Social Interactions through the Eyes of Macaques and Humans

Abstract

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys' gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.

Full text

Social Interactions through the Eyes of Macaques and
Humans
Richard McFarland
1,2
, Hettie Roebuck
1
, Yin Yan
3
, Bonaventura Majolo
1
*,WuLi
3
*, Kun Guo
1
*
1School of Psychology, University of Lincoln, Lincoln, United Kingdom, 2School of Physiology, University of the Witwatersrand, Johannesburg, South Africa, 3State Key
Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China
Abstract
Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable
resources. Observing such social interactions between group members provides individuals with essential information (e.g.
on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners.
This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how
non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns
of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing
the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics
of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus
macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific
individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze
distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of
interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore,
the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions.
Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting
individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that
monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying
a homologous cognitive mechanism of social attention between rhesus macaques and humans.
Citation: McFarland R, Roebuck H, Yan Y, Majolo B, Li W, et al. (2013) Social Interactions through the Eyes of Macaques and Humans. PLoS ONE 8(2): e56437.
doi:10.1371/journal.pone.0056437
Editor: Piia Susanna Astikainen, University of Jyva
¨skyla
¨, Finland
Received October 29, 2012; Accepted January 9, 2013; Published February 15, 2013
Copyright: ß2013 McFarland et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by National Basic Research Program of China Grant 2011CBA00405; National Natural Science Foundation of China Grant
30970983, 31125014 and 30930031; Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning, China; the Leverhulme Trust Grant
No. RF/2/RFG/2009/0152. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: kguo@lincoln.ac.uk (KG); liwu@bnu.edu.cn (WL); bmajolo@lincoln.ac.uk (BM)
Introduction
In group-living mammal and bird species (e.g. primates,
dolphins and ravens), individuals display different social tactics
and select social partners based on their past interactions with
other group members [1]. By observing the social interactions of
their group companions, animals can gather a significant amount
of information about an individual, such as its dominance position,
fighting ability and response to affiliative social solicitations [2–4].
Such acquired information is considered fundamental to an
individual’s decision to choose social partners, form alliances or
avoid aggressive individuals [1,3]. Therefore, attending to social
interactions exchanged by other group members has fitness
consequences, as it affects an individual’s behaviour and social
tactics. Despite this, we know very little about the visual cues used
by animals to acquire information from relevant social interac-
tions, and whether social attention processes differ depending on
the type of interaction observed and the individuals involved.
Human eye tracking studies have clearly demonstrated that
active scene exploration is associated with a series of saccades to
direct our fixation and attention toward local regions that are
informative or important to us. The preferred regions within
a scene are often inspected earlier and attract more fixations and
longer viewing time. Therefore, gaze distribution provides a real-
time behavioural index of ongoing perceptual and cognitive
processing, and is reflective of our attention, motivation and
preference; especially when exploring scenes of high ecological
validity [5,6]. With visual stimuli in simplistic social context (e.g.
a face or human figure presented in isolation), previous studies
have demonstrated that the gaze behaviour of monkeys is
strikingly similar to that of humans during free-viewing. For
instance, when presented with a face picture, both species often
demonstrate a face-specific natural gaze bias towards the left hemi-
face [7], and direct a disproportionate amount of fixations to the
socially informative local facial features (i.e. eyes, nose and mouth
region); with a strong preference towards the eyes [8–15]. It seems
that monkeys and humans are broadly tuned to the same local
visual cues in the processing of simplistic social scenes, suggesting
a close evolutionary connection in the organisation of their visual
system, as well as the visual and social behaviour observed in the
two species. The simplified scenes used in these studies, however,
do not represent naturalistic social interactions of which primates
have prior experience. This issue can limit and potentially bias our
understanding of social attention in primates. For instance,
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presenting a face or an animal in isolation, or in an artificially
structured image (e.g. two animals combined together in a single
scene), is clearly less ecologically-relevant than an image depicting
a real-life social interaction. Therefore, gaze preference to certain
facial or body regions embedded in these images may not
necessarily be a true representation of primates’ social attention
under natural conditions.
A few human eye tracking studies have examined gaze
allocation in free-viewing of social scenes containing multiple
people. Overall, the observers tend to spend the majority of their
time looking back and forth between individuals in the scenes, and
their attention is biased towards the faces, and in particular the
eyes [16–18]. Furthermore, gaze allocation towards individual
people or body regions is influenced by social action, content and
context. For instance, the viewers tended to look more, and for
longer, at the eyes of the face as the number of people in the scene
increased, especially when these people were active [17]. In
comparison with other people in the scene, individuals perceived
as holding a higher social status [19], or were talking [18], tended
to attract more fixations.
Like humans, monkeys also seem to respond to the content of
biologically relevant social scenes [20–23]. When viewing video
clips they tend to gaze towards individual people or animals in the
scene, and look more often at their faces [20,21]. When watching
video clips of conspecifics, rhesus macaques altered their gaze and
head orientation (i.e. aversion or following) according to their
interest in, and actions of, monkeys within the video [22].
Moreover, increased visual attention and pupil diameter (i.e.
sympathetic arousal) has been observed in rhesus macaques
watching social, compared to non-social videos [23]. Finally, in
a study comparing the pattern of visual attention of humans and
rhesus macaques watching video clips [21], the gaze behaviour of
both species was correlated with the biological relevance of the
stimuli, driven by both content- and context-specific social cues.
Although these recent eye-tracking studies have examined
human and monkey gaze behaviour when viewing biologically
relevant social videos often containing more than one individual
[22,23], there has been no systematic investigation and direct
comparison of how humans and non-human primates allocate
their attention to different individuals in scenes of different social
context (e.g. affiliation or aggression), and how this is affected by
the viewed species.
