Applying well-established psychological
paradigms to our closest relatives represents a
promising approach for providing insight into
similarities and differences between humans and
apes. Numerous articles have been published on
the dot-probe task, showing that humans have an
attentional bias toward emotions, especially
when threatening. For social species like
primates, efficiently responding to others'
emotions has great survival value. Observational
research has shown that, compared with humans
and chimpanzees, bonobos excel in regulating
their own and others' emotions, thereby
preventing conflicts from escalating. The
present study is an initial effort to apply a
psychological test to the bonobo, and
demonstrates that they, like humans, have
heightened attention to emotional - compared
with neutral - conspecifics, but are mostly
drawn.
Abstract
In social animals, the fast detection of
group members' emotional expressions promotes
swift and adequate responses, which is crucial
for the maintenance of social bonds and
ultimately for group survival. The dot-probe
task is a well-established paradigm in
psychology, measuring emotional attention
through reaction times. Humans tend to be biased
toward emotional images, especially when the
emotion is of a threatening nature. Bonobos have
rich, social emotional lives and are known for
their soft and friendly character. In the
present study, we investigated (i) whether
bonobos, similar to humans, have an attentional
bias toward emotional scenes compared with
conspecifics showing a neutral expression, and
(ii) which emotional behaviors attract their
attention the most. As predicted, results
consistently showed that bonobos' attention was
biased toward the location of the emotional
versus neutral scene. Interestingly, their
attention was grabbed most by images showing
conspecifics such as sexual behavior,
yawning, or grooming, and not as
much&emdash;as is often observed in
humans&emdash;by signs of distress or
aggression. The results suggest that protective
and affiliative behaviors are pivotal in bonobo
society and therefore attract immediate
attention in this species.
Efficiently responding to others' emotions
has great survival value, especially for social
species, such as primates, who establish close,
long-term bonds with group members (1-3).
Previous research in humans has shown that one
component of this strong sensitivity to others'
emotions is heightened attention to their
affective states (4-6). Together with the
chimpanzee, the bonobo is the closest living
relative of humans. Studying components of their
emotional behavior, such as emotional attention,
may help us not only to understand this rarely
studied species better, but also provide insight
into (human) emotions and their evolutionary
past (7-9). In the present study, we
investigated whether bonobos, like humans, show
increased attention to scenes depicting
conspecifics showing an emotion or are involved
in emotion regulatory behaviors, compared with
scenes where conspecifics are in a neutral
state.
In natural environments, attention is
preferentially sustained by stimuli that have
affective significance, in contrast to routine,
emotionally neutral events (6, 10). This
attentional bias reflects a functional mechanism
where fast and automatic attention allocation to
emotional information can aid humans in
threatening situations by fostering fast actions
(11, 12).
Experimentally, this has, for example, been
demonstrated with the dot-probe task. Previous
dot-probe studies have shown that emotional
signals induce a bias in spatial attention, in
that participants respond faster to a presented
dot (the target, henceforth, "probe") when it
appears at the location of a previously
presented emotion compared with neutral stimulus
(13-17). Although in humans a bias toward
threatening compared with neutral stimuli is
most commonly observed, some studies also report
increased attention toward positive versus
neutral stimuli (18-21). Other research has
shown that there are marked individual
differences in biases and that these are, for
example, modulated by mood (22, 23). From an
evolutionary perspective, it is most adaptive to
be able to quickly attend to relevant stimuli,
whether those are threats in the environment or
an affiliative signal from an individual who
could provide support and care (24, 25).
Most primates spend their lives in social
groups. To prevent conflicts, they keep close
track of others' behaviors, emotions, and social
debts. For example, chimpanzees remember who
groomed whom for long periods of time (26). In
the chimpanzee, but also in the rarely studied
bonobo, grooming is a major social activity and
a means by which animals living in proximity may
bond and reinforce social structures. It is also
used as a form of reconciliation and a means of
conflict resolution. Despite their general
similarities and close phylogenetic
relationship, bonobos, chimpanzees, and humans
show clear differences in their social behavior.
Although chimpanzee and human societies are
dominated by males and encounters between
different groups frequently result in violence
and sometimes the killing of conspecifics
(27-29), bonobo society is controlled by females
and aggression is usually prevented through
nonconceptive sexual behavior, grooming, and
play (30-33). Compared with chimpanzees, bonobos
live in more predictable environments with low
seasonality and stable food availability, which
is why they have a lower degree of
fission-fusion and which, next to the
peace-keeping role of the females, may also
explain the lower rates of competition
(31).
