Received: 10 November 2020 | Revised: 6 January 2021 | Accepted: 9 January 2021

DOI: 10.1002/jnr.24787

REVIEW

Sex differences in the social brain and in social

cognition

Alice Mado Proverbio

Milan Center for Neuroscience, Department

of Psychology, University of Milano-­Bicocca,
Milan, Italy
Correspondence
Alice Mado Proverbio, Department of
Psychology, University of Milano-­Bicocca,
Piazza dell’Ateneo Nuovo 1, 20126, Milan,
Italy.
Email: mado.proverbio@unimib.it
Funding information
Università degli Studi di Milano-­Bicocca
Abstract
Many studies have reported sex differences in empathy and social skills. In this review,
several lines of empirical evidences about sex differences in functions and anatomy
of social brain are discussed. The most relevant differences involve face processing,
facial expression recognition, response to baby schema, the ability to see faces in
things, the processing of social interactions, the response to the others’ pain, interest
in social information, processing of gestures and actions, biological motion, erotic,
and affective stimuli. Sex differences in oxytocin-­based parental response are also
reported. In conclusion, the female and male brains show several neuro-­functional
differences in various aspects of social cognition, and especially in emotional cod-
ing, face processing, and response to baby schema. An interpretation of this sexual
dimorphism is provided in the view of evolutionary psychobiology.

KEYWORDS

baby schema, empathy, facial expression, gender, sex differences

1 | I NTRO D U C TI O N the reactivity to/efficacy of drugs and pharmaceutical molecules, as

Genetic and hormonal influences are long known to affect the human
brain and determine a variety of anatomical and functional differ-
ences between the two sexes. These sex differences would concern:
overall brain volume (Zaidi, 2010), neuronal density and white mat-
ter thickness (Luders & Toga, 2010), microstructure of the thalamus,
corpus callosum, and cingulum (Menzler et al., 2011), structure/size
of anterior hypothalamus, of the bed nucleus of the stria terminalis,
of the posterodorsal region of the medial amygdala, and of the preop-
tic area (see Cahill, 2006; Hines, 2020) for comprehensive reviews).
The cerebral sexual dimorphism would support marked diversities
in reproductive, parental, and social behavior. In addition, prenatal
and postnatal differences in testosterone concentration (between
females and males) would heavily affect the brain physiology, also
modulating dendritic growth, spine density, density of brain recep-
tors, neurogenesis, and gliogenesis (McCarthy et al., 2012). A rapidly
burgeoning literature now documents significant sex differences in
well as in the incidence of neurodegenerative, neurological, and psy-
chiatric diseases (see the entire volume dedicated to sex differences
in the brain and edited by Cahill, 2017).
Besides anatomical and physiological diversities, some func-
tional and mental differences between men and women have long
been identified (e.g., Kimura, 1980) and more recently supported
by neuroimaging studies (e.g., verbal fluency Sokołowski et al.,
2020) and empathy (Baron-­Cohen, 2002) in favor of female gen-
der and spatial rotation ability (Voyer et al., 1995) in favor of the
male gender. Lately an increasingly large amount of evidence has
accumulated indicating a sex difference in social and affective pro-
cesses (e.g., Anderson et al., 2013; McDuff et al., 2017; Perrett
et al., 1998; Stevens & Hamann, 2012; Thompson & Voyer, 2014).
In this review, we will examine a large corpus of behavioral, EEG/
event-­related potentials (ERPs), and neuroimaging evidence in the
recent literature supporting the existence of sex differences in the
social brain.

Edited by Sara Bulgheroni and Junie Warrington. Reviewed by Larry Cahill and Ruben Gur.

