Accepted: 27 December 2016

DOI: 10.1111/jmp.12251

ORIGINAL ARTICLE

Pattern of novel object exploration in cynomolgus monkey

Macaca fascicularis

Hong Zou1,2 | Ming Liu2 | Yi Luan2 | Qinglian Xie2 | Zhiheng Cheng2 | 

Guoping Zhao1,2,* | Meilei Jin2,* | Ning Guo3,4,* | Gang Jason Jin4,* | Lei Yu5,*,#

1
Department of Microbiology and Microbial
Engineering, School of Life Sciences, Fudan
University, Shanghai, China
2
Shanghai Institutes for Biological
Sciences, Chinese Academy of Sciences,
Shanghai, China
3
Shanghai University of Traditional Chinese
Medicine, Shanghai, China
4
ShanghaiBio Corporation, Shanghai, China
5
Department of Genetics and Center
of Alcohol Studies, Rutgers University,
Piscataway, NJ, USA
#
Sent inquiries to
Lei Yu, Department of Genetics and Center
of Alcohol Studies, Rutgers University,
Piscataway, NJ, USA.
Email: yu@biology.rutgers.edu
Funding information
ShanghaiBio Corporation.
Abstract
Background: Primates exhibit substantial capacity for behavioral innovation, expand-
ing the diversity of their behavioral repertoires, and benefiting both individual survival
and species development in evolution. Novel object exploration is an integral part of
behavioral innovation. Thus, qualitative and quantitative analysis of novel object ex-
ploration helps to better understand behavioral innovation.
Methods: To study the pattern of novel object exploration, two different sized balls
were sequentially introduced to singly caged cynomolgus monkeys. Two aspects of
monkeys’ behaviors were analyzed: the types of motor activities in toy playing and
whether there is an orderly sequence of such motor activities during novelty
exploration.
Results: Four types of behavioral activities (oral contact, gross and fine forelimb motor,
and hind limb motor) followed a pattern: first forelimb gross motor and oral contact,
followed by forelimb fine motor and hind limb activities. Oral contact appeared to be
an important behavior in monkeys’ repertoire of novelty exploratory behaviors, both
as an early appearing activity, and showing a consistent pattern of high cumulative
time for two different novel objects.
Conclusions: These results provide a profile of novel object exploratory behaviors in
cynomolgus monkeys, contributing to a better understanding of this aspect of behav-
ioral innovation.

KEYWORDS
cynomolgus monkey, non-human primate, novel object exploration

1 |  INTRODUCTION
Compared to non-­primates, primates exhibit substantial capacity for
behavioral innovation,1,2 thus expanding the diversity of their be-
havioral repertoires, to the benefit of individual survival as well as
species development in biological evolution. Behavioral innovation
is the development of novel behavioral patterns, such as in forag-
ing and mate-­seeking, and reflects individual primates’ positions in
*Co-corresponding authors.
their respective social ranking.3 Novel object exploration is an inte-
gral part of behavioral innovation, likely to aid in food source inves-
tigation, danger assessment, stress response, and adaptation to new
environments. Successful patterns of novelty exploration may play an
evolutionary role through social learning and transmission in primate
populations.4
Non-­human primates have been used to study various behaviors,
including novelty exploration behavior. When exploring novel objects,
two issues are relevant: types of behavioral activities displayed and
the sequence of such activities.