An individual’s attention to a social interaction depends on how
biologically relevant the interaction is, which ultimately is affected
by phylogeny and/or prior experience. Various behavioural
patterns, such as affiliation and aggression, share some homolo-
gous characteristics across different species [3,24] and therefore
might attract similar patterns of social attention and gaze
behaviour. However, if phylogeny plays a dominant role in
guiding social attention, we may expect that an individual’s gaze
behaviour for viewing conspecifics and non-conspecifics would
become increasingly different with the increasing phylogenetic
distance between the two viewed species. For example, rhesus
macaques and Barbary macaques (M. sylvanus) share similar body
postures and facial displays for aggressive, submissive or affiliative
exchanges - due to their phylogenetic relatedness [24]. Therefore,
the gaze pattern of rhesus monkeys toward social interactions of
their conspecifics is likely to be more similar to those patterns
observed when viewing social interactions of Barbary macaques,
when compared to those observed when viewing lions. Alterna-
tively, if past experience shapes an individual’s viewing behaviour
to social interaction scenes, similar gaze patterns may appear when
observing the same type of social interaction in conspecifics and in
familiar non-conspecifics (e.g. humans for laboratory-raised rhesus
monkeys), regardless of the phylogenetic relatedness of the two
viewed species.
In this study we aimed to compare gaze distribution in viewing
naturalistic photographic images of social interactions in five
different species (rhesus macaque, Barbary macaque, baboon:
Papio spp., lion: Panthera leo, and humans, respectively). We
examined how rhesus macaques and humans distribute visual
attention to different social interactions (i.e. affiliation or
aggression) between their conspecifics and between individuals of
other species within a range of phylogenetic distance and differing
in terms of prior experience (i.e. familiar or unfamiliar species).
Given laboratory-raised monkeys have limited social contact with
non-human non-conspecifics, this comparison would help us to
understand to what extent the social attention to conspecific
interactions is a learned or innate trait. Furthermore, as rhesus
monkeys are the most commonly used animal model of human
perceptual and cognitive processes, it is essential to understand
how close these two species are in their processing of social
interaction scenes.
All images used in this study represented either a positive (i.e.
affiliation) or negative (i.e. aggression) social context, and consisted
of two ‘social roles’, a giver and a receiver of the relevant
behaviour. Affiliative behaviours are pro-social behaviours that
bring two or more individuals in to physical contact. We chose
grooming exchange to represent positive social interaction, as it is
the most common form of affiliation in primates [25]. Moreover,
contact affiliation can also be observed across a range of mammals,
including lions [26]. Aggression (i.e. one animal chasing and/or
attacking another) was chosen to represent negative social
interaction, as aggressive displays often share similar features
across mammal species and can be easily recognized by (at least
human) viewers. With these images representing naturalistic social
interactions, we intended to address the following questions: 1)
Can rhesus macaques differentiate between conspecific individuals
based on their roles in different social interactions? That is, do they
spend proportionally more time looking at the giver or receiver in
positive and negative social interactions of other rhesus macaques?
2) Do rhesus macaques generalise this gaze behaviour across non-
conspecific social interactions (i.e. Barbary macaques, baboons,
lions and humans) and is this affected by phylogenetic distance
between their own and other species, or by prior experience? 3)
Which local regions (e.g. head, face or body) do rhesus macaques
attend more frequently to extract diagnostic visual cues for
processing scene contents? 4) Do rhesus macaques share similar
viewing behaviour to humans in the viewing of the same social
scenes?
Materials and Methods
Subjects
Four male adult rhesus macaques (5–9 kg, 5–9 years old)
participated in this study. The animal experiments were conducted
at Beijing Normal University. Ethical approval was granted by the
Institutional Animal Care and Use Committee of Beijing Normal
University, with all procedures in compliance with the National
Institutes of Health Guide for the Care and Use of Laboratory
Animals. The monkeys were born in captivity and socially housed
indoors. Before the experiment, a custom-made biocompatible
titanium head restraint (a small post on a cross-shaped pedestal
with screw holes) was attached to the animal’s skull with titanium
bone screws under aseptic conditions. The animals were prepared
under general anesthesia induced with ketamine (10 mg/kg,
intramuscular) and maintained, after intubation, by ventilation
with O
2
(100%) mixed with isoflurane (1.5–2.5%). Vital signs
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including SpO
2
,CO
2
, ECG and heart rate were continuously
monitored by a patient monitor (PM-9000 Express, Mindray)
during the surgery. Antibiotics and analgesics were used after the
surgery.
After the animals were fully recovered, they were trained to
fixate a small fixation point on a computer screen for a couple of
seconds in exchange for a juice reward, which was delivered
through a small tube to the monkey’s mouth by a solenoid valve
under computer control [27]. The animals were seated in
a custom-made primate chair with their head restrained by fixing
the implanted head post to the chair, which was in turn fixed to
a rigid frame. Care was taken to maximize animal welfare and
minimize suffering. Through visual and social stimulation, the
monkeys were provided with enrichment according to National
Institutes of Health Guide for the Care and Use of Laboratory
Animals to maximize psychological well-being. During the
experimental period, they were single housed but had auditory
and visual contact with the rest of the colony. They had free access
to food but were on controlled fluid access in the housing cage.
They earned roughly 80% of their total daily fluid ration during
the testing sessions. Out of the experimental period or during the
weekends, the monkeys had free access to food and water. The
monkeys’ weight and general health were monitored daily. After
all experiments in this and other studies were finished, the head
post was removed using surgical procedures similar to those for
implantation, and the animals were retired to their colony.
