Exp Brain Res (2015) 233:2373–2382
DOI 10.1007/s00221-015-4307-8
RESEARCH ARTICLE
Subliminal perception of others’ physical pain and pleasure
Patrizia Andrea Chiesa1,2 · Marco Tullio Liuzza1,2 · Adriano Acciarino1,2 ·
Salvatore Maria Aglioti1,2 
Received: 10 August 2014 / Accepted: 30 April 2015 / Published online: 15 May 2015
© Springer-Verlag Berlin Heidelberg 2015
Abstract  Studies indicate that explicit and implicit pro-
cessing of affectively charged stimuli may be reflected in
specific behavioral markers and physiological signatures.
This study investigated whether the pleasantness ratings of
a neutral target were affected by subliminal perception of
pleasant and painful facial expressions. Participants were
presented images depicting face of non-famous models
being slapped (painful condition), caressed (pleasant con-
dition) or touched (neutral condition) by the right hand of
another individual. In particular, we combined the continu-
ous flash suppression technique with the affective misat-
tribution procedure (AMP) to explore subliminal empathic
processing. Measures of pupil reactivity along with empa-
thy traits were also collected. Results showed that par-
ticipants rated the neutral target as less or more likeable
congruently with the painful or pleasant facial expression
presented, respectively. Pupil dilation was associated both
with the implicit attitudes (AMP score) and with empathic
concern. Thus, the results provide behavioral and physi-
ological evidence that state-related empathic reactivity can
occur at an entirely subliminal level and that it is linked to
autonomic responses and empathic traits.
Electronic supplementary material  The online version of this
article (doi:10.1007/s00221-015-4307-8) contains supplementary
material, which is available to authorized users.
* Patrizia Andrea Chiesa
patrizia.chiesa@uniroma1.it
* Salvatore Maria Aglioti
salvatoremaria.aglioti@uniroma1.it
1
Department of Psychology, University of Rome
“La Sapienza”, Rome, Italy
2
IRCCS, Fondazione Santa Lucia, Rome, Italy
Keywords  Subliminal perception · Facial expressions ·
Priming
Introduction
Empathy can be broadly defined as the ability to share
one’s own emotional status with that of another individual
(Avenanti et al. 2006; Decety and Jackson 2004; Preston
and de Waal 2002; for a review see Bernhardt and Singer
2012). Although there is consensus regarding the defini-
tion of this phenomenon, its nature is still debated. Studies
indicate that empathy may imply shared representation of
firsthand and vicarious experience of emotional states (Bot-
vinick et al. 2005). Transcranial magnetic stimulation stud-
ies show that empathic sensorimotor reactivity to the pain
experienced by others occurs rapidly and possibly invol-
untarily (Avenanti et al. 2005, 2006, 2010; Botvinick et al.
2005; Han et al. 2009; Minio-Paluello et al. 2006). Thus,
empathic reactivity may provide a way to quickly adapt
affective states when interacting with conspecifics.
One of the most important skills for sharing others’
affective states may be the ability to read others emotions
through their facial expressions (Ekman 1999). Neuropsy-
chological findings indicate that face emotion processing
is subserved by a fast-subcortical neural pathway (Garrido
et al. 2012; Garvert et al. 2014; Vuilleumier et al. 2001),
thus suggesting that empathic reactivity may also occur
involuntarily. Studies on the mechanisms underlying sub-
liminal affective processing (e.g., Tamietto and de Gelder
2009) indicate that, being the system that processes affec-
tive information extremely fast, emotional inputs may be
processed even if people are perceptually unaware of them
(Whalen et al. 2004). Indeed, although not penetrable to
awareness, facial expressions of emotions, for example
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fear (Jiang and He 2006; Yang et al. 2007), anger (Almeida
et al. 2013), disgust (Flexas et al. 2013), happiness (Dim-
berg et al. 2000), surprise (Duan et al. 2010) and sadness
(Killgore and Yurgelun-Todd 2004), can nonetheless affect
cognitive and affective processing. For example, Jiang and
He (2006) showed that the implicit processing of invisible
erotic pictures, intrinsically related to the sexual prefer-
ences of the onlookers, modulated allocation of attention.
