behavioural and neuroscientific sex differences in...

Bachelor Degree Project in Cognitive Neuroscience Basic level 15 ECTS Spring term 2015 Elin Sterner Supervisor: Judith Annett Examiner: Paavo Pylkkänen

BEHAVIOURAL AND NEUROSCIENTIFIC SEX DIFFERENCES IN EMPATHY

SEX DIFFERENCES IN EMPATHY 2

Abstract

Empathy is a multidimensional phenomenon that consists of both emotional and cognitive

components. This paper gives an overview of behavioural and neuroscientific sex differences

in empathy, as well as potential explanations to those results. Research indicates existence of

sex differences in both emotional and cognitive empathy, although inconsistent findings

suggest both female superiority as well as male superiority. Gender roles, social desirability,

as well deficiencies in measurement and imprecise conceptualizations of empathy is argued as

contributors to found sex differences. With a restricted amount of research on sex differences

in empathy, inconsistent findings as well as a great proportion of critique towards both the

research field of empathy as well as towards focus on sex differences; the authors argue that

presented sex differences in empathy must be interpreted with a great caution.

Keywords: empathy, sex, gender difference, behaviour, neuroscience


Table of content

Introduction 5

Defining Empathy 6

Evolutionary and Developmental Perspective on Empathy 8

Affective Sharing 9

Self-other Awareness 10

Mental Flexibility 11

Regulatory Processes 12

Pro-social Behaviour 14

Play Behaviour 15

Behavioural and Psychological Sex Differences 16

Emotion Recognition

Facial expressions 17

Body language 18

Socioemotional priming 19

Mentalizing/Theory of Mind 20

Pro-Social Behaviour 21

Economic behaviour 22

Voluntary behaviour 24

Neuroscientific Sex Differences 25

Neuroanatomical Overview of Sex Differences in the Brain 27

Affective Sharing 29

Mirror neurons

Emotion contagion 32

Pain 35


Self-other awareness 38

Mental flexibility 39

Perspective taking

Theory of mind 40

Regulatory processes 43

Potential explanations 45

Discussion 47

Conclusion 52

References 55

Appendix 72


Introduction

With a difficult history characterized of both discrepancy and disagreements,

there is still no general agreement of the concept of empathy. Nevertheless, research on

empathy display consistent empirical data in relation to a wide range of species (Preston & de

Waal, 2002). Further, empathy is a vital element of social cognition, and social cognition is

essential for mental health. In light of this, it has been argued that it is important to investigate

sex differences (SD) in the neural mechanisms underlying empathy; more specifically

referring to that mapping SD in empathy might contribute to resolve the neurobiological bases

of many psychiatric disorders that differ between female and male (e.g. autism, antisocial

personality disorder, depression etc.)(Christov-Moore et al., 2014).

The terms sex and gender are used interchangeably within the research fields of

psychology, developmental, and neurocognitive sciences. For simplicity and consistency, as

well as with the purpose to emphasize the biological perspective taken, the author will refer to

sex differences throughout the paper, more specifically meaning biological differences

between females and males.

The aim of the paper is to give an overview of behavioural, psychological and

neuroscientific SD in empathy. First, the author will define the concept of empathy. Further,

evolutionary and developmental perspectives of empathy will be reviewed. Moreover, an

overview of behavioural and psychological SD in empathy will be presented. Further,

neuroscientific SD in empathy will be presented in line with the model of empathy proposed

by Decety and colleagues (Decety & Jackson, 2004; Decety & Moriguchi, 2007). Potential

explanations to the research findings presented will be proposed. Discussion of content and

limitations of findings will be followed by concluding remarks and future directions.


Defining Empathy

Empathy is a multidimensional phenomenon that has been studied for hundreds

of years, and generally is agreed to be a fundamental component of our social and emotional

lives (Preston & de Waal, 2002; Decety & Cowell, 2014). Still, there is no agreement among

researchers about a definition of empathy. Despite this, there is a general view of that

empathy consists of both emotional and cognitive components (e.g. Baron-Cohen &

Wheelwright, 2004; Berglund & Annett, in press; Decety & Jackson, 2004; Shamay-Tsoory,

Aharon-Peretz, & Perry, 2009;).

The emotional component of empathy refers to the ability to experience similar

emotional states as the emotional states in another person, further meaning having the

capacity to get affectively aroused by the other person’s emotions. The concept of sharing

emotions with anther person is also referred to as affective resonance (AR) and emotion

contagion (EC) (Decety & Cowell, 2014).

The cognitive component of empathy refers to a more cognitive role-taking

ability, meaning being able to engage in the cognitive process of adopting the psychological

point of view of another person (Frith & Singer, 2008). The capacity to create a theory of

another persons’ mental state and further cognitively take the perspective of that person is a

more complex form of empathy than emotional empathy (Shamay-Tsoory, 2011). Cognitive

empathy further involves abilities such as theory of mind (ToM), the capacity to put oneself

into another persons’ shoes and imagine their feelings and thoughts (Baron-Cohen, 2009).

Although researchers mostly agree that empathy contain both emotional and

cognitive aspects, there are differing opinions in how the two aspects relate to each other.

Researchers such as Baron-Cohen and Wheelwright (2004), Shamay-Tsoory et al. (2009),

Shamay-Tsoory (2011) as well as Hoffman (2011), view the two components of empathy as


potentially distinct, meaning that the emotional and cognitive components must not

necessarily be simultaneously present.

For example, Baron-Cohen (2002) has put forward the Empathizing-

Systemizing Theory (E-S theory), suggesting that while females more commonly empathize,

males preferably more often systemize. While empathizing refers to the drive to identify the

emotions and thoughts of another person, as well as respond appropriately to this emotion,

systemizing is more of an inductive process, where systemizing refers to gathering

information to further draw certain predictions from.

Furthermore, Shamay-Tsoory and colleagues (Shamay-Tsoory, 2011; Shamay-

Tsoory et al., 2009) has proposed there are two dissociable systems of empathy. The first

system refers to a basic emotional contagion system that enable us to empathize emotionally,

while the second system is described as a more advanced cognitive perspective-taking system,

enable us to understand perspectives of other people.

In contrast to both Baron-Cohen (2002) and Shamay-Tsoory and collegues

(Shamay-Tsoory, 2011; Shamay-Tsoory et al., 2009), Berglund and Annett (in press) argue

that there cannot be cognitive empathic processes without any emotional elements. Despite

arguing against the conceptually detachment of emotional and cognitive empathy, Berglund

and Annett (in press) albeit refer to the anatomically and physiologically evidence that

support the view of emotional and cognitive empathy as built upon distinct neural correlates

(see e.g. Shamay-Tsoory, 2011).

Further, Berglund and Annett (in press) request a rejection of the

conceptualization of emotional and cognitive empathy as a dichotomy, and instead propose

the view of the concept of empathy as containing both emotional and cognitive elements. This

is in line with an empathy model proposed of Decety and Jackson in 2004, where the

researchers presented the following subcomponents to being intertwined and compelled to


work together to produce the subjective experience of empathy: affective sharing, self-other

awareness, and mental flexibility. This model was refined in 2007 by Decety and Moriguchi,

resulting in the addition of the component regulatory, referring more specifically to emotion

regulation.

Throughout the thesis, the author will refer to both emotional and cognitive

components of empathy as proposed by Berglund and Annett (in press), use aspects proposed

by both Baron-Cohen (2002) and Shamay-Tsoory and colleagues (Shamay-Tsoory, 2011;

Shamay-Tsoory et al., 2009). Still, the main perspective on empathy will be based on the

model of empathy proposed by Decety and colleagues (Decety & Jackson, 2004; Decety &

Moriguchi, 2007).

Evolutionary and Developmental Perspective on Empathy

Empathy is an ancient biological phenomenon stemming from the practice of

caregiving, especially in species where survival of offspring depends on a prolonged postnatal

caring from the mother (Preston & de Waal, 2002). When offspring show emotions indicating

feelings of hunger, stress, pain or fear, the ability to perceive and respond with care towards

offspring is to act and understand basic empathic behaviour (Decety, Norman, Berntson, &

Cacioppo, 2012). The human infant has an innate biological system for endorsing proximity

seeking of a figure to attach to. Infants inborn system aim at increasing the probability of

survival to a reproductive age, and is more commonly called attachment (Sroufe, 2000).

Moreover, empathy did not become a capacity exclusively for parent and

offspring. Rather, once the ability of empathy had evolved, the capacity further got

disconnected from its ultimate goal (de Waal, 2008). In addition, empathy has roots in group

living (Decety, 2015). The ability to communicate with one another, sharing information of

intentions and emotions and further respond correctively to relatives and offspring in need,

have been essentially for the mammalian reproductive fitness and survival (Decety et al.,


2012). Depending on the social relationship and context, empathy not only promote affective

communication, but also may contribute with motivation to pro-social behaviour towards

other conspecifics (Decety, 2011).

With basis in Decety and Moriguchi’s (2007) model of empathy, evolutionary

and developmental perspectives of empathy will be presented below.

Affective Sharing

EC, also referred to as mimicry, is an automatically appearing ability to adopt

the emotional state of another person, and further agreed as the most basic form of empathy

(Berglund & Annett, in press; Christov-Moore, et al., 2014). One adaptive advantage of

humans ability to unconsciously and unintentionally mimic behaviours (e.g. rate of speech,

tone of voice, posture etc.), is that it bind people together and cultivate liking, interaction and

empathy (Decety & Jackson, 2004). In comparison to more advanced cognitive capacities,

basic affective circuits in the brain developed much earlier (Decety & Svetlova, 2012).

The involuntary and rapid response when a person mimics another persons’

facial expression is referred to as rapid facial mimicry (RFM) (Mancini, Ferrari, & Palagi,

2013). In a study on non-ape species, the Gelada, results showed that both the highest level of

RFM and fastest responses took place between mother and infant (Mancini et al., 2013).

Another mimicry behaviour is the contagious yawing, found in both human, non-human

animals, e.g. apes and non-ape gelada baboon (Palagi, Leone, Mancini, & Ferrari, 2009). In

relation to gelada baboons, the contagious yawning has been proposed to be more frequent

between the baboons that are in a closer relationship to each other, further proposed as

support for a nonhuman primate experience of empathy (Palagi et a., 2009). Moreover, in

relation to SD, the results showed that yawn contagion was especially noticeable in relation to

adult females, and that females exhibited more matching yawn types than did males.


Researchers’ interpret the findings as potential support for deeper bond between females than

males (Palagi et al., 2009). Further SD in EC will be reviewed later.

In relation to humans, human infants are biologically predisposed to affectively

resonate with basic positive and negative affective states of others (Decety & Svetlova, 2012).

