Empathy: Gender Effects in Brain and Behavior.

Abstract

Evidence suggests that there are differences in the capacity for empathy between males and females. However, how deep do these differences go? Stereotypically, females are portrayed as more nurturing and empathetic, while males are portrayed as less emotional and more cognitive. Some authors suggest that observed gender differences might be largely due to cultural expectations about gender roles. However, empathy has both evolutionary and developmental precursors, and can be studied using implicit measures, aspects that can help elucidate the respective roles of culture and biology. This article reviews evidence from ethology, social psychology, economics, and neuroscience to show that there are fundamental differences in implicit measures of empathy, with parallels in development and evolution. Studies in nonhuman animals and younger human populations (infants/children) offer converging evidence that sex differences in empathy have phylogenetic and ontogenetic roots in biology and are not merely cultural byproducts driven by socialization. We review how these differences may have arisen in response to males' and females' different roles throughout evolution. Examinations of the neurobiological underpinnings of empathy reveal important quantitative gender differences in the basic networks involved in affective and cognitive forms of empathy, as well as a qualitative divergence between the sexes in how emotional information is integrated to support decision making processes. Finally, the study of gender differences in empathy can be improved by designing studies with greater statistical power and considering variables implicit in gender (e.g., sexual preference, prenatal hormone exposure). These improvements may also help uncover the nature of neurodevelopmental and psychiatric disorders in which one sex is more vulnerable to compromised social competence associated with impaired empathy.

Full text

Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
Contents
lists
available
at
ScienceDirect
Neuroscience
and
Biobehavioral
Reviews
journal
h
om
epa
ge:
www.elsevier.com/locate/neubiorev
Empathy:
Gender
effects
in
brain
and
behavior
Leonardo
Christov-Moorea,
Elizabeth
A.
Simpsonb,c,
Gino
Coudéb,
Kristina
Grigaitytea,d,
Marco
Iacobonia,
Pier
Francesco
Ferrarib,∗
aAhmanson-Lovelace
Brain
Mapping
Center,
Brain
Research
Institute,
UCLA
(L
C-M,
KG,
MI),
Department
of
Psychiatry
and
Biobehavioral
Sciences,
Semel
Institute
for
Neuroscience
and
Human
Behavior,
David
Geffen
School
of
Medicine
at
UCLA
(MI),
660
Charles
Young
Drive
South,
Los
Angeles,
CA
90095,
USA
bDipartimento
di
Neuroscienze,
Università
di
Parma,
via
Volturno
39,
43125
Parma,
Italy
cEunice
Kennedy
Shriver,
National
Institute
of
Child
Health
and
Human
Development,
National
Institutes
of
Health,
16701
Elmer
School
Road,
Dickerson,
MD
20842,
USA
dThe
University
of
Edinburgh,
Edinburgh,
UK
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
27
March
2014
Received
in
revised
form
26
August
2014
Accepted
8
September
2014
Available
online
16
September
2014
Keywords:
Ontogeny
Gender
Sex
Contagion
Mimicry
Prosocial
Helping
Emotion
Mirror
neuron
system
Development
Evolution
a
b
s
t
r
a
c
t
Evidence
suggests
that
there
are
differences
in
the
capacity
for
empathy
between
males
and
females.
However,
how
deep
do
these
differences
go?
Stereotypically,
females
are
portrayed
as
more
nurturing
and
empathetic,
while
males
are
portrayed
as
less
emotional
and
more
cognitive.
Some
authors
suggest
that
observed
gender
differences
might
be
largely
due
to
cultural
expectations
about
gender
roles.
How-
ever,
empathy
has
both
evolutionary
and
developmental
precursors,
and
can
be
studied
using
implicit
measures,
aspects
that
can
help
elucidate
the
respective
roles
of
culture
and
biology.
This
article
reviews
evidence
from
ethology,
social
psychology,
economics,
and
neuroscience
to
show
that
there
are
funda-
mental
differences
in
implicit
measures
of
empathy,
with
parallels
in
development
and
evolution.
Studies
in
nonhuman
animals
and
younger
human
populations
(infants/children)
offer
converging
evidence
that
sex
differences
in
empathy
have
phylogenetic
and
ontogenetic
roots
in
biology
and
are
not
merely
cul-
tural
byproducts
driven
by
socialization.
We
review
how
these
differences
may
have
arisen
in
response
to
males’
and
females’
different
roles
throughout
evolution.
Examinations
of
the
neurobiological
under-
pinnings
of
empathy
reveal
important
quantitative
gender
differences
in
the
basic
networks
involved
in
affective
and
cognitive
forms
of
empathy,
as
well
as
a
qualitative
divergence
between
the
sexes
in
how
emotional
information
is
integrated
to
support
decision
making
processes.
Finally,
the
study
of
gender
dif-
ferences
in
empathy
can
be
improved
by
designing
studies
with
greater
statistical
power
and
considering
variables
implicit
in
gender
(e.g.,
sexual
preference,
prenatal
hormone
exposure).
These
improvements
may
also
help
uncover
the
nature
of
neurodevelopmental
and
psychiatric
disorders
in
which
one
sex
is
more
vulnerable
to
compromised
social
competence
associated
with
impaired
empathy.
©
2014
Published
by
Elsevier
Ltd.
Contents
1.
Introduction
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605
2.
Evolutionary
precursors
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2.1.
Emotional
contagion:
Yawning,
facial
mimicry,
and
pain
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608
2.2.
Consolation
and
prosocial
behavior
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608
2.3.
Sensitivity
to
others
in
play
and
caregiving
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609
2.4.
An
evolutionary
ancient
instinct
to
care
for
offspring
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609
3.
Behavioral
and
psychological
gender
differences
in
humans
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3.1.
Emotion
recognition,
priming,
and
emotion
contagion
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3.2.
Mentalizing
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3.3.
Prosocial
behavior
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612
∗Corresponding
author.
Tel.:
+39
0521903947;
fax:
+39
0521903900.
E-mail
address:
pierfrancesco.ferrari@unipr.it
(P.F.
Ferrari).
http://dx.doi.org/10.1016/j.neubiorev.2014.09.001
0149-7634/©
2014
Published
by
Elsevier
Ltd.

L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
605
3.3.1.
Economic
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Naturalistic
data:
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donating,
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other
altruistic
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4.
Sex
differences
in
the
development
of
empathy
in
humans
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4.1.
Precursors
to
empathy
in
infancy:
Emotion
contagion,
mimicry,
and
social
interest
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613
4.2.
Toddlers
and
older
children:
Prosocial
behavior
and
cognitive
empathy
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614
4.3.
Empathy
in
adolescence
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615
4.4.
Summary
and
conclusions
regarding
sex
differences
in
empathy
across
development
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615
5.
Neuronal
mechanisms
for
empathy
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616
5.1.
Mirror
neurons
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616
5.2.
Neural
human
gender
differences:
Foundational
issues,
tools,
and
methods
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617
5.2.1.
TMS:
Cortico-spinal
facilitation
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617
5.2.2.
TMS
‘virtual
lesion’
studies
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618
5.2.3.
Magnetoencephalography
(MEG)
and
electroencephalography
(EEG):
Beta
rebound
and
mu
suppression
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618
5.2.4.
Event
related
potentials
(ERP)
studies
of
gender
differences
in
empathy
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.
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618
5.2.5.
Activation
studies
using
functional
MRI
(fMRI)
and
mirroring
markers
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619
5.2.6.
Gender
differences
in
fMRI
studies
of
empathy
not
related
to
mirroring
.
.
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619
5.2.7.
Structural
MRI
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619
5.3.
Hormones,
sexual
preferences
and
gender
roles
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619
6.
Conclusions
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620
Acknowledgements
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621
References
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621
1.
Introduction
Empathy
–
the
ability
to
understand
and
share
in
the
internal
states
of
others
–
is
a
complex,
multidimensional
phenomenon
that
includes
a
number
of
functional
processes,
including
emotion
recognition,
emotional
contagion,
and
emotion
priming
(for
recent
reviews,
see
Decety
and
Jackson,
2006;
Singer,
2006;
Walter,
2012),
as
well
as
the
abilities
to
react
to
the
internal
states
of
others,
and
to
distinguish
between
one’s
own
and
others’
internal
states
(e.g.,
Tomova
et
al.,
2014).
From
the
perspective
of
evolutionary
and
developmental
biology,
empathy’s
purposes,
in
both
humans
and
nonhuman
animals,
can
be
broadly
divided
into
two
categories:
Promoting
prosocial,
cooperative
behavior,
and
understanding
or
pre-
dicting
the
behavior
of
others
(Smith,
2006).
Empathy
has
been
studied
from
many
perspectives
(Davis,
1980;
Decety
and
Moriguchi,
2007;
Zaki
and
Ochsner,
2012).
For
example,
social
psychology
has
examined
the
manifestations
of
empathy
within
moral
reasoning
and
social
behaviors
like
mimicry
(e.g.,
Sonnby-Borgström,
2002).
In
economics,
studies
have
con-
sidered
empathy’s
effects
on
decision-making
(e.g.,
Beadle
et
al.,
2012;
Loewenstein,
2005;
Ferrari,
2014).
Cognitive
neuroscience
studies
of
empathy,
on
the
other
hand,
are
mainly
divided
into
two
lines
of
research,
one
focused
on
preconscious
mechanisms
which
underlie/facilitate
sharing
(and
mimicry)
of
others’
behaviors
and
internal
states
(we
will
refer
to
it
as
mirroring);
the
other
line
of
research
is
focused
on
a
conscious,
deliberative
process
through
which
inferences
can
be
made
about
others’
bodily
and
affective
states,
beliefs,
and
intentions
(often
called
mentalizing)
(Keysers
and
Fadiga,
2008;
Zaki
and
Ochsner,
2012).
These
two
aspects
of
empathy
can
be
roughly
mapped
onto
affective
(or
pre-reflective)
and
cognitive
(reflective)
empathic
predispositions,
respectively
(Smith,
2006).
Affective
empathy
is
associated
with
activity
in
fron-
toparietal,
temporal,
and
subcortical
regions
classically
associated
with
movement,
sensation,
and
emotion,
while
neural
systems
involved
in
cognitive
control
and
decision-making
–
such
as
the
cingulate,
prefrontal,
and
temporal
areas
–
are
often
activated
dur-
ing
tasks
requiring
cognitive
empathy
(see
Fig.
1)
(Zaki
and
Ochsner,
2012).
How
are
these
two
primary
modes
of
empathizing
–
cogni-
tive
empathy
and
affective
empathy
–
related?
While
affective
empathy
involves
pre-reflective
processes,
humans
seem
never-
theless
capable
of
consciously
and
unconsciously
modulating
it.
Furthermore,
humans
are
capable
of
internally
evoking
emotions,
behaviors,
and
sensations
of
an
absent
other,
or
even
of
ourselves
at
another
point
in
time.
We
are
also
capable
of
inhibiting
our
internal
states
and
reflexive
responses
to
others.
Indeed,
numer-
ous
studies
have
shown
that
mirroring
is
modulated
by
numerous
contextual
factors,
such
as
social
distance,
status,
trustworthiness,
group
membership,
and
attention
(Bernhardt
and
Singer,
2012;
Gu
and
Han,
2007;
Guo
et
al.,
2012;
Hogeveen
et
al.,
2014;
Lamm
et
al.,
2007;
Liew
et
al.,
2011;
Loggia
et
al.,
2008;
Singer
et
al.,
2006),
and
is
controlled
by
systems
involved
in
cognitive
empathy
(Spengler
et
al.,
2010).
Conversely,
some
authors
propose
that
mentalizing
and
social
decision-making
may
employ
information
derived
from
mirroring
(Iacoboni
et
al.,
2005;
Obhi,
2012;
Zaki
and
Ochsner,
2009)
(Fig.
2).
Recent
studies
suggest
that
a
large
portion
of
the
ability
to
read
intentions
derive
from
pre-reflective
mechanisms
for
processing
biological
motion
(Obhi,
2012),
and
studies
of
empathic
accuracy
have
shown
that
accurately
discerning
the
internal
states
of
oth-
ers,
as
well
as
inferring
intentions
from
observed
behavior,
relies
on
the
interaction
between
mirroring
and
mentalizing
processes
(Liew
et
al.,
2011;
Zaki
and
Ochsner,
2012).
There
is
also
evidence
that
our
immediate
affective
responses
to
others’
pain
and
distress
can
increase
prosocial
decision-making
(Christov-Moore
and
Iacoboni,
under
revision;
Hein
et
al.,
2010;
Masten
et
al.,
2011;
Ma
et
al.,
2011;
Smith,
2006).
Indeed,
it
is
likely
that,
without
the
interactive
par-
ticipation
of
both
modes
of
empathizing,
social
interactions
would
be
impaired,
potentially
impacting
the
health
and
wellbeing
of
the
individual
as
well
as
those
around
him/her
(Gallese,
2003).
While
we
now
associate
the
mentalizing
system
with
decision-
making,
musing
about
others
etc.,
this
system
may
have
arisen
in
part
as
a
form
of
contextual
control
for
mirroring.
In
our
view,
this
seems
likely
for
two
reasons:
compared
to
the
mirroring
system,
both
the
mentalizing
system’s
cognitive
functions
and
the
brain
areas
that
underlie
mentalizing
(i.e.,
temporal
and
prefrontal
cor-
tices),
(1)
developed
more
recently
in
our
evolution
and
(2)
are
the
last
to
mature
during
ontogeny
(Preston
and
De
Waal,
2002).
Furthermore,
neural
systems
associated
with
mentalizing
have
been
implicated
in
the
control
of
behavioral
mirroring
(mimicry)
(Spengler
et
al.,
2010).
Indeed,
recent
evidence
from
our
group
(Christov-Moore
and
Iacoboni,
under
revision)
suggests
that
mir-
roring
areas
and
mentalizing
areas
exist
in
interaction
rather
than
as
independent
systems.
Rather
than
just
using
the
mirroring
sys-
tem
when
we
view
others
in
pain,
feeling
emotion,
or
having
fast
social
interactions
that
are
typically
thought
to
bypass
mentalizing

606
L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
Fig.
1.
Neuroscientific
approaches
to
studying
experience
sharing
and
mentalizing.
(a)
The
experimental
logic
underlying
first-person
perception
studies
of
experience
sharing.
The
blue
circle
represents
brain
regions
engaged
by
direct,
first-person
experience
of
an
affective
response,
motor
intention,
or
other
internal
state.
The
yellow
circle
represents
regions
engaged
by
third-person
observation
of
someone
else
experiencing
the
same
kind
of
internal
state.
To
the
extent
that
a
region
demonstrates
neural
resonance—common
engagement
by
first-
and
third-person
experience
(green
overlap)—it
is
described
as
supporting
a
perceiver’s
vicarious
experience
of
a
target’s
state
(regions
demonstrating
such
properties
are
highlighted
in
green
in
c).
(b)
Studies
of
mentalizing
typically
ask
participants
to
make
judgments
about
targets’
beliefs,
thoughts,
intentions
and/or
feelings,
as
depicted
in
highly
stylized
social
cues,
including
vignettes
(top
left),
posed
facial
expressions
(right),
or
even
more
isolated
nonverbal
cues,
such
as
target
eye
gaze
(bottom
left).
Regions
engaged
by
such
tasks
(blue
in
c)
are
described
as
contributing
to
perceivers’
ability
to
mentalize.
(c)
Brain
regions
associated
with
experience
sharing
(green)
and
mentalizing
(blue).
IPL,
inferior
parietal
lobule;
TPJ,
temporoparietal
junction;
pSTS,
posterior
superior
temporal
sulcus;
TP,
temporal
pole;
AI,
anterior
insula;
PMC,
premotor
cortex;
PCC,
posterior
cingulate
cortex;
ACC,
anterior
cingulate
cortex;
MPFC,
medial
prefrontal
cortex
(from
Zaki
and
Ochsner,
2012).
(Bohl
and
van
den
Bos,
2012),
and
using
the
mentalizing
system
when
we
need
to
consciously
make
decisions
in
a
social
setting,
guess
the
beliefs
and
intentions
of
others,
or
take
another
person’s
perspective,
we
may
use
both
at
all
times.
Obviously,
one
system
may
take
the
lead
over
the
other,
depending
on
the
situation’s
demands.
This
larger
dynamic
system
formed
by
the
interactions
between
mirroring
and
mentalizing
may
allow
individuals
to
revisit
past
experience
and
behavior,
predict
the
consequences
of
their
own
behaviors,
both
for
themselves
as
well
as
for
others,
and
to
selec-
tively
share
in
the
behavior
and
affective
states
of
others
in
response
to
context
(such
as
common
group
affiliation).
An
understanding
of
empathy
would
be
incomplete
without
a
consideration
of
individual
differences.
Popular
conceptions
of
gender1–
defined
here
as
reflecting
both
self-identification
(i.e.,
females,
males)
as
well
as
biological
classification
(i.e.,
female,
male)
–
contain
expectations
about
empathy
and
empathic
behav-
ior,
many
of
which
have
been
borne
out
by
extant
research.
1For
consistency
and
simplicity,
throughout
this
review
we
will
refer
to
sex
dif-
ferences
(i.e.,
biological
differences
between
males
and
females);
however,
we
also
report
a
number
of
studies
of
gender
differences
(i.e.,
social
differences
based
on
self-identification
of
participants
as
men
or
women).
We
recognize
that
sex
and
gender
each
make
unique
contributions
to
empathetic
skill;
however,
given
that
we
are
including
studies
of
nonhuman
animals
and
infants,
it
is
more
parsimo-
nious
in
these
cases
to
primarily
focus
on
biological
individual
differences
(i.e.,
sex
differences).
However,
empathy
and
gender
remain
difficult
to
define,
in
part
because
the
disciplines
that
study
them
use
distinct
and
often
non-
overlapping
methods
and
terminology.
While
this
difficulty
is
not
something
we
can
address
in
this
article,
we
should
keep
it
in
mind
when
considering
the
evidence
reviewed
here.
In
reviewing
gender
differences
in
empathy,
we
propose
to
address
two
questions:
first,
how
deep
do
gender
differences
in
empathy
go?
Cultural
and
societal
effects
on
gender
differences
are
most
pronounced
in
explicit
measures
in
which
adults
are
asked
to
describe
themselves
or
produce
a
behavior
which
is
clearly
related
to
“empathy”
or
“sympathy”
(Eisenberg
and
Lennon,
1983;
Gleichgerrcht
and
Decety,
2013).
However,
meta-analyses
examining
gender
and
sex
differences
in
empathy
provide
results
supporting
fairly
stable
gender
differences
across
a
broad
range
of
measures
(e.g.,
Cohn,
1991;
Eisenberg
and
Lennon,
1983;
Feingold,
1994;
Hall,
1978,
1984;
Hoffman,
1977;
O’Brien
et
al.,
2013;
Thompson
and
Voyer,
2014;
although,
for
null
results
see
Lamm
et
al.,
2007).
Additionally,
empathy
has
developmental
precursors
in
early
infancy
(Alexander
and
Wilcox,
2012;
McClure,
2000)
as
well
as
evolutionary
precursors
in
other
social
animals
(Preston
and
De
Waal,
2002).
Indeed,
there
is
considerable
overlap
between
empathetic
behaviors
demonstrated
in
young
humans
early
in
development
and
in
nonhuman
animals.
Thus,
in
addition
to
exam-
ining
implicit
measures
of
empathy,
we
can
look
to
developmental
and
evolutionary
precursors
of
empathy
for
a
more
complete
view
of
sex
differences.

