Neuroscience Letters 655 (2017) 68–75

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Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet

Research article

Neural functional correlates of empathic face processing

Antonio Del Casale a,b , Georgios D. Kotzalidis a , Chiara Rapinesi a,∗ , Delfina Janiri c ,
Massimiliano Aragona d , Antonella Puzella e , Edoardo Spinazzola c , Matteo Maggiora c ,
Giulia Giuseppin a , Stefano Maria Tamorri c , Alessandro Emiliano Vento f ,
Stefano Ferracuti g , Gabriele Sani a , Maurizio Pompili a , Paolo Girardi a
a
NESMOS Department (Neurosciences, Mental Health, and Sensory Organs), Sapienza University − Rome, Faculty of Medicine and Psychology, and Unit of
Psychiatry, Sant’Andrea Hospital, Rome, Italy
b
Department of Psychiatric Rehabilitation, “P. Alberto Mileno Onlus” Foundation, “San Francesco” Institute, Vasto, Chieti, Italy
c
Resident in Psychiatry, Faculty of Medicine and Psychology, Sapienza University, Rome, Italy
d
Crossing Dialogues Association, Rome, Italy
e
Studio Multiverso, ATC-SITCC, Rome, Italy
f
Faculty of Psychology, “Guglielmo Marconi” University, Rome, Mental Health Department ASL RM 2 and Addictions’ Observatory (ODDPSS), Rome, Italy
g
Department of Neurology and Psychiatry, Sapienza University, Rome, Italy

h i g h l i g h t s

• ALE meta-analysis is suitable for analysing standardized fMRI data.

• Emotional face processing is a measure of empathy.
• ALE meta-analysis of emotional face fMRI identified regions involved in empathy.
• Empathy activated BAs 32, 6, 9, 37, 13, 31, amygdala and putamen.
• Empathy is complex and involves cortico-limbic activations.

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: Empathy is a human trait related to the ability to share someone else’s feelings, and emotional
Received 5 April 2017 face processing is one of its measures. Functional Magnetic Resonance Imaging (fMRI) studies showed
Received in revised form 19 June 2017 significant neural correlates of empathic face processing. We aimed to identify those brain areas most
Accepted 30 June 2017
consistently involved in empathy for emotional faces.
Available online 1 July 2017
Methods: We carried ALE meta-analysis of whole-brain data from fMRI studies during empathic
face–processing tasks. We included 23 studies conducted on a total of 568 participants (247 males and
Keywords:
321 females, mean age 32.2 years).
Empathy
Emotional face processing
Results: Emotional vs. control faces processing significantly correlated with activations of the left anterior
Functional neuroimaging cingulate cortex (BA 32), right precentral gyrus (BA 6), left amygdala, right superior frontal gyrus (BA 9),
fMRI left middle occipital gyrus (BA 37), right insula (BA 13), left putamen, and left posterior cingulate cortex
ALE meta-analysis (BA 31).
Conclusions: Empathy is a complex process correlating with bi-hemispheric cortico-limbic activations
involved in emotional cue processing, self-other/same-different discrimination, perspective-taking, the-
ory of mind, emotional arousal, and decision-making.
© 2017 Elsevier B.V. All rights reserved.

1. Introduction and background

Empathy is one’s ability to put him/herself in others’ shoes. Its

∗ Corresponding author at: NESMOS Department (Neurosciences, Mental Health,
and Sensory Organs), Sapienza University − Rome, School of Medicine and Psychol-
ogy, Sant’Andrea Hospital, Via di Grottarossa 1035-1039, 00189 Rome, Italy
E-mail address: chiara.rapinesi@uniroma1.it (C. Rapinesi).
definition varies according to the setting considered. Empathic abil-
ity is an evolutionarily preserved property and continues to develop
in individuals throughout neurodevelopment and brain maturation
[1]. In humans, emotional empathy was found to rely on coordi-
nated functions of a network comprising the orbitofrontal cortex,
anterior insula, anterior cingulate cortex (ACC), temporal pole, and

http://dx.doi.org/10.1016/j.neulet.2017.06.058
0304-3940/© 2017 Elsevier B.V. All rights reserved.
 A. Del Casale et al. / Neuroscience Letters 655 (2017) 68–75 69