For example, one study found that when a calm infant heard the sound of another neonate cry,

the calm infant started crying. Moreover, they found that newborn babies responses were both

species- and peer-specific, and further that the babies could discriminate between their own

and other infants’ crying. The results show evidence for that human infant exhibits

rudimentary EC (Marin & Clark, 1982).

Further, there is support for SD in EC in human infants. Neonatal imitation is a

phenomenon that aims at newborn babies’ imitation of facial expressions (e.g. fear, surprise,

sadness)(Field, Woodson, Greenberg, & Cohen, 1982). In relation to newborn infants (3-96

hours old), researchers found that girls in comparison to boys, have more fine motor

movements, as well as exhibit a greater amount of specific imitative gestures. Additionally, in

comparison to boys, girls respond faster during imitation. Researchers argue that girls, as both

more accurate and faster in relation to imitative skills, might attain better social environment

(e.g. responsive and interactive) in comparison to boys (Nagy, Compagne, Orvos, & Pal,

2007). More SD in EC will be presented further below.

In relation to other species, humans exhibit more complex and advanced levels

of empathy; this coupled to self-awareness and perspective- taking, and further coupled to the

maturation of the prefrontal cortex (PFC) and its reciprocal relation to the limbic system

(Decety & Svetlova, 2012).

Self-Other Awareness

In addition to EC, to acquire a complete empathic experience, one must be able

to distinguish oneself from another (Decety & Meyer, 2008). Humans have an ability to


understand that the self and other people are similar, but yet separate; we do seldom confuse

first-person knowledge with third-person knowledge. This is an ability that starts to develop

around the second year of life (Decety & Svetlova, 2012), and the skill enable one to learn to

use the knowledge about the self to infer about other people’s mental states (Decety &

Jackson, 2004). The ability of self-awareness and hence a clear sense of self are supposed to

have developed to solve two adaptation problems; 1) though the self is an “archive” of social

feedback we have received from others, the self become a major impact in guiding adaptive

interpersonal strategies; 2) the self contribute with an understanding of other people’s

subjective world (Forgas & Williams, 2014).

According to de Waal (2008), the ability to recognize oneself from a mirror,

might be a capacity that coevolved with empathy. In order to be able to recognize oneself, one

must understand that one’s own reflection in the mirror represents oneself, not another

individual (Prior, Schwarz, Günrürkün, 2008). Self-recognition has been found in for

examples chimpanzees (Suarez & Gallup, 1981). From this finding, the researchers also

concluded that other apes did not exhibit this ability, and further made them speculate that the

self-recognition ability might not extend below humans and great apes. But in 2001,

researchers found self-recognition ability in dolphins (Reiss & Marino, 2001), and later also

in the European Magpie, Pica pica, supporting the notion that the neocortex in not necessary

to the self-recognition ability (Prior et al., 2008).

Mental Flexibility

Perspective taking is the human cognitive capacity to intentionally adopt the

subjective perspective of another person to represent their knowledge or emotional experience

as compared to one’s own knowledge and emotional experience (Decety et al., 2012). It has

been argued that the development of perspective-taking occur around the same age as the

emergence of self-recognition, based on the both abilities’ need for secondary representations


(Asendorpf, Warkentin, & Baudonnière, 1996). Further, when comparing younger and older

adolescents, results show that younger score lower on the factor Perspective taking, and

higher on Personal distress as measured by Interpersonal Reactivity Index (IRI) (Davis, 1980)

(Hawk et al., 2013). Furthermore, females scored higher on each subscale mentioned, and

Empathic concern, in comparison to males.

Another concept related to mental flexibility is theory of mind (ToM). ToM,

also referred to as mentalizing, is the ability to make implicit assumptions about the

behaviours of other people based on one’s own desires, attitudes and beliefs (Frith & Frith,

2003). The evolutionary perspective on ToM suggests that the ability must have evolved from

the capacity to monitor biological motion and from imitation behaviours (Abu-Akel, 2003).

Although it has been suggested that chimpanzees exhibit ToM (Premack & Woodruff, 1978),

the ability to mentalize is almost exclusively a human capacity (Gallagher & Frith, 2003).

Researchers argue that children around three to six years old, develop a new

cognitive skill that enable them to understand the concept of deception, as well as understand

other people’s beliefs and potential consequences of those beliefs although that might be in

conflict with either reality or the observing child’s beliefs (Wellman, Cross, & Watson, 2001;

Wimmer & Perner, 1983).

Regulatory Processes

As earlier stated, one important aspect of empathy is the ability to disentangle

oneself from others in a sense of self-other awareness, with the aim to avoid emotional

distress or anxiety, emotions that are not a part of the subjective experience of empathy

(Decety & Jackson, 2006). Moreover, there are clear adaptive advantages of the ability to

regulate one’s own emotions, both for the individual and the species (Eisenberg et al., 1994).

Researchers have showed that being able to regulate one’s emotions increase the likelihood of

both experience empathy as well as act in morally desirable ways (Eisenberg, Smith,


Sadovsky, & Spinrad, 2004). Regulating one’s emotions are referred to cognitive top-down

mechanisms that either aim at up-regulate or down-regulate emotions (Decety & Lamm,

2006).

All developmental periods consist of some regulatory processes, because

emotions incorporate regulatory processes (Thompson, 2011). Although, self-regulation as

well as emotional arousal is both influenced by the early maturation of the attentional

systems. These attentional systems enable voluntary control and the capacity to disengage

from emotionally arousing events (Rothbart, 2007). Moreover, the context is important in

understanding how emotional regulatory systems functions, both from a behaviourally and

neurobiological perspective. For example, cultural values, expectations, and situational

demands can shape emotional regulatory processes (Rothbart, 2007).

Furthermore, the hypothalamic pituitary adrenocortical (HPA) axis has been

suggested as influence regulatory processes as well (Thompson, 2011). This system helps to

account for decreasing emotional lability and enable a greater self-control (Gunnar &

Quevedo , 2007). Furthermore, the system is functional already in newborn’s but mature

significantly during the first years of life (Gunnar & Quevedo , 2007).

Moreover, oxytocin (OT) has been suggested as down-regulating the HPA axis

(Decety & Svetlova, 2012). OT is a small neuropeptide (Acher, 1996), which physiologically

influence on both emotions, behavioural states and on the autonomic nervous system (Decety

& Svetlova, 2012). For example, intranasal administration of OT in humans has been shown

to increase trust and thereby increase the benefits from social interactions (Kosfeld, Heinrichs,

Zak, Fischbacher, & Fehr, 2005). Although, other researchers have recommended a more

cautious approach towards OT, referring to the unlikeliness of a widely acting hormone as OT

to be funnelled to regulate mental processes specified for social cognition (Churchland &

Winkielman, 2012).


In addition to the components of empathy suggested by Decety and Moriguchi

(2007), the author will additionally go through the following components from an

evolutionary and developmental perspective; pro-social behaviour and play.

Pro-Social Behaviour

Pro-social behaviour refers to actions that aim at benefit or helping another

person or a group of persons (Decety et al., 2012). A motivator for pro-social behaviour in

human is ECN (Decety & Jackson, 2004). ECN can be evoked by the understanding and

sharing of an emotional state with another person (Echols & Correll, 2012), meaning

perspective-taking could be a motivator for ECN (Batson et al., 2003). ECN has been

observed in children in the second year in life, where the children more specifically have

developed affective, cognitive and behavioural capacities that enable concern for others in

distress (Bretherton, Frith, Zahn-Waxler, & Ridgeway, 1986). Pro-social behaviour has been

observed in both primates and other animals, as well as in humans, where behaviour such as

offering each other support when in need, repair relationship after conflicts etc. has been

argued as a sign of pro-social behaviour (Christov-Moore et al., 2014).

For example, a study investigating underlying motivation towards pro-social

behaviour in great apes, researchers focused on examining if helping behaviour were more

common towards conspecifics that had been harmed (vs. not harmed), comparing four species

of great apes (Liebal, Vaish, Haun & Tomasello, 2014). Although orangutans (but not

chimpanzees, gorillas and bonobos) exhibited more pro-social behaviour towards conspecifics

that has been harmed, compared to conspecifics that have not been harmed, researchers

conclude that overall great apes did not help more after a conspecific being harmed (Liebal et

al., 2014).


Play Behaviour

Play behaviour is argued to have developed to help children establish friendship

and get along with peers, develop fit bodies and strong bones, learn to control emotions and

impulses, as well as to learn and practice cultural skills and values (LaFreniere, 2011). In

relation to caregiving explored through play behaviour, there are studies indicating that SD

arises early in the human development (Christov-Moore et al., 2014). Although humans share

biology with primates, the aspect of socialization is argued as an important factor by

developmental psychologists, in relation to SD in play behaviour (LaFreniere, 2011).

In wild primate chimpanzees, SD appeared in juveniles in relation to play with

objects. Carrying sticks were seen as a primitive act of doll play, and this behaviour was more

common in females compared to males. The researchers suggest that the SD are due to that

stick-carrying is a form of play-mothering, hence the behaviour more prevalent in females

than males. Further the researchers suggest that the chimpanzees did not learn the stick-

carrying behaviour from adults, thus do they dismiss a more socialization focus view of

explanation (Kahlenberg & Wrangham, 2010). In line with this, earlier studies in vervet

monkey show similar results, with females playing with “feminine” toys, and males playing

with “masculine” toys more often, a behaviour researchers’ argue arise outside the influence

of social and cognitive mechanisms (Alexander & Hines, 2002).

An evolutionary and developmental background of empathy has been presented.

Next section will present findings of behavioural and psychological SD in empathy, based on

how research fields such as psychology, economy, and cognitive neuroscience divide and

approach the concept of empathy.


Behavioural and Psychological Sex Differences in Empathy

One way to approach investigating SD in empathy could be to divide the

concept to smaller pieces (Michalska, Kinzler, & Decety, 2013). Concepts that will be

presented are emotion recognition (ER), mentalizing, ToM, and pro-social behaviour.

Emotion Recognition

The ability to recognize emotional expressions is a crucial cognitive capacity

that enables humans to regulate emotionality in social interactions. In being able to

appropriately orient our own behaviour in a social context, cues such as facial expressions as

well as tone of the voice serves as fundamental guidelines (Collignon et al., 2010).

SD in psychological and physiological responses has been empirically observed

in relation to a range of emotional stimuli (Stevens and Hamann, 2012). However, observed

variability in experimental literature on affective SD might partly be explained by whether an

emotion is negative (unpleasant) or positive (pleasant). More specifically, there have been

more consistently observed SD in relation to negative emotions (NE), compared to the

prevalence of SD observed in relation to positive emotions (PE) (Stevens & Hamann, 2012).

