the trial, sometimes by a momentary
environmental noise, he did not typically reach out tothe hands or cups. This happened throughout all conditions, suggesting that the memory of the food location
with the aid of the biological cue was not retained afteran external disturbance and was limited within the capacity of the working memory.
This study offers the ﬁrst convincing evidence of theuse of biological cues in monkeys to relate to the location of food and keep it in memory. Our monkey associated the location of the food with the experimenter’s
hand whether it was the right or left, and kept it inmemory to solve the behavioural task. We used only
one monkey in the present study, and whether theﬁndings in our single animal could be generalized tothis animal species thus remains to be examined withlarger number of animals. We can however conclude at

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Ishibashi H, et al: Biological cue utilization in monkey

least that the above behavioural characteristics do exist
in this animal species.
Acknowledgments: This study was supported by a Grant-in-aid andby Support of Young Researchers With a Term from Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan.

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