L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
607
Fig.
2.
Proposed
relationship
between
mentalizing
and
mirroring
processes
and
their
accompanying
brain
systems.
The
second
question
this
review
will
address
is
the
nature
of
empathy
itself,
that
is,
what
are
its
core
biological
and
neu-
ral
underpinnings?
More
specifically:
are
individual
differences
in
cognitive
and
affective
subcomponents
of
empathy
independent
or
tightly
integrated
(or
somewhere
in
between)?
Are
individual
differences
in
the
behavioral
manifestations
of
empathy,
such
as
social
competence
or
prosocial
behavior,
due
to
differences
in
low-
level
processes
like
emotional
reactivity,
or
higher
level
functions
like
spatial
reasoning
or
theory
of
mind
(ToM)?
Which
compo-
nents
of
empathy
emerge
first
during
ontogeny,
and
does
each
component
accomplish
a
specific
proximate
or
ultimate
function
throughout
development?
To
what
extent,
and
in
what
way,
is
empathy
modulated
and
controlled
by
higher
cognitive
functions?
As
recent
cognitive
neuroscience
reviews
have
suggested
(Zaki
and
Ochsner,
2012),
the
relationship
between
the
principal
compo-
nents
of
empathy,
as
they
are
currently
studied,
remains
unclear.
Although
several
scholars
agree
that
emotional
and
cognitive
com-
ponent
of
empathy
underpin
a
broad
range
of
empathic
responses,
a
global
concept
of
empathy
remains
elusive,
and
this
is
in
large
part
due
to
a
lack
of
cross-talk
among
the
disparate
fields
that
study
it.
Studying
gender
differences
in
empathy
might
provide
insights
to
understanding
empathy
by
observing
whether
such
dif-
ferences
covary
across
different
measures.
For
example,
if
we
were
to
find
consistent
gender
differences
in
both
affective
empathy
and
prosocial
behavior,
but
less
consistent
differences
in
cognitive
empathy,
we
might
infer
that
affective
empathy
drives
prosocial
behavior.
To
address
these
issues,
we
structured
this
review
into
four
parts.
First,
we
will
examine
the
evolutionary
precursors
of
empathy.
Then,
we
will
review
gender
differences
related
to
the
psychological
and
behavioral
processes
associated
with
empathy.
Sex
differences
in
empathy
will
be
also
evaluated
from
an
ontogenetic
point
of
view.
Lastly,
we
will
review
evi-
dence
suggesting
that
gender
differences
assessed
at
behavioral
and
psychological
level
are
supported
by
specific
neural
sub-
strates.
2.
Evolutionary
precursors
of
empathy
In
the
last
few
decades,
as
outlined
above,
it
has
become
evident
that
empathy
is
not
limited
to
the
cognitive
manifesta-
tion
of
the
capacity
to
take
the
perspective
of
another,
putting
oneself
in
others’
shoes.
Instead,
empathic
responses
are
often
revealed
by
immediate
responses
of
the
body
(e.g.,
Levenson
and
Ruef,
1992),
suggesting
that
the
brain
mechanisms
mediating
such
responses
are
often
devoid
of
cognitive
efforts
(Shamay-Tsoory,
2014;
Shamay-Tsoory
et
al.,
2009).
Empathy
should
therefore
be
better
understood
as
a
multilay-
ered
phenomenon.
There
is
general
agreement
that
one
of
the
most
basic
forms
of
empathy
is
a
fast,
stimulus-driven
response
that
aligns
the
motor
behavior
of
the
observer
and
the
observed
(Carr
et
al.,
2003;
Zaki
and
Ochsner,
2012;
Preston
and
De
Waal,
2002;
De
Vignemont
and
Singer,
2006).
This
fast
response
appears
to
be
the
basis
of
emotional
contagion,
in
which
emotions
spread
from
indi-
vidual
to
individual
through
mimicry,
for
instance,
when
someone
smiles
and
observers
immediately
do
the
same
(Lakin
et
al.,
2003;
McIntosh,
2006).
A
number
of
studies
show
that
vocalizations,
pos-
tures,
and
movements
are
often
mimicked
without
awareness
(e.g.,
Hatfield
et
al.,
1992;
Chartrand
and
Lakin,
2013).
For
example,
as
Darwin
(1872)
wrote:
When
a
public
singer
suddenly
becomes
a
little
hoarse,
many
of
those
present
may
be
heard,
as
I
have
been
assured
by
a
gentle-
man
on
whom
I
can
rely,
to
clear
their
throats;
but
here
habit
probably
comes
into
play,
as
we
clear
our
own
throats
under
similar
circumstances.”
(p.
34)
As
we
review
below,
most
of
these
phenomena
are
likely
related
to
the
activity
of
a
mirror
mechanism
through
which
the
obser-
vation
of
others’
actions
or
emotions
activates
motor
programs
corresponding
to
observed
actions.
Recent
work
has
demonstrated
that
such
emotional
and
behav-
ioral
responses,
including
sensitivity
to
conspecifics’
distress,
are
common
in
the
animal
kingdom
as
well
(e.g.,
monkeys:
Nagasaka
et
al.,
2013;
pigs:
Reimert
et
al.,
2013;
rats:
Ben-Ami
Bartal
et
al.,
2014;
mice:
Sanders
et
al.,
2013;
Mancini
et
al.,
2013;
Palagi
et
al.,
2009).
Empathetic
behavior
appears
particularly
strong
in
social
species
with
prolonged
parental
care,
such
as
mammals
and
some
birds,
in
which
there
are
reports
of
behaviors
that
are
indicative
not
only
of
sensitivity
to
others’
emotional
states,
but
also
of
the
presence
of
some
basic
forms
of
empathy
(Gonzalez-Liencres
et
al.,
2013;
de
Waal,
2008;
Edgar
et
al.,
2011).
In
some
species,
the
bond
between
individuals
is
expressed
through
sophisticated
emotional
channels
that
have
been
shaped
through
a
long
natural
history.
For
example,
capacities
to
cooperate,
to
support
conspecifics
dur-
ing
conflicts,
and
to
provide
comfort
to
social
partners
in
distress
have
been
widely
described
in
primates
and
other
animals
(e.g.,
elephants:
Plotnik
and
de
Waal,
2014;
chimpanzees:
Romero
et
al.,
2010).
These
phenomena
imply
that
a
type
of
affective
channel
between
individuals
may
be
involved
in
some
species’
social
rela-
tionships.
In
support
of
this
hypothesis,
recent
empirical
studies
in
gelada
baboons
have
demonstrated
that
the
speed
and
frequency
of
rapid
facial
mimicry
(Fig.
3)
were
higher
among
individuals
with
strong
bonds,
such
as
mothers
and
their
infants
(Mancini
et
al.,
2013).
Interestingly,
in
bonobos
yawn
contagion
appears
stronger
between
kin
and
friends
than
with
unrelated
individuals
(Demuru
and
Palagi,
2012),
thus
suggesting
that
emotional
contagion
is
affected
by
the
quality
of
the
relationship
and
by
the
affective
attunement
between
individuals.
Recent
work
in
humans
supports
this
hypothesis
by
demonstrating
that
the
rate
of
contagion
is
greater
in
friends
and
kin
compared
to
strangers
and
acquaintances
(Norscia
and
Palagi,
2011).

608
L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
Fig.
3.
An
example
of
rapid
facial
mimicry
of
play
face
in
two
juvenile
gelada
baboons
(taken
by
PFF).
Although
a
number
of
studies
have
documented
empathic
or
proto-empathic
behaviors
in
the
animal
kingdom
(for
reviews,
see
Edgar
et
al.,
2012;
Panksepp
and
Panksepp,
2013),
few
studies
have
tested
whether
there
are
sex
differences
in
empathy.
This
is
pri-
marily
due
to
the
fact
that
animal
studies,
like
many
human
studies,
often
have
small
samples
or
samples
of
only
one
sex,
therefore
not
allowing
such
comparisons.
Such
studies
are
important
because
they
can
shed
light
on
the
evolutionary
mechanisms
that
were
selected
to
facilitate
empathy
in
some
individuals,
thus
leading
to
individual
differences
in
empathic
predisposition
(de
Waal
and
Suchak,
2010).
We
review
below
a
small
number
of
studies
in
ani-
mals
that
suggest
higher
levels
of
empathy
in
females
than
males,
a
motif
that
seems
to
recur
in
the
human
literature
as
well.
2.1.
Emotional
contagion:
Yawning,
facial
mimicry,
and
pain
One
behavioral
manifestation
of
empathy
is
mimicry,
including
facial
mimicry
(Niedenthal
et
al.,
2010;
Davila-Ross
et
al.,
2008)
and
contagious
yawning
(Platek
et
al.,
2003;
Campbell
et
al.,
2009),
both
of
which
occur
in
human
and
nonhuman
animals
(Figs.
3
and
4).
Gelada
baboons
exhibit
rapid
facial
mimicry,
with
the
highest
levels
of
mimicry
occurring
during
mother–infant
play
(Mancini
et
al.,
2013).
In
terms
of
sex
differences,
female
baboons,
com-
pared
to
males,
exhibit
stronger
and
more
specific
matching
of
yawn
types
(Palagi
et
al.,
2009).
This
may
reflect
stronger
bonds
among
females,
compared
to
males.
Interestingly,
in
this
species,
females
form
coalitions,
have
long-lasting
relationships,
and
share
in
infant
care,
thus
supporting
each
other
through
alloparental
care.
If
the
dominant
male
dies
or
is
replaced,
the
females
do
not
disperse
but
remain
assembled
in
the
group.
It
has
been
proposed
that
this
form
of
social
organization
may
favor
the
capacity
of
females
to
be
emotionally
tuned
to
one
another
(Palagi
et
al.,
2009).
In
bonobos,
yawn
contagion
is
strongest
when
the
model
is
a
female
(Demuru
and
Palagi,
2012).
This
finding
is
reminiscent
of
data
in
humans
showing
greater
empathy
directed
at
females
than
males
(Bryant,
1982;
Olweus
and
Endresen,
1998).
A
number
of
species
can
use
the
emotional
expressions
of
others
to
guide
their
own
behavior
(e.g.,
Morimoto
and
Fujita,
2011);
however,
few
studies
have
examined
whether
there
are
sex
differ-
ences
in
sensitivities
to
conspecifics’
emotional
expressions.
For
example,
when
viewing
a
conspecific
in
pain,
the
pain-associated
behaviors
in
the
viewer
(e.g.,
writhing)
can
indicate
the
amount
of
empathy.
Recent
work
in
rodents
suggests
females
have
greater
sensitivity
to
other’s
pain
compared
to
males.
In
mice,
for
example,
both
males
and
females
appear
to
increase
their
writhing
when
viewing
a
familiar
individual
in
pain
(Langford
et
al.,
2006).
However,
when
paired
with
an
unfamiliar
individual,
males,
but
not
females,
show
a
decrease
in
their
writhing,
suggesting
less
sensitivity
toward
the
pain
of
the
unfamiliar
mouse
(Langford
et
al.,
2006).
These
data
seem
to
be
in
accord
with
studies
in
humans
suggesting
that
males
tend
to
have
their
empathetic
responses
influenced
more
by
contextual
cues
compared
to
females
(Brehm
et
al.,
1984;
Ickes
et
al.,
2000;
Singer
et
al.,
2006).
2.2.
Consolation
and
prosocial
behavior
Consolatory
behavior,
that
is,
providing
comfort
to
victims
of
aggression
or
individuals
who
are
otherwise
upset,
appears
to
be
widespread
throughout
the
animal
kingdom.
This
behavior
has
been
documented
in
great
apes
(e.g.,
chimpanzees:
de
Waal
and
van
Roosmalen,
1979;
bonobos:
Palagi
et
al.,
2004;
gorillas:
Cordoni
et
al.,
2006),
canines
(e.g.,
dogs:
Cools
et
al.,
2008;
wolves:
Palagi
and
Cordoni,
2009),
corvids
(e.g.,
ravens:
Fraser
and
Bugnyar,
2010;
rooks:
Seed
et
al.,
2007),
and,
most
recently,
elephants
(Plotnik
and
de
Waal,
2014).
Most
of
these
studies,
however,
had
insufficient
sample
sizes
to
allow
for
examination
of
sex
differences.
Although
sex
differences
in
these
studies
were
rarely
examined,
in
chim-
panzees,
female
bystanders
were
more
likely
to
console
distressed
individuals
than
males
(Romero
et
al.,
2010),
and
in
lowland
goril-
las,
immature
females
offer
more
frequent
consolatory
contact
than
males
(Cordoni
et
al.,
2006).
One
important
aspect
of
empathetic
behavior
is
whether
indi-
viduals
come
to
the
aid
of
others
in
need
and
attempt
to
help
them.
While
this
phenomenon
has
been
well
described
in
nonhuman
primates
(e.g.,
capuchins:
Drayton
and
Santos,
2013;
orangutans:
Liebal
et
al.,
2014),
it
is
also
present
–
perhaps
somewhat
sur-
prisingly
–
in
rodents.
For
example,
female
mice
were
more
likely
than
male
mice
to
approach
cagemates
who
were
restrained
and
in
pain,
compared
to
an
unaffected
cagemate
(Langford
et
al.,
2010).
Females
did
not,
however,
approach
unfamiliar
mice
in
pain.
Stress
may
trigger
females,
but
not
males,
to
increase
their
affili-
ation
toward
familiar
social
partners,
as
well
as
improving
their
general
empathic
tendency,
a
phenomenon
known
as
the
“tend-
and-befriend”
response
(Taylor
et
al.,
2000;
also
see
Bull
et
al.,
1972;
Tomova
et
al.,
2014).
Another
study
in
rats
found
that
females,
com-
pared
to
males,
were
faster
and
more
likely
to
release
a
trapped
cagemate
(Ben-Ami
Bartal
et
al.,
2011).
This
form
of
helping
behav-
ior
occurred
even
when
rats
were
not
allowed
social
contact
after
releasing
the
cagemate,
and
even
when
offered
a
food
reward.
The
study
suggests
that
rats,
especially
females,
may
behave
in
intentionally
prosocial
ways,
without
training
or
reward,
and
act
prosocially
even
when
prosociality
decreases
food
intake
(i.e.,
hav-
ing
to
share
food
with
cagemate).
Similarly,
adult
female
rats
are
more
likely
than
male
rats
to
approach
50-kHz
vocalizations
–
appetitive
calls
that
occur
during
rough-and-tumble
play,
asso-
ciated
with
positive
affect,
and
which
may
serve
as
contact
calls
(Seffer
et
al.,
2014;
Willadsen
et
al.,
2014).
Sex
differences
in
other
animals
have
also
been
observed.
Jack-
daws
–
a
large-brained
corvid
species
–
were
given
the
option
of
either
choosing
a
prosocial
action,
in
which
both
the
actor
and
the
recipient
received
food,
or
a
selfish
action,
in
which
only
the
actor
received
food
(Schwab
et
al.,
2012).
Female
jackdaws
were
more
likely
than
males
to
behave
prosocially,
while
males
were
more
likely
to
behave
selfishishly.
In
another
study
where
males
were
not
tested,
female
chimpanzees
demonstrated
spontaneous
prefer-
ences
for
prosocial
rewards,
as
opposed
to
selfish
rewards
(Horner
et
al.,
2011).
Chimpanzee
mothers
and
their
offspring
exhibit
flexi-
ble
helping
behaviors,
providing
partners
with
tools
to
accomplish
their
goals
(Yamamoto
et
al.,
2012).
Female
chimpanzees
are
also
more
likely
than
males
to
share
food
with
individuals
with
whom
they
have
strong
affiliative
bonds
(Eppley
et
al.,
2013).