Bonobos have rich personalities and share
most of their traits with humans and
chimpanzees, suggesting these were also present
in their common ancestor (34). From early age
on, bonobos are sensitive to others' emotions,
which is demonstrated by their ability to
provide appropriate consolatory behaviors after
conflicts (35), a skill individuals with more
effective self-regulation capabilities excel in
particularly (35), but which is also
demonstrated by more automatic behavior,
including yawn contagion, an index of empathy
(36, 37).
Bonobos' personality characteristics and
complex social emotional behavior have rarely
been studied experimentally, but the conclusions
that can be drawn from the few studies available
are in line with the conclusions from
observational research, described above. It has
for example been demonstrated that great apes,
bonobos included, can reliably recognize human
emotions (38) and experiments with chimpanzees
show that they are also sensitive to the
emotions of conspecifics (39-42). By using an
experimental cofeeding set-up, it has been shown
that bonobos are more tolerant than chimpanzees
(43; but see ref. 44). In addition, an
eye-tracking study demonstrated that bonobos
make more eye contact than chimpanzees (45).
Finally, in a risky decision game, bonobos
showed more risk-aversion than chimpanzees (46,
47).
The present study investigates emotional
attention in the bonobo. [Although the
usage of the adjective "emotion" is debated when
it concerns animals, this term is used in
dot-probe studies in humans. To be able to
portray commonalities and differences with the
human literature, we feel that using the same
adjective is appropriate. We are also aware that
at this point we cannot tell what
bonobo-emotions are, and we therefore have to
rely on observational work and on research into
human and chimpanzee expressions. The term
"emotional attention" is therefore used when
attention is directed toward an emotional
expression, but also when directed toward scenes
showing emotion regulatory behaviors
(Methods).] For this purpose, four bonobos
completed a dot-probe task during which
emotional and neutral pictures of unfamiliar
bonobos and control animals were being presented
on a touch-screen (Fig. 1). Per individual, the
task was spread out over 13 sessions with 25
trials each (Methods
and Table S1). Given their highly social
nature, we predicted that bonobos would show
heightened attention toward the pictures showing
emotional compared with neutral bonobos. In
addition, as bonobos are known to be less
aggressive than chimpanzees and humans, and
spend a lot of time on positive social
behaviors&emdash;such as play, sex, and
grooming&emdash;we predicted seeing this
reflected in a specific attentional bias toward
these more affiliative or protective behaviors
than to signals of distress.
Discussion
Bonobos spend their lives in large social
groups and for their survival have to rely on
that group and its members. Observational
research has shown that bonobos are very social
and can adequately regulate their own and group
members' emotions, thereby often preventing
conflicts from arising or solving them quickly.
The present study is, to our knowledge, the
first to experimentally demonstrate that
bonobos, like humans, have heightened attention
for emotional compared with neutral signals of
conspecifics. With aid of the dot-probe task, a
paradigm designed for testing attentional biases
in humans, we here demonstrate that bonobos have
an attentional bias toward the emotions of
others. Most interestingly, bonobos were
particularly drawn toward scenes showing other
bonobos that were yawning, mating, or grooming,
but not toward scenes depicting distressed
bonobos, bonobos pant-hooting, playing, or
handling food compared with neutral scenes. In
addition to an attentional bias towards
emotions, Kumbuka showed more nose wipes - a
behavior indicating edginess, motivational
ambivalence, or frustration (48, 49) - on trials
where the probe was located on the side of the
emotional compared with the neutral picture. We
will now discuss the most attended emotional
behaviors in more detail, and the putative
drivers of their saliency.
The bonobos that were tested in the present
study showed the strongest attentional bias
toward pictures of yawning bonobos.
Yawning is an evolutionarily old behavior
that is widespread among vertebrates. Although
there is a scientific debate about the exact
function, different studies have demonstrated a
social signaling function. There is convincing
evidence that yawning serves a thermoregulatory
function (i.e., it cools the brain back to
homeostasis). It is thought that by cooling the
brain, yawning induces vigilance, which is why
it is evolutionary adaptive for the whole group
to pick up or mimic this behavior (50). Yawning
indeed is very contagious in many social
species, including bonobos, and its effect is
even stronger when the observed yawners are kin
or friends or of higher rank (36, 37, 51).
Research has shown the involvement of the mirror
neuron system during contagious yawning and
supports the premise of a connection between
this system and higher cognitive empathic
functions, including mentalizing. Hence, it has
been suggested that contagious yawning is based
on a functional substrate of empathy (52).
