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Neuroendocrinol Lett 2015; 36( 2) :10 6 – 111
REVIEW ARTICLE
Neuroendocrinology Letters Volume 36 No. 2 2015
ISSN: 0172-780X; ISSN-L: 0172-780X; Electronic/Online ISSN: 2354-4716
Web of Knowledge / Web of Science: Neuroendocrinol Lett
Pub Med / Medline: Neuro Endocrinol Lett
Facial expression of fear in the context of
human ethology: Recognition advantage
in the perception of male faces
Radek T 1,2, Peter T 2,3,4, Jozef H 3,5,6
1 Faculty of Humanities, Charles University in Prague, Prague, Czech Republic
2 Prague College of Psychosocial Studies, Prague, Czech Republic
3 OUSHI, Palacky University, Olomouc, Czech Republic
4 Health Psychology Unit, Institute of Public Health, Medical Faculty, P.J. Safarik University, Kosice,
Slovakia
5 Psychiatry Clinic, Trencin, Slovakia
6 St. Elisabeth University of Health and Social Sciences, Bratislava, Slovakia
Correspondence to: Radek Trnka, PhD.
Science and Research Department, Prague College of Psychosocial Studies
Milanska 471, 109 00 Prague 10, Czech Republic.
: +420 274774712 ; -: trnkar@volny.cz
Submitted: 2015-03-13 Accepted: 2015-03-20 Published online: 2015-05-18
Key words: facial expressions; facial displays; human ethology; fear; gender; sex
Neuroendocrinol Lett 2015; 36( 2) :10 6 – 111 PMID: 26071575 NEL360215R 02 © 2015 N euroe ndocr inolo gy Let ters • www.nel.edu
Abstract
Facial expression is one of the core issues in the ethological approach to the study
of human behaviour. This study discusses sex-specific aspects of the recognition
of the facial expression of fear using results from our previously published experi-
mental study. We conducted an experiment in which 201 participants judged
seven different facial expressions: anger, contempt, disgust, fear, happiness, sad-
ness and surprise (Trnka et al. 2007). Participants were able to recognize the facial
expression of fear significantly better on a male face than on a female face. Females
also recognized fear generally better than males. The present study provides a new
interpretation of this sex difference in the recognition of fear. We interpret these
results within the paradigm of human ethology, taking into account the adap-
tive function of the facial expression of fear. We argue that better detection of
fear might be crucial for females under a situation of serious danger in groups of
early hominids. The crucial role of females in nurturing and protecting offspring
was fundamental for the reproductive potential of the group. A clear decoding of
this alarm signal might thus have enabled the timely preparation of females for
escape or defence to protect their health for successful reproduction. Further, it is
likely that males played the role of guardians of social groups and that they were
responsible for effective warnings of the group under situations of serious danger.
This may explain why the facial expression of fear is better recognizable on the
male face than on the female face.
107
Neuroendocrinology Letters Vol. 36 No. 2 2015 • Article available online: http://node.nel.edu
Facial expression of fear and human ethology
INTRODUCTION
Facial expression is one of core issues in the ethological
approach to the study of human behaviour (Eibl-Eibels-
feldt 1989; Klein 2000). Human ethologists and behav-
ioural ecologists understand facial expressions as social
signals or social tools that facilitate social interactions
(Fridlund 1994). They are a kind of social releasers,
because their main function is to communicate informa-
tion from one individual to another (e.g. Plutchik 1980).
Different types of facial expressions form cooperative
signalling systems that bring benefits to the express-
ers as well as to the recipients (Schmidt & Cohn 2001).
Other scholars understand facial expressions more
as emerging instrumental actions, action tendencies,
or behavioural tendencies (Jakobs et al. 1997). This
approach is based on the assumption that each element
of behaviour is potentially informative and provides
recipients who know the importance of this behaviour
with information about what is likely to occur in the
next phases of interaction (van Hooff 1981). Facial
movements communicate the internal states of the
expressers and indicate their subsequent behaviour to
some extent (Plutchik 1980). This function allows par-
ticipants in a social interaction to adapt their behaviour
appropriately, e.g. to avoid conflict or facilitate mating
behaviour.