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609
Fig.
4.
A
yawn
response
of
one
chimpanzee
during
presentation
of
a
yawn
videotape
(from
Anderson
et
al.,
2004).
The
chimpanzee
(named
Ai)
watches
a
yawn
on
the
screen
(top
left),
starts
to
yawn
as
the
stimulus
yawn
ends
(top
right),
continues
to
yawn
(bottom
left),
and
completes
the
yawn
while
the
screen
is
blank
(bottom
right).
2.3.
Sensitivity
to
others
in
play
and
caregiving
Sex
differences
in
caregiving
can
emerge
early
in
development,
as
evident
in
studies
of
play
behavior.
Studies
investigated
how
individuals
manipulate
objects,
such
as
dolls,
that
traditionally
are
handled
differently
by
boys
and
girls.
In
chimpanzees,
juvenile
females
are
more
likely
than
males
to
carry
sticks
as
if
they
were
infants
(i.e.,
cradling
sticks
in
their
arms),
while
males
are
more
likely
to
use
sticks
to
hit
one
another
(Kahlenberg
and
Wrangham,
2010).
Other
studies
show
that
while
female
play
more
often
involves
caring
for
another
individual
(e.g.,
pretended
baby),
male
play
does
not
(e.g.,
Goldberg
and
Lewis,
1969;
Hines,
2008).
Indeed,
in
vervet
and
rhesus
monkeys,
males
played
longer
with
wheeled
toys
and
females
played
longer
with
dolls
and
plush
toys
(Hassett
et
al.,
2008;
Alexander
and
Hines,
2002),
similarly
to
human
chil-
dren
(Pellegrini
and
Smith,
2005).
This
may
occur
due
to
different
selective
pressures
on
males
and
females
because
of
their
differ-
ent
behavioral
roles,
with
females
more
often
being
the
primary
caretakers
of
offspring
(Alexander
and
Hines,
2002),
helping
to
practice
relevant
skills
for
survival
and
reproduction
(Smith,
2010).
However
the
proximate
mechanisms
underlying
these
different
preferences
remain
largely
unknown
(for
a
review,
see
Williams
and
Pleil,
2008).
In
Old
World
monkeys,
females
demonstrate
more
interest
in
infants,
engage
in
more
play
parenting
throughout
their
juvenile
years,
and
spend
more
time
handling
infants
than
males
(Geary,
1998;
Maestripieri,
1994;
Pryce,
1995).
Similarly,
while
male
dolphins
engage
in
more
solitary
object-based
play,
females
engage
in
more
social
play
(Greene
et
al.,
2011).
If
play
functions
to
prepare
males
and
females
for
different
social
roles,
then
sex
differences
in
play
would
only
be
present
in
species
in
which
males
and
females
have
different
roles.
For
example,
in
grey
wolves
(Canis
lupus
lupus)
males
and
females
have
similar
social
roles
(e.g.,
collectively
rear
offspring,
cooperative
hunting),
and
exhibit
no
differences
in
social
play
(Cordoni,
2009),
but
in
domes-
tic
dogs
(Canis
lupus
familiaris)
sex
differences
in
play
have
been
observed
(Pal,
2008;
Ward
et
al.,
2008).
For
example,
in
domes-
tic
dog
puppies,
when
males
played
with
females
they
initiated
more
offensive
interactions
(attack
and
pursuit)
and
more
self-
handicapping
behaviors
than
females,
while
females
were
found
to
initiate
play
more
with
other
females
(Ward
et
al.,
2008).
Play
may
be
important
in
helping
individuals
to
learn
to
interpret
emotional
signals
of
others
(LaFreniere,
2011),
a
skill
which
is
foundational
to
empathy.
2.4.
An
evolutionary
ancient
instinct
to
care
for
offspring
It
is
possible
that
parental
care
is
the
ancient
root
from
which
more
complex
forms
of
empathy
have
emerged
(Preston,
2013).
However,
in
several
species,
beyond
mammals
and
birds,
parents
show
complex
forms
of
energy-demanding
and
potentially
life-
threatening
parental
care,
such
as
in
spiders,
cephalopods,
fishes,
frogs,
and
reptiles
(Trumbo,
2012).
It
is
unclear
whether
empa-
thy
is
a
key
factor
in
motivating
such
behaviors,
given
that,
in
most
of
these
cases,
parent
intervention
is
not
triggered
by
the
needs
of
the
offspring
(which
could
reveal
sensitivity
to
others’
internal
states),
but
rather
by
external
danger
stimuli
activating
defensive
behavioral
responses
(Rosenblatt,
2003).
For
example,
in
some
species
of
spiders
the
young
remain
with
the
mother
for
an
extended
period,
during
which
time
the
mothers
provide
food
and
defense
(Yip
and
Rayor,
in
press).
Mammals
evolved
more
complex
behavioral
strategies
to
cope
with
immature
off-
spring,
possibly
because
such
prolonged
maternal
care
is
necessary
to
facilitate
offspring
weaning
and
independence
(Olazábal
et
al.,
2013).

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During
the
periods
that
precede
and
follow
birth,
mothers
in
all
mammalian
species
experience
changes
in
their
physiology,
anatomy,
and
behavior
(Olazábal
et
al.,
2013).
In
most
mammalian
species,
in
terms
of
energy
costs,
mothers
invest
more
in
each
offspring,
compared
to
fathers
(Martin
and
MacLarnon,
1985).
In
some
species,
like
chimpanzees,
a
mother
usually
gives
birth
to
one
infant
every
five
years,
and
keeps
nursing
for
years,
during
which
time
the
infant’s
only
source
of
food
is
the
mother’s
milk
(Tutin
and
McGinnis,
1981).
Unlike
humans,
females
of
most
Old
World
monkeys
and
apes
rear
their
infants
alone
and
largely
without
the
collaboration
of
other
females
(Hardy,
1976;
Rogers
and
Davenport,
1970).
The
mother–infant
relationship
in
primates
is
unique,
characterized
by
the
infant
constantly
clinging,
mother–infant
embracing,
and
prolonged
ventro-ventral
contact
(i.e.,
contact
in
which
the
infant
clings
to
the
front
of
the
mother
in
old-world
monkeys
and
apes;
e.g.,
Manning
et
al.,
1994;
Maestripieri,
1994).
Primates’
long
period
of
altriciality
(i.e.,
dependence
on
the
mother
for
food,
safety,
etc.)
may
have
produced
a
series
of
changes
in
females’
capacity
to
detect
and
respond
adaptively
to
newborns’
signals
and
needs,
that
may
impact
the
quality
of
mother-infant
relationships,
and
ultimately,
infants’
long-term
health.
First,
mothers
must
synchronize
their
own
biological
cycle
and
daily
activities
with
the
infants’
basic
needs
(e.g.,
being
fed
peri-
odically
and
for
a
long
period
of
time).
Given
their
extended
period
of
need,
infants
evolved
a
system
to
communicate
their
internal
states
to
their
mothers,
based
on
their
own
needs
and
goals.
In
addition,
the
infants’
process
of
gaining
independence
is
long
and
the
early
stages
of
environmental
exploration
are
mediated
by
the
presence
of
the
mother
who
provides
oversight,
food
and
protec-
tion.
This
process
is
commonly
framed
in
terms
of
‘attachment’
(Chisholm,
1996),
a
framework
that
provides
a
theoretical
under-
pinning
of
the
bond
between
infants
and
caregivers
(Bowlby,
1969).
One
of
the
central
concepts
in
attachment
theory
is
the
proxim-
ity
to
the
mother
(Maestripieri,
2001,
2003).
For
example,
in
old
world
monkeys,
apes,
and
humans,
the
mother
plays
a
key
role
in
the
evolution
of
attachment
because
mothers
play
an
active
role
in
breaking
and
making
contacts
with
their
infants
as
they
become
independent.
Furthermore,
in
primates,
the
mother–infant
communication
system
relies
on
a
complex
combination
of
visual
signals,
vocalizations,
and
gestures.
The
evolved
facial
communica-
tion
system
of
primates
is
particularly
suitable
to
express
emotions
and
to
externalize
internal
state.
Continuous
ventro-ventral
con-
tact
allows
for
face-to-face
interactions,
as
mothers
and
infants
are
already
facing
one
another
(Matsuzawa,
2007).
These
face-to-
face
interactions
have
profound
effects
on
mothers’
biology
and
psychology,
in
terms
of
mothers’
capacity
to
evaluate
the
infants’
distress,
to
anticipate
dangers,
to
re-establish
contact
with
off-
spring
when
it
is
lost,
and
to
reduce
the
infant’s
agitation
or
fear
associated
with
separation
(Maestripieri,
2003).
Females,
as
the
primary
caretakers
of
the
young
infants,
may
have
evolved
adaptations
to
be
sensitive
to
nonverbal
expressions,
as
such
sensitivities
may
have
increased
infant
survival
(Babchuk
et
al.,
1985;
Hampson
et
al.,
2006).
According
to
the
Primary
Care-
taker
Hypothesis,
males
did
not
experience
this
same
selective
pressure,
and
therefore
this
may
account
for
sex
differences
in
emotion
recognition
and
empathy.
Indeed,
maternal
sensitivity
and
a
healthy
attachment
influence
infants’
health
and
immune
functions
(Goldberg,
2000).
Human
newborns
are
also
sensitive
to
facial
signals
and
mother–infant
interactions
are
characterized
by
a
rich-repertoire
of
face-to-face
interplays
with
a
clear
tem-
poral
structure
(Feldman,
2007;
Stern,
1977;
Trevarthen,
1979).
During
these
shared
moments
mothers
provide
important
social
inputs
to
infants,
which
are
critical
for
infants’
social
and
cogni-
tive
development
(Trevarthen,
1998;
Nagy,
2006).
More
recently
it
has
been
shown
that
similar
patterns
of
face-to-face
interactions
are
present
in
monkeys
and
apes,
during
which
mothers
produce
a
variety
of
facial
expression
to
the
infants,
exaggerating
the
gestures
and
accompanying
them
with
vocalizations
(Ferrari
et
al.,
2009;
Maestripieri
and
Wallen,
1997;
Matsuzawa,
2007).
Might
this
primary
caretaker
selective
pressure
account
for
sex
differences
in
empathy?
An
attempt
to
answer
this
question
may
be
possible
through
future
studies
that
compare
species
with
higher
degrees
of
paternal
care
–
such
as
in
siamangs,
tamarins,
mar-
mosets,
titi
monkeys,
and
owl
monkeys
–
with
species
with
lower
degrees
of
paternal
care.
Sex
differences
in
empathy
should
be
predicted
by
the
species-typical
degree
of
relative
paternal
and
maternal
care.
For
example,
in
titi
monkeys
and
owl
monkeys,
the
fathers
are
the
primary
carriers
of
the
infants,
and
may
carry
infants
for
up
to
90%
of
the
time
(Fernandez-Duque
et
al.,
2009).
In
titi
mon-
keys,
in
fact,
infants
actually
prefer
their
fathers
to
their
mothers
(Mendoza
and
Mason,
1986).
To
summarize,
the
evidence
thus
far
is
consistent
with
the
idea
that
selective
pressures
shaped
females’
anatomy,
physiology,
and
neurobiology
to
facilitate
sensitivity
to
infants’
internal
states
and
resultant
nurturing
behavior.
Hence,
sex
differences
in
foundational
aspects
of
empathic
behavior
may
derive
from
a
common
evolu-
tionary
history
of
maternal
care.
3.
Behavioral
and
psychological
gender
differences
in
humans
3.1.
Emotion
recognition,
priming,
and
emotion
contagion
In
humans,
the
ability
to
recognize
other
people’s
emotions
varies
among
individuals
(Martin
et
al.,
1996).
Throughout
the
non-
verbal
perception
literature
there
appears
a
consistent
pattern
of
interindividual
differences:
a
female
advantage
in
nonverbal
emo-
tion
recognition,
in
both
visual
and
auditory
modalities
(Hall,
1990;
McClure,
2000;
Schirmer
et
al.,
2007;
for
recent
reviews,
see
Kret
and
De
Gelder,
2012;
Stevens
and
Hamann,
2012;
Thompson
and
Voyer,
2014).
Though
an
extensive
review
of
these
studies
is
out-
side
of
the
scope
of
the
present
review,
we
will
focus
on
a
few
key
areas
of
emotion
recognition
related
to
empathy,
including
emotion
conveyed
through
body
language,
emotion
contagion,
and
socioemotional
priming.
Studies
report
that
facial
expression
recognition
skill
for
briefly
presented
faces
–
which
therefore
must
be
processed
using
rapid,
prereflective
strategies
–
is
positively
correlated
with
self-reported
empathic
concern
(Davis,
1983).
In
contrast,
facial
expression
recognition
skill
for
expressions
presented
for
longer
lengths
of
time
–
therefore
allowing
more
cognitive-based
strategies
–
is
correlated
with
self-reported
cognitive
empathy
and
social
under-
standing
(Lawrence
et
al.,
2004).
Therefore,
both
types
of
empathy,
emotional
and
cognitive,
are
related
to
individual
differences
in
skills
for
identifying
other
people’s
emotions
(Besel
and
Yuille,
2010).
Females
are
faster
and
more
accurate
than
males
in
recogniz-
ing
facial
expressions
(e.g.,
Babchuk
et
al.,
1985;
Hampson
et
al.,
2006;
Thayer
and
Johnson,
2000).
There
is
also
a
small
but
growing
literature
on
gender
differences
in
the
ability
to
recognize
emo-
tional
body
language.
The
point-light
display
method
allows
for
the
study
of
biological
motion,
such
as
body
language,
and
con-
sists
of
displaying
little
spots
of
light
at
various
points
on
the
target’s
body,
which
then
move
when
the
target
moves,
on
a
dark
background,
and
therefore
reflect
the
motion
of
a
specific
move-
ment
(e.g.,
walking,
running,
jumping),
while
removing
all
other
cues
(Johansson,
1973).
Females,
compared
to
males,
appear
to
be
faster
(Alaerts
et
al.,
2011)
and
more
accurate
(Sokolov
et
al.,
2011)
at
recognizing
bodily
emotions,
such
as
identifying
actions
as
happier,
sadder,
angrier
or
no
different
from
a
preceding
neutral
action.
Specifically,
females
were
more
accurate
than
males
in
rec-
ognizing
angry
and
neutral
body
language,
while
males
were
more

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611
accurate
than
females
in
reading
happy
body
language
(Sokolov
et
al.,
2011).
Interestingly,
emotion
recognition
of
body
language
is
modulated
by
the
sex
of
the
target:
males
recognize
expres-
sions
of
happiness
in
female
locomotion
faster
and
more
accurately,
while
females
seem
to
be
better
and
faster
at
recognizing
angry
locomotion
of
males,
which,
from
an
evolutionary
perspective,
is
consistent
with
mating-related
and
threat-avoidance
goals
in
males
and
females,
respectively
(Krüger
et
al.,
2013).
This
finding
also
raises
another
important
issue,
that
is,
whether
different
natu-
ral
selection
pressures
acted
upon
specific
neural
circuits
to
sustain
abilities
that
confer
reproductive
advantages.
The
studies
reported
above,
in
fact,
may
suggest,
although
speculative,
that
sexual
selec-
tion
could
have
rendered
males
more
sensitive
to
females’
social
positive
signals
in
the
context
of
courtship
and
sexual
behavior.
The
capacity
to
detect
positive
emotions
in
females
could
allow
males
to
detect
female
interest
and
potential
mating
opportuni-
ties.
Recent
work
has
shown
that
social
cues,
such
as
smile,
can
affect
sexual
preference
and
the
transmission
of
sexual
preferences
in
others
(Jones
et
al.,
2007).
While
females,
by
being
more
accu-
rate
in
reading
emotions
through
body
language,
could
better
rate
the
behavioral/emotional
quality
of
the
potential
partner
in
terms
of
his
paternal
care
capacity
and
sensitivity
to
the
woman’s
and
children’s
needs.
Clearly
more
extensive
work
is
required
to
under-
stand
the
possible
functions
and
evolutionary
implications
of
the
above
described
gender
differences.
Although
emotional
contagion
seems
to
contribute
to
emotion
recognition
(Hatfield
et
al.,
1993),
there
are
few
studies
investigat-
ing
gender
differences
in
emotion
contagion.
In
one
study,
females,
compared
to
males,
reported
greater
susceptibility
to
contagion
and
displayed
more
overt
signs
of
contagion
in
a
semi-naturalistic
setting,
for
both
positive
and
negative
emotions
(Doherty
et
al.,
1995).
Similarly,
when
providing
support
for
a
troubled
friend,
females
experience
more
emotion
contagion
than
males
(Magen
and
Konasewich,
2011).
In
fact,
females
report
experiencing
emo-
tion
contagion
more
often
than
males
in
their
daily
lives
(Kevrekidis
et
al.,
2008).
Females,
compared
to
males,
exhibit
greater
facial
mimicry
when
viewing
expressions
(Dimberg
and
Lundquist,
1990;
Lundqvist,
1995;
Sonnby-Borgström
et
al.,
2003)
and
rely
more
than
males
on
facial
feedback
for
recognizing
facial
expressions
(Stel
and
van
Knippenberg,
2008).
Another
approach
to
the
study
of
emotional
contagion
exam-
ines
pre-reflective
emotional
processing
using
an
emotional
priming
method
in
which
participants
are
exposed
to
negative
or
positive
emotional
cues
outside
of
conscious
awareness,
such
as
happy
or
sad
faces
(Donges
et
al.,
2012).
In
one
study,
participants
were
presented
with
a
face
prime
expressing
either
happiness
or
sad-
ness,
followed
by
a
neutral
face,
and
then
asked
to
evaluate
how
happy
or
how
sad
the
neutral
face
appeared.
They
report
that
females
tended
to
identify
neutral
faces
as
happier
than
males,
and
hence
females,
compared
to
males,
were
more
affected
by
happy
face
priming
(Klauer,
1997).
This
suggests
that
females
might
have
a
greater
ability
than
males
to
perceive
happy
emotions
at
the
pre-reflective
level
in
visual
stimuli
(for
similar
findings
in
audi-
tory
stimuli:
Schirmer
et
al.,
2007).
In
another
study,
participants
were
primed
to
be
in
either
happy
or
sad
moods
using
short
film
scenes,
followed
by
measures
of
participants’
emotion
recognition
accuracy
(Schmid
et
al.,
2011).
They
report
that
males
primed
for
a
happy
mood
recognized
facial
emotions
more
accurately
than
when
primed
for
a
sad
mood,
while
females
did
not
show
any
significant
priming.
Additionally,
eye
tracking
research
revealed
that
females
tended
to
process
facial
expressions
more
globally
(i.e.,
attending
to
the
whole
face
rather
than
localized
areas)
than
males
and
were
more
accurate
in
emotion
recognition.
Further-
more,
participants
used
more
global
processing
after
being
primed
for
happy
mood
rather
than
for
sad
mood.
However,
only
males
became
more
accurate
in
recognizing
emotions
when
primed
for
happiness.
Together
these
results
suggest
that
females
seem
to
use
global
processing
by
default
and
therefore
are
not
as
affected
by
happy
mood
primes,
while
males
do
not
use
global
processing
by
default
and
are
therefore
more
sensitive
to
the
happy
prime.
In
related
work,
females
fixated
more
on
the
eye
regions
of
faces,
compared
to
males,
which
may
also
be
related
to
the
female
advan-
tage
in
facial
expression
recognition
(Hall
et
al.,
2010),
and
which
appears
positively
associated
with
empathetic
skill
(Cowan
et
al.,
2014).
While
generally
it
seems
that
females
are
either
significantly
faster
or
more
accurate
(or
both)
at
emotion
recognition,
some
studies
show
no
gender
differences
(Klein
and
Hodges,
2001).
This
failure
to
find
differences
may
be
due
to
variation
of
experimental
contexts
and
designs.
For
example,
females
were
less
accurate
than
males
at
judging
interpersonal
behavior
by
verbal
and
nonverbal
cues
if
they
thought
that
they
were
being
tested
on
interrogation
skills
in
the
military
(a
historically
masculine
occupation),
while
males
were
less
accurate
if
they
thought
the
test
measured
judg-
ment
skills
necessary
for
social
workers
(a
historically
feminine
occupation)
(Horgan
and
Smith,
2006).
Higher
empathic
accuracy
scores
in
females
might
be
driven
by
motivation
to
appear
more
empathic
(Klein
and
Hodges,
2001).
They
did
not
find
any
signifi-
cant
differences
in
empathic
accuracy
between
males
and
females
when
they
were
asked
to
complete
a
sympathy
questionnaire
after
the
empathic
accuracy
test.
However,
females
performed
better
if
they
had
to
fill
in
the
questionnaire
before
the
task.
The
results
sug-
gest
that
females
are
motivated
to
try
harder
to
understand
other
people’s
feelings
during
the
task
if
they
think
that
what
is
measured
is
relevant
to
a
stereotypical
female
role
(sympathy).
Although
moti-
vational
differences
between
males
and
females
may
account
for
some
of
the
reported
findings
of
female
advantages
in
empathy,
they
can-
not
explain
female
advantages
in
automatic/unconscious
nonverbal
perception
(e.g.,
Donges
et
al.,
2012),
or
female
advantages
in
popu-
lations
that
do
not
exhibit
social
desirability
biases,
such
an
nonhuman
animals
and
infants,
reviewed
below.
3.2.
Mentalizing
Mentalizing
is
a
largely
conscious,
deliberative
process
by
which
individuals
take
others’
perspectives
and
infer
others’
intentions
and
beliefs
(Zaki
and
Ochsner,
2012).
As
such,
it
is
a
major
component
of
empathy.
In
contrast
to
findings
on
affective
respon-
siveness
and
emotion
recognition,
there
is
inconsistent
evidence
for
gender
differences
in
ToM,
or
the
ability
to
conceive
of
oth-
ers’
mental
states,
including
what
others’
know,
want,
feel,
or
believe
(Premack
&
Woodruff,
1978).
While
there
are
a
num-
ber
of
studies
in
children
that
report
female
advantages
in
ToM,
reviewed
below,
there
are
fewer
studies
in
adults
examining
ToM,
in
general,
as
it
is
assumed
that
adults
already
have
mature
ToM
abilities.
In
a
study
on
visual
perspective-taking
(a
precursor
to
ToM),
males,
but
also
females
with
relatively
high
autism
spectrum
disorder
(ASD)-characteristic
personality
traits
were
slower
in
perspective-taking
than
females
with
low
ASD
traits,
suggest-
ing
that
high-ASD-trait
individuals,
regardless
of
sex,
may
show
lower
fluidity
in
adopting
another’s
visual
perspective.
This
dif-
ference
in
visual
perspective-taking
hints
at
differences
in
the
more
general
ability
to
understand
what
others
see,
think,
and
feel.
Some
sex
differences
in
ToM
tasks
may
be
driven
by
the
fact
that
males,
compared
to
females,
report
that
they
less
often
adopt
someone
else’s
perspective
during
everyday
situ-
ations
(Pearson
et
al.,
2013).
Studies
of
imagined
perspective
transformation
(in
which
the
participant
has
to
mentally
adopt
a
different
perspective
from
their
current
one,
relative
to
an
external
object)
suggest
an
increased
emphasis
on
visuospatial
processes
in
males
during
perspective-taking,
rather
than
the
social–emotional