Fig. 1. PRISMA diagram describing the ALE meta-analysis search strategy.

amygdala, and depends on the proper function of the right unci-
nate fasciculus [2], thus it appears to be a complex, multiarea
phenomenon. The ability to recognize others’ emotions is linked
to an unimpaired theory of mind function [11] and depends on
the extent to which someone is empathic [3]. Functional Magnetic
Resonance Imaging (fMRI) studies during empathic face processing
tasks showed important functional neural correlates in different
brain areas [4]. In this meta-analysis we aimed to identify through
an activation likelihood estimation (ALE) of data from fMRI studies
those brain areas that are involved in empathic face processing (i.e.
own emotional response to others’ emotional face expressions).
2. Method
We conducted a literature search on the PubMed database
including terms for empathic processing and fMRI data. We
included studies providing specific stereotactic Talairach [5] or
Montreal Neurological Institute (MNI) [6] coordinates in compar-
ing within-group neural activation differences. Further papers that
did not appear in the above database were searched from reference
lists of retrieved papers. The process of literature selection, includ-
ing inclusion and exclusion criteria, is shown in Fig. 1. We followed
the ‘preferred reporting items for systematic reviews and meta-
analyses’ (PRISMA) indications in study identification and selection
(Fig. 1) [7]. We performed on April 11, 2016 a PubMed search with
the following search strategy: “(empathy [title/abstract] NOT disor-
der [title/abstract] NOT schizophr* [title/abstract] NOT psychiatr*
[title/abstract] NOT autis* [title/abstract] NOT pain [title/abstract])
AND (fMRI[title/abstract] OR functional magnetic [title/abstract])”.
We did not include review articles or case reports, reports
of structural MRI or diffusion tensor imaging data or functional
connectivity data only, studies failing to provide stereotactic coor-
70 A. Del Casale et al. / Neuroscience Letters 655 (2017) 68–75

Table 1
Sample characteristics of the studies included in the ALE-meta-analysis.

Study Sample Men Women Mean age, y Handedness (L)

Acevedo et al. [11] 18 8 10 27.5 18 (0)

Bodden et al. [12] 30 15 15 25.3 30 (0)
Chakrabarti et al. [13] 26 13 13 23.4 N/A
De Greck et al. [14] 20 9 11 23 N/A
Fan et al. [15] 34 21 13 40.1 30 (4)
Kanske et al. [16] 25 11 14 32.6 25 (0)
Krendl et al. [10] 53 18 35 54,6 53 (0)
Kryklywy et al. [17] 18 9 9 23.3 N/A
Lawrence et al. [18] 12 6 6 32.2 12 (0)
Lee et al. [19] 38 12 26 22 N/A
Leslie et al. [20] 15 8 7 26 15 (0)
Moore et al. [21] 30 18 12 79.1 30 (0)
Morelli & Lieberman [22] 32 16 16 19.9 32 (0)
Nomi et al. [23] 14 7 7 28.6 14 (0)
Nummenmaa et al. [24] 10 0 10 26 N/A
Pehrs et al. [25] 26 9 17 30.3 26 (0)
Prochnow et al. [26] 31 8 23 23.9 31 (0)
Prochnow et al. [27] 26 14 12 38.3 26 (0)
Reniers et al. [28] 15 15 0 27 15 (0)
Schmitgen et al. [29] 21 12 9 23.7 21 (0)
Schnell et al. [30] 21 12 9 25.5 21 (0)
Takahashi et al. [31] 38 0 38 22.1 38 (0)
Van Den Stock et al. [32] 15 6 9 26.2 15 (0)

(L), left-handed, N/A, not available; y, years.