J Med Primatol. 2017;46:19–24. wileyonlinelibrary.com/journal/jmp © 2017 John Wiley & Sons A/S. |  19
Published by John Wiley & Sons Ltd
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20       ZOU et al.
When encountering a novel object, mammals may be attracted to
it. This tendency toward novelty has been well demonstrated in differ-
ent species of mammals, including rats,5 gerbils,6 marmosets,7 and ba-
boons.8,9 In terms of the types of behavioral activities displayed by the
mammals, visual observation, forelimb contact/exploration, and oral
8-10
contact have all been reported. However, it is not clear whether
monkeys use other body parts, such as hind limbs or buttocks, as part
of their behavioral repertoire during novel object exploration.
In studies of motor skill learning, rodents do not display a strong
tendency for a patterned sequence of activities, as they often per-
form motor movements in a seemingly random fashion, without any
discernable order.11,12 Non-­human primates, on the other hand, are
known to acquire an orderly sequence of discrete motor movements,
13,14
as shown in hand grasping activities. However, it is not well un-
derstood whether an orderly sequence of motor activities takes place
in novelty exploration.
Previous studies have used several methods to analyze reaction
to novel objects in non-­human primates. To compare the novelty-­
seeking trait of stump-­tailed macaques (Macaca arctoides) and spider
monkeys (Ateles geoffroyi), these two species were kept in groups
separately, and the risk-­taking index (facing a hazardous object) and
the curiosity index (facing a nonhazardous object) were assessed by
categorizing behaviors in four levels depending on the distance be-
tween the subjects and the objects and the frequency of the objects
being manipulated.15,16 By changing environmental stressors, free-­
choice novelty-­seeking behavior was assessed in vervet by coding the
novelty-­seeking score according to latency and times of the animal ap-
proaching the novel objects.17 Baboons kept in new cages individually
were exposed to a certain type of novel object, and the frequency and
duration of object contact were investigated, to assess their reaction
to changes in spatial and shape variation of novel objects.8 Baboons in
social groups were exposed to daily changes of novel objects in their
home cages, and their reactions were analyzed for both exploratory
behaviors (looking at and sniffing objects) and manipulative behav-
ior (touching, grasping, and transporting objects).9 Rhesus monkeys
of different ages were kept in individual home cages, and the types
of behaviors directed toward simple toys were studied.18 In terms of
the method for analyzing novelty exploration in non-­human primates,
these studies focused on rating animal behavior either by the extent
of their approaching/manipulating novel objects,15-17 or by the fre-
quency and duration of novel object contact,8 with some reference to
the specific types of exploratory behavior.9,18
In this study, we focused on the specific types of exploratory be-
haviors, and on whether there is an orderly sequence of such motor
activities during novelty exploration, using a paradigm of two different
sized balls as novel objects and introducing them sequentially to sin-
gly caged cynomolgus monkeys. Our rationale is based on the follow-
ing considerations. Firstly, novelty exploration involves different, and
sometimes complex, behaviors. By separating and categorizing spe-
cific types of behaviors, it helps pave the way for systematic and quan-
titative analyses. Secondly, various behaviors occur at different times
during an animal’s object exploration, and some behaviors may even
overlap. The timing and the sequence of these behaviors may reflect
the underlying biological functions,19 the understanding of which
would benefit from a better description of these behaviors. Thirdly,
the outcome from both qualitative and quantitative analyses of spe-
cific types of behaviors can serve as a frame of reference, with which
the results from further studies can be compared and contrasted for
investigating different types of behaviors. With this rationale in mind,
we report here the findings from the study.
2 | MATERIALS AND METHODS
2.1 | Animals and study site
This study used 17 male cynomolgus monkeys (Macaca fascicularis)
between 3 and 4 years old, with average body weight of 3.4±0.1 kg
(mean±SEM). All animals were supplied by Hainan Jingang Laboratory
Animal Co. Ltd., an AAALAC-­
accredited facility located in Hainan
Province in southern China. The local climate in Hainan Province
is similar to that of the natural habitat of cynomolgus monkeys in
the neighboring southeastern Asia area. All experimental protocols
were approved by the Institutional Animal Care and Use Committee
(IACUC) at Hainan Jingang Laboratory Animal Co. Ltd., adhered to the
guidelines of the Committee for Research and Ethical Issues of IASP,
and were consistent with the National Institutes of Health Guide for
the Care and Use of Laboratory Animals. Two months before the
study, monkeys were transferred from group housing to individual
cages (80 × 60 × 70 cm, LxWxH). There were two rows of cages fac-
ing each other in the laboratory, with solid dividers between neighbor-
ing cages; thus, the monkeys could not see their immediate neighbors,
but had visual contact with the monkeys in the opposite row in the
room. Animals also could reach out of the cage and had limb contact