For example, researchers have found that girls rate aversive pictures as more

unpleasant than boys do, while they do not rate neither neutral nor positive pictures as more

pleasant than boys (Sharp, Van Goozen, & Goodyer, 2006). The same study found that

children’s arousal rating to unpleasant pictures also increased with age, this unrelated to SD.

This was not observed in relation to neutral or pleasant pictures (Sharp et al., 2006).

Furthermore, from a review of SD in several observed emotion expressions from

infancy to adolescence, researchers found very small, but still significant “… gender-role-

consistent gender differences overall” (Chaplin, & Aldao, 2013, p. 754). While girls express

more PE as well as more internalizing NE (e.g. anxiety, sadness), boys express more

externalizing emotions (e.g. anger). Factors such as age, interpersonal context, and task type,


all contextual factors contributed to changes in these small SD they found. The researchers

suggest that the pattern of emotion expression that girl exhibit, might contribute to an increase

of girls’ probability of developing symptoms of anxiety and depression, as well as contribute

to their greater prosociality, compared to boys (Chaplin, & Aldao, 2013).

Below, ER will be reviewed through research focusing on facial expressions,

body language, and socioemotional priming.

Facial expression.

Facial emotions serve meaningful cues in social communication by providing

information about the character of the relationship between the interacting partners, as well as

give information about the sender’s emotional and intentional state. These facial emotions

serve as information that enables us to correctly recognise other people’s emotions, which is a

crucial factor in experiencing positive social interactions (Keltner & Kring, 1998).

With the aim to investigate multisensory processing (auditory, visually, or

audio-visually) of emotional expressions, participants’ were asked to categorize disgust and

fear expressions from dynamic visual and non-linguistic vocal clips of facial expressions.

Data from 46 participants (23 females and 23 males) indicated that females, under all stimulus

conditions, had an advantage in comparison to males. Researchers conclude there exist SD in

regard to multisensory perception of emotion expression (Collignon et al., 2010).

Another study investigated the perception of emotional facial expressions.

Results revealed that females in comparison to males were both more accurate and in addition

also more sensitive in labelling facial expressions (Montagne, Kessels, Frigerio, de Haan, &

Perrett, 2005). Furthermore, females have been observed as better able to recognize subtle

emotional expression when comparing with male (Hoffman, Kessler, Eppel, Rukavina, &

Traue, 2010). Although, these results were only true in regard to subtle emotional

expressions, while not in relation to full-blown emotions. Hence, the authors conclude that SD


in relation to ER depend on the intensity of the presented emotional expression (Hoffman et

al., 2010.)

Hampson, van Anders, and Mullin (2006) conducted a study resulting in

conclusion that females are both faster and better at recognizing PE and NE from facial cues,

than are males. The authors discuss the underlying mechanisms for the result and conclude

that females’ superiority is not due to neither SD in simple perceptual speed, or previous

experience of childcare. Rather, they suggest this be due to an evolved adaptation linked to

caring for preverbal offspring (Hampson et al., 2006).

With the aim to investigate recognition errors when reading facial emotional

displays, Thayer and Johnsen (2000), found that females in comparison to males, have a more

differentiated representation of emotions. Results indicated that females could distinguish

between different emotions regardless of the sex of the face displaying the emotion. Further,

researchers report that females potentially use subtle differences in arousal when trying to

extract affective information from a face displaying an emotion (Thayer & Johnsen, 2000).

Body language.

In contrast to facial expressions of emotions, bodily expressions give people

immediate knowledge about what specific action is coupled or associated with that specific

emotion, and decrease the need for interpretation (De Gelder, 2006).

With the aim to investigate potential SD in different socio-cognitive tasks,

participants were tested on recognition of distinct features from point light displays (PLDs)

that displayed bodily movements (Alaerts, Nackaerts, Mayns, Swinnen, & Wenderoth, 2011).

In comparison to males, females were better on PLD perception tasks involving both bodily

ER, and bodily action recognition (Alaerts et al., 2011).

In the similar manner, another study used PLD when investigating if there exist

SD in bodily emotional expressions, and further, how these differences gets modulated by sex


(Sokolov, Krüger, Enck, Krägeloh-Mann, & Pavlova, 2011). Researchers conclude existence

of SD in relation to body language reading, with females more accurate in reading bodily

emotions in comparison to males. No effect was found in relation to speed of body language

reading (Sokolov et al., 2011).

Socioemotional priming.

Socioemotional priming is a way to investigate whether facial emotional stimuli

has an impact on impressions, although presented outside conscious awareness (Donges,

Kersting, & Suslow, 2012).

With the aim to examine the effect of sex on affective priming based on positive

(happy) and negative (sad) facial expressions, researchers presented either happy or sad facial

expressions under the threshold of subjective conscious perception (33 ms.)(Donges et al.,

2012). Further, researchers showed the 81 participants (53 females, 28 males) a neutral face

that the subject had to evaluate. Results implicated that females in comparison to males, had a

greater ability to both perceive and respond to positive facial emotions, based on females

stronger positive evaluate shift in the happy prime condition. Emotional priming did not seem

to affect the male group in any priming condition, neither positive nor negative. The

researchers suggest that even without conscious awareness, females are able to recognize

positive valence of facial emotion (Donges et al., 2012).

In relation to ER in different moods, a study suggested that male recognize

emotions better when they are in a happy mood, compared to when in a sad mood. In

comparison, female’s ability to recognize emotions were not affected by their mood. In line

with one of the researchers hypothesis, females further performed better in the ER task than

did male (Schmid, Schmid, Bombari, Mast, & Lobmaier, 2011). Furthermore, from eye

tracking device, the researchers conclude that females process information more globally and

less locally, than male do, meaning females and male use different processing styles. The


researchers suggest their results as data supporting behavioural data for SD in information

processing when scanning faces (Schmid et al., 2011).

SD in ER, and more specifically in regard to facial expression, body language,

and socioemotional priming has been overviewed. Females seems to, in comparison to males,

be better at multisensory perception of emotions expression (Collignon et al., 2010), better

able to recognize subtle emotional expressions (Hoffman et al., 2010), be both faster and

better at recognizing PE and NE from facial cues (Hampson et al., 2006), and further have a

more differentiated representation of emotions (Thayer & Johnsen, 2000).

In relation to body language, females in comparison to males, seen to be better

in perception tasks involving both bodily emotions and action recognition (Alaerts et al.,

2011), as well as more accurate in reading bodily emotions (Sokolov et al., 2011). In relation

to socioemotional priming, females in comparison to males, had greater ability to both

perceive and respond to positive facial emotions (Donges et al., 2012), as well as were not as

much affected by their mood as males when recognizing emotions (Schmid et al., 2011).

Mentalizing/Theory of Mind

As previous described, mentalizing, also referred to as ToM, aim at the

cognitive part of empathy, enabling understanding of what another person’s thinking or

feeling due to the capacity to put oneself into the mind of another (Decety, 2015). There are

inconsistent findings in regard to SD in ToM, and further relatively few studies investigating

ToM in adults. Nevertheless, there are studies examine ToM in children (Christov- Moore,

2014).

A study examining ToM in 50 adults (25 females and 25 male) showed that

females in comparison to males performed significantly better in ToM-test (Baron-Cohen,

Jolliffe, Mortimore, & Robertson, 1997). In line with these results, a study investigating ToM

in one hundred eleven 3-5 years old children (63 girls and 48 boys) showed that girls in


comparison to boys, scored higher on ToM-tests. The same study further concluded that ToM

understanding predicted pro-social behaviour for girls, and aggressive or disruptive behaviour

for boys (Walker, 2005).

In contrast to these results, one study investigating ToM in 60 adult participants

(30 females and 30 male) did not find any SD in relation to ToM (Jarrold, Butler, Cottington,

& Jimenez, 2000). Furthermore, another study investigating ToM in 80 adult participants (40

females and 40 male), showed that male in comparison to females were superior in their

performance in ToM (Russell, Tchanturia, Rahman, & Schmidt, 2007).

Overall, there are inconsistent results in ToM. Some studies show that adult

females as well as girl are better in ToM abilities than are male and boys (Baron-Cohen et al.,

1997; Walker, 2005), while other studies do not support SD in ToM in adults at all (Jarrold et

al., 2000), or on the contrary show results indicating adult male are superior in ToM in

comparison to females (Russel et al., 2007).

Pro-Social Behaviour

Pro-social behaviours, such as helping, sharing and comforting another person,

are all actions that are intended to benefit another person (Bartal, Decety, & Mason, 2011). As

previous mentioned, prosocial behaviours could be motivated by ECN (Decety & Jackson,

2004).

There is research supporting that girl are more pro-social than boys (Baumrind,

1980). From a review article on SD in relation to peer relationships, the authors conclude that

girls in comparison to boys, have relationships that are characterized by pro-social behaviour

to a great extend, a pattern that seem to increase with age (Rose & Rudolph, 2006).

Furthermore, girls in comparison to boys seem to be more sensitive to distress observed in

other people, as well as tend to be more likely to seek support, express their emotions, as well

as ruminate in response to the stress (Rose & Rudolph, 2006).


Economic games are frequently used when studying pro-social behaviour in

adult human. One economic game is the Ultimatum Game, where a proposer and responder

divide an amount of money between them, based on the proposer’s proposal of a division of

the total sum of money. The responder’s task is to either rejects the offer, consequently both

get zero, or accept the money meaning that both get the money. There is a tendency to reject

the offer when it’s perceived as unfair (Christov-Moore et al., 2014). Similar to the

Ultimatum Game, there is the Dictator game where the main difference from the Ultimatum

game is that the receiver must always accept the offer (Christov-Moore, 2014).

SD in pro-social behaviour will be reviewed from the perspective of economic

and voluntary behaviour.

Economic behaviour.

When facing a situation of making decisions, people usually have to front some

risks. Compelling evidence from psychology and sociology suggest that females are more

averse to risks than are males (Croson & Gneezy, 2009). A meta-analysis conducted by

Byrnes, Miller, and Schafer (1999) analysed 150 studies in regard to risk-taking tendencies in

female and male subjects in relation to different settings. Based on over 100,000 participants,

the authors conclude that male participants were more likely to take risks than female

participants, although more specifically authors argue that SD varied according to both age

level and context (Byrnes et al., 1999).