Twenty six undergraduate students (10 males and 16 females,
mean age 6SEM = 20.360.6 years) with normal visual acuity
participated in this study. The human experiments were con-
ducted at the University of Lincoln. The Ethical Committee in the
School of Psychology, University of Lincoln, approved this study.
Written informed consent was obtained from each participant
prior to testing, and all procedures complied with the British
Psychological Society ‘‘Code of Ethics and Conduct’’ and the
World Medical Association Helsinki Declaration as revised in
October 2008.
Stimuli and Apparatus
Digitized images were presented through a ViSaGe graphics
system (Cambridge Research Systems) and displayed on a gamma-
corrected colour monitor (Mitsubishi Diamond Pro 2070SB for
human experiments; Iiyama Vision Master Pro 514 for monkey
experiments) with a resolution of 10246768 pixels and frame rate
of 100 Hz. The viewing distance was 57 cm and 100 cm for
human and monkey experiments respectively.
Colour photographs of dyadic social interactions of five different
species (rhesus macaques, Barbary macaques, baboons, lions and
humans) were sampled from the internet or the authors’
collections. Each photograph represented either a positive (i.e.
affiliation: two individuals grooming, embracing or in social
contact with one another) or negative (i.e. aggression: an
individual being aggressed by another) social interaction, and
consisted of two ‘social roles’, a giver and a receiver of the relevant
behaviour (see Fig. 1 for an example). In total, four positive and
four negative images from each of the five species were used as
stimuli. To control for directional scanning bias (e.g. left gaze bias
[7]), stimuli were presented in both their original and mirrored
orientation. Given the difficulty to standardize individual’s body
size and the distance between two individuals in naturalistic
scenes, these images often varied in size. Depending on their width
to height ratio, images were consistently fixed to a width of 22.8u
(if width was the longer dimension) or a height of 17.1u(if height
was the longer dimension). The images were gamma-corrected
and displayed at the centre of the screen.
The comparable testing procedure was used for monkey and
human subjects. During the recording, the monkeys were seated in
a primate chair with their head restrained; the humans sat in
a chair with their head supported by a chin rest. All subjects
viewed the display binocularly. The horizontal and vertical eye
positions of monkey subjects were measured by EyeLink 1000 (SR
Research Ltd) with 500 Hz sampling frequency, 0.25–0.5u
accuracy and 0.01uroot-mean-square resolution; eye positions of
human subjects were measured using a Video Eyetracker Toolbox
(Cambridge Research Systems) with 250 Hz sampling frequency,
0.125–0.25uaccuracy and 0.05uroot-mean-square resolution.
To calibrate the eye-tracker a 5-point paradigm was used for
monkey subjects. The five points were presented respectively in the
center (0, 0), top (0, 7.25u), bottom (0, 27.25u), left (210.1u, 0) and
right (10.1u, 0) of the monitor. A 9-point paradigm was used for
human subjects. The nine points were arranged in a 3 63 matrix
covering the image viewing area. The central point was at the
center of the monitor and the distance between adjacent points
was 10u. During the calibration, a small fixation point (0.2u
diameter, 15 cd/m
2
luminance) was displayed randomly at one of
the 5 or 9 positions across the monitor. The subject was required
to follow the fixation point and maintain fixation for 1 s.
After calibrating eye movement signals, a trial was started with
a fixation point displayed on the centre of the monitor. If the
participant maintained fixation for 1 s, the fixation point
disappeared and an image was presented for 10 s. During the
free-viewing presentation, the monkeys passively viewed the
images, and the humans were instructed to ‘‘view the images as
you would normally do’’. The inter-trial interval was 1 s within
which the monkeys received a juice reward without any specific
task requirement related to the stimuli.
Each monkey was tested during two sessions separated by at
least 48 hours. Each testing session was composed of three
consecutive blocks. Within each block, monkeys were randomly
presented with eight positive and eight negative (four original and
four mirrored) images of each of the five species (total N = 80).
Each human participant was tested in a single session. Subjects
viewed either the original (17 viewers) or mirrored (9 viewers)
images containing four positive and four negative images of each
of the five species (total N = 40). After the testing, human
participants were asked to categorize each image as either
affiliation or aggression in a self-paced free-viewing task. All
participants could correctly label the context of social interaction
from different animal species.
Data Analysis
Fixations were extracted from raw eye-tracking data using
velocity and duration criteria (lasting longer than 50 ms with less
than 0.2ueye displacement at a velocity less than 20u/s [10]). To
determine fixation allocation within the image a set of consistent
criteria were adopted to divide local regions of different images
into: a) the giver or receiver of the affiliation or aggression in each
image, b) the background (image area not occupied by the giver or
receiver), c) the head and face, or the body region (excluding the
head and face) of individuals within each image. See Table 1 for
details of the sizes of these regions within different image types (in
the majority of cases, the same body region from two individuals
within the same image had comparable size). Each fixation was
then characterized by its location among local regions and its time
of onset relative to the start of the trial. As we required the subjects
to fixate a central fixation point prior to image presentation, the
first recorded fixation following the image appearance could be
interfered with by this central fixation point procedure and was
therefore removed from further analysis.
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The number of fixations and viewing time directed at each local
region were normalized as a proportion of the total number of
fixations and viewing time sampled in that trial. As the same type
of local region varied in size across intra- and inter-species images
(e.g. two individuals in the same image could vary in body size),
the proportion of the image area constituting each local region was
subtracted from the proportion of viewing time directed at that
region in a given trial. This measure gave us ‘normalized’ viewing
time as a percentage for each image region, with positive or
negative values indicating more or less viewing time than predicted
by a uniform looking strategy [13,14].