with the neighboring monkeys. The room was well ventilated. Room
lighting was supplied mainly by natural lighting, with some fluorescent
lighting to facilitate nighttime video recording of behavior. Monkeys
were served three meals a day with regular monkey chow, plus sea-
sonal fruits in the afternoon. Drinking water was provided ad libitum.
Meal service, room cleaning, and animal care were performed by the
technicians at Hainan Jingang Laboratory Animal Co. Ltd., with the
supervision of certified veterinarians.
2.2 | Behavioral monitoring
The behavioral experiments were conducted in the laboratories at
Hainan Jingang Laboratory Animal Co. Ltd, from 2009 to 2010. A be-
havioral monitoring system was used, which consisted of digital cam-
eras, digital video recorders, and computers running video monitoring
software. Digital cameras were mounted both in front of and on top
of monkey cages, so that both frontal view and top view of monkey
behaviors were recorded.
2.3 | Basketball and tennis ball playing
Monkey’s basketball-­playing behavior was recorded when a toy bas-
ketball (175 mm in diameter, surface made of rubbery plastic material
ZOU et al.
F I G U R E   1   Sequence of behaviors upon novel object introduction.
Time of the first appearance for each behavior is plotted for the
basketball (A) or the tennis ball (B). Data are shown as mean±SEM
(n=17 for the basketball; n=16 for the tennis ball). *, significant
difference between the two behaviors (P<.05)
with yellow/purple stripes and black-­line marking, fully inflated with
air) was placed in a monkey’s cage. Each toy basketball was used only
for one monkey.
Seventeen hours after the basketball was introduced, a tennis ball
(regular sports grade, 67-­mm in diameter, with green velvet surface)
was placed in a monkey’s cage as a new toy. Each tennis ball was used
only for one monkey.
For both basketball and tennis ball playing, the following proce-
dure was used for behavioral analysis. Video recording was analyzed of-
fline. To determine the first-­appearance time of various behaviors, the
first 30 minutes of video footage upon novel object introduction was
examined, and the time of the first appearance of each behavior was
noted. If a particular behavior was not observed in an animal during
the 30-­minute video, the cutoff time of 30 minutes was assigned as
the value. To determine the cumulative time of object exploration,
1 hour of video footage was divided into two consecutive 30-­minute
blocks after the ball was introduced. For the first 30-­minute block, be-
haviors were analyzed for the first 2 minutes for every 5-­minute time
segment. For the second 30-­minute block, behaviors were analyzed
for the first 2 minutes for every 10-­minute time segment. The follow-
ing criteria and behavioral categories were used:
|
      21
1. Oral contact: when a monkey contacts the ball with any part
of its mouth, including lips and teeth.
2. Forelimb (fine motor): various fine motor activities using the mon-
key’s forelimbs, such as peeling off the label on the ball, or attempt-
ing to pull out the air valve of the ball.
3. Forelimb (gross motor): various gross motor activities using the
monkey’s forelimbs, such as holding up the ball, rolling the ball
against the cage wall, patting the ball, or pushing the ball away.
4. Hind limb: using hind limbs, such as touching/holding/pushing the
ball, or attempting to stand on the ball.
5. Overall ball playing: cumulative time when a monkey touches the
ball with any part of its body (except its tail). This behavior was
scored independently; thus, it was not an arithmetic sum of the
other behavior scores.
2.4 | Statistics
For the time of the first appearance of various behaviors, data are
expressed as mean±SEM. To compare the first-­appearance time of
various behaviors upon basketball introduction, one-­way ANOVA
with Tukey’s test was used for multiple comparisons. To compare the
first-­appearance time of various behaviors upon tennis ball introduc-
tion, because of unequal variance (significantly different), Kruskal-­
Wallis test was used. Dunn’s test was used for multiple comparison
test. To compare the mean duration times for oral contact, forelimb
gross motor contact, forelimb fine motor contact, and hind limb con-
tact, one-­way ANOVA with Tukey’s test was used for basketball and
Kruskal-­Wallis with Dunn’s test was used for tennis ball. T test was
used to compare cumulative play time (for each of the four play types)
between basketball and tennis ball.
3 | RESULTS
3.1 | Behaviors during basketball and tennis ball
playing
When a toy basketball was introduced into a monkey’s cage, various
ball-­
playing behaviors were observed. It was observed that mon-
keys tended to use their forelimb first for ball manipulation (gross
motor), followed by oral contact (Figure 1A). Later on, monkeys dis-
played forelimb fine motor and hind limb activities, with similar first-­
appearance time values (Figure 1A). Statistical analysis by one-­way
ANOVA showed significant differences among the time of the first
appearance for these four behaviors (F3,67=4.357, P<.05). Multiple
comparison analysis with Tukey’s test showed that the time of the
first appearance of both the forelimb fine motor and the hind limb
activities was significantly later than that of forelimb gross motor ac-
tivity (for forelimb fine motor, q=4.206, P<.05; for hind limb, q=4.162,
P<.05).
When a tennis ball was introduced to the cage as another novel
object, monkeys displayed the same four behaviors, with a similar