Furthermore, with the aim to study behavioural SD in relation to the Ultimatum

Game, researchers conclude that there is systematic SD (Eckel & Grossman, 2001). Results

suggest that females are significantly more cooperative, based on that females are more

willing to accept a given offer, than are males. Moreover, the researchers propose context as


an important factor, referring to that the sex of the respondent’s partner effect the subject’s

decision. More specifically, the offers’ are most likely to be accepted when proposed by a

female opponent. Female’s proposals are further more often more generous than compared to

male’s offers, but this independent of the sex of the respondent. This further meaning,

females’ both get rejected and reject less frequently, than do males, and make the authors to

argue that this builds strong solidarity between females (Eckel & Grossman, 2001).

Although, in contrast to these results, another study using the Ultimatum Game

showed that females’ get rejected by both other females and male, more often than are male.

Furthermore, the lowest acceptance frequency was found in the pairing of female-female

(Solnick, 2001).

From a study using the Dictator Game, researcher conclude that females on are

less selfish, as well as donate twice as much to an anonymous partner, in comparison to male

(Eckel & Grossman, 1998). In another study using the Dictator Game, researchers conclude

that knowing the sex of the person the participant gives money to affects the amount given.

Although, this was only true for females, not male, and more specifically observed females

giving less to females than to male and persons of unknown sex (Ben-Ner, Kong, &

Putterman, 2004).

Overall, males are more willing to take risks than are females (Byrnes et al.,

1999; Croson & Gneezy, 2009). Furthermore, there are inconsistent findings in relation to

economic games. While some researchers suggests that females tend to be more cooperative,

more generous in their economic offers, and tend to less often both get rejected and self reject

economic offers, in comparison to males (Eckel & Grossman, 2001), others suggest that

females get rejected by both sexes more often than do males (Solnick, 2001). Moreover,


females are less selfish, donate more money (Enckel & Grossman, 1998), and get more

affected in their economic decisions by the sex of the recipient (Ben-Ner et al., 2004).

Economic games such as the Ultimatum Game and the Dictator game may be

argued to have little ecological validity. But there is research supporting these experimental

findings, more specifically research studies that examine voluntary behaviour (Christov-

Moore et al., 2014).

Voluntary behaviour.

Bekkers and Wiepking (2011) have suggested several mechanisms that enable

people to give. One study chose two of the suggested mechanisms, ECN and the principle of

care, and examined them in relation to giving and potential SD (Mesch, Brown, Moore, &

Hayat, 2011). Overall, both ECN and the principle of care were mechanisms that affected

giving, more specifically meaning both mechanisms were positively related to giving in both

sexes. Furthermore, results showed SD in relation to both what motivates females and males

to give, and also suggest that these differences influences actual charity giving. Results

showed that females scored higher on both ECN and the principle of care, and were both

more capable to give and also give more, in comparison to male (Mesch et al., 2011).

Another study aimed at studying whether or not sex, race and/or marital status

influence giving and voluntary behaviour (Mesch, Rooney, Steinberg, & Denton, 2006).

When controlling for differences in age, income, educational attainment and survey

methodology, researchers found that single females were more likely to give at all, and further

also to give more than single male. In a similar manner, single females in comparison to

single male, were more likely to volunteer, and further also volunteer more hours than single

male. Both married females and male in relation to single male were more willing to donate,


albeit not more money than single male. The researchers highlight the interesting results

referring to the fact that both married and single female are associated with an increase in

likelihood of giving, indicating that females potentially socialize males in relation to

philanthropic giving (Mesch et al., 2006).

To summarize, females score higher in both ECN and principle of care, are

more capable to give and further give more money, than do males (Mesch et al., 2011). In

addition, both single and married females are more willing to give, in comparison to males,

whereas single males are most less likely to give (Mesch et al., 2006). Single females are also

more likely to volunteer as well volunteer more hours than single male (Mesch et al., 2006).

Evolutionary background, developmental perspective, as well as psychological

and behavioural SD, all in relation to empathy, have been presented. Next, there will be a

review of neuroscientific SD in empathy.

Neuroscientific Sex Differences of Empathy

As previous discussed, the concept of empathy can be approached from different

perspectives. Baron-Cohen (2002) and the proposed E-S theory, as well as Shamay-Tsoory

(Shamay-Tsoory, 2011; Shamay-Tsoory et al., 2009) and the dissociable system of empathy,

view the emotional and cognitive components of empathy as separable at times. Other

researchers such as Berglund and Annett (in press) view the emotional and cognitive

components as intertwined, meaning cognitive empathy cannot exist without emotional

elements. Although Berglund and Annett (in press) deny the conceptual detachment of

emotional and cognitive empathy, they still, in line with Baron-Cohen (2002) and Shamay-

Tsoory (2011) approach neuroscientific underpinnings of empathy with focus on the

emotional and cognitive distinct neural correlates.


The model of empathy proposed of Decety and colleagues (Decety & Jackson,

2004; Decety & Moriguchi, 2007) is based on theories and data from behavioural neurology,

developmental psychology and cognitive neuroscience. As precious discussed, their model

contain the following subcomponents of empathy; (1) affective sharing, (2) self-other

awareness, (3) mental flexibility, and (4) regulatory processes (Decety & Moriguchi, 2007).

With basis in Decety and colleagues model of empathy, neuroscientific SD in empathy will be

reviewed.

From en cognitive neuroscientific perspective, empathy is often approached

from either an affective (pre-reflective) or a cognitive (reflective) point of view (Christov-

Moore et al., 2014). The affective components of empathy are often examined through

preconscious mechanisms underlying and facilitating sharing (and mimicry) of both

behaviours and other people’s mental states, often referred to as mirroring (Zaki & Ochsner,

2012). Affective empathy is generally associated with sensation, movement and emotions,

and is further related to activity in frontoparietal, temporal and subcortical regions (Zaki &

Ochsner, 2012).

In contrast, the cognitive components are investigated through conscious

processes from what assumptions about other people’s affective and bodily states, beliefs and

intentions can be made, often referred to as mentalizing (Christov-Moore, 2014; Zaki &

Ochsner, 2012). Cognitive empathy is associated with decision-making and cognitive control,

tasks that are associated with activity in areas such as the cingulate, prefrontal, and temporal

areas (Zaki & Ochsner, 2012).

Research support that the experience of empathy is facilitated through an

interaction between the mirroring and mentalizing areas, rather than enabled from the two

distinct systems alone (Christov-Moore et al., 2014). Furthermore, from a developmental

perspective, the affective components develop earlier than both the cognitive and regulatory


components (Decety, 2011).

The neuroscientific section begins with an overview of neuroanatomical sex

differences in the brain. Moreover, based on the model of empathy proposed of Decety and

colleagues (Decety & Jackson, 2004; Decety & Moriguchi, 2007), a review of the

neuroscientific underpinnings of the previous mentioned components of empathy will be

presented, followed by an overview of the neuroscientific SD observed in relation to those

specific components.

Neuroanatomical Overview of Sex Differences in the Brain

There are different theories concerning emotion and brain. For example,

researchers have suggested that both hemispheres process emotions, but that e.g. PE is mainly

enabled through the left hemisphere, and NE are specialized through the right hemisphere

(Gur, Skolnick, & Gur, 1994). Other theories have suggested that the left hemisphere is

specialized on cognitive processes while the right hemisphere is mainly concern with emotion

processing (Wager, Phan, Liberzon, &Taylor, 2003). Although, a quantitative meta-analyses

of 65 neuroimaging studies of emotion, and concluded that the emotional brain is much more

complex and region specific than what has been suggested from previous hemisphere-level

hypothesis (Wager et al., 2003).

Furthermore, females in comparison to males exhibit more gray matter (GM)

volume in the cingulate cortex, traditionally part of the limbic system. More specifically,

females had increased GM volume near the depths of both the central sulci as well as the left

superior temporal sulcus, in right Heschl’s gyrus and planum temporale, in right inferior

frontal and frontmarginal gyri and in the cingulate gyrus. Furthermore, females had increased

GM concentration in the cortical mantle, parahipocampal gyri, and in the banks of the

cingulate and calcarine sulci (Good et al., 2001). Furthermore, researchers have found that the

mirror neuron system (MNS) display SD in regarding neuroanatomical volume (Cheng et al.,


2009). In comparison to males, females exhibit larger GM volumes in the right inferior frontal

gyrus (IFG), and in the pars opercularis and inferior parietal lobule (IPL) of the RH, structures

suggested as core areas of the MNS, and further located near the MNS (10 mm)(Cheng et al.,

2009). Moreover, females exhibited greater GM volumes in brain regions associated with

social information processing, such as bilateral posterior inferior frontal and left anterior

mPFC (Yamasue et al., 2008). In comparison, males showed increased GM volume bilaterally

in mesial temporal lobes, entorhinal and perirhinal cortex, and in the anterior lobes in the

cerebellum. No increased GM concentration was found in males (Good et al., 2001).

Older studies support these findings, suggesting females, in comparison to

males, have a higher percentage of GM (Gur et al., 1999). Further, males in comparison with

females, exhibit a higher percentage of white matter (WM) and cerebrospinal fluid. The

percentage of GM in male were higher in the left hemisphere, while the WM was symmetric

across both hemispheres. The percentage of cerebrospinal fluid was higher in the right

hemisphere in male. These asymmetries were not observed in females. Researchers conclude

that the sex differences and asymmetry of GM, WM, and cerebrospinal fluid could be a factor

contributing to differences in cognitive functioning (Gur et al., 1999). Furthermore, males

exhibited larger amygdala and cerebellum volumes. Females with larger volume of the MNS

also had greater volume in the social brain regions Cheng et al., 2009).

To summarize; Females in comparison to males exhibit more GM volume in the

cingulate cortex, pars opercularis, IPL of the RH, and in parts of the mPFC, as well as have

increased GM concentration in areas such as the cortical mantle parahipocampal gyri and in

the banks of the cingulate and calcarine sulci (Cheng et al., 2009; Good et al., 2001). Males

show increased GM volume in bilateral mesial temporal lobes, entorhinal and perirhinal

cortex, and in the anterior lobes in the cerebellum (Good et al., 2001). Further, males have

higher percentage of WM and cerebrospinal fluid, as well as larger amygdala and cerebellum


volumes in comparison to females (Cheng et al., 2009; Gur et al., 1999).

Below, SD in relation to the subcomponents of empathy suggested of Decety

and colleagues will be presented (Decety & Jackson, 2004; Decety & Moriguchi, 2007).