dinates, studies focusing on empathy for pain, mother-infant

relationship, and involving subjects with mental disorders or phys-
ical illnesses.
We used the BrainMap Project GingerALE software (version 2.3)
to carryout meta-analyses. Talairach space data were converted to
MNI space co-ordinates using the icbm2tal brain template [8].
Pairwise ALE meta-analyses used random effects methodology
to evaluate fMRI data obtained during empathic face processing,
including emotional conditions versus neutral (i.e., exposure to a
face with a non-emotional content) or control (for example, watch-
ing a significant other vs. a stranger or nonpsychiatric sexually
offended participants vs. non-offended) baseline. We summarized
in Table 1 the included and excluded task contrasts of each included
study. According to this split, we obtained a dataset reflecting brain
activations related to empathic face processing during experimen-
tal conditions, and we conducted a single dataset analysis.
ALE meta-analyses use random-effects methods, with ALE val-
ues determined by the sample size of each study. Pairwise ALE
meta-analyses involved GingerALE software computing the ALE
Fig. 2. Hyperactivation of the left anterior cingulate cortex (BA 32) during empathic
values for each voxel in the brain, testing the null distribution of
face processing.
ALE statistics at each voxel [9]. The p values were used to compute
thresholds for the ALE map using an uncorrected p algorithm with
a minimum cluster size of significant activations set to 0 mm3 and additional sample data from one study [10] directly from the cor-
a p-value set to 0.0001. Finally, we performed cluster analysis on responding author.
the thresholded map, based on the above minimum cluster size. The ALE meta-analysis of data obtained from 23 studies
A MNI anatomical template (http://www.brainmap.org/ale/ (reporting 527 foci) [10–32] focused on empathic emotional face
Colin27 T1 seg MNI.nii.gz) was used for anatomical representation processing vs. neutral or control conditions processing significantly
of significant clusters in figures. correlated with activations of the left ACC (BA 32), right precentral
gyrus (BA 6), left amygdala, right superior frontal gyrus (SFG) (BA
3. Results 9), left middle occipital gyrus (BA 37), right insula (BA 13), left puta-
men, and left posterior cingulate cortex (PCC) (BA 31) (Fig. 2 and
Our PubMed search yielded 124 papers. Reviews were not used Table 3) (Figs. 3–5).
for the analysis, but were commented upon when appropriate, and
their reference lists were further searched for undetected relevant 4. Discussion
papers; through this search 2 more papers were identified and
included in the meta-analysis. Summarizing, we obtained a total Our data support literature showing bilateral hemisphere acti-
of 126 articles; of these, the greatest number focused on empathic vation changes correlated to empathic processing of emotional
face processing. According to our inclusion and exclusion criteria stimuli, in particular emotional faces [4].
we finally included 23 fMRI studies for the ALE meta-analysis, for Right SFG. A major involvement of this area emerged in empathic
a total of 568 healthy participants (247 males, 321 females), with face processing, extending to the medial frontal gyrus (BAs 9 and
a weighted mean age of 32.2 years (Fig. 1; Table 2). We obtained 10). Structural neuroimaging found the ability to manifest empathy
 A. Del Casale et al. / Neuroscience Letters 655 (2017) 68–75 71

Table 2
Design characteristics of the ALE-meta-analysis included studies.