We hypothesized that such empathic reactivity may arise
even when empathy-triggering stimuli are not explicitly
perceived. To explore this issue, reactions to being sublimi-
nally exposed to faces in images were tested, in terms of
how painful or pleasant touches on those faces affect the
affective state of the onlooker.
Various methods have been developed to assess the
affective processing under conditions in which ‘invis-
ible’ stimuli are presented. The continuous flash suppres-
sion (CFS) technique is a form of interocular suppres-
sion, wherein a visual stimulus presented to one eye is
suppressed from awareness (Tsuchiya and Koch 2005;
Tsuchiya et al. 2006). CFS consists in presenting con-
tinuously flashing (at 10 Hz) high-contrast images to the
dominant eye, while a stationary image is presented to the
other. The higher perceptual saliency of the dynamic movie
suppresses awareness of the image presented to the non-
dominant eye. As a result of this perceptual mismatch, only
the flashing stimuli are perceived, and suppression of the
stationary stimulus can be long lasting. CFS is considered
to be a robust and reliable technique, used in psychophysi-
cal and fMRI experiments (Jiang and He 2006; Pasley et al.
2004). For this reason, CFS was adopted here.
Research on implicit social cognition (Nosek et al. 2011)
has largely focused on developing tools to assess how our
emotions are influenced by affective-laden social stimuli.
One of these instruments is represented by the affective
misattribution procedure (AMP), which has shown that
pleasantness judgments of apparently neutral stimuli (e.g.,
Chinese pictograms) are affected by the brief presentation
(usually 100 ms) of affective-laden priming stimuli (e.g.,
insects vs. flowers, Payne et al. 2005; Payne et al. 2010).
The basic AMP was modified in the present study by
presenting priming stimuli (faces receiving either a pleas-
ant, painful or neutral hand touch) in a CFS paradigm
that allowed the stimuli to be kept below the threshold of
explicit awareness. It was predicted that the valence of the
suppressed priming stimuli would affect pleasantness judg-
ments accordingly. More specifically, the subliminal per-
ception of faces receiving painful touches would increase
the likelihood of rating the neutral stimuli (Chinese picto-
graphs) as unpleasant. The involvement of the sympathetic
branch of the autonomic nervous system during the implicit
perception of the suppressed stimuli was also explored by
measuring participants’ pupil size, the variation of which
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Exp Brain Res (2015) 233:2373–2382
seems to reflect affective processes (Partala and Surakka
2003). Furthermore, we tested whether autonomic reactiv-
ity correlated with pleasantness ratings and participants’
dispositional empathy, which was assessed through the
Interpersonal Reactivity Index (Davis 1980).
Based on the notion that individual differences in per-
sonality traits can modulate state-dependent sensorimotor
reactivity (Avenanti et al. 2009), also whether empathic
dispositions modulate the affective misattribution triggered
by affective-laden subliminal stimuli was tested. It was
hypothesized that people with high empathy traits would
display stronger implicit misattribution, contingent upon
subliminal presentation of empathogenic stimuli. Finding
this relationship would suggest that implicit misattribution
may index the ability of individuals to be affected by the
emotional states of others.
Method
Participants
Thirty-eight healthy volunteers (24 females; mean age
27.3  ± 3.1 SD), who were naïve as to the purposes of
the study, gave their written informed consent and were
paid €10 per hour for their participation. The study was
approved by the independent Ethics Committee of the
Santa Lucia Foundation (Scientific Institute for Research,
Hospitalization and Health Care) and was carried out in
accordance with the principles of the 1964 Declaration of
Helsinki.
Stimuli and procedure
Sixteen non-famous models (eight females) were asked to
pose with their eyes closed to avoid any distracting effects
of their gaze direction (Stein et al. 2011). For each model,
four photographs were taken depicting their face being
touched (neutral), slapped (painful) or caressed (pleasant)
by the right hand of another individual. Thus, the entire
dataset consisted of 192 images.