It is possible that as a sign of threat,
bonobos' attention was caught by the display of
canines (which are less impressive compared with
the chimpanzee). However, after close inspection
of the different pictures and their associated
reaction times, we can conclude that this is
unlikely. First, the pictures where the canines
were most visible did not attract more attention
than the pictures where they were less visible.
Second, the canines were also visible during
fear grimaces, which did not attract attention
more than did neutral images.
Touch is a powerful tool for communicating
positive emotions. Human and nonhuman primates
use social touch for maintenance and
reinforcement of social structures (53). Most
primate species communicate affection and reduce
group tension by means of so-called grooming,
the act of tidying or cleaning one another's
body or appearance. Grooming is regarded as a
service given by one individual that confers
benefits to the recipient in terms of hygiene
and has possible calming effects (54). Grooming
is a recipe for social support and releases
oxytocin in both the groomer and groomed (55).
Bonobos keep close track of who groomed whom,
reciprocate grooming, and distribute their
grooming according to the rank of the receivers
(56). Given that grooming plays such a prominent
role in bonobo society, it is not surprising
that their attention was drawn toward scenes
showing this behavior.
The third category that attracted bonobos'
attention were pictures showing scenes with
bonobos involved in sexual behavior. In humans,
sexual frequency has been found to be a strong
positive predictor of general wellbeing and of
the quality of the social relationship (57).
Sexual activity plays an even bigger role in
bonobo society. In bonobos, sex is being used as
a form of greeting, a means of forming social
bonds, conflict resolution, and postconflict
reconciliation. Bonobos are the only nonhuman
animal to have been observed engaging in
face-to-face genital sex, tongue kissing, and
oral sex (58). Bonobos do not form permanent
monogamous sexual relationships with individual
partners and do not discriminate in their sexual
behavior by sex or age (with the possible
exception of abstaining from sexual activity
between mothers and their adult sons). When
bonobos find a new food source or feeding
ground, the increased excitement will usually
lead to communal sexual activity, presumably
decreasing tension and encouraging peaceful
feeding (58). The attentional bias for sexual
images as observed in our study reflects the
high frequency and importance of this behavior
in their daily lives.
Despite their great genetic similarity,
bonobos' behavior is strikingly different from
that of chimpanzees. Whereas males are the
dominant sex in the chimpanzee, bonobo society
is female-dominant. Remarkably, like humans,
chimpanzees make war with rivaling groups and do
not take kindly to strangers. In stark contrast,
bonobos live in friendly and tolerant societies
and, although they sometimes hunt smaller
animals for consumption, never kill one of their
own (9, 31, 32). Intriguingly, bonobos prefer to
share food and mate with strangers than with
acquaintances (33). The social and emotional
differences between the two species of Pan are
reflected in the anatomy of the brain. A
neuroimaging study comparing both species showed
that bonobos not only have more gray matter in
the amygdala and insula, regions involved in
perceiving emotions in self and others, they
also have a larger pathway linking the amygdala
with the anterior cingulate cortex, which is
implicated in top-down control of aggressive
impulses (59). The results are in line with
earlier work showing that bonobos have more Von
Economo neurons, which are involved in social
cognition, in the anterior cingulate cortex than
chimpanzees, and showed a pattern that closely
resembled that seen in humans (59_-61).
The present study showed that bonobos
have heightened attention toward conspecifics'
yawns, grooming, and sexual behaviors. Based
on the results of the present study, can these
behaviors be interpreted as emotional behaviors?
Heightened attention as measured via shorter
reaction times in the dot-probe task has in the
human literature been widely interpreted as an
emotional bias. Can we then draw the same
conclusion for bonobos? For the following
reasons, we indeed think we can. First, reaction
times of all four subjects reflected an
attentional bias toward conspecifics' emotional
behaviors. Second, the scenes that were rated by
four experts as being emotionally intense for
bonobos, especially grabbed bonobo's attention
most. Third, one subject showed more nose wipes
following trials where she had to approach
emotional compared with neutral scenes. A nose
wipe is considered a sign of edginess,
motivational ambivalence, or frustration (48,
49).
To conclude, bonobos' attention is
quickly captured by the emotional expressions of
others. Interestingly, this attentional bias was
strongest for affiliative behaviors (grooming
and mating) and behaviors that are highly
contagious (yawning) and not significant
for scenes depicting distress. The results
suggest that protective and affiliative
behaviors are pivotal in bonobo society and
therefore prioritized.
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