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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
of
empathy
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607
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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610
3.1.
Emotion
recognition,
priming,
and
emotion
contagion
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610
3.2.
Mentalizing
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611
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
behavior.
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612
3.3.2.
Naturalistic
data:
Volunteering,
donating,
and
other
altruistic
behavior
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612
4.
Sex
differences
in
the
development
of
empathy
in
humans
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613
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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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