J Neurosci Res. 2021;00:1–9. wileyonlinelibrary.com/journal/jnr© 2021 Wiley Periodicals LLC | 1

2 |
The main known sex differences in social cognition refer to: hemi-
spheric lateralization for face processing (Bourne, 2005; Proverbio,
De Gabriele, et al., 2011; Proverbio et al., 2006a, 2010, 2012), facial
expression encoding (e.g., Connolly et al., 2019; Orozco & Ehlers,
1998; Sawada et al., 2014; Wingenbach et al., 2018), face gender
encoding (Proverbio et al., 2010a), interest in social scenes and
human faces (Pavlova et al., 2014, 2015; Proverbio, 2017; Proverbio
et al., 2008), emotional response to negative affective informa-
tion (Hofer et al., 2007; Klein et al., 2003), empathy for pain (Han
et al., 2008; Proverbio et al., 2009; Singer et al., 2004), understand-
ing gestures, body language, and intentions (Canessa et al., 2012;
Proverbio, De Gabriele, et al., 2011), parental response to baby
schema (Glocker, Langleben, Ruparel, Loughead, Gur, et al., 2009;
Glocker, Langleben, Ruparel, Loughead, Valdez, et al., 2009; Sander
et al., 2007; Seifritz et al., 2003).
1.1 | Hemispheric asymmetries for face processing
While the classical neuroimaging literature reports a right hemi-
spheric dominance for face processing in humans (Kanwisher
et al., 1997; Rossion et al., 2003; Sergent et al., 1992), regardless of
gender of viewers, new recent data have shown that face process-
ing is less lateralized in females than males (Kiesow et al., 2020; Liu
et al., 2020; Proverbio et al., 2010b; Proverbio & Galli, 2016). Others
authors suggested that facial processing involved both the right and
left hemispheres (Haxby et al., 1999) but that they would contrib-
ute differently in response to familiar or unfamiliar faces. Overall,
the literature is very inconsistent about hemispheric lateralization of
facial processing since virtually no neuroimaging study has ever con-
sidered viewer's sex in the past. At this regard, it is of great interest
to note that face-­specific N170 responses of ERPs are found to be
bilateral or even left-­sided in studies in which female participants are
the majority (e.g., Jemel et al., 2005).
Two ERP studies (Proverbio et al., 2006b, 2012) have shown a
face-­specific activation of the left occipito-­temporal area, namely of
the fusiform face area (FFA), in females during processing of facial
stimuli (as reflected by N170 component of ERPs) and of the right
homologous FFA, in males. More in detail, Proverbio and coworkers
(2012) recorded ERPs to ~400 stimuli (faces of adults, children, and
infants, tools) in 50 participants, in a landscape detection task. The
results showed a lack of difference in the amplitude of N170 to ob-
jects in the two sexes. However, it was found that N170 to faces was
of greater amplitude over the right in males, and bilateral in females.
Furthermore, the left face area in males was not responding to peo-
ple's age (it did not discriminate between adult, children, or baby
faces) but only the right one, while the age discriminative response
was bilateral in females.
Overall, these findings fit with previous data providing evidence
of a sex difference in the hemispheric lateralization of perceptual
and cognitive processes. For example, several studies have shown
more strongly lateralized functions in males versus females, in-
cluding language and visuospatial processes. In particular, females
PROVERBIO
Significance
This review is particularly relevant because it focuses on
an extensive neuroimaging and electrophysiological lit-
erature on functional and anatomical sex differences in
social cognition, thus revealing new and hitherto unknown
knowledge.
would rely more on interhemispheric communication during tasks
involving 3D mental rotation (Kurth et al., 2018), and would show
a more bilateral activation of brain areas devoted to linguistic func-
tions (Hausmann, 2016; Kansaku & Kitazawa, 2001; Shaywitz et al.,
1995). Bourne (2005) investigated the existence of hemispheric
asymmetries during face processing. The task consisted of viewing
chimeric faces with different facial expressions and determining
which one looked more positive. Again, the data provided evidence
of a stronger hemispheric asymmetry in men compared to women,
with a perceptual advantage of the left visual field (right hemisphere)
in the latter group. Tiedt et al. (2013) reported similar findings in
an ERP study on the interhemispheric transfer-­time (IHTT) of facial
information estimated through N170 latency. They showed a sex
difference in IHTT with earlier N170 latencies in the right-­to-­left di-
rection (170 ms) as opposed to the left-­to-­right direction (185 ms),
while IHTT was symmetric in women. Quite similar findings were
also reported by Proverbio et al. (2012) who concluded that asym-
metry in callosal transfer times in males might be ascribed to quicker
transfer times of facial inputs through pathways departing from the
more efficient (right) to the less efficient (left) hemisphere. Likewise,
the lack of asymmetry in females might suggest that both face areas
are equally specialized.
1.2 | Affective facial expressions and emotions
Empirical evidence of females’ greater accuracy in interpreting fa-