RECOGNITION OF HUMAN
FACIAL SIGNALS
Facial processing covers plenty of areas like brain reac-
tivity in response to viewing emotional faces (Zhang
et al. 2011), lateralization of facial processing (De
Winter et al. 2015; Bourne 2011), temporal character-
isticsoffacial-emotionprocessing (Utama et al. 2009),
mother’s brain activation to infant’s facial expressions
(Strathearn et al. 2009; Strathearn et al. 2010), or recog-
nition of facial expressions in people with mental dis-
orders (Binelli et al. 2014; Thomas et al. 2014). One of
paradigmatic research questions is: how are people able
to distinguish individual facial expressions and what
factors may influence recognition accuracy? Gaspar
(2001) believed that understanding facial expressions is
one of the oldest communication skills in human soci-
ety, and the work of Paul Ekman suggested that some
facial expressions are recognized across various cultures
(Ekman et al. 1982; Ekman & Friesen 1986). These basic
facial expressions are anger, contempt, disgust, happi-
ness, sadness, surprise and fear. The problem of facial
expressions of contempt is contentious, because there
are arguments to include it among basic facial expres-
sions as well as arguments against.
How are various facial configurations of the human
face processed? The human brain has a specific part
which has substantial influence on the processing
of human faces and changes in the configuration of
facial elements. The gyrus fusiformis (FFA, fusiform
face area) is activated when participants process visual
stimuli, included faces or facial expressions (Koukolik
2007). The level of activation is higher than in cases
when processing non-facial stimuli. The function of the
gyrus fusiformis is domain-specific (Rhodes et al. 2004).
This means that this neuro-anatomical structure is spe-
cialized for the processing of human faces and facial
expressions.
Let’s turn our attention to the underlying cognitive
mechanism that is responsible for processing human
faces and changes in the configuration of facial ele-
ments. The human cognitive system processes pre-
sented faces using several functional components
(Bruce & Young 1986). Analysis of the configuration of
facial features and analysis of facial speech are present
in the early stage of face processing, during so-called
“structural encoding”. The meaning of a seen configu-
ration of facial features is derived during expression
analysis, which is based on the experiences stored in the
semantic memory. Expression-independent descrip-
tions are further used for a face-recognition unit. Each
face-recognition unit contains stored structural codes
describing one of the faces known to a person. The cog-
nitive system analyzes the resemblance of a seen face to
the stored descriptions. Person recognition is supported
by identity-specific semantic codes held in the associa-
tive memory, the so-called “person identity nodes”
(Bruce & Young 1986).
It is reasonable to expect that facial morphology may
influence the processing of human facial expressions.
Our cognitive system is able to clearly distinguish if the
observed face is male or female. From this position, one
may ask how the sex of the expresser influences rec-
ognition accuracy for facial expressions. This was also
the challenge for our previous study. We conducted an
experiment in which 201 participants judged seven
standardized facial expressions: anger, contempt, dis-
gust, fear, happiness, sadness and surprise (Trnka et al.
2007). Photographs of facial expressions were presented
using a data-projector on the projecting screen in the
experimental room while participants judged individ-
ual facial expressions of emotion. The number of male
and female faces in this study was the same. Regardless
of gender, respondents did not recognize facial expres-
sions more easily on female faces than on male faces.
However, the facial expression of fear was recognized
significantly more easily on male faces than on female
faces. There were no significant interactions between
the sex of expresser and the other specific emotions
– anger, contempt, disgust, happiness, sadness and
surprise – in the above-mentioned study. Females rec-
ognized the facial expression of fear in 90% of the male
faces shown, and males recognized the same expression
in 80% of the male faces shown. In the case of percep-
tion of the female facial expression of fear, the recogni-
tion accuracy was 69% for female perceivers and 62%
for male perceivers. Ex-post chi-square tests revealed
that females also recognized the facial expression of fear
108
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Radek Trnka, Peter Tavel, Jozef Hašto
significantly better than males (Trnka 2006). The ques-
tion is: why was only the facial expression of fear better
recognized on the male face than on the female face?
ADAPTIVE SIGNIFICANCE OF
FEARFUL FACIAL SIGNALS
Human ethology traditionally seeks explanations for
the function of communication signals in their signifi-
cance for survival of the individual or social group. Fear
is the primordial emotion within the fight-flight system
(Keltner & Haidt 2001) with a specialized neural mech-
anism for the perceptionoffearful facial signals (Santos
et al. 2008). Fear activates the individual to avoid death
by predation or serious physical attacks. In contempo-
rary humans, fear may be related to a specific trigger,
for example, pain-related fear (Raudenska et al. 2013).
The interconnection of physiology and behav-
iour has been reported by studies in various fields of
neuroendocrinology (e.g., Fischer-Shofty et al. 2010;
Putman et al. 2007). The amygdala contains special-
ized areas that scan incoming sensory information for
patterns that may be associated with potential danger
(Mattavelli et al. 2014; Betz et al. 2013; Adams et al.