Study Coordinates Contrasts Excluded Contrasts

Acevedo et al. [11] MNI Partner happy vs. Partner neutral Partner happy vs. Stranger happy
Partner sad vs. Partner neutral Partner sad vs. Stranger sad
Stranger sad vs. Stranger neutral Partner sad vs. Stranger sad
Stranger sad vs. Stranger neutral
Bodden et al. [12] MNI Cognitive > Physical Affective > Cognitive
Affective > Physical
Chakrabarti et al. [13] TAL Happy vs. Neutral
Angry vs. Neutral
Sad vs. Neutral
Disgusted vs. Neutral
De Greck et al. [14] MNI Intentional empathy > Baseline Intentional empathy > Skin color evaluation
Fan et al. [15] MNI Emotional vs. control faces
Kanske et al. [16] MNI Emotionally negative > Neutral video (Emotional > Neutral video) vs. (ToM > nonToM
questions)
ToM > nonToM question (ToM > nonToM questions) vs. (Negative >
Neutral video)
Krendl et al. [10] TAL Stigma Face > Control Contrast
Kryklywy et al. [17] TAL Whole-brain amplitude modulated Whole brain T-test–related contrasts
Lawrence et al. [18] TAL Social Perception > Nonsocial Labeling task Personal distress
Lee et al. [19] MNI Overall interference Highest interference
effect of emotion Lowest interference
expression Discordant (concordant; uncorrected)
Brain activation correlated with self-overlap
on the trait task
Leslie et al. [20] TAL Face imitation and Face view
Moore et al. [21] TAL Negative faces vs. Shapes
Morelli & Lieberman MNI Happy empathize > Neutral, Sad empathize > Neutral, Anxiety Happy watch > Neutral, Sad watch > Neutral,
[22] empathize > Neutral; Anxiety watch > Neutral;
Empathize > Neutral and Watch > Neutral Happy memorize > Neutral, Sad memorize >
Neutral, Anxiety memorize > Neutral;
Nomi et al. [23] TAL Emotional vs. Scrambled faces
Emotional face expression processing related areas
Nummenmaa et al. [24] MNI Emotional > Neutral Emotional vs. Cognitive empathy
pictures Cognitive vs. Emotional empathy
Pehrs et al. [25] TAL Emotional Supraliminal faces–related activations
faces–related Subliminal faces–related activations
activations Supra- vs. Sub-liminal faces
Prochnow et al. [26] TAL Emotional faces related activations
Emotional facial expressions of high social impact related
activations
Emotional facial expressions of low social impact related
activations
Reasoning about emotional states of high social impact related
activations
Prochnow et al. [27] TAL Main effect of emotional context
Reniers et al. [28] MNI EFE > nonEFE A3rdPP > V1stPP
NonEFE > EFE
EFE > nonEFE vs. RT reduction by EFE
nonEFE > EFE vs. RT reduction by EFE
(EFE ToM − nonEFE ToM) − (EFE nonToM −
nonEFE nonToM)
(EFE nonToM − nonEFE nonToM) − (EFE ToM
− nonEFE ToM)
Schmitgen et al. [29] MNI Main effect of affective 3rdPP > 1stPP
content (V3rdPP > V1stPP) > (A3rdPP > A1stPP)
(A3rdPP > A1stPP) > (V3rdPP > V1stPP)
Schnell et al. [30] MNI 3rd person affective > 3rd person visuospatial judgements 3rd person visuospatial > 1st person
visuospatial judgements
1st person affective > 1st person visuospatial judgements
Takahashi et al. [31] MNI Tears vs. no tears Sad < Neutral expressions
Supra-additive effect between tears and sad
expressions
Van Den Stock et al. TAL Emotional conditions vs. Neutral baseline
[32]

A, affective; EFE, emotional face exposure; MNI, Montreal Neurological Institute space coordinates; PP, person perspective; TAL, Talairach space coordinates; ToM, theory of
mind; V, visual.

to correlate with dorsolateral (dl) PFC grey matter volume [33].
Functional neuroimaging showed that the right SFG is involved in
the response to self vs. familiar face [34,35]. The discrimination
between self and familiar other is correlated to activations of the
right prefrontal and inferior parietal cortices, where the right PFC
is likely important for active self/other discrimination [36,37], and
parietal activation could be involved in representing self-face in the
context of the general awareness of one’s own body [38].
Right Precentral Gyrus. Activation of this area has been earlier
involved in recognizing the emotional state of others [39], receiving
emotionally empathic comments after negative performance feed-
back [40], and empathic paraphrasing. The precentral gyrus has
72 A. Del Casale et al. / Neuroscience Letters 655 (2017) 68–75

Table 3
Brain regions exhibiting significant activity across the full set of executive tasks.

Cluster # Volume (mm3 ) Extrema Value x y z Label

1 312 0.025785 −4 50 −12 Left cerebrum. Limbic lobe. Anterior cingulate.