The normalized data were analyzed using a series of generalized
linear mixed models (GLMMs) in STATA v10.1 (StataCorp
2007). All the analyses were run using each image presentation as
a single data point with subject ID as a random factor to control
for the non-independence of the data points [28]. To test whether
subjects could differentiate the context of different social interac-
tions, we used GLMMs with Poisson distribution and log link to
analyze whether the number of attention shifts between the giver
and receiver (i.e. count data) was dependent on the context of the
image (i.e. negative or positive). To test whether subjects could
differentiate individuals in different social interactions, we used
GLMMs with Gaussian error structure and identity link to analyze
whether the normalized viewing time was dependent on an
individual’s role in the image (i.e. giver or receiver). To test what
figure cues were used by subjects to ascertain social role, we used
GLMMs to analyze whether viewing time was dependent on the
individual’s figure region in the image (i.e. head/face or body). As
the same figure region (e.g. animal body) could provide different
amounts of information in different social interactions, this analysis
was repeated separately on positive and negative images, for each
of the five species. For monkey subjects, ‘session ID’ (1–2) and
‘block ID’ (1–3) were control fixed factors in all GLMMs as these
variables might affect the subjects’ attention toward stimuli. For
human subjects, ‘participant sex’ (male or female) was entered as
a control fixed factor as this variable may affect the subjects’
attention toward different sexed stimuli (only male rhesus
macaques were tested). GLMM results can be found in Tables 2
to 5.
Results
Across all images, rhesus subjects spent significantly more time
viewing images of their own species (on average 36% of 10 s image
presentation time) compared to images of Barbary macaques
(29%), baboons (29%), lions (30%) and humans (31%; all
comparisons conspecific versus other species images: GLMM, p
values,0.001). The social context of the scene, on the other hand,
did not affect their viewing time (positive images = 30%, negative
images = 31%; GLMM, p= 0.47) but had an impact on the rate of
their attention shifts between the giver and receiver in the images
(Table 2). Compared to negative images, rhesus subjects tended to
look back and forth between individuals more frequently when
viewing positive interactions between rhesus macaques, Barbary
Figure 1. Example of Barbary macaque social interaction scenes.
doi:10.1371/journal.pone.0056437.g001
Table 1. Proportion (Mean 6SEM) of positive and negative social interaction images occupied by an individual’s body and head/
face regions.
Image Species Body region Head and face region
Negative Positive Negative Positive
Giver Receiver Giver Receiver Giver Receiver Giver Receiver
Human 14.9760.72 16.2260.20 15.1160.71 17.0061.14 1.9160.15 1.9060.07 2.7160.23 3.6660.34
Rhesus macaque 10.6760.81 10.5561.28 21.4860.26 23.0760.43 1.9760.17 1.8960.22 4.6260.18 4.4960.12
Barbary macaque 6.2360.29 7.2160.22 16.8460.82 17.8160.90 1.7160.08 1.7560.09 4.8060.12 4.7760.34
Baboon 11.6660.30 8.4660.57 20.8260.64 25.5360.63 1.9660.14 1.7060.07 4.7960.15 6.1660.11
Lion 14.8760.90 11.2860.43 12.2660.85 21.2360.80 4.0760.42 3.5760.18 9.9760.93 5.6860.38
doi:10.1371/journal.pone.0056437.t001
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macaques, baboons and lions. There was no significant difference
in the number of attention shifts when rhesus subjects viewed
positive and negative human images.
1) Can Rhesus Macaques Differentiate between
Conspecific Individuals Based on their Roles in Different
Social Interactions?
The comparison of normalized viewing time directed at the two
individuals within an image indicated that rhesus subjects could
differentiate the roles of conspecific individuals in images of
different social contexts (Fig. 2, Table 3). Specifically, they spent
proportionally more time viewing the receiver than the giver in
both positive (18% on the groomee vs. 7% on the groomer) and
negative (23% on the victim vs. 14% on the aggressor) rhesus
macaque images (also see Table 4 for normalized fixation
distribution which was closely correlated with viewing time
distribution). This gaze preference towards the receiver, however,
was not consistent when viewing social interactions of non-
conspecifics. Instead, the role of the most viewed individual within
an image was species- and context-dependent.
2) Do Rhesus Macaques Generalise their Gaze Behaviour
Across Non-conspecific Social Interactions?
For the negative non-conspecific social interaction scenes,
rhesus subjects displayed the same viewing behaviour towards
humans as they did towards conspecific images, with more gaze at
the receiver than the giver. However, they directed an in-
distinguishable amount of gaze at the two individuals in Barbary
macaque images, and viewed longer at the giver than the receiver
in baboon and lion images (Fig. 2A). Interestingly, their viewing
behaviour towards non-human images seemed to be correlated
with the phylogenetic distance from the viewed species. The
difference in viewing time allocated at the receiver and the giver
was 9% for rhesus macaques, 2% for Barbary macaques, 26% for
Baboons and 29% for lion images.
For the positive non-conspecific social interaction scenes, rhesus
subjects inspected longer at the receiver than the giver in Barbary
macaque images, similar to the viewing of their own species.
However, they spent an equal amount of time viewing two
individuals in both baboon and lion images, and directed
significantly more gaze at the giver than the receiver in human
images (Fig. 2B). Similarly to the negative scenes, the viewing
behaviour towards non-human positive scenes also changed with
the phylogenetic distance from rhesus subjects. The difference in
viewing time allocated at the receiver and the giver was 11% for
rhesus macaques, 4% for Barbary macaques, and did not
significantly differentiate from 0 for baboon and lion images.