2010). This cue may also be a fearful facial expression
of another member of a social group (Vuilleumier &
Schwartz 2001; Pourtois et al. 2004). The reaction of
the amygdala is very quick. The amygdala can trigger
a fear response even before the incoming information
has been sent to the occipital cortex for full cognitive
processing (LeDoux 1996). When an individual expe-
riences fear, the hypothalamic-pituitary-adrenocorti-
cal axis pumps a quick dose of cortisol and other stress
Our previous experiment revealed that there are
some sex-specific differences in decoding the facial
expression of fear. Females recognized the facial expres-
sion of fear significantly better than males. The ques-
tion is: why does the fearful facial expression have this
recognition advantage in females? The importance of
clear recognition of fear was probably very high for
females in the human past, and we can turn our atten-
tion to the reproductive significance of females in the
social groups of early hominids.
The crucial role females play in nurturing and pro-
tecting offspring is fundamental for the reproductive
potential of the whole group. Reproduction is a funda-
mental factor for species survival, and the good health
of females is a key precondition for successful mating.
The maintenance of good female somatic and psy-
chological health was also very important for quality
investment in any existing offspring.
Taking all of these matters together, it is reasonable
to hypothesize that quick a clear recognition of a fearful
alarm signal (van Heijnsbergen et al. 2007) was more
important for females than for males. Under a threat-
ening situation, females should quickly and correctly
detect a fearful alarm signal to initiate an adequate
behavioural reaction, for example to escape. The study
of Schwabe et al. (2013) revealed also different effects
of stress mediator noradrenaline onfearprocessingin
men and women. The potential impacts of situations
in which a perceiver fails to recognize an alarm signal
would be very high (for example serious injury or
death). This is one of the explanations for why females
recognized the facial expression of fear significantly
better than males in our previous study.
Chaotic environment with
frequent turbulencies and
variations
Real danger for social group
Alarm signalling
Perception of alarm signal
by group members
Corresponding behavior
for defense of social group
hormones into the blood-
stream and these prepare
the organism for fight or
for flight.
Wu et al. (2012) pointed
out that individuals behave
on the basis of identifying
others’ facial expressions.
Correct recognition of a
facial display reflects good
discriminability within a
given species according
to animal communication
theory (Rowe 1999). Signals
designed to stimulate other
group members to escape
should be clear, with high
discriminability. The facial
expression of fear probably
informed other members
of the group about serious
threats and dangers in early
hominids; that is, it worked
as a kind of alarm signal
(Figure 1).
Fig. 1. General schema of alarm signalling.
109
Neuroendocrinology Letters Vol. 36 No. 2 2015 • Article available online: http://node.nel.edu
Facial expression of fear and human ethology
However, the facial expression of fear was also recog-
nized significantly more easily on a male face than on a
female face. It is not likely that this advantage is caused
by more expressive facial behaviour of males. Indeed,
previous experimental research has indicated that
females are generally considered to be more emotion-
ally expressive than males (Gross et al. 2000; Hall et al.
2000), with more expressive faces than males (Shields
1991). Therefore, we should seek another explanation.
It is likely that males played the role of guardians of
the social unit in early hominid evolution because of
their more sturdy physical constitution. Males should
detect potential danger and inform other members in
the group. Therefore, it is hypothesized that alarm sig-
nals were probably produced more often by males than
by females. For this reason, the facial configuration of
fear might be better recognizable on male faces.
There are also processes that might accompany the
communication of a fearful signal between members
of the social group. Affective resonance, emotional
contagion, facial mimicry or the so-called “Chame-
leon Effect” – all these concepts are names relating to
the same effect in social interaction. People reflexively
mimic facial movements in response to the perception
of such states in other people (Gump & Kulik 1997).
In the case of facial expressions, the recipient simul-
taneously and symmetrically mirrors the emotional
expression of another person (Dimberg et al. 2000),
which induces him or her into a very similar emo-
tional state. This reflexive and unconscious imitation
may lead directly to physiological changes that cause
an emotional state similar to that being experienced
by the interacting partner. This is an automatic process
that does not depend on the simultaneous processing of
intended goals during the interaction. It makes affec-
tive resonance a very powerful mechanism for passive
transmission of emotional information, which facili-
tates the sharing of feelings and behaviours in socially
living mammals.
Scholars have assumed that the cause of emotional
contagion is closely related to the individual facial feed-
back effect (Blairy et al. 1999). Individual facial feed-
back means that changes in facial configuration also
cause changes in the emotional state of the individual.