Grey matter. Brodmann area 32
2 264 0.0273 48 4 32 Right cerebrum. Frontal lobe. Precentral gyrus.
Grey matter. Brodmann area 6
3 216 0.023235 −26 −6 −16 Left cerebrum. Limbic lobe. Parahippocampal
gyrus. Grey matter. Amygdala
4 184 0.023153 8 62 16 Right cerebrum. Frontal lobe. Superior frontal
gyrus. Grey matter. Brodmann area 9
5 168 0.023621 −50 −70 −4 Left cerebrum. Occipital lobe. Middle occipital
gyrus. Grey matter. Brodmann area 37
6 144 0.022547 34 22 6 Right cerebrum. Sub-lobar. Insula. Grey matter.
Brodmann area 13
7 136 0.022865 −22 18 0 Left cerebrum. Sub-lobar. Lentiform nucleus.
Grey matter. Putamen
8 56 0.01978 −6 −50 28 Left cerebrum. Limbic lobe. Posterior cingulate.
Grey matter. Brodmann area 31
9 32 0.020125 −22 8 4 Left cerebrum. Sub-lobar. Lentiform nucleus.
Grey matter. Putamen
10 8 0.018844 22 6 6 Right cerebrum. Sub-lobar. Lentiform nucleus.
Grey matter. Putamen
11 8 0.019034 52 −40 12 Right cerebrum. Temporal lobe. Superior
temporal gyrus. Grey matter. Brodmann area
41
12 8 0.018741 6 56 24 Right cerebrum. Frontal lobe. Medial frontal
gyrus. Grey matter. Brodmann area 9

Fig. 3. Hyperactivation of the right precentral gyrus (BA 6) during empathic face
processing. Fig. 4. Hyperactivation of the left amygdala during empathic face processing.