However, unlike negative human images (20% time on the
receiver vs. 12% on the giver), which attracted the same viewing
pattern as rhesus macaque images, positive human images induced
an opposite gaze pattern, with the giver receiving more inspections
(7% on the receiver vs. 22% on the giver). In summary, the
amount of viewing time directed at an individual within social
interaction scenes was role-, species- and context-dependent,
implying that rhesus subjects can differentiate different types of
social interaction (at least from those closely-related species).
3) Which Local Regions do Rhesus Macaques Attend
More Frequently to Extract Diagnostic Visual Cues for
Processing Scene Contents?
Rhesus subjects spent proportionally more time viewing the
head and face region, compared to the rest of the body, in the
majority of cases (Table 5; Fig. 3A and 3B), suggesting
a stereotypical gaze pattern of frequent inspection towards the
face/head region when observing social interactions. Quantita-
tively, the amount of viewing time directed at the face/head and
body region was also species- and context-dependent. The
monkeys inspected the body region for longer when viewing
negative images, compared to positive, regardless of the viewed
species (compare empty bars in Fig. 3A with 3B). In fact, when
viewing positive images of all species, the majority of viewing time
was at the head/face region and very little at the body region.
When viewing the negative images, the monkeys viewed longer at
the head/face of the rhesus and Barbary macaques, but shorter at
the baboons’ head/face. The head/face and body regions in lions
and humans, on the other hand, attracted the same proportion of
viewing time. Taken together, these results suggest that different
figure regions provide different diagnostic cues for the interpre-
tation of different types of social interaction.
4) Do Rhesus Macaques Share Similar Viewing Behaviour
to Humans in the Viewing of the Same Social Scenes?
The rhesus subjects on average spent 3.1 s (including time for
fixations and saccades) out of 10 s trial duration to inspect the
Table 2. Poisson GLMM results for the relationship between the number of attention shifts and image type (i.e. negative or
positive) in conspecific and non-conspecific social interaction scenes.
Subject
Stimuli
Species
Negative
(mean 6SEM)
Positive
(mean 6SEM) b6SEM 95% CIs
ZNP
Rhesus macaque Human 3.1760.18 2.9860.19 20.0660.06 20.18–0.05 21.11 383 0.27
Rhesus macaque 2.6860.12 3.7160.18 0.3360.06 0.22–0.44 5.69 383 ,0.001
Barbary macaque 1.9760.11 2.7560.15 0.3360.07 0.20–0.47 4.95 382 ,0.001
Baboon 2.2860.11 3.0260.17 0.2860.06 0.16–0.41 4.47 384 ,0.001
Lion 2.6760.14 3.1360.16 0.1660.06 0.04–0.27 2.61 384 0.01
Human Human 3.3560.17 2.5460.20 20.2760.08 20.43– 20.11 23.27 204 ,0.001
Rhesus macaque 2.0760.15 2.4560.14 0.1760.09 20.01–0.35 1.84 208 0.07
Barbary macaque 2.2360.13 2.6960.16 0.1960.09 0.01–0.36 2.13 207 0.03
Baboon 1.8660.13 2.4960.16 0.2960.10 0.10–0.47 3.01 206 0.003
Lion 2.2560.15 2.6560.18 0.1760.09 20.01–0.34 1.87 207 0.06
doi:10.1371/journal.pone.0056437.t002
Gaze Behaviour in Viewing of Social Interactions
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presented images, which was shorter than humans during the 10 s
of image presentation. To make the gaze patterns comparable
between human and monkey subjects, we only analyzed human
gaze distribution for the first 3.1 s of image inspecting time per
trial. Consistent with previous reports that monkeys tend to
explore the spatial extent of the natural scene more thoroughly
[20] and scan the background scene (image area not occupied by
humans/animals) more often than humans [21], we observed that
human’s gaze was much more concentrated on the humans/
animals while viewing the same set of social interaction scenes.
The normalized viewing time directed at the figures (receiver+-
giver) within each image was 58% and 30% for human and
monkey subjects respectively.
Like monkey subjects, human subjects made or tended to make
more attention shifts between the giver and receiver when viewing
positive, compared to negative, interactions between rhesus
macaques, Barbary macaques, baboons and lions. Unlike monkey
subjects, human subjects made significantly more attention shifts
when viewing negative human images than positive ones (Table 2).
The pattern of gaze allocation towards the two individuals
within a social interaction image, however, was strikingly similar
between rhesus and human subjects (Fig. 2, Table 3). Indeed, the
negative images from a given species elicited qualitatively identical
gaze distribution from rhesus and human subjects (compare
Fig. 2A with 2C): both species tended to inspect longer at the
receiver in rhesus macaque, Barbary macaque and human images,
but shorter at the receiver in baboon and lion images. The positive
images elicited a somewhat less consistent gaze distribution from
rhesus and human subjects (compare Fig. 2B with 2D). On the one
hand, both species spent longer viewing the receiver in rhesus and
Barbary macaque images, and shorter at the receiver in human
images. On the other hand, while rhesus subjects spent an equal
amount of time viewing the two individuals in baboon and lion
Figure 2. Proportion of normalized viewing time directed at the giver and receiver in negative (A and C) or positive (B and D) social
interaction scenes between conspecifics or non-conspecifics. Error bars represent SEM. * p,0.05, ** p,0.01, *** p,0.001.
doi:10.1371/journal.pone.0056437.g002
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images, humans directed more gaze at the receiver in baboon
images, and more at the giver in lion images.