sequence of appearance: first was forelimb gross motor, followed by
 |
22       ZOU et al.
F I G U R E   2   Mean cumulative time of behaviors for basketball and
tennis ball playing. The cumulative time of object exploration for each
behavior was determined from video footage for each animal for the
basketball (A) or the tennis ball (B). Data are shown as the mean±SEM
(n=17 for the basketball; n=16 for the tennis ball). *, significant
difference between the two behaviors (P<.05)
oral contact, and then forelimb fine motor and hind limb activities
(Figure 1B). Kruskal-­Wallis test showed a significant difference among
the time of the first appearance for these four behaviors (P<.05).
Multiple comparison analysis by Dunn’s test showed that the time of
first appearance of both the forelimb fine motor and the hind limb ac-
tivities was significantly later than either that of forelimb gross motor
activity (P<.05) or that of oral contact (P<.05).
3.2 | Cumulative time for individual behaviors during
basketball and tennis ball playing
To compare individual behaviors during basketball and tennis ball play-
ing, the cumulative time for each of the four behaviors was measured.
For basketball (Figure 2A), statistical analysis by one-­way ANOVA
showed significant difference (F3,67=8.505, P<.05). Monkeys spent sig-
nificantly more time (P<.05) for oral contact (89.9±16.0 seconds) and
forelimb fine motor contact (88.8±16.3 seconds), compared to fore-
limb gross motor contact (18.9±9.1 seconds) and hind limb contact
(23.9±11.0 seconds). The overall basketball-­playing activities were
measured separately, showing 408.6±48.7 seconds. For tennis ball
(Figure 2B), Kruskal-­Wallis test showed a significant difference for cu-
mulative time of these behaviors (P<.05). Monkeys spent significantly
more time (P<.05) for forelimb gross motor contact (342.8±39.1 sec-
onds) than forelimb fine motor contact (56.7±14.3 seconds) or hind
limb contact (106.2±26.4 seconds). They also spent significantly more
time (P<.05) for oral contact (157.9±20.7 seconds) than forelimb fine
motor contact. The overall tennis ball-­playing activities were meas-
ured separately, showing 479.7±59.5 seconds. Comparing cumula-
tive play time (for each of the four play types) between basketball
and tennis ball, monkeys spent significantly more time when playing
tennis ball on oral contact (P=.0134), forelimb gross motor contact
(P<.0001), and hind limb (P=.0093) than playing basketball. However,
there is no significant difference for overall ball-­playing time between
object types (P=.36).
4 | DISCUSSION
In the present study, we performed quantitative analysis of novel
object-­playing behaviors in cynomolgus monkey Macaca fascicularis,
as a way to characterize monkeys’ behavioral pattern in exploring
novel objects. Novelty exploration opportunities for monkeys were
created by first introducing a toy basketball, and later a tennis ball, to
singly caged monkeys. By analyzing the video recording, a number of
characteristics were noted:
When a monkey encountered novel objects, four types of be-
havioral activities were observed: oral contact, forelimb motor
(both gross and fine), and hind limb motor. The process of novel
object exploration appeared to follow a sequence: forelimb gross
motor activities and oral contact appeared first, followed by fore-
limb fine motor and hind limb activities. This sequence of behavioral
activities during novelty exploration was evident when monkeys
first encountered the basketball (Figure 1A). When the tennis ball
was subsequently introduced, monkeys followed a similar pattern
(Figure 1B). It is worth noting that the first appearance of all four
behaviors occurred earlier for the tennis ball than for the basketball.
It is possible that the small size of a tennis ball compared with the
larger size of a toy basketball represented a less threatening situ-
ation for monkeys, resulting in monkeys’ prompt physical engage-
ment with the tennis ball. Also, as the monkeys had already played
with the first novel object, the toy basketball, a sense of familiarity
with a novel object may have contributed to the shorter lapsed time
between novel object introduction and a monkey’s physical contact
with the novel object.
Studies of non-­human primates have shown that discrete motor
movements are often sequenced in an orderly fashion; that is, cer-
tain motor actions take place first, followed by subsequent motor ac-
tions, demonstrating the stability of a sequential pattern. Thus, in hand
grasping activities, motor movements are shown to follow a specific
sequence.13,14 This pattern of sequential order in non-­human primates
parallels that in humans—infants follow a sequence of coordinated
ZOU et al.
visual and motor activities when reaching for objects.20 Our work con-
firms this general activity pattern in cynomolgus monkeys.
It should be noted that an orderly motor sequence does not
appear to be present in rodents, as rodents often perform motor
movements in a seemingly random fashion, without any discernable
11,12,21,22
order. In primates, correct order of motor sequence appears
to be the norm.14,23,24 Specifically, the orderly appearance of several
submovements becomes stable over time, and these primitives even-
tually are integrated into a whole, more complex, skilled movement
for a purpose.25-27 Human infants have also been shown to display
the purposeful order of motor activities and to integrate these sub-
movements into a whole movement to achieve a simple purpose.20