cial mimicry has also been provided (Connolly et al., 2019; Sawada
et al., 2014; Thompson & Voyer, 2014; Williams et al., 2009;
Wingenbach et al., 2018). This finding is typically interpreted in an
evolutionary perspective, considering the primary role of moth-
ers in the early interactions with infants. In this regard, Proverbio
and coworkers (2007) examined the role of biological sex and ex-
pertise in understanding infant expressions in a large group of men
and women who differed in their experience with babies. Women
showed a better performance and decoding accuracy than men;
furthermore, familiarity with babies (linked to profession) improved
decoding of facial expressions but only in women. These results sug-
gest an interaction between expertise and a biologically driven fe-
male inclination to better comprehend babies’ facial expressions (i.e.,
an interaction between sex and cultural factors).
In an electrophysiological study performed on the same set of
stimuli (Proverbio et al., 2006b), it was investigated whether viewers’
PROVERBIO
sex affected the perceptual response at different stages of visual
processing during a decision task of infant joy/pain expressions.
All infants were unknown to participants. Overall, the occipital P1
response was earlier and much greater in female than male par-
ticipants. Furthermore, P1 latency was faster in response to pain
than neutral expressions only in women, thus showing a prioritized
processing of biologically relevant information in the female brain
(Figure 1).
The role of sex in the emotion comprehension and psycholog-
ical reaction to emotional visual stimuli has been also investigated
(Proverbio, 2017; Stevens & Hamann, 2012). Quite recently Li
et al. (2020) analyzed a large data set of 970 subjects (508 women)
engaged in identifying negative facial emotions and neutral shape
targets finding that women were more sensitive to fearful stimuli,
whereas men were more sensitive to anger-­provoking stimuli.
In general, stimuli producing a larger arousal response would
undergo a prioritized processing because of their biological rel-
evance, for example, baby faces would stimulate an instinctual
parental response, especially in women. In contrast, erotic stimuli
(such as nudity) would be particularly arousing for males versus
females. Sabatinelli et al. (2004) showed that perceiving erotic
images induced a much larger activation of associative visual
areas in males than women. Indeed, Huynh and coworkers (2012)
reported that high-­intensity (vs. low-­intensity and neutral) erotic
movies deactivated the primary visual area in women. Conversely,
perception of scenes stimulating an empathic response (such as,
body mutilations) triggered a greater activity in the extra-­s triate
visual area of females versus males. These findings seem to in-
dicate that brain arousal and attentional allocation devoted to
social stimulus depends on their specific biological relevance for
the viewers.
F I G U R E 1 Mean latency of P1 component recorded at lateral occipital area (independent of hemispheric site) and analyzed according to
viewer's sex and type of facial expression (taken and modified from Proverbio et al., 2006b study, protected by CC BY 2.0)
| 3
1.3 | Parental response
A wide literature shows that the visual and the orbitofrontal cortices
of adult viewers are particularly aroused by the view of baby faces
(Nitschke et al., 2004). Viewing an infant would provide a positive
feeling (e.g., tenderness or cuteness) especially in women, but also
in men, via the dopaminergic reward system. This effect is known
as “baby schema” effect, and besides the enhanced affective valance
it results in a deeper processing and attentional orienting toward
children versus adult faces (Brosch et al., 2007; Glocker, Langleben,
Ruparel, Loughead, Gur, et al., 2009; Luo et al., 2011; Proverbio, De
Gabriele, et al., 2011; Proverbio, Riva, Zani, et al., 2011; see also the
review by Hahn & Perrett, 2014). Other behavioral studies showed
how women might be more responsive to baby schema than men
and more skilled in comprehending infant expressivity (Babchuk
et al., 1985; Proverbio et al., 2007). For example, in an EEG/ERP study
(Proverbio et al., 2006a) aimed at investigating the neural response
to baby schema in female and male adult people, data showed the
sensory response to faces (P1) was of greater amplitude in women
than men. This might suggest a greater perceptual sensitivity or at-
tentive response in females versus males at the view of unrelated in-
fants. Other studies showed that baby faces were more perceptually
salient for women than men (Hahn et al., 2013; Parsons et al., 2011,
2013). In addition, infant faces would capture females’ attention to a
greater extent than adult faces; conversely, infant faces would cap-
ture male's attention much less than faces of the opposite sex, that
is, female faces (Cárdenas et al., 2013).
Several interesting neuroimaging studies (Glocker, Langleben,
Ruparel, Loughead, Valdez, et al., 2009; Kringelbach et al., 2008;
Leibenluft et al., 2004) have investigated which neural systems are
involved in the “parental response” to infants, and identified a neural
4 | PROVERBIO