The gaze distribution within different figure regions was also
remarkably similar between rhesus and human subjects (Fig. 3,
Table 5). Both species tended to view longer at the head/face than
the body region when inspecting individuals (especially in positive
scenes), and gazed more at the body in negative interactions
compared to positive interactions. There were, however, some
quantitative differences between the two viewer species. Specifi-
cally, humans viewed the head/face significantly longer than the
body region regardless of the nature of the social interaction. Such
allocation difference in viewing time at the head/face and body
region was more evident when inspecting baboons and lions. The
rhesus subjects, on the other hand, directed similar or even slightly
higher proportion of viewing time at the body in comparison with
the head/face region when inspecting negative interactions in
baboons, lions and humans, implying a gaze strategy difference in
detecting threatening cues between human and monkey observers.
Overall, in spite of some small or quantitative differences, our
results (Figs. 2 and 3) point towards largely overlapping gaze
Table 3. Linear GLMM results for the relationship between normalised proportion of viewing time and target role (i.e. giver or
receiver) in conspecific and non-conspecific social interaction scenes.
Subject
Stimuli
social context
Stimuli
Species
Giver
(mean 6SEM)
Receiver
(mean 6SEM) b6SEM 95% CIs
ZNP
Rhesus macaque Positive Human 22.2261.53 7.0461.50 215.1862.11 219.32– 211.04 27.19 382 ,0.001
Rhesus macaque 7.1261.28 18.4361.61 11.3162.06 7.21–15.34 5.50 384 ,0.001
Barbary macaque 8.5061.21 12.4661.55 3.9661.95 0.13–7.79 2.03 382 0.04
Baboon 11.1061.53 9.3261.63 21.7762.22 26.13–2.58 20.80 384 0.42
Lion 12.3161.49 12.4561.62 0.1462.16 24.10–4.38 0.07 384 0.95
Negative Human 11.9861.28 20.2861.38 8.3061.85 4.67–11.92 4.48 384 ,0.001
Rhesus macaque 14.0561.34 23.0661.30 9.0161.70 5.68–12.34 5.30 382 ,0.001
Barbary macaque 16.7561.43 18.9461.36 2.1961.74 21.22–5.59 1.26 382 0.21
Baboon 21.7061.53 15.3461.24 26.3761.85 29.99– 22.74 23.44 384 ,0.001
Lion 22.1661.52 12.8261.30 29.3461.94 213.13– 25.55 24.83 384 ,0.001
Human Positive Human 36.9462.89 21.1562.78 215.7964.02 223.66– 27.91 23.93 200 ,0.001
Rhesus macaque 19.0662.17 25.3662.36 6.3063.22 0.00–12.60 1.96 208 = 0.05
Barbary macaque 18.2561.95 32.2762.39 14.0163.08 7.97–20.05 4.55 208 ,0.001
Baboon 15.7062.32 25.9862.37 10.2763.33 3.75–16.80 3.09 206 ,0.01
Lion 35.0162.57 14.1262.65 220.8863.70 228.13– 213.63 25.65 206 ,0.001
Negative Human 29.0262.03 34.4262.95 5.4062.89 20.25–11.06 1.87 208 0.06
Rhesus macaque 22.2162.06 38.0962.39 15.8863.15 9.70–22.05 5.04 208 ,0.001
Barbary macaque 31.7362.17 41.7062.24 9.9763.11 3.87–16.06 3.20 206 ,0.01
Baboon 47.7962.37 24.3962.26 223.4063.28 229.83– 216.97 27.14 206 ,0.001
Lion 35.3262.51 28.8062.75 26.5263.73 213.84–0.80 21.75 208 0.08
doi:10.1371/journal.pone.0056437.t003
Table 4. Linear GLMM results for the relationship between normalised proportion of fixations and target role (i.e. giver or receiver)
in conspecific and non-conspecific social interaction scenes.
Subject
Stimuli
social context
Stimuli
species
Giver
(mean 6SEM)
Receiver
(mean 6SEM) b6SEM 95% CIs
ZNP
Rhesus macaque Positive Human 20.7561.37 6.7661.36 214.0061.91 217.73– 210.26 27.35 382 ,0.001
Rhesus macaque 7.8561.22 18.0861.50 10.2361.93 6.45–14.02 5.30 384 ,0.001
Barbary macaque 8.6061.20 12.2861.47 3.6861.88 20.01–7.37 1.95 382 0.05
Baboon 11.8861.52 8.7361.62 23.1562.21 27.48–1.18 21.43 384 0.15
Lion 12.3861.45 12.6161.51 0.2362.06 23.81–4.26 0.11 384 0.91
Negative Human 11.8361.21 20.0061.33 8.1861.77 4.71–11.64 4.62 384 ,0.001
Rhesus macaque 14.2161.26 22.3961.18 8.1861.58 5.10–11.27 5.20 382 ,0.001
Barbary macaque 15.9561.31 19.0061.28 3.0561.57 20.03–6.12 1.94 382 0.05
Baboon 21.3161.43 16.3361.20 24.9861.75 28.41– 21.56 22.85 384 ,0.01
Lion 21.3461.44 12.8461.25 28.4961.84 212.10– 24.89 24.62 384 ,0.001
doi:10.1371/journal.pone.0056437.t004
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strategies between monkeys and humans in their visual analysis of
social interactions.
Discussion
The capacity to discriminate biologically relevant social stimuli
based on their relevance to individual fitness is likely to be under
selective pressure. From an evolutionary perspective, primate
social attention should be guided by selectively analyzing the most
informative cues associated with social interactions and beha-
viours. For example, when presented with images of familiar
monkeys of different dominance status, male rhesus macaques
needed above-average juice reward to view monkey faces of
subordinates, but were willing to sacrifice fluid to view faces of
dominant males [29]. This is because a dominant animal
represents both a potential threat and a more valuable social
partner (e.g. in terms of agonistic support) than subordinates, and
thus a more relevant target of visual attention. In the current
study, with naturalistic social interaction scenes, we found that
rhesus monkeys could spontaneously discriminate individual
conspecifics based on their roles in social interactions. Between
the two characters within a scene, they gazed more at the receiver
than the giver in both negative and positive scenes.