The image selection procedure was based on the rat-
ings of 24 participants (14 females, mean age 27.6 ± 3.2
SD), who did not take part in the main experiment. The
participants of the stimulus selection study were asked to
rate the images on a seven-point Likert scale for valence
(1  =  extremely unpleasant; 7 =  extremely pleasant) and
arousal (1 = not at all arousing; 7 = extremely arousing)
by means of an online survey (www.surveymonkey.com).
Stimuli were selected for: (1) highest valence for caressing
touch (pleasant image, M  = 5.6, 95 % CI [5.4, 5.8]), (2)
lowest valence for slapping touch (painful image, M = 2.1,
95 % CI [1.9, 2.3]), (3) middle values of valence for the
Exp Brain Res (2015) 233:2373–2382 2375
Fig. 1  Six examples of de-saturated pictures of two models (a female and a male) experiencing a a hand touching (neutral), b a slapping (pain-
ful) or c caressing (pleasant)
neutral touch (M = 4.2, 95 % CI [4.0, 4.4]), (4) high val-
ues of arousal for both caressing and slapping touches
(M = 4.5, 95 % CI [4.4, 4.7]; M = 4.6, 95 % CI [4.3, 4.8],
respectively), (5) low arousal values for neutral touch
(M  = 2.9, 95 % CI [2.7, 3.2], statistical significances for
all comparisons p < .05). In this way, positive and negative
images were matched on arousal ratings to ensure that any
differences across prime conditions were driven by valence.
Based on the above criteria, three images for each condi-
tion were obtained from each of the eight models (four
females), summing to 24 priming stimuli for each condi-
tion (painful, pleasant and neutral touches), and a total of
72 trials. All face borders were faded into background of
the pictures in order to decrease the contrast. This was done
to reduce the probability of supraliminal detection of the
priming stimuli (Fig. 1).
The position of the head was matched within and across
all image sets (Gobbini et al. 2013). All images were modi-
fied using Adobe Photoshop, for equal sizing (1024 × 768
pixels) and matching of brightness and contrast.
The experiment was performed in a dark and quiet
room. Participants were seated in front of a monitor screen
at a distance of approximately 72 cm, with a chin support
to provide a stable head position, eye-level with the center
of the screen.
The experimental procedure included both a sublimi-
nal task and supraliminal task. The supraliminal task was
presented second, to prompt implicit perception and to
minimize the ‘breakthrough’ effects. Indeed, occasionally,
primes can appear briefly, especially if it is a known or a
meaningful image such as a face. This can interfere with
the requirement to be unaware of the stimuli. Therefore,
the contrast level of the primes was adequately adjusted
to maximize the chances of complete suppression. In both
tasks, each trial started with a black central fixation cross
(0.4° × 0.4°, Fig. 2).
The dynamic mask was presented in order to suppress
the affective-laden videos and consisted of a de-saturated
red video, made of high-contrast neutral faces segmented
into 128 × 128 pixel squares, randomly rearranged and
rapidly (10 Hz) flashing (Fig. 2a). Participants viewed the
stimuli through red-cyan anaglyph glasses that filtered the
images, so that each eye could see only one image. The
central fixation cross was also shown during the entire
video presentation to facilitate stable convergence of the
two eyes’ images.
Previous studies have combined the CFS implicit affec-
tive paradigm with an affective misattribution procedure
(AMP) task (Almeida et al. 2013; Murphy and Zajonc
1993). The AMP task consists of presenting either a posi-
tive or negative prime (subliminal stimuli) for durations
that are too brief to induce conscious awareness, followed
by a neutral target (e.g., an unfamiliar Chinese pictogram,
presented for 150 ms). This experimental procedure relies
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Fig. 2  Experimental procedure. Both tasks started with a fixation
cross on the center of the screen. a Subliminal task: videos con-
sisted of a cyan picture and a dynamic red mask, randomly rear-
ranged and flashing at 10 Hz. The red–cyan anaglyph glasses, worn
on considering ratings of the neutral target as an indirect
measure of implicit attitudes. Rather than briefly presenting
a prime, the CFS technique (see above) was used to keep
the prime (painful, neutral or pleasant touch) inaccessible
to aware perception for longer. Participants were instructed
to focus their attention on the pictogram for 150 ms, which
was followed by the on-screen presentation of the choice
regarding the pleasantness of the Chinese pictograph. Spe-
cifically, participants were instructed to compare the target
to an ideal average Chinese character and indicate their
response by pressing the appropriate key on the computer
keyboard. (Choice 1: The Chinese pictograph was pleasant/
unpleasant).