F I G U R E 2 Event-­related potential (ERP) difference waves obtained by subtracting ERPs to congruent from ERPs to incongruent actions
separately for men and women, over anterior scalp sites. It can be appreciated a much larger N400 response to incongruent actions in
women than men (original figure, relative to Proverbio et al., 2010, courtesy of the authors)

network of structures based primarily on the orbitofrontal cortex.
For example, Leibenluft and coauthors (2004) recorded the brain ac-
tivation of mothers while viewing photographs of their own infants.
They wished to get some knowledge on the neural correlates of “ma-
ternal love.” It was found a focus of activity in the orbitofrontal area
and in related regions belonging to the pleasure/reward system, in-
cluding the periaqueductal gray matter.
In an electrophysiological study (Peltola et al., 2014), it was
tested the associations between motherhood and genetic variations
in oxytocin receptors, and bioelectrical and behavioral responses to
facial expressions of babies and adults. Both mothers (as opposed
to nulliparous females) and women carrying the rs53576 GG vari-
ant of OXTR gene showed larger discriminative N170 responses to
strong versus mild negative facial expressions of infants. This result
suggests that the visual cortex responsivity to baby schema de-
pends both on genetic (individual differences) and biological factors
(being a mother or not). Overall, being a parent has been associated
with a greater sensitivity to infant facial expressions. This has been
demonstrated in an electrophysiological study performed in parent
versus nulliparous adults where it was found that perceptual N160
response reflected the earliest discrimination of mild versus strong
painful facial expressions in parents (especially in mothers) but not in
nulliparous individuals, thus suggesting again a strong interaction of
genetic predisposition and parental status (Proverbio et al., 2006a).
Again, the data showed larger P3 responses in mothers versus all
other groups (i.e., males and nulliparous females), possibly indicating
a greater perceptual sensitivity (or enhanced arousal) in mothers, at
the view of unknown babies.
As far as for auditory social information are concerned, the neu-
roscientific literature reported larger brain responses in women than
men while listening to infant vocalizations such as cry and laugh-
ter (e.g., Sander et al., 2007; Seifritz et al., 2003). These data also
seem to suggest the hypothesis of a sex difference in the parental
response to infantile nonverbal signals. It is conceivable that many
of the sex differences in social cognition might be related to the ge-
netically determined role of human females as primary caregivers of
the offspring (instead of fighters/hunters, as suggested by Kuhn &
Stiner, 2006). For example, the robust evidence linking testosterone
exposure to sex-­t yped play (e.g., playing or not with dolls) suggest
how behavior is strongly modulated by sexual genes (Hines, 2020;
Leveroni & Berenbaum, 1998), but it cannot be rule out the role of
socialization and upbringing style.
1.4 | Interest in social stimuli
Some electrophysiological literature provided evidence of a greater
female electrocortical response to social information (e.g., faces or
people) as opposed to inanimate stimuli. In a study by Proverbio
et al. (2008), participants viewed hundreds of pictures depicting real
PROVERBIO
persons versus sceneries (urban or natural landscapes) while their
EEG signals were recorded. The results showed larger amplitude N2
responses in women, but not in men, in response to social than inani-
mate information. Source reconstruction of brain signals evidenced
a bilateral activation of face-­related regions in response to persons.
In addition, sex differences were found with the unique activation of
the superior temporal gyrus and the right extra-­striate body area in
women, and of the left para-­hippocampal area in men. This was in-
terpreted as female greater interest in (or attention to) social signals
(i.e., bodies and faces).
This interest for social information might draw more attention
to visual stimuli. Indeed, a considerable literature has accumulated
showing that females are more accurate than males in decoding fa-
cial mimicry. Many studies have reported sex differences in the abil-
ity to perceive, process, express, and experience emotions. Overall,
females seem better skilled in the analysis and comprehension of
social signals, and more interested in conspecifics. Again, female
children typically spend more time with infants, younger siblings,
and dolls than male children. While it is problematic to determine
whether this socially oriented behavior is due to cultural factors (e.g.,
society models, upbringing style) or to genes, comparative studies