612
L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
perspective-taking
processes
in
which
females
typically
show
an
advantage
(Gardner
et
al.,
2012;
Meneghetti
et
al.,
2012).
Only
one
study,
to
our
knowledge,
reported
a
male
advantage
in
ToM
(Russell
et
al.,
2007).
In
this
study,
participants
viewed
12
cartoons,
half
of
which
require
an
understanding
of
the
cartoon
character’s
mental
state
in
order
to
“get”
the
joke,
and
half
of
which
require
an
understanding
of
physical
state
to
“get”
the
joke.
Males
outperformed
females
on
both
the
mental
and
physical
state
car-
toons.
The
authors
concluded
that
this
advantage
was
potentially
due
to
a
greater
emphasis
on
cognitive-systematizing
strategies
in
males.
These
studies
suggest
that
there
may
be
gender
differences
in
cognitive
forms
of
empathy,
such
as
perspective
taking
and
ToM.
These
differences,
however,
may
also
be
influenced
by
contextual
factors
(hence
some
apparently
inconsistent
findings).
This
con-
textual
modulation
may
be
key
to
a
better
and
more
nuanced
understanding
of
gender
differences
in
empathy
based
on
the
inter-
action
between
multiple
processes.
Indeed,
there
is
evidence
to
suggest
that
cognitive
and
affective
forms
of
empathy
operate
in
an
interactive
way,
with
each
contributing
information
and
mod-
ulation
to
the
other
(Decety
and
Moriguchi,
2007;
Chrisov-Moore
and
Iacoboni,
under
review).
3.3.
Prosocial
behavior
Since
empathy
aids
in
understanding
others’
emotions,
it
is
also
likely
to
be
a
major
driving
force
in
pro-social
behavior.
There
has
been
a
growing
body
of
research
investigating
altruistic
behavior
(e.g.,
helping,
sharing,
volunteering)
by
means
of
economic
games
and
self-report
studies
linking
empathy
to
pro-sociality.
As
we
review
next,
these
studies
indicate
not
only
that
the
level
of
empa-
thy
is
positively
correlated
with
pro-social
behavior,
but
also
that
females
may
be
more
empathic
and
thus
more
altruistic
than
males.
3.3.1.
Economic
behavior
One
of
the
most
common
ways
of
investigating
pro-social
behavior
in
human
adults
is
with
economic
games.
In
the
Ultima-
tum
Game,
two
individuals
(a
proposer
and
a
responder)
divide
up
a
sum
of
money
between
them,
based
on
the
proposer’s
offer
of
a
division
of
the
total
sum.
The
responder
can
then
either
accept
(both
get
the
money)
or
reject
the
offer
(both
get
zero).
It
is
impor-
tant
to
note
that
offers
are
rejected
mostly
when
considered
to
be
unfair.
One
study
found
that
females
accept
offers
more
frequently,
and
also
that
females’
offers
are
accepted
more
often,
although
there
were
no
sex
differences
in
the
amount
offered
(Eckel
and
Grossman,
2001).
In
contrast,
another
study
reported
the
opposite:
that
female
offers
are
rejected
more
often
by
both
sexes,
with
the
lowest
acceptance
frequency
in
female-female
pairings,
suggest-
ing
that
females’
expectations
for
a
fair
behavior
is
higher
when
facing
another
female
(Solnick,
2001).
This
may
explain
why
coop-
eration
rates
among
females
are
lower
than
among
males
or
among
mixed-sex
pairings
(Balliet
et
al.,
2011);
it
could
be
that
females
have
higher
expectations
of
other
females
and/or
are
more
likely
to
try
to
take
advantage
of
other
females,
compared
to
interactions
with
male
partners.
Additionally,
participants
had
to
identify
the
minimum
offer
they
would
still
accept
which
revealed
that
the
responders
of
both
genders
set
their
minimum
acceptable
offers
higher
when
paired
with
female
proposer.
The
inconsistency
of
the
results
in
these
two
studies
is
likely
due
to
different
experimen-
tal
conditions.
In
Eckel
and
Grossman
(2001)
the
participants
had
face-to-face
interactions
while
in
Solnick
(2001)
they
did
not
see
each
other,
and
greater
strategic
thinking
might
have
been
invoked
when
participants
were
asked
to
indicate
their
minimum
accept-
able
offer.
In
a
three-party
Ultimatum
Game,
where
a
proposer
had
to
divide
the
money
between
him/herself,
a
responder
and
a
non-
responding
third
player,
females
are
more
likely
to
offer
an
equal
three-way
split
then
males
(Guth
et
al.,
2007).
This
suggests
that
female
behavior
in
economic
games
might
in
fact
be
altruistic
rather
than
strategic.
These
findings
indicate
a
higher
level
of
altruistic
behavior
in
females
(Croson
and
Gneezy,
2009).
In
the
Dictator
Game
–
a
similar
game
to
the
Ultimatum
Game
except
the
recipient
must
always
accept
the
offer
–
females
give
twice
as
much
as
males
when
the
gender
of
receiver
is
anonymous,
compared
to
when
the
gender
is
known
(Eckel
and
Grossman,
1998).
In
another
study,
female
participants,
compared
to
male
par-
ticipants,
gave
less
to
females,
while
female
participants’
sharing
with
males
or
with
individual
of
unknown
gender
did
not
differ,
and
male
participants’
behavior
was
not
influenced
by
the
target’s
gen-
der
(Ben-Ner
et
al.,
2004).
In
a
two-sided
dictator
game,
a
proposer
divides
the
given
sum
of
money
between
him/herself
and
a
respon-
der.
The
responder
gets
triple
the
amount
of
what
the
proposer
offers
and
then
has
to
divide
that
sum
between
him/herself
and
the
proposer.
Using
this
design
with
the
players’
genders
unknown,
females
responders
tended
to
return
more
money
(i.e.,
act
more
prosocially)
than
males
(Croson
and
Buchan,
1999).
The
self-report
questionnaires
filled
in
by
the
participants
after
the
game
indi-
cated
that
females
felt
more
obliged
to
return
at
least
the
same
amount
as
they
were
given.
This
suggests
that
females’
decisions
in
this
particular
experimental
setting
might
be
driven
by
reciprocity
rather
than
altruistic
behavior.
Indeed,
there
were
no
significant
gender
differences
in
the
amounts
offered
by
the
proposers.
These
results
are
inconsistent
with
those
of
Eckel
and
Grossman
(1998)
because
they
do
not
show
greater
altruistic
behavior
in
females.
In
fact,
experiments
investigating
how
specific
situational
factors
influence
altruistic
behavior
showed
that
females
appear
more
gen-
erous
when
the
motivation
for
reciprocity
is
eliminated,
e.g.,
during
the
dictator
game
where
there
is
no
interaction
between
the
pro-
poser
and
the
responder.
Furthermore,
the
social
distance
of
the
participant
to
the
recipient,
where
knowing
the
name
of
the
respon-
der
indicated
low
social
distances,
and
not
knowing
indicated
high
social
distances,
could
predict
the
level
of
generosity
in
females.
This
suggests
that
inconsistent
findings
across
studies
may
be
due
to
complex
modulatory
factors
as
well
as
due
to
greater
female
sensitivity
to
different
experimental
conditions
(Cox
and
Deck,
2006).
Furthermore,
Andreoni
and
Vesterlund
(2001)
performed
a
dictator
game
study
in
which
participants
had
to
allocate
eight
different
budgets
of
money
consisting
of
tokens
of
different
values.
Each
budget
had
different
relative
prices
of
self-payoff
and
other-
payoff
meaning
that,
for
some
budgets,
keeping
value
was
higher
than
giving
value
and
vice
versa.
The
study
revealed
that
females
gave
more
than
males
when
giving
was
expensive,
which
caused
more
fair
sharing.
Males
gave
more
than
females
when
giving
was
cheaper,
ensuring
higher
payoff
for
themselves.
These
results
sug-
gest
that
males’
sharing
behavior
is
more
sensitive
to
contextual
factors
than
females’
sharing
behavior.
In
a
nutshell,
the
presented
collection
of
economic
behavior
studies
suggests
that
females
are
more
inequality-averse
while
males
base
their
decisions
on
effi-
ciency.
However,
taken
together,
findings
from
the
economic
literature
seem
to
indicate
a
higher
level
of
altruistic
behavior
in
females
(Croson
and
Gneezy,
2009).
3.3.2.
Naturalistic
data:
Volunteering,
donating,
and
other
altruistic
behavior
One
may
argue
that
the
results
yielded
by
economic
game
stud-
ies
do
not
necessarily
apply
to
real
life
situations.
In
other
words,
they
may
have
little
ecological
validity.
However
there
are
reports
of
charitable
giving
and
hours
of
volunteering
between
males
and
females
that
do
support
the
experimental
findings.
Empathic
con-
cern
and
helping
behavior
is
positively
correlated
with
generosity
for
both
genders
(Mesch
et
al.,
2011).
Females
tend
to
score
higher
as
well
as
donate
more
and
more
often
(Mesch
et
al.,
2011).
Further-
more,
females
tend
to
volunteer
more
often
and
more
hours
than

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613
males
(Mesch
et
al.,
2006).
In
experimental
studies,
females
are
usually
more
likely
to
help
than
males
(Eckel
and
Grossman,
2008).
Females
exhibit
more
caring
prosocial
moral
judgment
(Jaffee
and
Hyde,
2000)
and
exhibit
more
sophisticated
forms
of
prosocial
moral
reasoning
(Eisenberg
et
al.,
2014).
Females
give
more
of
their
time
and
money
to
charities
(for
a
review,
see
Einolf,
2011).
Further-
more,
in
a
study
by
Aguiar
et
al.
(2009)
participants
were
instructed
to
choose
between
male
and
female
boxes
containing
slips
of
paper
describing
their
intake
from
the
dictator
game
(participants’
pay-
offs
depended
on
the
amount
written
on
the
slips).
63%
of
the
participants
chose
the
female
box
and
79%
of
female
participants
chose
the
female
box.
This
suggests
that
female
participants
are
also
expected
to
be
more
altruistic.
However,
in
terms
of
amount
donated
per
person,
males
give
higher
amounts
than
females
(Piper
and
Schnepf,
2008);
although,
this
may
be
due
to
higher
incomes,
on
average,
for
males,
or
due
to
the
fact
that
males
are
more
likely
to
display
their
resources
as
a
mating
signal
(e.g.,
Iredale
et
al.,
2008).
While
males
help
more
often
in
certain
contexts,
females
help
more
in
other
contexts.
For
example,
females
are
more
likely
to
help
in
low-risk–low-physical-strength
(LRLS)
situations,
such
as
to
look
after
neighbor’s
pet
or
give
clothes
to
charity
(Erdle
et
al.,
1992).
Males,
on
the
other
hand,
tended
to
help
more
in
high-risk–high-physical-strength
(HRHS)
situations
(e.g.
helping
to
push
a
car,
giving
a
stranger
a
lift
in
a
car).
Both
helping
dimensions
were
positively
correlated
with
outgoing
personality
characteristics
and
conventionality
(value
for
responsibility
and
organization)
in
males.
In
contrast,
HRHS
was
negatively
corre-
lated
with
conventionality,
and
LRLS
was
positively
associated
with
open-mindedness
in
females.
These
results
are
consistent
with
both
social
roles
(nurturing
and
caring
by
females
vs.
heroic
defend-
ing
and
chivalry
by
males)
as
well
as
biological
perspectives
(greater
physical
strength
and
size
of
males).
Social
distance
was
also
shown
to
have
an
effect
on
the
tendency
to
help.
A
study
using
self-report
questionnaires
found
that
the
likelihood
of
helping
could
be
pre-
dicted
by
social
closeness
only
in
females,
with
females,
but
not
males,
being
more
likely
to
help
a
friend
then
a
stranger
(George
et
al.,
1998).
Moreover,
male
helping
in
general
was
more
action-
oriented
(e.g.,
helping
change
a
tire)
while
females
seemed
to
be
more
likely
to
help
with
emotional
concepts
and
provide
sympathy.
Although
it
seems
females
are
more
altruistic,
there
are
also
sex
differences
in
females’
and
males’
reasoning/justification
for
helping
(or
not
helping).
While
males
and
females
tend
to
be
prosocial
when
given
hypothetical
situations,
their
reasoning
dif-
fered:
Females’
decisions
seemed
more
empathy-related
and
they
appeared
happier
about
their
decision
compared
to
men,
as
indi-
cated
by
self-report
questionnaires
(Mills
et
al.,
1989).
In
addition,
males’
decisions
on
giving
were
more
influenced
by
descriptive
norms
(beliefs
of
what
most
people
do),
which
also
indicated
that
men
were
more
concentrated
on
self-presentation
rather
than
exhibiting
truly
altruistic
behavior
(Croson
et
al.,
2010).
In
summary,
studies
of
experimental
economic
games
and
the
analysis
of
naturalistic
data
of
charitable
and
volunteering
behavior
show
that
the
majority
of
the
data
does
reflect
higher
altruism
in
females.
4.
Sex
differences
in
the
development
of
empathy
in
humans
4.1.
Precursors
to
empathy
in
infancy:
Emotion
contagion,
mimicry,
and
social
interest
Rudimentary
forms
of
empathy
may
exist
in
infants
–
perhaps
facilitated
by
the
matching
and
synchronization
of
emotional
facial
expression
–
behaviors
that
appear
to
promote
emotional
closeness
of
mothers
and
infants
(e.g.,
Murray
et
al.,
1996).
The
degree
of
emotional
synchrony
can
be
determined
by
monitoring
mother–infant
physiology
(e.g.,
heart
rate:
Feldman
et
al.,
2011),
or
behavior
(de
Waal,
1989;
Sagi
and
Hoffman,
1976).
For
instance,
contagious
crying
is
a
phenomenon
in
which
human
infants
cry
when
they
hear
others
cry
(Martin
and
Clark,
1982;
Sagi
and
Hoffman,
1976;
Simner,
1971;
Ungerer,
1990;
Zahn-Waxler
and
Radke-Yarrow,
1982),
but
not
when
they
hear
other
control
sounds
(Dondi
et
al.,
1999;
Martin
and
Clark,
1982;
Sagi
and
Hoffman,
1976;
Simner,
1971).
Thus,
infants’
reactive
crying
is
more
than
simply
an
arousal
response
to
an
aversive
noise,
but
rather
appears
a
specific
response
to
emotional
social
stimuli,
possibly
reflecting
emotional
contagion.
Although
we
know
of
no
studies
that
have
examined
sex
dif-
ferences
in
newborns’
physiology
in
response
to
emotional
social
stimuli,
a
number
of
studies
have
examined
sex
differences
in
new-
borns’
behavioral
reactions.
For
example,
from
birth,
there
appear
to
be
sex
differences
in
social
behaviors
(for
a
review,
see
Alexander
and
Wilcox,
2012),
including
potential
precursors
of
empathic
predisposition
(McClure,
2000).
Female
neonates,
compared
to
males,
are
more
likely
to
cry
and
cry
longer
when
hearing
another
infant
cry
(Hoffman,
1977;
Sagi
and
Hoffman,
1976;
Simner,
1971).
Female
neonates,
compared
to
males,
also
make
more
eye
contact
(Hittelman
and
Dickes,
1979)
and
are
more
likely
to
orient
to
faces
(Connellan
et
al.,
2000)
and
voices
(Osofsky
and
O’Connell,
1977).
This
general
social
interest
and
responsiveness
may
reflect
pre-
cursors
or
foundations
of
empathy
because
they
provide
infants
with
opportunities
to
learn
about
the
behavior
of
other
individ-
uals.
Infants
who
are
less
socially
interested
and/or
attentive
will
not
learn
as
much
about
other
people.
Some
have
proposed
reduced
social
tuning
may
be
a
potential
factor
contributing
to
autism
(i.e.,
Chevallier
et
al.,
2012),
a
disorder
characterized
by
impairments
in
social
competence
and
empathy
(Baron-Cohen
et
al.,
2005).
Specif-
ically,
typically
developing
infants
–
and
female
infants
especially
–
prefer
social
stimuli,
which
preferentially
capture
their
attention,
and
find
social
stimuli
particularly
rewarding,
creating
opportuni-
ties
for
social
learning
and
to
strengthen
social
bonds.
Children
that
will
eventually
develop
autism,
in
contrast,
spontaneously
attend
less
to
social
stimuli,
thereby
limiting
their
exposure
to
critical
opportunities
for
social
learning
(Chawarska
et
al.,
2013).
Thus,
early
differences
in
social
motivation
or
social
interest
may
account
for
some
individual
differences
in
social
functioning
later
in
life.
Human
infants’
sensitivity
to
facial
expressions
is
important
early
in
life,
as
it
aids
them
in
learning
about
their
environment.
For
example,
if
an
adult
produces
a
fearful
expression
in
response
to
a
novel
object,
infants
will
modulate
their
response
accord-
ingly.
As
Darwin
(1872)
noted,
“The
movements
of
expression
in
the
face
and
body,
whatever
their
origin
may
have
been,
are
in
themselves
of
much
importance
for
our
welfare.
They
serve
as
the
first
means
of
communication
between
the
mother
and
her
infant;
she
smiles
approval,
and
thus
encourages
her
child
on
the
right
path,
or
frowns
disapproval”
(pp.
365–366).
He
also
aptly
observed
“Every
one
must
have
noticed
how
readily
children
burst
out
crying
if
we
pity
them
for
some
small
hurt.”
(p.
218).
Thus,
children
can
use
others’
emotional
reactions
to
assess
their
own
situation
and
appropriate
emotional
reaction.
Newborns
also
imitate
these
facial
expressions,
including
expressions
of
fear,
sadness,
and
surprise,
a
phenomenon
known
as
neonatal
imitation
(Field
et
al.,
1982).
Only
one
study
to
date
has
specifically
examined
sex
differences
in
neonatal
imitation,
and
found
that
female
neonates,
compared
to
males,
were
more
skilled
at
imitating
finger
movements
(Nagy
et
al.,
2007).
More
studies
of
sex
differences
in
infants
seem
necessary,
given
that
the
ability
to
spontaneously
mimic
facial
expressions
may
be
a
skill
underlying
several
social
behaviors
and
competences,
including
empathy
(e.g.,
Oberman
et
al.,
2007;
Sonnby-Borgström,
2002).
Motor
mimicry
is
one
way
through
which
children
can
learn
about
the
experiences