Affective Sharing

As a component of affective empathy, affective sharing refers to the emotional

sharing between self and other, enabled by a perception-action connection resulting in shared

representations (Decety & Jackson, 2004). Shared representations between perception and

action have both behavioural and neurophysiological evidence (Decety & Jackson, 2004). For

example, infants have an innate capability to imitate from birth, which has been suggested as

robust evidence for the perception-action coupling. This simple motor resonance behaviour

mechanism, this neural activity automatically activated when observing gestures, movements

etc., cannot though solely explain infants’ ability to imitate from birth. Rather, infants’

capability of imitation has come to be considered as a social response (Decety & Jackson,

2004). Structures such as the amygdala, thalamus (TH) and the orbitofrontal cortex (OFC) are

considered to play a crucial role in relation to the perception- action connection. Furthermore,

the reciprocal connection between amygdala and OFC, and the superior temporal sulcus

(STS) enable a fast processing of affective information (Decety, 2011).

Sex differences in affective sharing will be reviewed through research findings

in relation to MNS, EC, and pain.

Mirror Neurons.

From a study on Macaque monkeys, researchers found neurons in the rostral

part of iPFC (F5) that fire both when the monkey themselves engage in specific hand

movements (e.g. grasping and holding) as well as when the monkey observe the experimenter


execute specific and meaningful hand movements (Di Pellegrino, Fadiga, Fogassi, Gallese, &

Rozzolatti, 1992). This discovery of the so-called mirror neurons has been considered as a

breakthrough in neuroscience, with the finding contributing to the research field with a better

understanding of the brains ability to feel what one would feel during the execution of a

similar action as the one observed (Keysers & Fadiga, 2008).

Although derived from indirect evidence, functional imagining studies have

proposed that humans exhibit mirror neurons as well. More specifically, mirror neurons have

been observed in area 44 (Brocca’s area) and the nearby ventral area 6 (Rizzolatti &

Craughero, 2004). Area 44 has been argued to be cytarchitechtonically homologous to the F5

in the PMC (Petrides, Cadoret, & Mackey, 2005), an area that has been reported as central to

the human MNS (Rizolatti, 2005) In another study, researchers used extracellular recording of

1177 cells in the medial frontal and temporal cortices in humans. The results made

researchers conclude that neural mirror mechanisms exist in multiple systems in the human

brain, with the aim to flexible integrate and differentiate perceptual and motor aspects of

action executed by the self and other (Mukamel, Ekstrom, Kaplan, Iacoboni, & Fried, 2010).

The mirror neurons importance for emotion perception is supported by e.g. one study that, in

relation to observation and imitation of facial expressions of emotion, observed activation in

IFG (Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003).

In relation to SD, a study using fMRI on 26 participants (14 females and 12

males), argue that their results support the notion of that females recruit areas containing

mirror neurons to a higher degree than do males, in face-to-face interaction (Schulte-Rüther,

Markowitsch, Shah, Fink, & Piefke, 2008). Furthermore, as previous mentioned, MRI studies

show evidence of that females, in comparison to males, exhibit larger GM volumes in the pars

opercularis and IPL of the right hemisphere, all areas involved in the MNS (Cheng et al.,

2009).


With background in that females are considered to be superior in interpersonal

sensitivity compared to males, and that the MNS is thought to contribute with the basic

mechanisms for social cognition, researchers did an EEG study indicating existence of SD in

MNS during action observation (Cheng et al., 2008). More specifically, the mu rhythm was

used as an indicator of the MNS activity, with the background of that mu suppression elicited

by watching hand actions is considered to indicate specific recruitment of the MNS. EEG

activity was measured in 40 participants (20 females and 20 males) while observed either a

moving dot or hand movements. Results showed that females displayed significantly greater

mu suppression when watching hand actions, compared to males). The mu suppression further

negatively correlated with the systemizing quotient (SQ) that measure the systemizing aspect

based on the E-S theory (Baron-Cohen, 2002), and positively correlated with the personal

distress subscale in the IRI (Cheng et al., 2008).

To summarize, mirror neurons is argued to have been found in area 44 in

humans, an area cytoarchitechtonically homologous to the F5 in the PMC (Petrides et al.,

2005). Other researchers have argued that mirror neurons exist in multiple systems in the

human brain (Mukamel et al., 2010). Further, mirror neurons are crucial for emotion

perception, based on findings of mirror neurons in IFG (Carr et al., 2003).

In face-to-face interaction, females recruit mirror neurons to a higher degree

than do males (Shulte-Rüter et al., 2008). Females also have larger GM volumes in areas

associated with the MNS, such as the pars opercularis and the IPL of the RH (Cheng et al.,

2009). Furthermore, females recruit mirror neurons to a greater extent when observing hand

movement, in comparison to males (Cheng et al., 2008).


Emotion contagion.

Bodily and facial expressions communicate similar information and are both

important and natural parts of the everyday life, as well as have strong biological

underpinnings (de Gelder et al., 2010).

From a review article on electrophyphysiological recording in neurosurgical

patients, authors argue that social perception are dependent on the STS, an area that seems to

be specialized for encoding complex visual stimuli, such as eyes and faces (Allison, Puce, &

McCarthy, 2000). Additionally, the researchers point out that STS is anatomically well placed

in relation for integration of information from the dorsal and ventral visual pathways.

Furthermore, in relation to face perception, researchers have suggested

amygdala as a central structure for the processing of social relevant information, especially in

regard to potential threat (Haxby, Hoffman, & Gobbini, 2002). For example, a study with the

aim to investigate the neural mechanisms underlying the human ability to detect more

complex facial expressions, researchers used a test of detection on participants with lesions to

the temporal lobe (54 participants) or frontal lobe (31 participants)(Shaw et al., 2005).

Researchers found that impairment in recognition of both cognitive and social expressions

was related to damage in both left and right amygdala. Furthermore, the ability to recognize

complex social expressions with negative valence was impaired in relation to damage to the

whole right PFC. Researchers conclude that the ability to process a wide range of emotional

expressions, from basic to more complex cognitive and social expressions, depend on the

contribution of amygdala (Shaw et al., 2005).

Based on psychological studies, there is evidence for that female in comparison

with males has better memory of emotional events. With this background, researchers wanted

to investigate potential neuronal SD in relation to the female superiority in emotional

memory. Researchers used fMRI on 24 participants (12 females and 12 males) while asked to


rate their experienced emotional arousal in relation to either emotionally negative or neutral

pictures (Canli, Desmond, Zheo, & Gabrieli, 2002).

In a follow up three weeks after, participants did a recognition memory test,

showing both females and males remembered emotional pictures the most, although females

remembered them better than males. Furthermore, the results showed that in relation to

encoding stimuli effectively into memory, females used significantly fewer brain structures

involving the left amygdala, than did males, while males used more structures in a network

including the right amygdala in relation to the same purpose. Moreover, both while on going

evaluation of emotional experience as well as with subsequent memory for the most

emotionally arousing pictures, females showed significantly more brain regions activated,

compared to males, which might explain why females have better emotional memory than

males (Canli et al., 2002)

Another study used fMRI with the aim to investigate SD in the brain activity in

regard to emotions elicited by (1) facial expressions and whole body images, (2) video clips,

and (3) further investigate the role of the sex of both observer and the one stimulus display

(Kret, Pichon, Grézes, & De Gelder, 2011). The results showed that when participants

observed male versus female actors expressing threat, the BOLD signal was higher in STS

(associated with face and body perception), extrastriate body area (EBA)(important for body

perception), and pre-supplementary motor area (pre-SMA)(involved in action preparation),

and PMC.

Furthermore, in the regions mentioned, plus fusiform gyrus (associated with

face and body perception), researchers found an interaction between category, emotion and

observer, indicating that male participants showed more activation if they were presented with

the male threatening in comparison to the neural body. Moreover, the highest activity in STS

was triggered by threatening bodies, not faces, also this particularly in male participants. In


relation to the EBA, male participants responded more to threatening body expressions than

did females. The activation in amygdala was in comparison to bodily expressions, greater in

facial expressions, no matter what kind of emotions observed. This was especially true for

males that were presented with female faces. Concluding remarks from the researchers was

their emphasis of the importance of whether a body or face is presented in relation human

emotion perception, as well as the importance of the sex of both observer and the observed

(Kret et al., 2011).

In conclusion, STS is an area crucial for social perception and encoding

complex visual stimuli such as eyes and faces (Allison et al., 2000). Furthermore, amygdala is

an important structure for processing both basic and complex cognitive and social information

(Haxby et al., 2002; Shaw et al., 2005). Moreover, the PFC is important for recognition of

social expressions with negative valence (Shaw et al., 2005).

In relation to SD in emotion memory, when evaluating and consolidating

memory, females recruit more brain regions than do male (Canli et al., 2002). Females

remember better as well recruit fewer brain areas involving the left amygdala to consolidate

stimuli into memory, than male. Male use more structures in a network including the right

amygdala than females do. (Canli et al., 2002).

Factors such as whether body or face, female or male express emotions, affect

the brain responses in the observer (Kret et al., 2011). When male express threat, higher

activation is observed in STS, EBA, the pre-supplementary motor areas, and PMC, in both

sexes. Threatening bodies (vs. faces) cultivate the greatest activity in, especially in male, who

further responded more to bodily threatening expressions than did females, cultivating

increased activity in EBA. Amygdala becomes activated more to facial expressions (vs

bodily), especially in male presented with female faces (Kret et al., 2011).


With background in that emotional tone of voice display the significance of the

communicated utterance, researchers investigated whether participants were able to recognize

this significance although attending to something else. Of special interest for the researchers,

was potential SD in regard to this. Analysis of ERP data from 80 participants’ showed that

both female and male were able to detect voice changes preattentively (Schirmer, Striano, &

Friederici, 2005).

Although, SD were detectable, suggesting that females exhibited larger

mismatch negativity in relation to emotional deviants than to neutral deviants. More

specifically, researchers conclude that females in comparison to male show enhanced

emotional processing at a relatively early and automatized stage where information is still

unattended (Schirmer et al., 2005).

Pain.

Pain expressions can serve as an important signal to motivate helping

behaviours in other people. Therefore, investigating how people perceive others in pain can

be a way to examine the neural mechanisms enabling empathy. Furthermore, there are studies

indicating that several brain areas are involved in the processing of both the observation of

pain in other people, as well as in the affective and motivational aspects if one’s own pain

(Decety & Jackson, 2006).

One study used fMRI to (1) test for unique and shared networks for experienced

and empathic pain (Singer et al., 2004). The researchers conclude that the rostral anterior

cingulate cortex (rACC) and anterior insula (AI) cortices, both areas associated with

activation for noxious stimuli play an important role in the experience of empathy. Pain-

related activation was found in primary somatosensory cortex (SI), secondary somatosensory

cortex (SII), bilateral insula cortex, ACC, TH, brainstem and cerebellum.