These findings indicate that in both non-­human primates and human
infants, the correct ordering of submovements and the integration into
a whole movement are to achieve a simple purpose, such as getting
an object. Therefore, it can be considered that an orderly sequence
of submovements is a necessity to achieving an actionable purpose.
What we have shown in this study is that, when encountering a
large playing object such as a basketball, monkeys employ discrete
motor behaviors. These behaviors are not only discernable from one
another, but also they appear to follow an orderly sequence. In other
words, distinct motor behaviors are used by non-­human primates in an
orderly nature and in a purposeful manner.
Oral contact appears to be an important behavior in monkeys’
repertoire of novelty exploratory behaviors. It appeared early when
a monkey encountered a ball. In fact, there was no significant differ-
ence between the first appearance for oral contact and forelimb gross
motor (Figure 1A,B), indicating that a monkey initiates physical explo-
ration of a novel object with forelimb gross motor and oral contact be-
haviors. Additionally, oral contact showed a consistent pattern of high
cumulative time, for both basketball and tennis ball (Figure 2), whereas
forelimb gross motor, which was also an early activity, showed a rather
low level of cumulative time for basketball (Figure 2A). Taken together,
these results suggest that oral contact may serve as a primary sensory
input in monkeys’ novelty exploration.
This is consistent with the pattern of novelty exploration in
human and other non-­human primates. When human infants see a
novel object, their first physical action toward it is to engage in oral
contact—attempting to touch with lips, bite, chew, even swallow.28-30
In gray mouse lemurs, extensive mouth use was observed when the
animals retrieve food items.31 As lips contain the densest sensory
nerve terminals for body surface of human and other primates, oral
contact would be very informative in terms of providing sensory sig-
nals for a novel object. With such initial characterization of an object,
subsequent contact with hands and feet would provide additional
information.
It is worth noting that the pattern of behavior differences differs
between that for basketball playing and that for tennis ball playing,
in that in tennis ball playing, both the first-­appearance time of fore-
limb (gross motor) and oral contact show significant difference with
forelimb (fine motor) and hind limb (Figure 1B), whereas in basket-
ball playing, only the first-­appearance time of forelimb (gross motor)
shows significant difference with fine forelimb motor and hind limb
|
      23
(Figure 1A). In other words, oral contact is not significantly different
from forelimb and hind limb (Figure 1A). One possibility may be related
to the size of the novel object. The tennis ball is relatively small, similar
to certain fruits (such as apples and pears) that monkeys are used to
handle and eat. Therefore, when they explore a small object such as
a tennis ball, monkeys may intuitively initiate oral contact, but quickly
abandon the effort once they realize the tennis ball is non-­edible. For
a large object such as a basketball, the beginning of oral contact explo-
ration was delayed. As a result, the time of first oral contact with the
basketball is similar to that of the forelimb (fine motor) and hind limb
behaviors. Therefore, for basketball playing, there is no statistically
significant difference between the time of first oral contact with those
of the forelimb (fine motor) and hind limb movements. And forelimb
gross motor, which was also an early appearance behavior, showed a
rather low level of cumulative time for basketball (Figure 2A). Thus, the
different patterns of statistical significance between a large object (the
basketball) and a small object (the tennis ball) may reside in the size of
the object, which reflect the monkey’s innate interest in exploring a
potential edible subject and the amount of exploration it may take to
explore that object.
It should be pointed out that, because the current study was not
repeated with a reverse order of novel object introduction (the ten-
nis ball first, and the basketball second), the interpretations based on
object size are tentative until such time that the reverse presentation
can be completed.
In conclusion, we showed that in novelty exploration, monkeys
displayed an orderly sequence of activities, beginning with forelimb
gross motor and oral contact, followed by forelimb fine motor and hind
limb activities. Furthermore, oral contact appeared to be an import-
ant behavior in monkeys’ repertoire of novelty exploratory behaviors,
both as an early appearing activity, and showing a consistent pattern
of high cumulative time for two different novel objects. These results
provide a profile of object exploratory behaviors in cynomolgus mon-
keys, contributing to a better understanding of this aspect of behav-
ioral innovation.
AC KNOW L ED G M ENTS
We thank Hainan Jingang Laboratory Animal Co. Ltd. for providing
technical support. This work was partially supported by funding from
ShanghaiBio Corporation.
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How to cite this article: Zou H, Liu M, Luan Y, et al. Pattern of
novel object exploration in cynomolgus monkey Macaca
fascicularis. J Med Primatol. 2017;46:19–24. https://doi.
org/10.1111/jmp.12251
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