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of
others
(McDonald
and
Messinger,
2011).
Interestingly,
typically
developing
children
automatically
mimic
facial
expressions,
while
children
with
autism
do
not
appear
to
do
so
(Oberman
et
al.,
2009).
Disorders
characterized
by
impaired
empathy,
including
autism,
are
more
common
in
males
than
females
(Blair,
1995;
Charman
et
al.,
1997;
Dodge,
1980;
Baron-Cohen,
2002),
and
males
also
appear
to
be
more
susceptible
to
impairments
in
empathy.
For
example,
one
way
in
which
male
infants
appear
more
susceptible
to
impairments
in
empathy
is
through
their
pacifier
use.
Specifically,
infants’
pacifier
use
–
which
decreases
facial
mimicry
–
predicts,
and
is
negatively
associated
with,
later
perspective
taking
and
emo-
tional
intelligence
in
males,
but
not
in
females
(Niedenthal
et
al.,
2012).
In
other
words,
males
may
be
more
negatively
impacted
by
interference
with
their
facial
mimicry
early
in
development,
which
impacts
their
later
emotion
understanding
(Niedenthal
et
al.,
2012).
With
increasing
age,
infants
demonstrate
increased
under-
standing
of
others’
facial
expressions.
At
3
to
4
months,
females
may
discriminate
and
understand
expressions
better
than
males
(McClure,
2000)
as
suggested
by
the
fact
that
they
exhibit
more
distress
than
males
in
response
to
a
maternal
still-face,
a
paradigm
in
which,
after
a
face-to-face
social
interaction
with
the
mother,
the
mother
assumes
a
neutral
face
and
is
unresponsive
to
the
infant
(e.g.,
Mayes
and
Carter,
1990).
Such
differential
facial
pro-
cessing
may
be
due
to
differences
in
visual
attention
to
faces
at
this
age,
with
females
focusing
more
on
internal
facial
features
(e.g.,
eyes,
mouth),
compared
to
males,
who
shift
their
gaze
more
between
internal
and
external
features
(outer
contours)
(Rennels
and
Cummings,
2013).
These
sex
differences
in
social
attention
continue
later
during
development.
Around
12
months
of
age,
female
infants,
but
not
male,
prefer
to
view
the
biological
motion
of
facial
expressions
to
non-biological
motion
(Lutchmaya
and
Baron-
Cohen,
2002),
and
when
confronted
with
novel
situations,
females,
but
not
males,
are
influenced
by
maternal
facial
and
vocal
signals
of
happiness
or
fear
(Rosen
et
al.,
1992).
Interestingly,
when
moth-
ers
were
instructed
to
direct
fearful
expressions
at
their
infants,
mothers’
expressions
were
less
intense
when
directed
at
female
infants
compared
to
male
infants,
perhaps
reflecting
the
mothers’
awareness
of
their
infants’
sensitivity
to
such
expressions
(Rosen
et
al.,
1992).
These
findings
are
consistent
with
other
reports
that
by
the
end
of
the
first
year
of
life,
female
infants,
compared
to
males,
are
more
responsive
to
their
mother’s
voice,
initiate
more
mater-
nal
social
interactions,
and
spend
more
time
in
close
proximity
to
their
mothers
(Gunnar
and
Donahue,
1980;
Wasserman
and
Lewis,
1985).
4.2.
Toddlers
and
older
children:
Prosocial
behavior
and
cognitive
empathy
Rather
than
simply
becoming
personally
distressed
upon
seeing
another
individual
in
distress,
older
children
may
better
recog-
nize
and
understand
distress
in
others,
although
personal
distress
may
be
a
precursor
to
recognizing
and
understanding
distress
in
others
(Batson
and
Shaw,
1991;
Hoffman,
1975).
One
way
of
measuring
this
distinction
is
through
assessing
prosocial
behav-
ior.
While
1
to
1.5-year-olds
often
respond
to
distressed
others
by
exhibiting
distress
themselves,
by
2
years
of
age,
nearly
all
children
demonstrate
helping
behaviors
when
others
appear
in
distress
(Radke-Yarrow
and
Zahn-Waxler,
1984;
Zahn-Waxler
and
Radke-Yarrow,
1982)
and
sometimes
imitate
distressed
behaviors
of
others
(Zahn-Waxler
et
al.,
1977),
perhaps
to
try
to
under-
stand
such
expressions
(Thompson,
1987).
By
1
to
2
years
of
age,
female
children
in
these
situations
show
greater
concern
(e.g.,
sad-
ness,
sympathetic
vocalizations,
comforting)
than
male
children
(Hoffman,
1977;
Volbrecht
et
al.,
2007;
Zahn-Waxler
et
al.,
1992a).
Similarly,
a
twin
study
of
infants
aged
14
to
20
months
reported
that
females,
compared
to
males,
had
higher
empathy
scores
in
their
empathetic
reactions
to
others’
distress,
and
that
empathy
was
moderately
heritable
(Zahn-Waxler
et
al.,
1992b),
consistent
with
another
twin
study
in
14
to
36-month-olds
(Knafo
et
al.,
2008).
This
work
is
generally
consistent
with
the
notion
that
at
least
some
aspects
of
empathy
–
including
empathetic
concern
and
personal
distress
–
are
moderately
heritable
(e.g.,
Chakrabarti
and
Baron-
Cohen,
2013;
Davis
et
al.,
1994;
Volbrecht
et
al.,
2007),
and
in
fact,
it
is
estimated
that
approximately
half
of
all
variability
in
self-
reported
altruism
may
be
due
to
genes
(Rushton,
2004).
In
addition,
it
appears
that
the
heritability
of
empathy
may
differ
for
males
and
females
(e.g.,
Ragsdale
and
Foley,
2012;
Lewis
and
Bates,
2011).
As
children
get
older,
their
empathic
predisposition
acquires
more
cognitive
layers,
including
what
is
often
called
perspective
taking.
In
a
study,
4-
to
5-year-old
children
were
shown
videos
to
elicit
personal
distress,
including
videos
of
children
frightened
by
a
thunderstorm,
saddened
by
the
loss
of
a
pet,
or
struggling
to
walk
due
to
deformities
(Eisenberg
et
al.,
1988).
Though
there
were
no
sex
differences
in
heart
rate,
children
did
vary
in
their
self-reported
emotions
(i.e.,
verbal
reports
and
pointing
to
facial
expressions),
with
females
reporting
more
vicarious
emotions.
In
another
study,
when
4-year-olds
were
shown
photos
of
children
in
various
emotion-evoking
situations
and
were
asked
how
they
felt,
females
reported
more
empathetic
emotions
than
males
(Hoffman
and
Levine,
1976).
A
study
of
5-
to
13-year-old
children’s
reac-
tions
to
an
infant
crying
found
that
females
were
better
than
males
at
both
guessing
causes
of
the
infant’s
distress
(indicating
better
perspective-taking)
and
thinking
of
ways
to
comfort
the
infant
(Catherine
and
Schonert-Reichl,
2011).
By
2
to
6
years
of
age,
females
outperform
males
in
false
belief
tasks
(Charman
et
al.,
2002),
a
classical
test
of
ToM.
A
study
of
preschool
children’s
theory-
of-mind
understanding
and
social
competence
reported
that,
after
controlling
for
age,
theory-of-mind
understanding
significantly
predicted
aggressive
or
disruptive
behavior
for
boys
and
prosocial
behavior
for
girls
(Walker,
2005).
Theory-of-mind
understanding
also
was
related
to
lower
scores
of
shyness
or
withdrawn
behavior
for
boys.
This
may
suggest
that
ToM
is
devoted
toward
differing
goals
in
males
and
females,
with
males
tending
to
seek
dominance
and
females
tending
to
seek
conciliation
(Walker,
2005).
In
self-reports
of
empathy,
females
report
higher
levels
than
males
from
about
5
to
9
years
of
age
(Chapman
et
al.,
2006;
Hughes
et
al.,
2005).
In
this
line
of
studies,
experimenters
often
show
pho-
tos
or
videos
of
individuals
in
varying
emotional
states
and
ask
children
to
describe
their
own
emotional
response
to
the
picture
(e.g.,
Feshbach
and
Feshbach,
1969;
Feshbach
and
Roe,
1968;
Levine
and
Hoffman,
1975),
to
pick
a
corresponding
emotion
that
matches
a
film
(Hamilton,
1973),
or
to
match
a
facial
expression
to
an
emo-
tional
picture,
during
which
time
children’s
expressions
are
rated
(Buck,
1975).
In
one
of
these
studies,
second
and
fifth
graders
watched
a
video
about
individuals
who
had
been
in
car
accidents
and
were
now
in
the
hospital
with
injuries.
The
study
shows
that
females
exhibited
more
sad
expressions
and
reported
more
sym-
pathy
and
distress
than
males
(Eisenberg
et
al.,
1991),
consistent
with
other
studies
in
older
children
that
found
greater
empathy
in
females
than
males
(Feshbach
and
Feshbach,
1969;
Feshbach
and
Roe,
1968;
Levine
and
Hoffman,
1975).
It
must
be
noted
that
both
male
and
female
children
appear
more
empathetic
toward
same-
sex
individuals
(i.e.,
males
more
empathetic
to
males,
and
females
more
empathetic
to
females;
Feshbach
and
Roe,
1968).
In
10-
to
13-year-old
children,
females
appear
to
be
better
than
males
at
understanding
feelings
and
intentions
of
story
characters
(Bosacki
and
Wilde
Astington,
1999),
a
finding
that
is
consistent
with
sim-
ilar
findings
in
late
adolescence
(age
9
to
17
years;
Hatcher
et
al.,
1990).
Female
children,
age
7
to
11
years,
are
also
more
likely
than
male
children
to
recognize
faux
pas,
such
as
when
a
speaker
says
something
without
a
consideration
of
the
listener
(e.g.,
socially
awkward
or
tactless),
resulting
in
negative
social
consequences

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et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
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615
(Baron-Cohen
et
al.,
1999).
Compared
to
males,
females,
age
3
to
12
years,
are
more
concerned
about
sharing,
turn
taking,
and
coop-
erating
(Charlesworth
and
Dzur,
1987;
Knight
et
al.,
1989).
By
late
childhood,
females
are
better
at
identifying
nonverbal
emotional
cues
(Blanck
et
al.,
1981;
Hall,
1978).
Male
children
may
have
more
control
over
their
empathy
or
may
not
empathize
as
automatically
as
female
children.
For
exam-
ple,
in
6-
to
7-year-old
children,
male
children
show
higher
rates
of
donations
to
those
in
need
when
instructed
to
be
empathetic
(i.e.,
imagine
themselves
in
the
other
person’s
situation),
while
females
are
equally
empathetic
whether
instructed
to
do
so
or
not
(Brehm
et
al.,
1984).
Such
effects
may
be
similar
to
findings
in
adults
that
males,
but
not
females,
are
less
empathetic
toward
social
partners
who
are
perceived
as
behaving
unfairly
(Singer
et
al.,
2006).
In
this
way,
males
may
be
more
sensitive
to
contextual
influences
on
their
empathy
and
their
empathy
may
be
more
dependent
on
their
motivational
state
(Ickes
et
al.,
2000).
As
mentioned
previously,
facial
mimicry
seems
associated
with
empathic
predisposition
(e.g.,
Oberman
et
al.,
2007;
Sonnby-
Borgström,
2002).
In
6
to
7
year-old
children,
individuals
with
autism
who
score
lower
on
social
responsiveness
also
are
less
likely
to
mimic
fearful
expressions,
as
measured
by
facial
electromyog-
raphy
(Deschamps
et
al.,
2013).
Contagious
yawning
may
also
be
associated
with
empathy
(Preston
and
De
Waal,
2002).
This
behav-
ior
does
not
appear
until
around
5
years
of
age
(Anderson
and
Meno,
2003).
While
there
are
no
studies
that
specifically
exam-
ined
whether
there
were
sex
differences
in
contagious
yawning
throughout
childhood,
when
contagious
yawning
was
compared
between
7
to
15
year
old
children,
with
and
without
autism,
only
typically
developing
children
displayed
the
behavior
(Senju
et
al.,
2007).
When
children
with
autism
were
instructed
to
focus
their
attention
on
the
eyes,
however,
they
were
just
as
likely
to
contagiously
yawn
as
typically
developing
children
(Senju
et
al.,
2009),
consistent
with
the
proposal
that
atypical
social
orient-
ing
may
negatively
impact
empathy
in
autism
(Chevallier
et
al.,
2012).
4.3.
Empathy
in
adolescence
Females
are
more
prosocial,
sympathetic,
and
empathetic
than
males,
from
childhood
through
adolescence
(for
reviews,
see
Chaplin
and
Aldao,
2013;
Rose
and
Rudolph,
2006).
The
transi-
tion
into
adolescence
appears
to
widen
the
differences
in
empathy
between
males
and
females
(e.g.,
Lam
et
al.,
2012).
In
one
study,
high
school
students
completed
four
empathy
questionnaires,
and
while
overall
there
were
improvements
in
empathy
with
age,
females
scored
higher
than
males
on
all
measures
(Davis
and
Franzoi,
1991),
a
finding
that
is
consistent
with
previous
studies
of
empathy
in
adolescents
(e.g.,
Adams
et
al.,
1979;
Auyeung
et
al.,
2012;
Davis,
1980;
Feshbach,
1982;
Hawk
et
al.,
2013;
Mehrabian
and
Epstein,
1972;
Mestre
et
al.,
2009).
Adolescent
females
scored
significantly
higher
in
empathy
and
appeared
to
help
victims
being
bullied
more
in
comparison
to
males
(Jolliffe
and
Farrington,
2006).
Female
adolescents
also
outperform
males
on
tests
of
ToM
(Ibanez
et
al.,
2013).
Interestingly,
in
adolescence,
it
appears
that
the
sex
of
the
individual
in
the
stimulus
modulates
empathy
in
males
but
not
females
(Bryant,
1982;
Olweus
and
Endresen,
1998).
Specifically,
in
students
aged
13
to
16
years,
females
showed
developmental
increases
in
empathy
toward
both
males
and
females,
while
males
showed,
with
age,
increases
in
empathy
to
females,
but
decreases
in
empathy
to
males
(Olweus
and
Endresen,
1998).
Similarly,
another
study
found
that
in
7th
graders,
but
not
in
1st
or
4th
graders,
males
exhibited
greater
empathy
for
females
than
for
males,
but
females
exhibited
equal
levels
of
empathy
for
both
sexes
(Bryant,
1982).
These
differences
in
empathy
as
a
function
of
target
sex
have
been
interpreted
in
terms
of
different
evolutionary
selective
pressures
on
males
and
females,
especially
with
regard
to
issues
associated
with
mating
(Olweus
and
Endresen,
1998).
4.4.
Summary
and
conclusions
regarding
sex
differences
in
empathy
across
development
Together,
this
work
suggests
that
there
may
be
sex
differences
in
emotional
attunement
and
empathy
beginning
early
in
onto-
genetic
development.
From
this
body
of
developmental
work,
it
is
clear
that
there
are
sex
differences
in
empathy
from
birth,
and
sex
differences
appear
to
be
consistent
and
stable
across
the
lifes-
pan
(e.g.,
Michalska
et
al.,
2013;
O’Brien
et
al.,
2013),
with
females
demonstrating
higher
levels
of
empathy
than
males,
and
chil-
dren
who
are
higher
in
empathy
early
in
development
continue
to
be
higher
in
empathy
later
in
development
(Eisenberg
et
al.,
1999).
This
developmental
stability
suggests
that
sex
differences
are
unlikely
to
be
caused
exclusively
by
postnatal
experiences
(e.g.,
maternal
care),
but
rather
reflect
some
evolutionarily
impor-
tant
difference
between
males
and
females
that
is
present,
at
least
in
some
form,
from
birth,
consistent
with
reports
that
empa-
thy
is
moderately
heritable
(e.g.,
Baron-Cohen,
2002;
Chakrabarti
and
Baron-Cohen,
2013;
Knafo
et
al.,
2008;
Rushton,
2004;
Zahn-
Waxler
et
al.,
1992a,b;
Zahn-Waxler
et
al.,
2001).
Darwin
was
likewise
interested
in
the
extent
to
which
sympathetic
reactions
were
learned
or
present
prior
to
experiences.
He
reported
anecdo-
tally
about
his
son:
I
attended
to
this
point
in
my
first-born
infant,
who
could
not
have
learnt
anything
by
associating
with
other
children,
and
I
was
convinced
that
he
understood
a
smile
and
received
pleasure
from
seeing
one,
answering
it
by
another,
at
much
too
early
an
age
to
have
learnt
anything
by
experience.
When
this
child
was
about
four
months
old,
I
made
in
his
presence
many
odd
noises
and
strange
grimaces,
and
tried
to
look
savage;
but
the
noises,
if
not
too
loud,
as
well
as
the
grimaces,
were
all
taken
as
good
jokes;
and
I
attributed
this
at
the
time
to
their
being
preceded
or
accompanied
by
smiles.
When
five
months
old,
he
seemed
to
understand
a
compassionate
expression
and
tone
of
voice.
When
a
few
days
over
six
months
old,
his
nurse
pretended
to
cry,
and
I
saw
that
his
face
instantly
assumed
a
melancholy
expression,
with
the
corners
of
the
mouth
strongly
depressed;
now
this
child
could
rarely
have
seen
any
other
child
crying,
and
never
a
grown-up
person
crying,
and
I
should
doubt
whether
at
so
early
an
age
he
could
have
reasoned
on
the
subject.
Therefore
it
seems
to
me
that
an
innate
feeling
must
have
told
him
that
the
pretended
crying
of
his
nurse
expressed
grief;
and
this
through
the
instinct
of
sympathy
excited
grief
in
him.
(Darwin,
1872;
pp.
359–360).
Sex
differences
appear
to
grow
larger
with
age,
especially
around
puberty,
perhaps
driven
by
greater
age-related
improve-
ments
in
empathy
in
females
relative
to
males
(e.g.,
Eisenberg
et
al.,
1989;
Michalska
et
al.,
2013;
Van
Tilburg
et
al.,
2002).
However,
the
use
of
different
(age-appropriate)
measures
at
different
ages
may
account
for
some
of
these
apparent
age-related
changes
in
the
degree
of
sex
differences.
In
other
words,
measures
used
at
later
ages
in
development
(e.g.,
adolescence)
may
be
more
sen-
sitive
for
detecting
sex
differences
than
measures
used
earlier
in
development
(e.g.,
infancy).
A
number
of
studies
emphasize
the
role
of
social
influences
on
empathy,
proposing
that
parents
can
support
empathy
in
their
chil-
dren,
either
as
role
models
or
through
fostering
healthy,
secure
attachments
(e.g.,
Barnett
et
al.,
1980;
Eisenberg
and
Valiente,
2002;
Knafo
and
Plomin,
2006;
Koestner
et
al.,
1990;
Mehrabian
et
al.,
1988;
Miklikowska
et
al.,
2011;
Strayer
and
Roberts,
2004).
However,
these
differences
could
also
be
due
to
genetic
predispo-
sitions
shared
between
parents
and
children,
as
some
data
suggest