Following previous studies (Murphy and Zajonc 1993;
Payne et al. 2005), each pictograph was paired with a prime
picture. Seventy-two different Chinese characters were
used as targets and presented to each participant follow-
ing a randomized order controlled by in-house MATLAB
software. In order to assess indirectly whether the primes
were explicitly perceived, participants were asked to report
on which side the suppressed stimulus was presented:
left or right of the fixation cross (Choice 2: ‘The priming
appeared on the Left/Right’). Moreover, if participants
correctly reported on which side the suppressed stimulus
appeared, they were asked to report whether any objects or
parts of objects stood out from the mask (Choice 3: ‘I have
perceived the priming Consciously/Unconsciously’), even
if they were not able to verbally recognize them. The tri-
als where even partial explicit stimulus detection occurred
were excluded from the analysis (4 % of the total trials).
During the inter-trial interval (range 1000–2000 ms; mean
1500 ms), only the fixation cross was presented.
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Exp Brain Res (2015) 233:2373–2382
by the observer, filtered the images, so that each eye could only see
one image; b supraliminal task: the same de-saturated image was pre-
sented to both eyes. In this condition stimuli were perceived explic-
itly, in spite of the glasses (color figure online)
Supraliminal task: In this task (Fig. 2b), i.e., the con-
trol session, the same de-saturated picture was presented to
both eyes (duration 500 ms). The absence of a flickering
mask made the prime stimuli completely visible. As in the
subliminal task, subjects were asked to judge the pleasant-
ness of Chinese pictographs after the image presentation.
Subjects were instructed not to let the images influence
their responses.
Stimuli were generated and presented by the Cogent
Toolbox (Cogent, www.vislab.ucl.ac.uk/Cogent/) for MAT-
LAB (MathWorks, Natick, MA, USA) on a monitor with a
refresh rate of 60 Hz. The presentation order of the images
depicting the three conditions (neutral, painful and pleas-
ant) was randomized across subjects in both tasks.
Measures
As an index of AMP, the percentage of trials in which par-
ticipants judged the pictographs as pleasant was computed.
Eye position and movements were recorded by an infra-
red eye tracker system (ASL Eye Track 6000, sample rate
of 50 Hz) based on the corneal reflection from the infra-
red light source. The participants’ pupil diameter was also
monitored in each trial and sampled every 20 ms. The base-
line was calculated as the mean diameter of the first eight
data points (160 ms) at the start of each trial, coherently
with the smoothing applied on the data points. This average
was then subtracted from each pupil diameter of that trial
(raw data). Finally, an eight-point moving unweighted aver-
age was applied to smooth the data (Azevedo et al. 2012).
To assess trait empathy, three subscales of the Ital-
ian version of the Interpersonal Reactivity Index (IRI,
Exp Brain Res (2015) 233:2373–2382 2377

Davis 1980) were administered: (1) empathic concern

(EC), which taps into emotional reactivity and measures
the affective dimension of empathy, (2) perspective taking
(PT), which refers to the tendency to spontaneously adopt
the psychological point of view of others, measuring cog-
nitive aspects of empathy and (3) personal distress (PD),
which assesses self-oriented anxiety when experiencing
others in distress.
The questionnaires were administered at the beginning
or end of the experiment in a counterbalanced order across
participants.

Results

AMP: Six subjects who explicitly perceived the priming

stimulus in more than 25 % of trials were removed from the
analysis. The AMP score was computed as the percentage
of pleasant ratings for the Chinese pictographs in each con-
dition (painful, neutral and pleasant). Scores falling above
or below two standard deviations from the mean of the con-
dition were removed. The average percentage of pleasant
judgments (Table S1) was then entered in a 2 × 3 repeated-
measures analysis of variance (ANOVA) with task (sub-
liminal vs. supraliminal) and the suppressed prime images
condition (painful, neutral, pleasant touches) as within-sub-
ject factors (Fig. 3).