on monkeys seem to point to the second direction.
1.5 | Action and body language understanding
Several sex differences have been found in the way female and male
brain processes actions and gestures. Proverbio et al. (2010)’s study,
for example, reported earlier and greater ERP responses to incon-
gruent actions in women than men. Perception of congruent actions
(e.g., a woman looking attentively at road map) was compared with
that of incongruent actions (e.g., a man in a kitchen cutting a carrot
with an axe). Data showed an earlier discrimination between congru-
ent and incongruent actions in women, indexed by a parietal N200
to response. The inverse solution applied to this component located
the neural sources of this effect in the inferior parietal and left in-
ferior frontal cortex (among other areas), corresponding to the mir-
ror neuron network. In addition, the later anterior N400 component
(greater to incongruent behavior) was found enhanced in women
versus men (see Figure 2). The N400 source analysis showed slightly
different neural circuits in two sexes, with an activation of the limbic
system and cingulate cortex in women, and of the ventromedial pre-
frontal cortex in men, which has been interpreted as a more rational
than affective reaction in men than women.
A conjoined fMRI and ERP study from our group (Canessa
et al., 2012; Proverbio, Riva, Paganelli, et al., 2011) reported a greater
female activation of the so-­called action understanding system, the
ventral premotor cortex and the superior temporal sulcus (STS) in
a task involving the observation of social interactions with a coop-
erative or an affective goal. Other studies provided several lines of
evidence of sex differences in the brain development of perceptual
systems devoted to biological motion. fMRI data collected during
visual perception of coherent versus incoherent biological motion
| 5
have found enhanced activity in females versus males especially fo-
cused in areas devoted to social perception (such as, the temporal
pole and the medial temporal gyrus).
1.6 | Face pareidolia
Due to the social bias, females would also be more inclined than
men at seeing faces in things (face pareidolia), as recently shown by
behavioral and electrophysiological findings (Pavlova et al., 2015;
Proverbio & Galli, 2016; Zhou & Meng, 2020). Pavlova et al. (2015)
compared women and men in a face recognition task involving
Arcimboldo-­like food patterns and found that women were more
inclined to recognize a face in the food configuration and gave
food displays higher face-­likeness ratings. Interestingly, Proverbio
and Galli (2016) further investigated this issue by recording EEG/
ERP in women and men engaged in viewing photographs of animals
(targets), objects, faces in things, and faces. Overall, compared to
men, women were more inclined to see faces in perfectly real ob-
jects, as shown in the preliminary face-­likeness ratings assessment.
Furthermore, vertex positive potential of the ERPs showed a dis-
criminative response between faces and faces in things in men (with
larger responses to faces), while it was of comparable amplitude in
women, clearly reflecting a face pareidolia effect. The analysis of
intracranial generator of this response in women identified the or-
bitofrontal cortex, the right STS and the posterior cingulate cortex
as the stronger sources of activity for the affective processing (face
likeness) of things. According to the authors, this network would
support the anthropomorphizing bias in females.
1.7 | Empathy for pain
Recent findings have demonstrated that women might be more re-
active than men at the view of suffering conspecifics (vicarious re-
sponse to pain), and therefore more empathic (Han et al., 2008). This
sex difference fully agrees with Baron-­Cohen model, as well as with
a recent survey examining the empathy quotients of 671,606 indi-
viduals (Greenberg et al., 2018). In a study by Proverbio et al. (2009)
it was investigated whether the two sexes differed in their cerebral
response to affective pictures, depicting people in different positive
or negative contexts compared to natural or urban landscapes. More
than 400 stimuli from the International Affective Picture System
(IAPS) were shown to a group of female and male students. An emo-
tional impact scale was administered to all participants showing
higher emotional psychological reactions in women than men to a
variety of emotional stimuli.
Visual P1 response was larger in amplitude to persons than to
landscapes and was modulated by the emotional valence of the
social information. A late positive response to negatively valence
social information (suffering humans, visible in Figure 3, blue line)
far exceeded the response to negative nonsocial information in
females but not in males. Again, a low-­resolution electromagnetic
6 | PROVERBIO