616
L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
that
empathy
may
be
heritable,
as
already
mentioned.
It
is
also
possible,
however,
that
social
motivation
–
which
appears
to
differ
between
the
sexes
–
may
be
a
driving
force
behind
developmen-
tal
sex
differences
in
social
skills,
such
as
empathy
(e.g.,
Chevallier
et
al.,
2012).
Early
differences
in
social
attention
between
male
and
female
infants
seem
to
occur
prior
to
socialization,
appearing
even
in
newborns
(Alexander
and
Wilcox,
2012)
and
thus
proba-
bly
contributing
to
females’
greater
sensitivity
to
others’
emotions,
compared
to
males.
Finally,
though
it
has
been
explored
little,
it
appears
that
the
type
of
stimulus
(e.g.,
sex
of
stimulus)
has
an
important
impact
on
male
but
not
female
empathy
(Bryant,
1982;
Olweus
and
Endresen,
1998).
Although
speculative,
it
is
possible
that
this
differential
responding
as
a
function
of
target
sex
may
account
for
some
of
the
sex
differences
reported
across
development.
Specifically,
it
may
be
the
case
that
males
are
not
necessarily
less
empathetic
than
females,
but
that
they
direct
varying
levels
of
empathy
at
different
types
of
social
partners,
with
female
targets
eliciting
equal
levels
of
empathy
from
male
and
female
viewers
and
male
targets
eliciting
greater
empathy
in
female
viewers
compared
to
male
viewers.
Of
course,
this
would
still
render
males,
on
average,
less
empathetic
than
females.
In
addition,
males
have
more
deliberate
control
over
their
production
of
expressions,
and
this
control
increases
with
age
(e.g.,
Eisenberg
et
al.,
1989),
so
many
of
these
measures
that
rely
on
overt
signals
of
empathy
may
find
lower
levels
in
males
than
females.
Given
that
males
have
more
control
over
their
emotional
expressions,
they
may
likewise
have
more
control
over
their
empathy
(Brehm
et
al.,
1984).
Though
this
hypothesis
has
not
been
directly
tested
in
healthy
populations
–
to
our
knowledge
–
it
is
consistent
with
data
demonstrating
associations
between
various
disorders
and
empathetic
control.
For
example,
studies
report
a
positive
asso-
ciation
between
control
of
empathy
and
depression
(Thoma
et
al.,
2011),
a
disorder
significantly
more
common
in
females
than
males
(Weissman
et
al.,
1996),
while
psychopathy
and
autism
–
disorders
both
associated
with
less
spontaneous
empathy
(Gillespie
et
al.,
2014;
Senju
et
al.,
2009)
–
are
more
common
in
males
than
females
(Baron-Cohen
et
al.,
2005;
Cale
and
Lilienfeld,
2002).
In
fact,
in
both
psychopathy
and
autism,
though
individuals
may
exhibit
less
auto-
matic
empathy,
when
explicitly
instructed
to
be
empathetic
(i.e.,
under
effortful
control),
they
are
capable
of
exhibiting
significantly
higher
levels
of
empathy
(Gillespie
et
al.,
2014;
Meffert
et
al.,
2013;
Senju
et
al.,
2009;
related,
spontaneous
vs.
deliberate
mimicry
in
autism:
McIntosh
et
al.,
2006;
Oberman
et
al.,
2009).
Together,
these
studies
suggest
that
sex
differences
in
empathetic
control
may
play
a
role
in
various
disorders
associated
with
abnormally
high
or
low
levels
of
empathy,
and
that
the
distinction
between
empathy
abil-
ity
and
propensity
is
particularly
relevant
for
examining
individual
differences
(Keysers
and
Gazzola,
2014;
Keysers
et
al.,
2014).
Nonetheless,
a
developmental
perspective
can
provide
insights
about
the
proximate
and
ultimate
causes
of
individual
differences
in
empathy.
Based
on
the
evidence
summarized
here,
it
is
diffi-
cult
to
deny
that
there
are
differences
in
empathy
between
males
and
females.
The
evolutionary
and
proximate
causes
of
these
dif-
ferences,
however,
remain
largely
unexamined,
and
are,
we
think,
an
important
future
direction
for
this
work.
5.
Neuronal
mechanisms
for
empathy
5.1.
Mirror
neurons
In
emphasizing
that
empathy
is
a
multilayered
phenomenon,
several
scholars
converge
in
considering
an
action–perception
mechanism
as
central
for
automatically
reproducing
others’
affec-
tive
states
(Preston
and
De
Waal,
2002;
Iacoboni,
2009).
Much
theoretical
discussion
has
been
stimulated
by
the
discovery
of
mirror
neurons
in
the
ventral
premotor
cortex
and
the
inferior
parietal
lobule
of
the
monkey
(Di
Pellegrino
et
al.,
1992;
Gallese
et
al.,
1996;
Rizzolatti
et
al.,
1996).
These
neurons
have
the
peculiar
feature
of
firing
both
when
a
specific
action
is
observed
and
when
another
individual
performs
the
same
action.
In
the
original
work,
and
in
most
studies
that
have
followed,
monkeys
were
trained
to
perform
or
observe
a
goal-directed
hand
action.
The
most
impor-
tant
property
of
mirror
neurons
is
the
congruence
they
show
in
their
responsivity
between
the
effective
observed
and
the
effective
executed
action
(Rizzolatti
and
Craighero,
2004).
This
property,
together
with
the
fact
that
mirror
neurons
have
been
found
in
cortical
areas
involved
in
motor
control
(Keysers
and
Fadiga,
2008),
has
led
to
the
proposal
that
others’
actions
can
be
translated
into
a
motor
code
exploiting
one’s
own
action
knowledge,
in
terms
of
an
individual’s
cortical
motor
representations
(Iacoboni
et
al.,
2005).
This
translation
allows
an
observer
to
map
others’
actions
onto
the
internal
motor
representation
of
that
action,
allowing
the
observer
to
understand
the
observed
actions.
This
mechanism
became
even
more
significant
for
empathy
research
when
subsequent
findings
showed
that
mirror
neurons
consisted
of
not
only
visuomotor
neurons
discharging
for
hand
actions,
but
also
that
some
made
up
a
class
of
neurons
specifi-
cally
driven
by
actions
performed
with
the
mouth
(Ferrari
et
al.,
2003).
Crucial
to
the
involvement
of
mirror
neurons
in
empathy,
a
percentage
of
mirror
neurons
were
revealed
to
respond
while
the
monkey
observed
affiliative
communicative
gestures
(i.e.,
lips-
macking)
(Fig.
5).
These
were
the
first
single-unit
data
recorded
from
the
classi-
cal
mirror
neuron
system
that
strongly
suggest
that
the
postulated
mechanism
by
which
a
mapping
of
the
observed
action
onto
an
internal
motor
representation
could
be
reasonably
extended
into
the
emotional
domain.
Another
interesting
aspect
of
mirror
neurons
in
relation
to
empathy
is
that
some
mirror
neurons
show
a
multimodal
nature.
In
fact,
a
study
found
that
some
of
them
fire
not
only
during
the
obser-
vation
of
action,
but
also
while
listening
to
the
sound
of
that
action,
alone
(Kohler
et
al.,
2002).
The
responses
of
these
neurons
were
specific
for
the
type
of
action
seen
and
heard.
For
example,
they
responded
to
peanut
breaking
when
the
action
was
only
observed,
only
heard,
or
both
heard
and
observed,
and
did
not
respond
to
the
vision
and
sound
of
another
action,
or
to
non-action
sounds
(e.g.,
environmental
noise).
Neurons
responding
selectively
to
specific
action
sounds
were
named
“audio-visual”
mirror
neurons
(Kohler
et
al.,
2002).
This
finding
exemplifies
the
idea
that
the
matching
can
be
generated
not
only
through
a
mapping
of
a
single
sensory
modality
with
the
motor
representation
of
the
action,
but
that
the
matching
can
be
multimodal.
During
empathic
experiences,
in
fact,
subjects
can
activate
shared
motor
representations
by
exploiting
multiple
sensory
channels,
including
visual,
tactile,
and
auditory
channels.
Despite
these
early
studies,
no
other
work
explored
the
issue
of
mirror
neurons
and
empathy
through
single
cell
recording.
This
leaves
open
a
number
of
interesting
questions,
such
as
the
extent
to
which
there
are
individual
differences
–
including
sex
differences
–
in
the
activity
of
mirror
neurons,
and
whether
such
differences,
if
they
exist,
might
be
associated
with
empathetic
skills.
Animal
models
of
autism,
combined
with
single
cell
recordings,
might
be
insightful
for
disentangling
differences
in
the
brains’
response
to
social
stimuli,
as
well
as
for
assessing
potential
therapies.
In
humans,
single
cell
recordings
have
demonstrated
that
a
mir-
ror
mechanism
is
present
and,
despite
limited
evidence,
findings
are
supportive
of
the
proposal
of
a
basic
action–perception
mech-
anism
involvement
in
empathy
(Hutchison
et
al.,
1999;
Mukamel
et
al.,
2010).
In
one
study
on
patients
undergoing
surgical
proce-
dures
for
psychiatric
treatment,
there
were
anecdotal
observations
of
a
few
neurons
in
anterior
cingulate
cortex
responding
not

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Neuroscience
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(2014)
604–627
617
Fig.
5.
An
example
of
mirror
neuron
(Unit
76)
activating
during
the
observation
of
an
affiliative
facial
gesture,
typical
of
macaques,
made
by
the
experimenter
(left)
and
during
the
observation
of
a
similar
gesture
performed
by
the
monkey
(right)
(from
Ferrari
et
al.,
2003).
The
histogram
represents
the
average
of
10
trials.
Rasters
and
histograms
are
aligned
with
the
moment
in
which
the
facial
gesture
was
fully
expressed.
only
while
they
received
painful
stimulation
but
also
when
the
patient
watched
the
surgeon
apply
a
painful
stimulation
to
himself
(Hutchison
et
al.,
1999).
A
more
extended
study
with
depth
elec-
trode
recordings
in
human
mirror
neurons
investigated
21
patients
undergoing
surgery
for
otherwise
intractable
epilepsy
(Mukamel
et
al.,
2010).
The
patients,
in
addition
to
executing
and
observing
grasping
actions,
also
performed
two
facial
expressions
(smiling
and
frowning)
and
observed
the
same
facial
expressions.
Mirror
neurons
were
observed
in
the
SMA,
hippocampus,
parahippocam-
pal
gyrus,
and
enthorinal
cortex.
Among
the
68
units
with
mirroring
properties,
14
had
opposite
firing
rate
changes.
The
majority
of
these
cells
had
increased
firing
rate
for
action
execution,
and
decreased
firing
rate
for
action
observation.
Together,
these
findings
support
the
proposal
that,
during
the
observation
of
facial
expressions,
mirror
neurons
in
several
areas
are
recruited
and
might
support
basic
forms
of
facial
mimicry
or
emotional
contagion,
so
well
described
at
the
behavioral
level.
Clearly
these
types
of
rare
and
invasive
investigations
are
not
suit-
able
for
exploring
the
possible
gender
differences
related
to
these
basic
forms
of
brain
mirroring.
Therefore,
in
the
next
sections
we
will
review
how
the
principles
of
brain
mirroring
are
explored
by
means
of
other,
more
feasible,
neuroscience
methods
and
whether
the
brain
responses
during
perception
and
expression
of
facial
expression
differ
in
males
and
females.
5.2.
Neural
human
gender
differences:
Foundational
issues,
tools,
and
methods
It
is
especially
important
to
better
understand
gender
differ-
ences
in
neural
systems
relevant
to
empathy.
Indeed,
there
is
general
consensus
that
empathy
is
a
cornerstone
of
social
cog-
nition
and
that
social
cognition
is
a
key
component
of
mental
health.
Since
the
prevalence,
age
of
onset,
and
symptomatology
of
many
psychiatric
conditions
differ
between
males
and
females
(for
instance
autism,
attention
deficit/hyperactivity
disorder,
antisocial
personality
disorder
are
more
common
in
males
whereas
depres-
sion,
anxiety
disorder,
and
anorexia
nervosa
are
more
common
in
females),
a
better
understanding
of
empathy-related
gender-
differences
in
neural
organization
may
provides
clues
to
unravel
the
neurobiological
bases
of
these
disorders.
As
we
have
already
seen,
at
cellular
level
we
know
of
a
mech-
anism
–
mirror
neurons
–
that
is
a
strong
candidate
for
being
associated
with
empathy.
Obviously,
mirror
neurons
cannot
be
the
only
cellular
elements
that
enable
empathy.
Yet,
of
all
cellular
mechanisms
already
discovered
by
neurophysiological
investi-
gations,
mirroring
seems
the
easiest
and
most
natural
one
to
be
associated
with
empathy,
given
its
functional
properties.
In
humans,
however,
single
cell
recordings
can
only
be
performed
under
extremely
unusual
circumstances.
These
circumstances,
as
stated
before,
typically
preclude
the
study
of
gender
differences,
due
to
the
small
number
of
patients
investigated.
Hence,
the
study
of
mirroring
in
humans
is
typically
performed
in
an
indirect,
non-
invasive
way
by
using
Transcranial
Magnetic
Stimulation
(TMS),
electroencephalograhy
(EEG),
magnetoencephalography
(MEG),
and
functional
magnetic
resonance
imaging
(fMRI).
These
tech-
niques
can
also
be
used
to
study
the
neural
correlates
of
empathy
and
its
gender
differences,
both
in
mirroring
systems
and
in
neu-
ral
systems
that
have
little
or
nothing
to
do
with
mirror
neurons
(i.e.,
mentalizing
systems),
but
which
may
also
support
empa-
thetic
abilities.
We
discuss
each
of
these
techniques,
first
addressing
the
studies
inspired
by
mirror
neuron
research,
and
then
studies
encompassing
other
systems
in
the
brain.
5.2.1.
TMS:
Cortico-spinal
facilitation
The
first
human
TMS
study
that
was
associated
with
the
fir-
ing
of
mirror
neurons
used
TMS
to
measure
levels
of
cortico-spinal
excitability
of
the
motor
system
(Fadiga
et
al.,
1995).
The
logic
behind
this
kind
of
study
is
as
follows.
The
premotor
cortex
con-
tains
mirror
neurons
that
fire
during
action
observation.
The
firing
in
premotor
cortex
should
make
the
primary
motor
cortex
more
excitable.
Hence
TMS
of
the
corticospinal
motor
system
should
reveal
this
increased
excitability.
Indeed,
other
studies
reported
larger
motor
evoked
potentials
(MEPs,
that
is,
muscle
twitch
evoked
by
the
stimulation
of
the
motor
cortex)
when
participants’
motor
cortex
is
stimulated
during
action
perception,
compared
to
control
conditions
(Aziz-Zadeh
et
al.,
2002,
2004)
and
that
they
corre-
late
with
self-reported
empathy,
especially
when
the
observed
action
has
emotional
significance
(Avenanti
et
al.,
2005).
Thus,
these
data
suggest
that
the
TMS-measured
motor
corticospinal
facilitation
during
action
observation
seems
a
viable
marker
of