When empathizing with others in pain, only part of the pain-related network was

activated, more specifically in left and right AI, ACC, lateral cerebellum and brainstem. The

authors view their empathy-related findings as support for an automatically triggered

engagement in empathic processes when people observe others in pain. Areas such as

contralateral SI, SII/posterior insula, and caudal ACC are pain-related areas more specifically

activated in relation to the experience of self-pain than perception of others-pain (Singer et al.,

2004). In line with these results, Morrison, Lloyd, Pellegrino, and Roberts (2004) conducted a

fMRI study showing that the right dorsal ACC was activated when participants experienced

moderately painful pinprick stimulus to the fingertips, as well as when they only observed

another person’s hand undergo similar stimulation.

Two years later, Singer et al. (2006) investigated if and in that case how, the

neuronal systems that underlie our own bodily and emotional states when empathizing, could

be modulated by the social relations between individuals. By using the economic game model

Prisoner’s Dilemma (PDG), with confederates’ actors either playing fair or unfair, the

researcher induced liking or disliking in the participants. After, by using fMRI on the

participants, the researchers investigated if the liking or disliking could modulate empathic

responses for pain, through applying painful stimulation to the confederates.

When observing unfamiliar but fair-playing person in pain, there was pain-

related empathy related activity, more specifically in AI ranging into fronto-insular cortex

(FI) and brainstem, in both sexes. While the ACC activation were more borderline in male,

the ACC activation in females was significant. Those male and females exhibiting higher

empathy-related bran activity in AI/FI and ACC, also displayed higher scores on standard

empathy scale22 (Singer et al., 2006).


Furthermore, results showed that when an unfair player was exposed to pain,

there was less empathy- related activity in the observer. This reduction of activity was very

small in females, while significant in male. When comparing fair and unfair players receiving

pain, females did not differ in activation in empathy related pain regions. On the contrary, a

significant increase in activation in bilateral FI was observed in males when a fair player was

observed getting pain, compared to observed non-fair players in pain (Singer et al., 2006).

In addition to these results, male showed increased activation in left ventral

striatum/nucleus accumbens (VS/NA), and left orbitofrontal cortex (OFC), areas related to

reward-processing, when researchers compared the painful trials in the fair and unfair-

condition. Male showed significantly higher activation in left NA in comparison to females,

when comparing painful trials in the unfair and fair condition. Further, not true for females,

but males, there was a greater activation in NA when perceiving an unfair player getting

painful stimuli (versus perceived fair player in pain), which also correlated positively with a

stronger desire for revenge measured by post-experiment questionnaires measuring a

subjectively expressed desire for revenge. This was not found in females. Both VS/NA and

OFC have been considered to be reward-processing areas (Singer et al., 2006).

Another study used EEG with the aim to investigate SD in neural mechanisms

underlying empathy for pain, where the researchers’ compared event-related brain potentials

(ERP) between females and male (Han, Fan, & Mao, 2008). Pictures of hands that were either

in neutral or painful situations were presented for participants. The subjects were asked to

perform a pain judgement task that either demand attention to perform a counting task that

withdrew their attention from the pain cues, or focus their attention to pain cues in the

presented stimuli. 140 ms after stimulus onset, there was a short-latency empathic response

over the frontal lobe, signalling differentiation between neutral and painful stimuli, both in


female and male. 380 ms after stimulus onset there was a long-latency empathic response in

both male and female, over the central-parietal regions.

Although, in comparison to male, females showed stronger modulation by task

demands in the long-latency empathic response. Furthermore, the subjective reports of the

degree of perceived pain of others and of unpleasantness of the self correlated with the ERP

amplitudes at 140-180 ms, only in females not in males. Researchers conclude that their study

provide ERP evidence for SD in processes of empathy for pain (Han et al., 2008).

To summarize, brain areas such as ACC and AI are important for the experience

of empathy. Some parts of the pain-related network are activated when empathizing with

other in pain, more specifically left and right AI, ACC, lateral cerebellum and brainstem

(Morrison et al., 2004; Singer et al., 2004).

Furthermore, both females and male recruit empathy-related activation in pain-

related areas, more specifically fronto-insular and ACC, when observing fair players

receiving pain. However, male exhibit a decrease in empathy-related responses when unfair

players receive pain, not seen on females. Furthermore, increased activation in reward-related

areas such as VS/NA, and left OFC, is observed in male but not females, when observing

unfair players receive pain (Singer et al., 2006). Researcher argue their result can be

interpreted as that empathic responses are shaped by valuation of other people’s social

behaviour, but only in male, not in females. Moreover, SD in processes of pain was found,

indicating that females showed stronger modulation by the task demands in the long-latency

empathic response, in comparison to male (Han et al., 2008).

Self-Other Awareness

The next subcomponent of the model of empathy is self-other awareness, which

as previous discussed, is the human ability to understand that self and other is similar but still

separate starts to develop around the second year of life (Decety & Svetlova, 2012). Decety


and Jackson (2004) propose that the inferior parietal cortex in combination with the PFC

together serve as critical structures in the sense of self by enabling discrimination of the

source of sensory signals. Hence, the mentioned areas are crucial in the distinction between

the self and others, and thus necessary for the experience of empathy. Furthermore, areas such

as the frontopolar, the somatosensory cortex, and the right IPL has been argued to be crucial

for the ability to distinguish between self and other (Ruby & Decety, 2004).

For more recent results, an fMRI study showed that by processing degrees of

self-relatedness, the mPFC might sustain the process of identifying oneself with current

representations of the self. Furthermore, the researchers propose that the right inferior parietal

cortex might be engaged in distinguishing the present self from temporally distant selves

(D’Argembeau et al., 2010). Moreover, from a meta-analysis of fMRI studies focusing on the

role of the right temporo-parietal junction (TPJ), Decety and Lamm (2007) argue that the

brain area of interest play a crucial role in both low-level and high-level cognitive functions.

Self-awareness seems to have similar cognitive processes as well as neural

circuitry as the concept of ToM (Decety & Svetlova, 2012; Leslie, 1987), and therefore, SD

will be reviewed under the subtitle ToM.

Mental Flexibility

Mental flexibility refers to the ability to adopt the subjective perspective of another person

(Decety & Moriguchi, 2007), an effortful and controlled process that further serves as a

crucial component in ToM (Decety & Jackson, 2004).

Perspective taking.

As previous stated, perspective taking is the human cognitive ability to adopt the

subjective perspective of another person, an ability that requires both working memory and


inhibitory control (Decety et al., 2012).

Regions such as the posterior STS/TPJ, the temporal poles (TPs) and the mPFC

has been considered to be involved in the processes of one thinking about the mental states of

another person. Based on research in relation to each area, authors have theorized about how

each region mentioned contributes in the mentalizing ability. While the mPFC is though to

enable decoupling the mental state representations from physical state representations, the

STS is hypothesized to enable detection of agence. The role of the TPs seems to be to

contribute with social knowledge in the form of scripts (Frith & Frith, 2003). In line with this,

a more recent fMRI study concludes that the mPFC are crucial in multiple forms of self-

reflection (Jenskins & Mitchell, 2011). Moreover, and as previous mentioned, there are data

serving evidence for that the MNS, more specifically the IFG are involved in emotional

perspective taking (Schulte-Rüther et al., 2008).

Although the IFG are suggested as involved in emotional perspective taking in

both females and males, activation in IFG and STS is stronger in females; suggesting females

rely more on mirror neurons in assessing emotional states of other people and their own

emotional response to the feelings of others. In contrast, males recruited increased activation

in the TPJ in self-related emotional processing, suggesting they have a stronger recruitment of

ToM related areas (taking (Schulte-Rüther et al., 2008.)

Theory of Mind.

As previous declared, ToM is a mentalizing ability enabling one to make

implicit assumptions about the behaviours of other people based on one’s own desires,

attitudes, and beliefs (Frith & Frith, 2003).

Drawn upon the facts available up to 2003, researchers concluded that the


mPFC, associated with different mentalizing tasks, are activated when people attend to certain

states of the self or others. Furthermore, the researchers suggest that the TPs and the STS are

structures involved in the ability to represent mental states of others (Frith & Frith, 2003). In a

review article, authors conclude that the medial frontal cortex (mFC) play a special role in

social cognition (Amodio, & Frith, 2006).

Other studies have not found support for the mPFC as essential in ToM, but

rather proposed the right TPJ as selectively recruited for attribution of mental states (Saxe &

Kanwisher, 2003; Saxe & Wexler, 2005). In her review article, Blakemore (2008) summarize

with that both the mPFC, the ACC, the IFG, the STS, the amygdala and AI are brain areas

that are involved in social cognitive processes, such as recognizing and evaluation mental

states in other people.

With background in that it long has been hypothesized about that females and

males differ in their mentalizing abilities, researcher conducted an fMRI study on 24

participants (12 females & 12 males), investigating the impact of sex and game partner

(human vs. computer) on ToM and associated neural activity in mPFC (Krach et al., 2009).

Researchers conclude that the medial frontal regions as well as TH regions were significantly

more pronounced engaged in males compared to females (Krach et al., 2009).

In another fMRI study with 24 participants (12 females and 12 males)

researchers found SD in the neural correlated underlying emotional perspective- taking

(Derntl et al., 2010). Females particularly recruited IFG, the hippocampi, the superior

temporal gyrus and the calcarine gyri as well as the right amygdala. In contrast, males showed

stronger activation in areas such as TPJ. The researchers summarize with arguing their data

supports the notion of females activate more emotion and self-related areas, whereas males

recruit more cortical and cognitive-related regions.


As previous described, Baron-Cohen (2002) has proposed the E-S theory, more

specifically arguing females are more empathizing with the motivation to identify emotions

and thoughts of others, while male as more systemizing with a drive to gather information to

draw predictions from. Moreover, Baron-Cohen (2002) has proposed the Extreme Male Brain

(EMB) theory of autism, arguing that autistic children exhibit an extreme version of a typical

male brain. Autism is a neurodevelopmental spectrum of conditions with subgroups such as

classic autism and Asperger’s syndrome (AS) (Baron-Cohen, 2010). Children within this

spectrum fail to normally develop their ability of social interaction, use their imagination and

verbally and nonverbally communicate (Morrison, 1995). Children within this spectrum have

delayed development of ToM, further argued as a type of mindblindedness (Baron-Cohen,

1995).

In relation to SD, more boys than girls falls within the autism spectrum

conditions (ASC)(Baron-Cohen, 2010). Furthermore, in ToM, girls develop ToM faster than

do boys, and children within the ASC develop this ability even slower than do boys (Baron-

Cohen, O’Riordan, Jones, Stone, & Plaisted, 1999). This pattern of females overall better than

male in ToM, and furthermore people within the ASC below male in ToM, has been observed

also in adult population, drawn upon data from the Reading the Mind in the Eyes Test (Baron-

Cohen et al., 1997).