been functionally involved in empathy-related social perception

and social cognition [41], which could be linked to the action per-
ception model that postulates imitation as the basis for the correct
perception of others’ mental states.
Left Middle Occipital Gyrus. Together with the superior temporal
sulcus (STS), one of the classical ventral stream functions is related
to process of recognizing static and dynamic characteristics of the
observed face [42]. The ventral stream originates in the occipital
areas and spreads through the occipital face area and fusiform face
area (FFA). The STS has been implicated in dynamic facial feature
processing and facial emotional decoding [43], while the FFA could
be more related to the decoding of fine-grained static facial char-
acteristics [44].
Left ACC. The individual ability in manifesting empathy directly
correlated with grey matter volumes of the left ACC, right insula,
and dlPFC and mPFC [45]. From a functional viewpoint, the left ACC
showed enhanced functional connectivity during face processing
with the right FFA [46]. Activations in left ACC have been involved Fig. 5. Hyperactivation of the right superior frontal gyrus (BA 9) during empathic
in recognition of own vs. unknown faces [47], and representation face processing.
 A. Del Casale et al. / Neuroscience Letters 655 (2017) 68–75
of emotional faces over a delay period [48]. Together with our
data, these findings suggest that the left ACC activation is mainly
involved in empathic face processing.
Left PCC. Bilateral activations of the ventral PCC have been cor-
related with happiness conditions produced by personally relevant
memories and facial expressions [49]. Left PCC activations were
related to responses to deviant face stimuli, depending on the
attribute of the deviance (fear vs. happiness vs. identity) [50]. This
area could also play a role in initiating positive emotions [51].
The precuneus/PCC and the medial prefrontal cortex demon-
strated an important role in integrating tears and facial expressions
during affective mentalizing [52]. This kind of emotional processing
could be importantly affected by gender differences 53].
Right Insula. Structural neuroimaging studies showed that the
right insular grey matter volume correlated with an individual’s
ability to show positive empathy [33]. Right insular activation is
involved in distinguishing between one’s own face and that of
others [47], early reactions to internal sensations produced by
recognition of emotional states in others [54], as well as in empathic
social communication [55]. During imitation of emotions, enhanced
activity within the right insular region has been related to the
representation of feelings’ states that may have their origin in
interoception [56]. While viewing emotional faces, right insular
activation has been considered a main functional neural correlate
of the “gut reaction” to one’s face [57]. Consistently with Damasio’s
[58] somatic marker hypothesis and the Paulus et al. [59] model
of performance, right insula activation could be related to the re-
representation of bodily state that is fundamental for predicting
how emotions will change decision-making to enhance survival. It
may also be a neural correlate of an optimal reaction to emotion for
group-based performance.
Left Putamen. Ventral putamen neurons receive inputs from the
inferior temporal visual cortex [60]; this circuit could be involved
in empathic face recognition. In fact, the left putamen and bilateral
supplementary motor area showed metabolic changes related to
laughter/smile (and its magnitude) induced by visual comics [61].
Left Amygdala. Structural neuroimaging showed that left amyg-
dala volume negatively correlated with accuracy of recognition of
fearful facial expressions and positively with misrecognition of fear
as surprise [62]. The left amygdala has been involved in human
fearful face processing 63,64], early perceptual emotional face pro-
cessing [65], recognition of personally familiar vs. famous faces
[149] and unknown vs. familiar faces [66].
Left amygdala hyperactivation correlated with exposure to fear-
ful vs. happy face expressions, and significantly interacted with the
intensity of emotion [67]. The extent of functional connectivity
between left amygdala and face-processing–related regions cor-
related with subjective threat rating of faces [68]. Furthermore,
changes in amygdalar functional connectivity with the rest of the
brain occurs with various emotions, for example anger and relate,
besides the left/right distinction, to basolateral vs. centromedial
localization [69,70] and are emotion-specific, thus constituting a
dynamic signature [71].
Our data match the involvement of the left amygdala in a neural
system associated with social cognition (i.e., left amygdala, bilat-
eral insula, fusiform gyrus, STS, and reward-related areas), whose
function can consist in rapid learning about others’ moral status
[72].
Summarizing, the amygdala is very important as a relay in var-
ious networks subserving emotion recognition and may offer us a
clue as to how the brain deals with emotions, i.e., according to a top-
down monitoring of sensory paths [73] or through the interplay
between motivation and executive functions [74], or reconciling
both dual stage and dual route models [75].
Limitations. The main limitation of our meta-analysis consists in
the fact that we included different emotional contrasts (for example
73
happy, fearful, angry, and sad faces vs. neutral faces), due to the
existence of a small number of studies investigating specific single
emotions, or different emotions considered separately. We did not
conduct analyses of co-variates of group empathy, because not all
studies provided measurements of high or low empathy of their
participants.
5. Conclusions
Our ALE meta-analysis of studies of empathic face processing
suggested that exposure to emotional vs. neutral (or control) faces
correlates with activations in the context of a bilateral neural net-
work, which includes the left ACC (BA 32), right precentral gyrus
(BA 6), left amygdala, right SFG (BA 9), left middle occipital gyrus
(BA 37), right insula (BA 13), left putamen, and left PCC (BA 31), thus
pointing to a cortical-subcortical integrated circuitry. These data
reflect the possibility that empathy for emotional faces is a complex
process correlating with brain activations consistently involved
in emotional cue processing, self-other/same-different discrimina-
tion, perspective-taking, theory of mind, emotional arousal, and
decision-making.
Author contributions
A. Del Casale, D. Janiri, C. Rapinesi, and M. Aragona have con-
ceived and designed this study. A. Del Casale, C. Rapinesi, G.
Giuseppin, M. Maggiora, E. Spinazzola, S. M. Tamorri, A.E. Vento,
A. Puzella, G. Sani, and G. D. Kotzalidis carried out the literature
search and created a database of relative data. A. Del Casale and
C. Rapinesi performed the meta-analyses. A. Del Casale, S. Ferra-
cuti, M. Pompili, G. D. Kotzalidis, and P. Girardi have supervised
the entire work. All authors shared manuscript writing, discussed
results, commented on the manuscript, and approved the final ver-
sion of this manuscript
Financial & competing interests disclosure
All the authors of this paper have no relevant affiliations or
financial involvement with any organization or entity with a finan-
cial interest in, or financial conflict with the subject matter or
materials discussed in the manuscript. This includes employment,
consultancies, honoraria, stock ownership or options, expert testi-
mony, grants or patents received or pending, or royalties
Acknowledgments
We gratefully acknowledge Prof. Anne Catherine Krendl who
provided us with additional data from her study; the Librarians
of the School of Medicine and Psychology of Sapienza University,
Ms. Mimma Ariano, Ms. Felicia Proietti for the localization of rele-
vant literature; our secretary Ms. Lucilla Martinelli who assisted us
during the writing of the manuscript
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