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Neuroscience
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Reviews
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(2014)
604–627
empathic
predisposition.
Notably,
studies
on
gender
differences
in
TMS-measured
motor
corticospinal
facilitation
are
lacking.
It
is
possible
that
such
striking
absence
is
related
to
the
sample
size
of
the
studies.
Indeed,
these
TMS
studies
tend
to
enroll
fairly
small
sample
sizes,
which
make
it
difficult
to
properly
investigate
gender
differences.
In
principle,
however,
TMS-measured
corticospinal
facilitation
should
reveal
gender
differences,
if
behavioral
studies
tend
to
show,
on
average,
higher
self-reported
empathy
in
females.
One
measure
that
has
more
commonly
been
employed
to
study
sex
differences
in
empathy
is
facial
electromyographic
(EMG),
which
measures
facial
mimicry,
and
is
positively
associated
with
empathy
(Dimberg
et
al.,
2011;
Dimberg
and
Thunberg,
2012)
and
facial
expression
recog-
nition
(e.g.,
Sato
et
al.,
2013).
Indeed,
a
number
of
studies
report
greater
facial
muscle
reactivity
in
females,
compared
to
males,
when
exposed
to
facial
expressions
(Dimberg
and
Lundquist,
1990;
Lundqvist,
1995).
Facial
EMG
activity
was
measured
from
the
cor-
rugator
and
zygomatic
muscles,
typically
activated
during
angry
and
happy
facial
expressions,
respectively.
This
muscle
reactiv-
ity
can
be
considered
as
a
form
of
motor
resonance,
likely
the
expression
of
mirroring
mechanisms
that
also
produce
the
TMS
effects
described
above.
In
this
particular
study,
female
subjects
demonstrated
higher
EMG
activity,
compared
to
male
subjects,
thus
supporting
the
idea
that
pre-reflective
processes
that
may
be
foundational
for
empathy
are
more
enhanced
in
females.
Similarly,
individuals
with
higher
levels
of
autistic
traits
show
less
automatic
facial
mimicry,
as
measured
by
EMG
(e.g.,
Sims
et
al.,
2012).
5.2.2.
TMS
‘virtual
lesion’
studies
Another
way
of
using
TMS
to
study
neural
systems
in
humans
and
their
relations
with
behavior
is
the
so-called
‘virtual
lesion’
methods.
Repetitive
stimulation
of
a
brain
area
interferes
with
its
activity.
When
such
stimulation
results
in
a
behavioral
change,
it
is
assumed
that
the
functions
of
the
stimulated
area
are
some-
what
associated
with
the
behavior
that
was
modified,
(see
for
instance
Heiser
et
al.,
2003).
There
is
a
vast
literature
on
this
type
of
study.
The
power
of
these
studies
is
that
they
make
explicit
brain–behavior
relationships,
revealing
the
causal
role
of
a
given
brain
region
to
a
given
behavior.
Indeed,
a
study
combining
the
‘virtual
lesion’
method
over
the
ventral
premotor
cortex,
and
the
TMS
motor
cortico-spinal
facilita-
tion
approach,
described
in
the
section
above,
recently
provided
evidence
in
support
of
the
main
idea
behind
TMS
studies,
that
the
activation
of
premotor
mirror
neurons
makes
the
motor
cor-
tex
more
excitable.
The
interference
of
premotor
activity
with
the
TMS
‘virtual
lesion’
method
should
abolish
the
expected
increased
motor
excitability
during
action
observation.
Confirming
the
valid-
ity
of
the
basic
assumption
behind
TMS
motor
excitability
studies
of
mirroring,
repetitive
TMS
over
the
ventral
premotor
cortex
abol-
ished
motor
facilitation
during
action
observation
(Avenanti
et
al.,
2007).
TMS
‘virtual
lesion’
studies,
especially
when
combined
with
eco-
nomic
games
testing
explicit
prosociality
(see
previous
behavioral
section)
are
powerful
experimental
approaches
to
examine
the
role
of
neural
systems
in
modulating
empathy
and
prosocial
behavior.
In
one
such
study,
participants
stimulated
over
the
right
dorsolat-
eral
prefrontal
cortex
(DLPFC)
demonstrated
a
higher
willingness
to
accept
unfair
offers
from
other
players
(Knoch
et
al.,
2006).
Typ-
ically,
in
these
games,
unfair
offers
(generally
offers
of
less
than
25%
of
the
available
money
to
be
shared)
are
rejected,
even
though
rejecting
them
means
renouncing
the
monetary
gain
(but
at
the
same
time
precluding
the
unfair
offerer
from
making
an
unfair
gain).
This
is
considered
evidence
that
humans
tend
to
modulate
self-interest
with
social
norms
and
moral
values
such
as
reciprocal
fairness,
being
willing
to
punish
unfair
behavior
even
if
it
means
hurting
self-interest.
In
this
study,
stimulation
of
the
left
DLPFC
did
not
change
the
low
acceptance
rate
of
unfair
offers,
suggesting
a
striking
laterality
difference
in
the
DLPFC
with
regard
to
recipro-
cal
fairness.
The
behavioral
change
brought
about
by
TMS
has
been
interpreted
as
‘increased
selfishness’,
that
is,
higher
willingness
to
accept
unfair
offers
in
order
to
make
a
monetary
gain.
This
inter-
pretation
rests
on
the
fact
that
when
asked
whether
offers
sharing
less
than
25%
of
the
available
money
were
fair
or
unfair,
partici-
pants
still
considered
them
unfair,
even
though
they
were
more
willing
to
accept
them.
However,
participants
were
asked
about
the
perceived
fairness
of
the
offer
only
after
the
economic
game
was
played,
leaving
open
the
possibility
that
the
effects
of
TMS
over
brain
activity
were
reduced
during
this
part
of
the
experiment
(TMS
effects
are
obviously
only
transient,
not
everlasting).
An
alter-
native
interpretation
regarding
the
higher
willingness
to
accept
typically
considered
unfair
offers
is
that
transiently
interfering
with
the
right
DLPFC
may
have
increased
mirroring
and
perspective
tak-
ing
and
potentially
compassion,
thus
making
it
more
likely
to
see
things
from
the
other
player’s
point
of
view.
In
this
view,
increased
acceptance
of
low
offers
is
not
due
to
increased
selfishness
but
to
increased
empathy.
Regrettably,
this
experimental
approach
has
not
yet
been
used
for
larger
scale
studies
that
would
allow
tests
of
sex
differences.
A
study
of
this
sort
would
require
a
much
larger
sample
size
than
is
typically
used
in
this
literature.
Given
that
TMS
reveals
causal
relationships
between
brain
activity
and
behavior,
it
is
surprising
that
there
are
no
TMS
studies
of
empathy
to
date
examining
gen-
der
differences.
Indeed,
this
may
prove
a
fruitful
avenue
for
future
research
in
this
field.
5.2.3.
Magnetoencephalography
(MEG)
and
electroencephalography
(EEG):
Beta
rebound
and
mu
suppression
Both
MEG
and
EEG
demonstrate
in
central,
sensory–motor
regions
oscillatory
activity
in
the
10–20
Hz
range
at
rest
that
desynchronizes
during
action
performance
and
observation.
The
oscillatory
activity
resumes
when
participants
go
back
to
a
‘resting
state.’
This
pattern
of
neural
activity
is
interpreted
as
representing
another
marker
of
mirroring
at
the
level
of
neuronal
ensem-
bles,
because
desynchronization
during
both
action
execution
and
action
observation
is
typically
framed
in
terms
of
‘motor
activa-
tion’
(Hari
et
al.,
1998).
In
the
mirroring
literature,
two
parameters
have
been
used
to
quantify
these
changes
in
MEG
and
EEG
signal
in
central
sensory–motor
regions:
the
beta
rebound
around
20
Hz
(Hari
et
al.,
1998)
and
the
mu
rhythm
suppression
around
9–13
Hz
(Muthukumaraswamy
and
Johnson,
2004).
The
latter
parameter
has
been
also
correlated
with
empathic
predisposition
(Cheng
et
al.,
2008a,b).
Two
groups
have
reported
increased
mu
suppression
in
female
subjects,
compared
to
males,
thus
supporting
the
hypothe-
sis
of
higher
mirroring
and
potentially
empathy
in
females
(Cheng
et
al.,
2008a;
Yang
et
al.,
2009).
5.2.4.
Event
related
potentials
(ERP)
studies
of
gender
differences
in
empathy
Gender
differences
in
empathy
using
event-related
potentials
(ERP)
have
been
demonstrated
in
a
handful
of
studies.
A
study
looking
at
an
early,
frontal
waveform
and
a
late,
parietal
waveform
associated
with
pain
perception
demonstrated
two
kinds
of
gender
differences:
the
early
waveform
was
correlated
with
self-reports
of
perceived
pain
in
females
only,
and
the
late
component
was
more
easily
modulated
by
concurrent
attentional
task
demands
in
females
too
(Han
et
al.,
2008).
Two
ERP
studies
investigated
both
the
emotional
valence
(e.g.,
suffering
vs.
happiness)
and
the
presence
or
absence
of
humans
in
pictures
(Groen
et
al.,
2013;
Proverbio
et
al.,
2009).
Taken
together,
the
results
show
increased
amplitudes
of
ERP
waveforms
to
humans
suffering
in
females.
The
only
study
(Groen
et
al.,
2013)
that
measured
also
self-reported
empathy,
however,
found
similar

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/
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(2014)
604–627
619
levels
of
correlation
between
neural
activity
and
affective
empathy
in
males
and
females.
In
a
rather
unusual
take
on
the
investigation
of
gender
differ-
ences
in
empathy,
a
recent
study
looked
at
the
role
of
social
context
in
language
processing
(van
den
Brink
et
al.,
2012).
Females
demon-
strated
a
larger
N400
compared
to
males
in
such
situations.
Notably,
the
N400
also
correlated
with
self-reported
empathy
in
this
study,
thus
suggesting
that
different
degrees
of
empathy
also
affect
the
processing
of
linguistic
information
in
social
contexts.
A
number
of
studies,
however,
report
sex
differences
in
ERPs
during
emotion
processing,
including
emotion
in
the
voice
(e.g.,
Schirmer
et
al.,
2007)
and
in
the
face
(e.g.,
Xu
et
al.,
2013),
suggest-
ing
that
females
may
be
more
sensitive
to
emotional
signals.
For
example,
females
process
emotion
in
the
voice
more
automatically
than
males
(Schirmer
and
Kotz,
2003).
5.2.5.
Activation
studies
using
functional
MRI
(fMRI)
and
mirroring
markers
The
most
common
non-invasive
technique
to
study
functional
brain
responses
in
human
living
subjects
is
fMRI,
because
it
allows
full
brain
coverage
and
good
spatial
and
temporal
resolution.
Indeed,
a
recent
meta-analysis
includes
more
than
a
hundred
fMRI
studies
(Caspers
et
al.,
2010)
and
supports
the
early
conclusions
that
there
are
human
brain
hubs
showing
strong
patterns
of
activ-
ity
suggesting
mirroring,
including
the
posterior
inferior
frontal
and
the
anterior
inferior
parietal
cortex
(Iacoboni
et
al.,
1999;
Iacoboni,
2005;
Iacoboni
and
Dapretto,
2006).
An
early
fMRI
study
proposed
that
empathy
is
made
possible
through
the
interactions
between
mirror
neuron
areas
and
emo-
tional
brain
centers
(Carr
et
al.,
2003).
More
recent
fMRI
studies
focusing
on
gender
differences
in
empathy
seem
to
confirm
this
general
idea.
Indeed,
a
recent
fMRI
study
on
empathy
has
revealed
gender
differences
in
the
inferior
frontal
cortex,
suggesting
that
these
gender
differences
may
be
due
to
differences
in
the
mirror
neuron
system
(Schulte-Rüther
et
al.,
2008).
Subjects
were
asked
to
focus
on
either
their
own
feelings
when
seeing
facial
emotional
expressions
or
the
feelings
of
the
other
person.
In
both
the
‘self’
and
‘other’
oriented
attentional
focus,
females
activated
more
the
inferior
frontal
cortex,
compared
to
males.
5.2.6.
Gender
differences
in
fMRI
studies
of
empathy
not
related
to
mirroring
In
a
study
on
the
modulatory
role
of
social
reputation
in
pain
perception,
subjects
first
played
an
economic
game
with
coop-
erative
and
non-cooperative
confederates
and
then
watched
the
confederates
inflicted
with
pain
(Singer
et
al.,
2006).
When
watch-
ing
someone
in
pain,
a
typical
brain
response
is
to
activate
a
set
of
neural
systems
associated
with
experiencing
pain.
This
mir-
roring
vicarious
activation
is
generally
interpreted
as
a
form
of
empathy,
a
kind
of
“I
feel
what
you
feel”
automatic
reaction.
This
mirroring
response,
however,
is
not
entirely
automatic;
it
can
be
modulated.
Indeed,
in
this
study
on
social
reputation
in
pain
perception,
while
both
males
and
females
demonstrated
similar
activation
of
pain-associated
neural
systems
while
watching
coop-
erative
players,
males
had
reduced
activation
of
pain-associated
neural
systems
while
watching
non-cooperative
players
inflicted
with
pain.
This
reduced
empathic
response
was
also
associated
in
males
with
activation
of
reward-related
structures
while
watch-
ing
non-cooperative
players
in
pain.
These
rather
striking
gender
differences
suggest
again
that
males
are
much
more
sensitive
than
females
to
contextual
modulation
of
empathic
brain
responses.
This
study
also
suggests
that
mirroring
responses
during
observation
of
others’
emotions
do
interact
with
those
brain
structures
that
are
involved
in
cognitive
empathy.
5.2.7.
Structural
MRI
A
handful
of
studies
have
reported
empathy-related
gender
dif-
ferences
in
brain
structures
(Cheng
et
al.,
2009).
Females
have
larger
grey
matter
volumes
in
both
posterior
inferior
frontal
and
anterior
inferior
parietal
cortex,
two
areas
typically
associated
with
mirror-
ing
in
the
fMRI
literature.
Furthermore,
empathic
predisposition
in
females
correlated
with
grey
matter
volume
in
the
inferior
frontal
cortex,
providing
additional
evidence
in
favor
of
gender
differences
in
mirroring.
Studies
on
structural
connectivity
demonstrated
correlations
between
white
matter
tracts
and
empathic
predisposition
in
anatomical
connections
between
mirror
neuron
areas
and
emo-
tional
brain
centers
(Takeuchi
et
al.,
2013),
supporting
the
findings
from
fMRI
on
the
role
of
this
large
scale
network
including
both
mirror
neuron
areas
and
emotional
brain
centers
in
empathy.
5.3.
Hormones,
sexual
preferences
and
gender
roles
Prior
to
the
introduction
of
neural
measures
of
emotional
responsiveness,
it
was
unclear
how
much
sex
differences
in
empa-
thy
were
simply
due
to
differing
gender
stereotypes
and
strategies.
In
a
1983
review
by
Eisenberg
and
Lennon,
they
examined
males
and
females’
empathic
abilities
and
found
mixed
evidence
for
inherent
sex
differences.
Indeed,
sex
differences
were
found
to
vary
dramatically
when
taking
into
account
the
manner
of
report-
ing
empathy
and
the
circumstances
under
which
this
was
done.
Sex
differences
in
empathy
favoring
females
were
most
evident
when
individuals
were
asked
to
rate
themselves
on
empathetic
behaviors
and
affective
responses,
while
weaker
differences
were
found
when
subjects
were
simply
asked
to
rate
their
emotional
responses
in
hypothetical
scenarios.
In
contrast,
sex
differences
were
inconsistent
when
empathy
was
assessed
with
physiologi-
cal
measures
(primarily
skin
conductance
and
heart
rate)
and/or
facial/vocal/gestural
measures
(the
latter
of
which
only
included
studies
of
children).
Indeed,
there
is
evidence
to
suggest
that
males
and
females
may
differ
in
how
empathetic
they
would
like
to
appear,
given
that
emotional
responsiveness
and
nurtur-
ing
behavior
are
part
of
stereotypical
feminine
roles.
For
example,
sex
differences
in
responsiveness
to
the
young
(a
stereotypically
feminine
behavior)
have
been
found
in
several
studies,
but
only
in
situations
in
which
it
is
clear
that
subjects
are
being
evaluated
on
that
dimension,
or
that
role
expectations
or
obligations
are
salient.
Self-ratings
of
adults’
femininity
have
been
positively
related
to
males’
and
females’
self-report
of
empathy,
whereas
self-reported
of
masculinity
has
been
negatively
associated
with
empathy
scores
(Eisenberg
and
Lennon,
1983).
Indeed,
while
biological
gender
is
clearly
important,
sexual
pref-
erences
(e.g.,
Perry
et
al.,
2013;
Sergeant
et
al.,
2006),
within-gender
differences
in
prenatal
hormone
exposure
(e.g.,
Chapman
et
al.,
2006),
hormone
reactivity,
and,
in
females,
effects
of
ovulatory
hormones
(Derntl
et
al.,
2013)
are
highly
important,
suggesting
that
the
complexity
of
defining
gender
is
reflected
in
individual
differences
in
empathy.
Individuals
sexually
attracted
to
males
showed
greater
empathy
(in
behavioral
measures)
and
greater
activation
during
an
emotional
judgment
task
in
an
area
whose
activation
was
correlated
with
self-reported
empathizing,
than
subjects
attracted
to
females
(Perry
et
al.,
2013).
According
to
the
Empathizing-Systemizing
Theory,
individuals
vary
on
two
factors
–
empathizing
(ability
to
understand
others’
emotions
and
thoughts)
and
systemizing
(ability
to
analyze
or
construct
systems)
–
that
can
help
us
understand
sex
differences
(Baron-Cohen,
2002).
A
study
of
empathizing
and
systematizing
tendencies
found
that
males
and
non-heterosexual
females
showed
higher
systematizing
ten-
dencies
than
heterosexual
females,
further
suggesting
that
both
biological
gender
and
sexual
preferences
underlie
differences
in
empathy
(Nettle,
2007).