Such discrimination between social roles may involve different
social cognition processes. In the negative social interactions, the
more frequent looking at the receiver (i.e. the victim) could be due
to three inter-dependent processes: avoidance towards the
aggressor (i.e. the giver), gaining of social benefits through
observation and/or empathy towards the victim. Firstly, eye
contact is a threatening display in macaques [24]. In fact, male
rhesus monkeys produce appeasement gestures and avoid gaze
contact in response to videos of threatening males [22,23].
Secondly, focusing on the identity and behaviour of the victim
of aggression may give social benefits to the animal observing an
Figure 3. Proportion of normalized viewing time directed at the head/face and body region while inspecting individuals in
negative (A and C) or positive (B and D) social interaction scenes between conspecifics or non-conspecifics. Error bars represent SEM. *
p,0.05, ** p,0.01, *** p,0.001.
doi:10.1371/journal.pone.0056437.g003
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agonistic interaction between conspecifics. For example, victims of
aggression are more likely to give grooming to a bystander in the
aftermath of a conflict than when they have received no aggression
[30]. Moreover, the ‘loser effect’ predicts that victims of aggression
who have lost a fight tend to lose fights again in the future, either
with the former opponent or with other group members, other
things being equal (e.g. agonistic support) [31,32]. As such, by
attending agonistic interactions monkeys can gather information
on which animal to aggressively target to raise or maintain their
rank position, and/or to coerce for grooming opportunities
[30,33]. Thirdly, showing empathy or concerns for others in
distress is evident in humans (even in two-year-old infants [34])
and might also exist in non-human primates [35,36]. Although the
role of empathy here is speculative, the former two processes
described above can lead to relatively longer viewing at the
receiver in negative scenes. The receiver in the positive
interactions, on the other hand, represents the groomee in our
images. Dominant animals receive more grooming than sub-
ordinates in a range of primate species, including rhesus macaques
[37]. Frequent looking at the receiver may reflect the viewer’s
intention to attend to high-status individuals as they have a higher
impact on the viewer’s own behaviour [29]. Additionally, focusing
on the receiver of grooming is beneficial for the occurrence of
generalized reciprocity, as the receiver is the individual more likely
to give grooming to a third animal later (e.g. the one attending to
the grooming interaction [4]).
To what extent can this social role-sensitive gaze behaviour in
rhesus macaques be relatively attributed to experience or
phylogeny? The comparison of their gaze distribution at
conspecific and non-conspecific interactions provided some in-
sights. Although these laboratory-raised rhesus monkeys had
frequent interactions with conspecifics and human carers/
researchers, their viewing patterns toward rhesus macaque and
human images were context- and species-dependent. For the
negative interactions, they gazed longer at the receiver in both
rhesus macaque and human images, suggesting the adoption of
a similar social attention pattern. For the positive interactions, they
looked more at the conspecific receiver but more at the human
giver, suggesting the adaptation of gaze behaviour according to
their social contact experience.
Interestingly, the monkey’s gaze distribution in viewing un-
familiar non-conspecific images was systematically varied with
their phylogenetic distance from the viewed species. The more
phylogenetically distant the taxon (i.e. from Barbary macaque,
belonging to the same genus; to baboon, same order; and lion,
same class), the less the monkeys attended at the victim and the
more at the aggressor in the negative interactions (Fig. 2A);
implying a shift of gaze pattern (from displaying empathy to
examining threat) that may be phylogenetically-based. For the
positive interactions (Fig. 2B), monkeys attended to the groomee
(with the same viewing pattern displayed for conspecific images
but with decreased viewing time) in Barbary macaques but did not
differentiate between groomee and groomer in baboons and lions.
Given that the studied animals have never encountered species
other than conspecifics and humans, it seems that their social
attention to interactions (especially negative interactions) between
unfamiliar species is strongly influenced by innate bias. In other
words, the more phylogenetically distant a species is, the less
relevant their social interactions become. This is possibly due to
different species-specific facial displays and body postures in
different social contexts.
Table 5. Linear GLMM results for the relationship between normalised proportion of viewing time and target body region (i.e.
head/face or body) in conspecific and non-conspecific social interaction scenes.