F I G U R E 3 Event-­related potentials (ERPs) recorded at midline frontal and centro/parietal sites as a function of stimulus valence and
viewer's sex. It is visible a large effect of both emotional content (that can be appreciated by comparing ERPs to negative vs. positive
unanimated scenes), and an effect of empathy for pain, especially in women (that can be appreciated by comparing ERPs to negative scenes
vs. ERPs to pictures portraying humans). Original figure, relative to Proverbio et al. (2009)’s study, reproduced with permission of the authors
and of Elsevier

tomography applied to ERP data showed an enhanced activation of
the right amygdala and of the right frontal areas in women (compared
to men) for the contrast suffering-­minus-­happy humans. This func-
tional difference possibly suggests a stronger empathic response in
the female brain at the sight of the others’ pain.
Hofer et al. (2007) found larger activation of the right superior
temporal area, right insula, right putamen, and anterior cingulate
cortex (ACC) during processing of affective words for women versus
men, and interpreted this finding as reflecting the greater emotion-
ality of female individuals. Again, Klein et al. (2003) found increased
activation of the ACC and the amygdala in women in response to
negative IAPS pictures. In the study by Proverbio and coauthors
(2009), sex differences in the response to negative versus positive
stimuli were much greater for social than nonsocial information.
This might suggest that visual images of humans have a special
status for the female brain, especially in interaction with negative
valence. These data are consistent with other literature suggesting
the women might be more empathic than men at the view of suffer-
ing humans (Han et al., 2008; Schulte-­Ruether et al., 2008; Singer
et al., 2004).
In summary, we have here outlined a series of sex differences in
social behavioral and psychological processes that seem biologically
associated with female chromosomal karyotype. They are: efficient
and bilateral face processing, marked empathic attitude, sensitivity
to facial mimicry and gestures, attachment to infants (induced by
oxytocin), early interest for infants, curiosity about people and social
information, emotional responsivity, lesser incidence of autistic, psy-
chopathic, and sociopathic disorders. Knowledge of sex differences
in the brain is essential for understanding how to treat male and fe-
male patients with sex-­specific medications (Cahill, 2017), or how
to recognize and treat gender-­specific symptoms in socially related
disorders (e.g., autistic spectrum disorder, attention deficit/hyperac-
tivity disorder, personality disorder and psychopathy, conduct disor-
der, alexitimia, depression, social anxiety etc., American Psychiatric
PROVERBIO
Association, 2013). The greater incidence of some of these disorders
in the male population might ultimately be due to sex differences in
social cognition.
AC K N OW L E D G M E N T S
This work was supported by 13974 2015-­ATE-­0 052 grant entitled
“Emotional responses and gender differences in individuals with high
traits of psychopathy, impulsivity and empathy” from the University
of Milano-­Bicocca.
C O N FL I C T O F I N T E R E S T
No conflicting interests exist.
PEER REVIEW
The peer review history for this article is available at https://publo​
ns.com/publo​n/10.1002/jnr.24787.
ORCID
Alice Mado Proverbio https://orcid.org/0000-0002-5138-1523
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How to cite this article: Proverbio AM. Sex differences in the
social brain and in social cognition. J Neurosci Res. 2021;00:​
1–­9. https://doi.org/10.1002/jnr.24787