There is neuroscientific evidence supporting the EMB theory as well (Baron-

Cohen, Knickmeyer, & Belmonte, 2005). Brain areas such as the ACC, superior temporal

gyrus, PFC, and the TH are on average smaller in male than in females, and these regions are

further even smaller in people within the ASC (Baron-Cohen et al., 2005). Furthermore, areas

such as the amygdala, cerebellum, overall brain size/weight, as well as head circumference,

that generally is greater in male than in females, are bigger in people within the ASC than in

typical males (Baron-Cohen et al., 2005). In line with this data, as previous described, the SD


found in relation to the MNS during action observation with females’ greater mu suppression

in comparison to males, served as indirect support the EMB theory (Cheng et al., 2008).

To summarize, brain areas such as mFC/mPFC, TPs, STS, as well as the TPJ

has been argued as central to mentalizing tasks (Frith & Frith, 2003; Saxe & Kanwisher,

2003; Saxe & Wexler, 2005). Furthermore, areas such as ACC, IFG, STS, the amygdala and

AI are also associated to social cognitive processes such as evaluating mental states in others

(Blakemore, 2008).

In relation to SD, males recruit medial frontal regions and TH significantly more

than do females in mentalizing tasks (Krach et al., 2009). In relation to emotional perspective-

taking, males display stronger activation in TPJ, while females recruit IFG, hippocampi,

superior temporal gyrus, the calcarine gyri and right amygdala (Derntl et al., 2010).

Furthermore, boys fall within the ASC more often than do girl (Baron-Cohen,

2010). Brain areas such as amygdala and cerebellum are generally greater in males than in

females, and further even bigger in people within the ASC than in the typical male brain

(Baron-Cohen et al., 2005).

Regulatory Processes

The ability to regulate one’s emotions refers to cognitive topdown-mechanisms

that either aims at up-regulate or down-regulate emotions, and further increases the likelihood

of experience empathy (Decety & Lamm, 2006; Eisenberg et al., 2004).

The ability to regulate one’s emotions, affect, drive and motivation lies on

executive functions that are enabled through the dlPFC, ACC and the vmPFC through their

mutually connections with the widespread cortical areas including the STS as well as the

amygdala (Decety, 2011). For example, an fMRI study showed that the cognitive strategy of


volitionally regulating emotions was associated with activity in the medical prefrontal/anterior

cingulate (AC) and the anterolateral PFC (Kalisch et al., 2005). Another fMRI study focused

on both up- and down-regulation of negative emotions, with results showing that both up- and

down- regulation of NE was associated with activation in prefrontal and AC regions (Ochsner

et al., 2004). Furthermore, according to the regulatory goal, the activation in amygdala was

changed. Moreover, up-regulation was specifically coupled to activation of left rostromedial

PFC (associated with retrieval of emotional knowledge), while down-regulation activated

orbital PFC (associated with inhibition of behaviour)(Ochsner et al., 2004). In line with this,

Thompson (2011) argue that areas such as medial and ventral PFC as well as the AC, are all

regions involved in emotion regulation.

With the aim to investigate SD in a cognitive emotion regulation strategy

(reappraisal), researchers used fMRI on 25 participants (13 females and 12 males) while they

were asked to down-regulate their emotional responses to negatively valence pictures

(McRae, Ochsner, Mauss, Gabrieli, & Gross, 2008). In comparison to males, females showed

higher increases in the prefrontal regions associated with reappraisal, increases in the

amygdala (associated emotional responding), as well as more engagement of ventral striatal

regions (associated with reward processing).

Another study, used fMRI on 33 participants (16 females and 17 males) to

investigate SD in emotional regulation with a delayed cognitive reappraisal paradigm (Domes

et al., 2010). Results showed that females in comparison to males, when presented with

aversive stimuli and asked to increase emotions, showed enhanced amygdala responding as

well as an increased activity in small clusters within the PFC and the temporal cortex. While

emotional reactions were decreased through cognitive strategies, females in comparison to

males showed less activity in the OFC, the AC, and the dorsolateral PFC. When asked to

cognitively increase emotional reactions, male showed an increase of regulatory cortical


areas, associated with an increase in amygdala activity (Domes et al., 2010).

To summarize, brain areas involved in regulatory processes of emotions are

regions such as the PFC, ACC, STS, and amygdala (Decety, 2011; Kalisch et al., 2005;

Thompson, 2011). Furthermore, amygdala activation is modulated in accord with regulatory

goal, and activation in left rostromedial PFC is more associated with up-regulation, while

activation in orbital PFC is more coupled to down-regulation (Ochsner et al., 2004).

SD has been observed in relation to down-regulation to negative pictures, with

females recruiting prefrontal regions, amygdala, and the ventral striatal regions than do male

(McRae et al., 2008). Furthermore, also in relation to down-regulation of aversive emotions,

females show less activity in the OFC, the AC, and the dorsolateral PFC in comparison to

male (Domes et al., 2010). When asked to increase emotions, females show enhanced activity

in amygdala, PFC, and temporal cortex, while male show increase activity in cortical areas,

associated with amygdala activity (Domes et al., 2010).

Neuroscientific SD in empathy has been reviewed, preceded by an overview of

behavioural and psychological SD in empathy. So, where does the results come from and how

to interpret this data?

Potential Explanations

Just as biology affects behaviour, so does behaviour affect biology. With basis in

biological research, authors suggest that a more productive theoretical and empirical strategy

to approach human behaviour is to recognize how social roles and biology together in an

unseparatable way, are involved in the flexibility of the human behaviours (Taylor et al.,

2000).

For example, gender roles have been considered as a potential explanation to SD


observed. Chaplin and Aldao (2013) argue that SD is not something human children are born

with. With background in that SD in positive, externalizing and general NE expressions were

not evident in infancy, but rather did not emerge until toddler/preschool period and childhood,

the authors suggest these emotion expressions as socialized. In relation to that girls displayed

greater internalizing emotion expression already in infancy, in comparison to boys, the

authors nevertheless argue that some emotion expressions could be innate or learned through

socialization responses of care givers in a very early age (Chaplin, & Aldao, 2013).

Additionally, social desirability has been considered to contribute to the observed SD

in empathy. From a study with the aim to test for SD in EC, researchers suggest that females

in comparison to males are more susceptible to EC following brief interaction with a friend

(Magen, & Konasewich, 2011). The researchers propose potential explanation for their

results, suggesting factors such as social desirability, the possibility that females consider

being an effective support is much more important than did males, and in line with the results,

that females in comparison to males are more susceptible to EC (Magen & Konasewich,

2011).

Another perspective argues that SD observed in relation to empathy can be due to the

specific measurement used. In a review article in 1983 (Eisenberg & Lennon, 1983), authors

focused on SD in empathy and related capacities. With more specifically focus on emotional

empathy, referring to “vicarious affective responding to the emotional state of another”

(Eisenberg & Lennon, 1983, p. 100) authors argue that the observed SD were primarily due to

the methods used to measure empathy. More specifically, females appeared more empathetic

compared to males, when measuring empathy with self-report scales. This result was not

visible in relation to neither physiological nor unobtrusive observations of nonverbal reactions

to another persons’ emotional state. Females’ superiority in empathy in comparison to males


was observed but labelled as moderate, in relation to self-report measures in laboratory

setting, and in regard to reflexive crying (Eisenberg & Lennon, 1983).

Although there are possibilities with different measurements, it also comes with

potential restrictions in regard to analysis of results. Michalska et al. (2013) propose a

potential explanation to those claimed theoretical and empirical SD observed in relation to

empathy, meaning that rather than being due to actual SD, results could be explained by that

different measurements focus of diverse components of empathy. Further, they argue it would

be beneficial to focus on studies investigating diverse measures of empathy and also be able

to understand the basis and nature of SD across indices.

Further, it has been argued for a potential bias in the literature on SD, more

specifically meaning that journals are more likely to publish paper that do find SD than paper

that do not. Moreover, this could consequently mean that researchers devote more effort in

finding differences than to find no difference (Croson & Gneezy, 2009).

Discussion

The aim of this paper was to give an overview of behavioural, psychological and

neuroscientific SD in empathy. Central findings including behavioural and psychological, as

well as neuroscientific SD in empathy have been presented. In relation to behavioural and

psychological SD, the central aspects have been emotion recognition, mentalizing abilities,

pro-social behaviour. Regarding neuroscientific SD in empathy, central aspects have been

affective sharing, self-other awareness, mental flexibility, and regulatory processes.

Starting with ER, there is evidence for superiority in females of multisensory

processing of emotion expression (Collignon et al., 2010). However, there is evidence for that

SD has been more observed in relation to NE than in relation to PE (Steven & Hamann,

2012). Hence, this might contribute with a restriction in interpreting the data from the study

focusing on multisensory processing of emotion expressions, where researchers only used


either disgusted or fearful facial expressions (Collignon et al., 2010). Although, evidence for

that females are both better and faster in ER in both PE and NE facial expressions is still

evident (Hampson et al., 2006). Furthermore, females compared to males are both more

accurate and sensitive in labelling facial expressions (Montagne et al., 2005), better able to

recognize subtle emotional expressions (Hoffman et al., 2010), regardless of the sex of the

person displaying the emotion (Thayer & Johnsen, 2000). Moreover, in relation to body

recognition, females seems superior in PLD perception tasks in bodily ER and bodily action

recognition (Alaerts et al., 2011), with females more accurate rather than faster than males

(Sokolov et al., 2011). The trend of female’s superiority in ER goes further beyond conscious

awareness, with females better at recognize positive valence of facial emotions, an effect not

found in males (Donges et al., 2012). In line with this, females in comparison to males also

show enhanced emotional processing from tone of voice in a preconscious stage of processing

(Schirmer et al., 2005). Moreover, mood affects males with happy mood meaning better ER,

which was not found in females (Schmid et al., 2011). Overall, support for SD in ER was

found, more specifically pointing towards a female’s superiority in comparison to males.

In relation to ToM, both girl/females in comparison to boys/males have been

found to be better performers in different ToM-tests (Baron-Cohen et al., 1997; Walker,

2005). Nevertheless, there are inconsistent findings with results indicating no SD (Jarrold et

al., 2000), as well as male superiority in ToM (Russel et al., 2007). With SD evident in both

children and adults in relation to ToM (Baron-Cohen, Jolliffe, Mortimore, & Robertson, 1997;

Walker, 2005), one might argue that gender roles may not explain these results, unless gender

roles are learned in very early childhood. Furthermore, the study conducted by Walker (2005),

with the aim to test relationship between ToM and peer-related social competence, the ones

rating the children’s peer-related social behaviour were their teachers, not the children


themselves. When teachers are rating children’s behaviour, gender roles could be a

contributor to the results.