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(2014)
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Fetal
testosterone
has
been
suggested
to
be
one
of
the
major
factors
determining
sex-differences
of
empathy
(Chapman
et
al.,
2006).
Testosterone
decreases
the
ability
to
empathize
(van
Honk
et
al.,
2011).
Fetal
testosterone
levels
in
males
and
females
were
predictive
of
their
tendency
to
use
intentional
or
neutral
statements
when
describing
characters
in
cartoons,
suggesting
that
testos-
terone
exposure
can
modulate
the
ratio
between
empathizing
and
systematizing
traits
(Knickmeyer
et
al.,
2006).
Variability
among
healthy
children
in
their
prenatal
hormone
exposure
is
related
to
individual
variability
in
postnatal
behavior.
As
in
studies
of
atypical
exposure,
higher
levels
of
androgen
predict
more
male-typical,
and
less
female-typical,
behavior.
A
study
of
females’
moral
judgments
found
that
changes
in
utilitarian
judgments
following
exposure
to
testosterone
were
dependent
on
second-to-fourth
digit
ratio
(a
marker
of
prenatal
androgen
exposure)
(Montoya
et
al.,
2013).
Hormone-induced
alterations
in
brain
development
are
thought
to
underlie
these
behavioral
outcomes,
although
there
is
little
information
on
specific
neural
differences
associated
with
early
hormone
differences
(Hines,
2008).
Another
important
field
of
research,
which
is
becoming
increas-
ingly
popular
is
the
potential
role
of
the
neuromodulator
oxytocin
(OT),
an
endogenous
neuropeptide
associated
with
bonding
and
nurturing
behavior.
Following
intranasal
administration
of
oxy-
tocin
(OT),
the
serum
level
of
OT
is
positively
correlated
with
empathetic
ability
and
generosity
(Domes
et
al.,
2007).
A
study
of
OT
and
vasopressin
(AVP)
administration’s
effect
on
prisoner’s
dilemma
behavior
with
human
and
computer
partners,
both
OT
and
AVP
caused
females
to
treat
computer
partners
more
like
humans,
and
AVP
increased
their
conciliatory
behavior.
In
men,
AVP
selectively
increased
reciprocation
of
cooperation
from
both
human
and
computer
partners.
No
common
drug
effects
on
behav-
ior
were
found
in
both
males
and
females,
though
both
OT
and
AVP
increased
activity
in
males
in
areas
known
to
be
rich
in
OT
and
AVP
receptors,
and
in
areas
important
for
reward,
arousal,
mem-
ory
and
social
bonding.
Importantly,
both
OT
and
AVP
increased
activity
in
males
during
cooperation,
while
in
females,
OT
and
AVP
either
decreased
activity
or
had
no
effect
in
these
and
other
regions
(Rilling
et
al.,
2014).
These
results
suggest
that,
as
with
andro-
gens,
while
somewhat
similar
behavioral
effects
are
observed,
the
neural
processes
for
reacting
to
these
substances
may
differ
between
males
and
females,
resulting
in
distinct
dose–response
curves
between
genders.
Indeed,
another
OT
administration
study
found
that
OT
exerted
a
greater
effect
on
perspective
taking
in
men.
This
study
also
found
that
self-report
measures
might
be
less
sensitive
to
OT
effects
than
more
implicit
measures
of
empa-
thy.
If
these
assumptions
are
confirmed,
one
could
infer
that
OT
effects
on
empathic
responses
are
more
pronounced
in
males
than
females,
and
that
any
such
effect
is
best
studied
using
more
implicit
measures
of
empathy
rather
than
explicit
self-report
measures
(Theodoridou
et
al.,
2013).
The
implication
of
these
studies
is
that
in
assessing
differences
in
such
a
complex
construct
as
gender,
researchers
should
take
into
account
gender
roles,
circumstances
of
data
collection,
sexual
preference,
prenatal
androgen
exposure
and
hormone
reactivity.
6.
Conclusions
The
construct
of
empathy
is
relevant
to
several
disciplines,
from
psychology
and
neuroscience,
to
behavioral
economics
and
animal
behavior.
For
years,
theories
on
altruism
and
kin
selection
have
emphasized
the
selfish
nature
of
humans
and
other
animals.
How-
ever,
the
‘selfish
gene’
paradigm
faced
serious
challenges
to
the
idea
that
individuals
are
complex
organisms
whose
activities
ultimately
function
to
increase
reproductive
success,
and
do
so
through
care-
ful
calculations
of
costs
and
benefits.
Work
on
primates
and
other
animals
has
shown
that
individuals
prefer
to
act
prosocially
and
in
cooperation,
they
need
to
repair
relationships
after
conflicts,
sup-
port
each
other
when
in
need,
and
ask
for
comfort
because
they
know
that
companions
are
sensitive
to
their
own
pain
and
suffer-
ing.
Interestingly,
most
of
these
examples
do
not
necessarily
imply
genetic
relatedness
or
reciprocal
benefits.
So
what
drives
this
empathetic
nature?
We
propose
that
an
examination
of
interindividual
differences
in
empathetic
skill
–
and
sex/gender
differences,
specifically
–
can
be
informative
for
understanding
the
nature
of
empathy,
including
its
proximate
and
ultimate
causes.
To
this
end,
the
present
review
had
two
primary
goals:
(1)
determine
whether
sex/gender
differences
in
empathy
may
be
largely
driven
by
cultural
rather
than
biological
causes
through
studies
of
younger
populations
and
nonhuman
animals,
and
(2)
extend
our
understanding
of
the
phenomenon
of
empathy
itself—specifically,
whether
emotional
and
cognitive
components
are
independent
or
related
through
neuroimaging
and
behaviors
studies
of
gender
differences
in
adult
humans.
Empathy,
at
its
core,
is
an
ancient
biological
phenomenon
and,
according
to
one
hypothesis,
the
roots
of
empathy
can
be
found
in
the
practice
of
caregiving,
particularly
in
altricial
species,
whose
offspring
depend
on
the
mother
for
a
prolonged
postnatal
period
(Preston
and
De
Waal,
2002).
Parents
tune
their
behavior
with
that
of
their
immature
offspring.
Such
sensitivity
is
not
only
confined
within
the
mother–infant
relationship,
but
it
includes
other
group
members.
In
primates,
living
in
large
groups,
such
as
in
macaques
or
in
chimpanzees,
families
or
other
social
units
are
formed
through
relationships
that
can
last
the
entire
lifespan.
Such
complex
social
networks
are
sustained
and
maintained
by
the
capacity
of
each
individual
to
respond
to
the
emotional
signals
of
companions
in
various
contexts,
including
situations
of
danger
or
discomfort,
as
well
as
during
play
and
excitement.
In
primates,
these
phenom-
ena
are
strikingly
more
evident
if
one
looks
at
the
complex
and
sophisticated
anatomy
of
facial
muscles,
which
primarily
function
to
express
emotions
and
to
support
emotional
communication.
Psy-
chologically
and
cognitively
demanding
processes
have
shaped
the
mind
of
our
ancestors,
resulting
in
human
social
behaviors
and
empathic
sensitivities
to
the
internal
state
of
others.
Indeed,
in
nonhuman
animals,
including
primates
and
rodents,
sex
differences
have
been
reported
for
a
diverse
number
of
behaviors
believed
to
be
indicative
of
empathy,
including
emo-
tional
contagion,
facial
mimicry,
contagious
yawning,
sensitivity
to
conspecific’s
pain/distress,
consolation,
and
prosocial
behavior.
Together,
reports
of
these
behaviors
in
nonhuman
animals
make
a
convincing
case
that
females
possess
greater
levels
of
empathy
compared
to
males,
in
at
least
some
species.
If
such
sex
differences
were
purely
cultural
in
cause,
then
this
implies
that
either
animals
are
likewise
transmitting
cultural
expectations
of
gender
(possible,
but
unlikely),
or,
more
parsimoniously,
that
such
sex
differences
in
humans
are
driven
by
some
biological
root,
which
humans
share
with
other
animals.
Furthermore,
studies
of
human
infants
report
evidence
that
females
exhibit
higher
rates
than
males
in
various
rudimentary
forms
of
empathy,
such
as
contagious
crying,
neonatal
imitation,
social
referencing
(i.e.,
looking
to
social
partners
for
information
in
ambiguous
situations),
and
general
social
interest
and
sensitiv-
ity.
These
studies
allow
us
to
rule
out
response
biases
(e.g.,
social
desirability
bias)
as
the
sole
cause
of
sex
differences
in
humans,
as
well
as
allowing
us
to
examine
individual
differences
prior
to
much
socialization,
therefore
ruling
out
cultural
influences
as
the
primary
cause
of
sex
differences,
at
least
in
young
infants.
With
age,
the
pattern
of
sex
differences
remains
stable,
or,
if
anything,
it
appears
to
grow
larger
with
age,
potentially
due
to
increases
in
empathetic
skill,
the
increased
sensitivity
of
empathetic
mea-
sures
that
can
be
used
in
older
children,
or
through
actually
larger
gains
by
females
than
males
in
empathy.
Nonetheless,
by
the
time

L.
Christov-Moore
et
al.
/
Neuroscience
and
Biobehavioral
Reviews
46
(2014)
604–627
621
they
are
toddlers,
females
appear
more
prosocial,
recognizing
and
willing
to
help/comfort
individuals
in
distress,
and
sex/gender
dif-
ference
in
empathy
continue
to
be
consistent
through
adolescents
and
into
adulthood.
Indeed,
twin
studies
reveal
that
empathy
is
largely
heritable,
consistent
with
the
notion
that
much
variabil-
ity
in
empathetic
skills
is
due
to
genetic
causes.
In
summary,
studies
in
nonhuman
animals
and
younger
human
populations
(infants/children)
offer
converging
evidence
that
sex
differences
in
empathy
have
phylogenetic
and
ontogenetic
roots
in
biology
and
are
not
merely
cultural
byproducts
driven
by
socialization.
The
second
goal
of
our
review,
as
described,
was
to
extend
our
understanding
of
the
phenomenon
of
empathy
itself;
namely,
whether
emotional
and
cognitive
components
are
independent
or
related,
through
surveying
neuroimaging
and
behavioral
studies
of
sex/gender
differences
in
adult
humans.
In
terms
of
affec-
tive
empathy,
females,
compared
to
men,
show
higher
emotional
responsivity
and
mirroring
responses
to
others’
pain,
as
well
as
better
emotion
recognition
abilities.
Relative
to
men,
females
also
seem
to
engage
more
emotional
areas
during
social
cognition.
Females
also
tend
to
show
more
prosocial,
altruistic
behavior
as
well,
which
supports
the
notion
that
affective
empathy
drives
prosocial
behavior.
On
the
other
hand,
when
it
comes
to
cognitive
empathy,
males
seem
to
show
more
utilitarian
behavior
as
well
as
greater
recruitment
of
areas
involved
in
cognitive
control
and
cognition.
Evidence
regarding
ToM
is
mixed,
though
it
points
to
differing
strategies
in
how
it
is
implemented
between
genders
and
to
what
ends,
which
may
be
underpinned
by
differences
in
affective
forms
of
empathy.
In
general,
although
there
do
appear
to
be
sex
differences
in
cognitive
empathy,
females
do
not
appear
to
show
the
same
obvious
advantage
over
males,
as
they
do
with
affective
empathy,
which
may
indicate
that
these
systems
are
somewhat
independent.
These
behavioral
data
are
consistent
with
the
neurobiological
literature
showing
that
different
circuits
mediate
at
least
two
forms
of
empathy.
Affective
empathy,
compared
to
cognitive
empathy,
is
more
automatic
and
activates
shared
motor
representation
and
through
neural
simulation
individuals
are
capable
to
understand
others’
emotions.
Part
of
this
affective
empathy
network
involves
the
mirror
neuron
system
as
well
as
structures
belonging
to
the
limbic
system,
such
as
the
anterior
insula
and
the
anterior
cin-
gulate
cortex.
In
contrast,
a
different
system
supports
cognitive
aspects
of
empathy,
including
perspective
taking
and
mentalizing.
This
cognitive
empathy
system
includes
cingulate,
prefrontal,
and
temporal
areas,
such
as
the
ventromedial
prefrontal
cortex,
tem-
poroparietal
junction,
medial
temporal
lobe,
and
Brodmann
areas
10
and
12
(Zaki
and
Ochsner,
2012).
We
reviewed
several
findings
that
support
this
cognitive/affective
distinction.
Moreover,
devel-
opmental
work
and
the
ethological
studies
on
emotional
contagion
suggest
that
the
first
forms
of
empathy
that
emerge
are
character-
ized
by
sharing
the
same
affective
states,
and
by
simultaneously
activating
the
same
motor
programs
that
control
emotions
and
the
visceral
responses
associated
with
them.
Although
the
neuro-
science
literature
has
little
information
about
brain
development,
the
evidence
from
psychological
and
behavioral
studies
supports
the
notion
that,
in
females,
the
basic
networks
involved
in
affec-
tive
empathy
are
more
developed.
In
contrast,
there
are
few
studies
comparing
males
and
females
in
the
neural
underpinnings
of
cogni-
tive
empathy,
so
this
is
an
area
in
which
further
research
is
needed.
Based
on
behavioral
work,
we
suspect
that
sex
differences
in
neural
systems
responsible
for
cognitive
empathy
may
not
be
as
great
at
those
for
affective
empathy.
We
also
have
shown
that
there
are
social,
contextual,
and
cul-
tural
influences
that
may
foster
some
of
these
observed
behavioral
and
neural
differences
in
affective
empathy
between
males
and
females.
Especially
in
adulthood
it
seems
that
males
vary
more
than
females
in
some
aspects
of
emotional
processing
and
altruistic
behavior,
suggesting
that
even
though
it
appears
that
males
express
less
empathy,
their
higher
discrimination
in
targeting
helping
behavior
supports
the
idea
that
males
actually
outperform
females
in
their
empathetic
control.
In
fact,
even
in
childhood,
males
appear
to
have
more
control
over
their
empathy
than
females,
because,
although
they
are
capable
of
empathy,
they
exhibit
it
less
auto-
matically.
Indeed,
examining
the
different
contexts
in
which
males
and
females
differentially
exhibit
empathy
can
be
quite
insight-
ful.
For
example,
males,
but
not
females,
are
more
empathetic
towards
female
targets
and
targets
who
they
perceive
as
deserv-
ing
of
help.
Females,
in
contrast,
appear
more
indiscriminately
empathetic.
Although
speculative,
it
is
possible
that
these
sex
differences
in
empathy
may
be
the
consequence
of
different
evo-
lutionary
selective
pressures
on
males
and
females,
in
addition
to
females’
role
as
primary
caretaker,
with
females
exhibiting
stronger
links
between
emotional
and
cognitive
empathy
(Smith,
2006).
For
males,
increased
empathy
specifically
directed
at
females
may
have
improved
their
chances
of
reproduction,
as
both
sexes
prefer
mates
that
are
more
kind
(Li
et
al.,
2002),
while
decreased
affective
empathy
directed
at
males
may
have
been
adaptive
in
competitive
contexts
(Galinsky
et
al.,
2008),
such
as
competing
for
mates.
While
parts
of
our
original
questions
have
begun
to
be
answered,
important
parts
still
remain
to
be
clarified.
Why
and
how
are
males
more
influenced
by
contextual
factors,
such
as
the
qualities
of
the
target
(e.g.,
sex,
perceived
fairness)
and
are
these
effects
also
present
in
nonhuman
animals
and
younger
individuals?
Are
sex
differences
reversed
in
species
in
which
males
are
the
primary
care-
takers
(i.e.,
in
this
case,
are
males
more
empathetic
than
females)?
In
addition
to
caring
for
offspring,
are
there
other
evolutionary
selective
pressures
(e.g.,
sexual
selection,
competition
for
mates)
have
differently
shaped
empathy
in
males
and
females
during
phy-
logenesis?
Why
are
disorders
of
empathy,
such
as
autism
and
psychopathy,
more
common
in
males
than
females?
What
are
the
contributions
of
early
experiences
and
how
do
they
interact
with
genetic
and
epigenetic
mechanisms
to
tune
mirror
system
sensi-
tivities?
Are
the
consequences
of
empathetic
behavior
different
for
males
and
females?
Are
the
neural
underpinnings
for
cognitive
empathy
different
in
males
and
females,
and
do
females
exhibit
stronger
connections
between
emotional
and
cognitive
empathy
systems?
We
propose
that
a
consideration
of
interindividual
differences,
and
specifically
sex/gender
differences,
can
inform
our
understand-
ing
of
empathy,
including
its
evolution,
the
extent
to
which
it
is
shared
with
other
animals,
its
development,
and
its
neural
under-
pinnings.
Despite
the
challenges
studies
of
sex/gender
differences
must
overcome
(e.g.,
necessity
for
large
sample
size),
we
think
it
is
worthwhile
to
explore
such
differences.
Such
an
understanding
may
ultimately
help
to
identify
and
treat
disorders
of
empathy
that
present
sexual
dimorphisms,
including
ASD.
Acknowledgements
This
work
was
supported
by
NICHD
P01HD064653
to
P.
F.F.,
by
NIH
grant
1R21MH097178
to
M.I.,
and
by
NSF
Graduate
Fellowship
DGE-1144087
to
L.C.-M.
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