Proprio-receptive feedback of the face depends on the
level of activity of facial muscles. People pretending the
facial expression of some emotion tend to experience
that particular emotion. Specific muscle contractions
present in the facial expression of fear and sadness
induced a similar emotional experience in the experi-
ment of Blairy et al. (1999).
Emotional contagion and individual facial feedback
framed the function of fearful facial expression as an
alarm signal. We may expect that these processes were
also present in the minds of our ancestors in the past.
Male guardians produced alarm signals under a situa-
tion of serious danger in a group of early hominids. The
alarm signals were seen and then re-produced by other
group members, eliciting similar physiological changes
in them. When taking into account the hypothalamic-
pituitary-adrenocortical axis that pumps out a quick
dose of cortisol and other stress hormones in a situation
when an individual experiences fear, we may expect the
complex system of fearful signalling to be very effec-
tive (Figure 2). Such kind of physiological changes is
situation-focused and this link between physiology and
behaviour is different than in the case of physiologi-
cal changes relating with stable personal dispositions
(Galecki et al. 2013). Good discriminability of the facial
expression of fear with the work of emotional conta-
gion and individual facial feedback represent an adap-
tive feature for mobilizing the whole group under the
situation of serious danger. Clear informing of group
members about actual threats might constitute the basis
for an effective defence of the group and survival of the
species.
Current research provides further arguments implic-
itly supporting the above-mentioned interpretations of
sex differences in the perception of facial expression
of fear. Archer (2009) discussed greater risk-taking by
males and greater fear of physical danger by females
in relation to sexual selection and sex differences in
aggression. Females are more prone to avoid serious
physical conflicts because of their reproductive role.
Archer (2009) suggested that these factors represent
the way the motivational system underlying aggression
responded to evolutionary costs and benefits. Although
heightened sensitivity for fearful signals is considered
maladaptive (Williams et al. 2007), the costs of failure in
the detection of the true facial signal of fear might have
a detrimental effect for individuals in groups of early
hominids. Fear and risk-taking seem to be very impor-
Perception
Activation of amygdala
Behavioral response
Heightened levels of
stress hormones
Fig. 2. Neuroendocrinological responses to fearful facial signal.
110
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Radek Trnka, Peter Tavel, Jozef Hašto
tant variables when discussing the function of commu-
nication signals and their evolutionary significance.
CONCLUSIONS
Human nonverbal perceptual abilities were shaped over
thousands and thousands of years during the course of
evolution of the human brain. We used the theoretical
background of human ethology for a better understand-
ing of sex differences in perception of facial expres-
sions. The ethological paradigm has, however, some
limitations when searching for evolutionary origins of
human behaviour. For example, it is difficult to imagine
how our ancestors communicated, because fossils pro-
vide us with only limited information about patterns
of communication. Recent human social interactions
are accessible for empirical investigation; however, we
cannot approach the patterns that emerged in the early
stage of human evolution directly. Reconstructions of
the communication of early hominids are, therefore,
mostly based on the hypothetical thinking and on par-
allels with recent species.
Further, the ethological approach is mostly focused
on the evolutionary context of communication signals
and on the relationship to survival of the individual or
social group. However, current research also stresses
developmental influences on shaping the human mind
(Hruby et al. 2013). Gender-specific aspects of a new-
born’s interactions with the mother as well as further
socialization in the family and peer-groups may be
crucial for the development of, for example, the differ-
ent attention to facial behaviour in males and females
during their development. Such gender-specific learn-
ing of nonverbal signal decoding is suggested as another
important factor possibly influencing the different rec-
ognition of fear in males and females.
This study provides several insights into the com-
plexity of human communication systems. We utilized
an ethological approach, focusing our attention on the
problem of sex-specific patterns in decoding the facial
expression of fear. Participants in our previous study
were able to recognize the facial expression of fear
better on a male face than on a female face. Females also
recognized fear generally better than males. We argue
that one possibility is to consider the adaptive function
of the fearful facial expression. Detection of fear as an
alarm signal might be crucial for females to protect their
health from the viewpoint of their reproductive func-
tion in groups of early hominids. On the other hand, it
is likely that males played the role of guardians of the
social group in early hominid evolution, which explains
why the facial expression of fear is better recognizable
on the male face than on the female face. The theo-
retical basis provided by the present study may inspire
future ethological research of human communication
and bring a new interpretative framework for experi-
mental research on the recognition of facial expressions.
ACKNOWLEDGEMENTS
This work was supported by the Zdenek Klein Award
2007 and the Grant Agency of the Czech Republic via
the project “Spirituality and Health among Adolescents
and Adults in the Czech Republic” (GA 15-19968S).
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