In relation to pro-social behaviour, evidence suggests that females are more

cooperative than males (Eckel & Grossman, 2001). However, contextual factors such as sex

of the respondent might affect the subject’s behaviour (Eckel & Grossman, 2001), potentially

through both gender roles and social desirability. This might further be a contributor to that

females are more able to give money as well as volunteer more hours than do males,

especially given the author’s concluding remarks that females in relationship with males seem

to socialize males in relation to philanthropic giving (Mesch et al., 2006).

Continuing to neuroscientific SD, the existence of SD in neuroanatomy is

evident, showing females exhibit greater GM volumes in cingulate cortex (Good et al., 2001),

the right IFG, in pars opercularis as well as in IPL (Cheng et al., 2009), and in parts of mPFC

(Yamasue et al., 2008). Males have higher percentage of WM and CSF (Gur et al., 1999).

Amygdala and cerebellum is larger in males (Cheng et al., 2009).

Regarding affective sharing, in relation to the MNS, females in comparison to

males have greater GM in pars opercularis and IPL of RH, areas involved in the MNS

(Cheng, et al., 2009). Further, females in comparison to males seem to recruit mirror neurons

to a greater extent when watching hand movements (Cheng et al., 2008). Hence, both

neuroanatomical and functional SD is found in relation to mirror neurons. Nevertheless, there

is a controversy about the existence of mirror neurons. Some researchers argue that the

properties of mirror neurons map well onto emotion contagion, as well as argue that most

studies support the notion of existence of mirror neurons from that findings of activation of

brain networks involved in first hand experience also activates when observing affective state

in others (Bernthardt & Singer, 2012; Iacoboni, 2011). Although, other researchers argue that


the existence of mirror neurons in humans lack direct empirical support, where they among

other things refer to that fMRI cannot give such good spatial resolution. Furthermore, it has

been argued that even though mirror neurons would exist in humans, it would not necessarily

mean that mirror neurons underlie empathy (Lamm & Majdandzic, 2014). Because of this

controversy regarding mirror neurons, the author suggests careful interpretations of the

findings presented.

In relation to EC, both amygdala and STS are crucial for social perception

(Allison et al., 2000; Haxby et al., 2002; Shaw et al., 2005). In relation to emotion memory,

females use significantly fewer brain areas including amygdala, while males use more

structures including right amygdala (Canli et al., 2003). Amygdala gets more activated in both

sexes when observing faces versus bodily expression, especially in males observing female

faces (Kret et al., 2012), potentially reflecting males bigger amygdala (Cheng et al., 2009).

Further, increased activity in STS is more coupled to threatening bodies versus faces, also this

specifically in males. Existence of SD in relation to EC is evident, although depending on

contextual cues such as the sex of the one displaying emotion, as well as if it is a body or face

showing emotions (Kret et al., 2011), factors that potentially could get affected by gender

roles. Further, empathize with others in pain can elicit activity in AI, ACC, cerebellum and

the brainstem (Morrison et al., 2004; Singer et al., 2004). Although, social relation affect the

emotional and bodily experience of empathizing, indicating that seeing fair players in pain

activated AI and brainstem in both sexes, although the effects was greater in females. In

contrast, unfair players perceiving pain decreased empathy-related activity to a small degree

in females, but significantly in males (Singer et al., 2006). Further, increased activation in

NA, a suggested reward-processing area, was observed in males when observing unfair player

receive pain (Singer et al., 2006). This could potentially have evolutionary roots, referring to

the origin of empathy in care giving and group living (Decety, 2015).


Continuing, areas such as mPFC, STS, TPJ, IFG, and TPs is central in different

mentalizing tasks such as perspective-taking and ToM (Amodio & Frith, 2006; Frith & Frith,

2003; Jenskins & Mitchell, 2011; Saxe & Kanwisher, 2003; Schulte-Rüther et al., 2008).

Females show stronger activity in IFG and STS, while males show increased activity in TPJ

(Schulte-Rüther et al., 2008). Similar results has been showed, adding calcarine gyri and

amygdala to structures activated more in females than in males (Derntl et al., 2010). In

relation to ToM, medial frontal regions and TH are more engaged in males than in females

(Krach et al., 2009). Furthermore, in relation to ToM and ASC, a disorder more prevalent in

boys than in girls (Baron-Cohen, 2010), there is evidence for that areas such as PFC, superior

temporal gyrus, ACC, and TH, often smaller in boys than girls, are even smaller in children

within the ASC than in boys (Baron-Cohen et al., 2005). As mentioned in relation to

neuroanatomical SD, the amygdala and cerebellum is greater in males than in females (Cheng

et al., 2009). Children within the ASC exhibit greater amygdala and cerebellum as well

(Baron-Cohen et al., 2005).

Continuing with regulatory processes, showing that PFC and AC, with their

connections to cortical areas, including STS and amygdala, have been coupled to emotion

regulation (Decety, 2011; Kalisch et al., 2005). Down-regulating NE activates PFC,

amygdala, and ventral striatal regions, more in females than in males (McRae et al., 2008).

When asked to increase emotions in relation to aversive stimuli, females in comparison to

males showed increased activity mainly in amygdala, but also in PFC and temporal cortex.

Under same conditions, males showed increased amygdala activity (Domes et al., 2010).

From the research reviewed, there is evidence supporting both behavioural,

psychological and neuroscientific SD in empathy, although inconsistencies have been

presented regarding behavioural SD in ToM and pro-social behaviour. From what the author


has presented, one could further argue that the most extensive support for SD in empathy

seems to be regarding emotion processing.

So what are the implications of these findings? First of all, there is a restricted

amount of research in relation to behavioural and neuroscientific SD in empathy. Further, the

studies that do exist, present inconsistent findings. Moreover, in relation to some of the

concepts, e.g. mirror neurons, there is a controversy about actual existence of these specific

neurons in humans, which make results difficult to interpret. Furthermore, SD in empathy is

controversial, and even when leaving the perspective of SD out, the research field with focus

on the broad perspective of empathy has also been criticized (Michalska et al., 2013). More

specifically, empathy research has been accused for being too artificial in their settings,

resulting in simplification of social cues, models of empathy etc. Further, empathy research

has been argued to lack connection between neuroscientific and behavioural research fields,

consequently leading to an imprecision in terminology (Zaki & Ochsner, 2012). Because of

these controversies about central concepts, the criticism regarding how the research field

approach the concept of empathy, as well as the controversial aspects of sex differences as

well as the inconsistent findings; this cause the author to argue that one should approach these

findings presented with great caution, being aware of difficulties in interpreting the data.

Conclusion

The aim of this paper was to give an overview of behavioural, psychological and

neuroscientific sex differences in empathy. With evolutionary basis in caregiving (Preston &

de Waal, 2002), and group living (Decety, 2015), empathy enables sharing of information of

intentions and emotions, as well as contributes with the capacity to appropriately respond to

that information (Decety et al., 2012). Although there is no general agreement of defining

empathy, most researchers agree that empathy consists of both emotional and cognitive


components (e.g. Baron-Cohen & Wheelwright, 2004; Berglund & Annett, in press; Decety &

Jackson, 2004; Shamay-Tsoory, Aharon-Peretz, & Perry, 2009).

Behavioural and psychological sex differences in empathy were presented, with

research findings supporting females’ superiority in emotion recognition (Anders & Mullin,

2006; Donges et al., 2012; Montagne et al., 2005; Sokolov et al., 2011). In relation to sex

differences in both theory of mind and pro-social behaviour, inconsistent findings was

presented (Baron-Cohen et al., 1997; Eckel & Grossman, 2001; Mesch et al., 2006; Russel et

al., 2007; Solnick, 2001).

Moving on, neuroscientific sex differences in empathy was presented, based on

Decety and colleague’s model of empathy (Decety & Jackson, 2004; Decety & Moriguchi,

2007), starting with an overview of neuroanatomical sex differences. Both neuroanatomical

and functional sex differences were found in relation to the mirror neuron system, emotion

contagion, as well as in relation to pain research (Canli et al., 2003; Cheng et al., 2008; Cheng

et al., 2009; Kret et al., 2011; Singer et al., 2006). Research indicating existence of sex

differences in relation to perspective-taking, theory of mind, as well as regulatory processes

was presented (Baron-Cohen et al., 2005; Chulte-Rüter et al., 2008; Derntl et al., 2010;

Domes et al., 2010; Krach et al., 2009; McRae et al., 2008).

Potential explanations to observed sex differences in empathy were presented,

including factors such as gender roles, social desirability and limitations of measurements.

These factors were further discussed in relation to the behavioural, psychological and

neuroscientific research findings of sex differences in empathy presented.

To conclude; sex differences was found in relation to both affective and

cognitive components of empathy, However, there is still both a restricted amount of research

available as well as inconsistent findings. Furthermore, with controversies regarding main


concepts related to empathy, with for example proposed central neural mechanisms such as

mirror neurons, there is a great limitation in how to interpret the findings.

For future research, clear and agreed definitions of subcomponents of empathy

with consistent terminology between behavioural and neuroscientific research fields, could

contribute to a solid foundation for empathy research to stand on. To refer to the beginning of

this paper, it has been proposed that social cognition is an important component of mental

health, and hence therefore important to investigate sex differences in the neural mechanisms

underlying empathy (Christov-Moore et al., 2014). However, with empathy as an uncertain

and controversial concept, turning to investigating sex differences in empathy could be

considered not to be relevant until the research field has a common picture of what empathy is

and what neural mechanisms enable empathy.


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Appendix

Table 1

Most recurring abbreviations used in the paper

Abbreviation Refer to

ACC……............................Anterior cingulate cortex

AI………………......……..Anterior insula

FI…………………..……...Fronto-insular

IFG…………………..…....Inferior frontal gyrus

IPL…………………...…....Inferior parietal lobule

MNS………….………..….Mirror Neuron System

NA………….……...…..….Nucleus accumbens

NE………….…….…….….Negative emotions

OFC………..……………...Orbitofrontal cortex

PE……................................Positive emotions

PDG………...………….….Prisoner’s Dilemma Game

PFC……………...…….…..Prefrontal cortex

PMC….................................Premotor cortex

SD……................................Sex differences

STS……...………………...Superior temporal sulcus

TH……................................Thalamus

TPJ……………...…………Temporo-parietal junction

VS…....................................Ventral striatum

behavioural and neuroscientific sex differences in...

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