Subject
Stimuli
social context
Stimuli
species
Head/Face
(mean 6SEM)
Body
(mean 6SEM) b6SEM 95% CIs
ZNP
Rhesus macaque Positive Human 24.1561.69 5.1161.74 219.0462.40 23.75– 214.33 27.92 382 ,0.001
Rhesus macaque 26.8561.51 21.3061.39 228.1562.05 232.17– 224.14 213.74 384 ,0.001
Barbary macaque 23.1461.53 22.1861.46 225.3262.10 229.44– 221.21 212.06 382 ,0.001
Baboon 26.1161.64 5.1861.72 220.9362.36 225.56– 216.30 28.86 384 ,0.001
Lion 30.6561.87 2.0161.38 228.6462.21 232.98– 224.31 212.95 384 ,0.001
Negative Human 15.9961.36 16.2661.50 0.2762.00 23.66–4.19 0.13 384 0.89
Rhesus macaque 25.4861.38 11.6261.52 213.86618.90 217.58– 210.14 27.30 382 ,0.001
Barbary macaque 21.4361.52 14.2661.44 27.1661.88 210.85– 23.49 23.82 382 ,0.001
Baboon 15.0861.18 21.9661.46 6.8861.75 3.46–10.31 3.94 384 ,0.001
Lion 18.4361.39 16.5561.85 21.8862.26 26.31–2.55 20.83 284 0.41
Human Positive Human 49.4162.95 8.6763.30 240.7464.43 249.43– 232.06 29.19 200 ,0.001
Rhesus macaque 38.8962.21 5.5362.18 233.3663.11 239.46– 227.27 210.73 208 ,0.001
Barbary macaque 49.7762.71 0.7562.98 249.0264.03 256.92– 241.11 212.15 208 ,0.001
Baboon 64.6862.10 223.0062.19 287.6763.04 293.64– 281.71 228.82 206 ,0.001
Lion 67.3161.84 218.1761.71 285.4862.52 290.42– 280.55 233.94 206 ,0.001
Negative Human 40.7662.65 22.6862.59 218.0863.72 225.37– 210.80 24.87 208 ,0.001
Rhesus macaque 47.4262.25 12.8762.78 234.5563.57 241.55– 227.55 29.67 208 ,0.001
Barbary macaque 48.6762.57 24.7662.78 223.9163.78 231.32– 216.50 26.32 206 ,0.001
Baboon 68.5262.42 3.6662.31 264.8563.35 271.41– 258.29 219.38 206 ,0.001
Lion 57.0762.39 7.0562.70 250.0263.62 257.11– 242.94 213.83 208 ,0.001
doi:10.1371/journal.pone.0056437.t005
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Being the major animal model of human visual perception,
rhesus monkeys have a close evolutionary connection with humans
in the neuroanatomical organization of the visual system, as well as
in visual and social behaviours. Earlier comparative studies have
found a remarkable similarity in gaze patterns between rhesus
monkeys and humans when exploring face images, natural scenes
and movie clips [7–15,20,21]. Here we extend this similarity to the
processing of more complex, naturalistic social interactions, in
which both species demonstrated a qualitatively similar role-
sensitive, species- and context-dependent gaze distribution (espe-
cially when inspecting negative social images, Fig. 2). Both species
also attended to the same local figure region to extract informative
social cues. They tended to gaze more at the face than the body
region, and inspect relatively longer at the body region in negative
relative to positive social interactions (Fig. 3). Taken together, the
current study suggests that monkeys and humans share a homol-
ogous social attention strategy when processing social scenes.
However, notable differences between human and monkey
observers in viewing conspecific and non-conspecific social scenes
can still be identified. Unlike monkey viewers, the quantitative
difference in viewing time directed at the receiver and the giver
from human viewers was not systematically influenced by the
viewed species in negative interactions (Fig. 2C), and was
significantly different when viewing baboons and lions in positive
interactions (Fig. 2D). These differences could be due to the fact
that humans have acquired knowledge about different non-
conspecific animals through various sources, which could bias
their gaze behaviour. Nonetheless, the capacity to perform social
evaluation through the observation of a conspecific’s social
behaviour, emerges very early in human development. Even
three-month old infants prefer individual characters behaving
prosocially to those behaving antisocially in various social
scenarios [38]. It seems that attending to and evaluating
individuals based on their mutual treatment is fundamental to
perceive the social world, and such capability could be largely
influenced by innate bias.
Furthermore, humans spent more time focusing on the
individuals in the image, especially on the face region, than
monkey viewers when examining both conspecific and non-
conspecific images (Fig. 3). Similar differences in gaze behaviour
also exist between human and chimpanzee viewers [39] which
could be related to species-specific forms of social interaction. In
monkey and chimpanzee societies, where long fixation towards
a conspecific face represents a strong signal of threat [25], viewers
may simply look at the face briefly to reduce direct gaze contact,
especially when inspecting figures in negative social interactions.
Taken together, our findings revealed that monkey and human
observers adopt role-sensitive, species- and context-dependent
gaze behaviour when inspecting conspecific and non-conspecific
social interactions, which is qualitatively similar but with some
marked quantitative differences between the two species. This
suggests that social attention in rhesus monkeys and humans share
some basic innate properties and mechanisms, but is also
modulated by experience. Thus, social attention is likely to be
a biological adaptation in these two species.
However, it should be noted that some types of social
interaction, such as aggression, could contain similar subject
action (e.g. chasing/running action) and image cues (e.g. motion
and distance cues) across many different species. These inherent
scene properties could partially drive the viewer’s gaze allocation.
Therefore, it is possible that the very basic properties of social
attention may be similar across all primate, as well as non-primate
species. Given we presented snapshots of social interactions on
a computer screen in this study, it also remains a question to what
extent the monkey viewers would interpret such scenes as
ecologically relevant. Moreover, different social interaction scenes
often differ in image properties. For instance, the distance between
two individuals in an aggression scene (e.g. one animal chasing
another) is likely to be larger than in an affiliation scene (e.g. one
animal grooming another), and an aggression scene may contain
more movement cues than an affiliation scene. Although many of
these variables are inherent properties of the scene and could be
essential to define the scene’s social context, the gaze allocation to
different individuals and/or different body regions in the image
could be partially affected by these image variables. Future studies
could systematically manipulate these variables (e.g. varying
distance between two individuals in the image without changing
its social context) to examine to what extent they affect gaze
behaviour when viewing social interaction scenes.
Acknowledgements
We would like to thank Piia Astikainen and two anonymous reviewers for
their helpful comments on our manuscript.
Author Contributions
Conceived and designed the experiments: KG BM WL. Performed the
experiments: RM HR YY. Analyzed the data: RM. Contributed reagents/
materials/analysis tools: YY WL KG. Wrote the paper: KG RM WL BM.
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