The Cohen’s d statistic, which is an effect size meas-
ure, was also computed. The within-subject effect size was
calculated using the adapted formula, where the mean dif-
ference is divided by its standard deviation (Cohen 1992;
Morris and DeShon 2002).
The analysis showed that the presence of the prime
image influences the pleasantness ratings of the neutral
Chinese pictographs (F2,56 = 16.784, p < .0001, η2 = .38).
Neither the main effect of the task nor the two-way interac-
tion reached statistical significance (F1,28 = .768, p = .388,
η2 = .03; F2,56 = .330, p = .720, η2 = .01, respectively).
This result was followed up by a set of Bonferroni-cor-
rected pairwise comparisons, which showed that the aver-
age ‘like’ ratings given in each condition differed signifi-
cantly from each other at ps <.029 (Table 1 shows means
with 95 % confidence intervals).
Since the main interest was the effect of the affective
reactivity to unaware percept, another repeated-meas-
ures ANOVA was run, only in the subliminal condition,
which confirmed the main effect of the prime stimuli
(F2,58 = 9.530, p < .0001, η2 = .35). In this case, the Bon-
ferroni-corrected pairwise comparisons showed a statistical
difference in the AMP-averaged scores between the pain-
ful condition (M  = 48.6, 95 % CI [43.4, 53.8]) and both
the neutral (M = 55.9, 95 % CI [50.7, 61.1], t29 = −3.087,
p  = .013, Cohen’s d  = .52) and the pleasant conditions
Fig. 3  Results of the subliminal task. Repeated-measures ANOVA
means of AMP scores (implicit attitudes) expressed in percentage as a
function of condition (painful, neutral or pleasant facial expressions).
Means of each subject are shown with light gray curves. *p < .05;
**p < .005
Table 1  Average percentage of pleasant ratings of the neutral target
for each condition
Prime conditions
Painful Neutral Pleasant
47.6 [42.5, 52.6] 53.1 [48.8, 57.3] 58.2 [54.1, 62.4]
n = 38 for all means. Numbers in brackets are 95 % confidence inter-
vals of each mean
(M = 58.8, 95 % CI [53.9, 63.7], t29 = −4.464, p < .001,
Cohen’s d  = .76), which in turn did not differ from one
another (t29 = −1.111, p = .827, Cohen’s d = .20).
The analysis of the supraliminal perception revealed
a significant main effect of the type of stimulus (neutral,
painful and pleasant) (F2,58 = 5.400, p = .007, η2 = .14).
Post hoc analysis, performed using Bonferroni-corrected
paired t tests, showed significantly higher ‘like’ ratings in
the pleasant condition than in the neutral and painful condi-
tions (ps <.017). On the contrary, the neutral and painful
explicit primes did not differ from one another (p = .919).
The percentage of correct responses in detecting the
position of the prime provided an index of whether par-
ticipants had implicitly detected the suppressed prime
images, differentially in the different conditions. The aver-
age percentage of position detection was then entered in a
one-way repeated-measures ANOVA with the suppressed
prime images condition (painful, neutral and pleasant)
as a within-subject factor. The analysis of variance of the

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Fig. 4  Regression test showing
indirect measure (AMP sensi-
tivity) as a function of direct
measure (position detection)
sensitivity. The scatter plot
shows the data for each subject
(n = 29). The fitted linear
regression function has been
estimated
mean percentage of the correct position detection did not
reveal any statistical difference between the conditions
(F2,58 = .265, p = .768, η2 = .009).
Furthermore, the signal detection theory (Green and
Swets 1966) was used to assess the degree to which partici-
pants were able to detect the signal (the affective stimulus)
in the subliminal condition. To this aim, assuming a two-
alternative forced-choice (2-AFC) which involves a forced
choice between two responses based on a presented stimu-
lus, D′ was computed for the spatial detection task in each
condition (painful, pleasant and neutral). The Ds′ were
entered in a one-way repeated-measures ANOVA with the
suppressed prime images condition (painful, neutral and
pleasant) as a within-subject factor. No significant effect
was found (F2,58 = . 938, p = .359, η2 = .031).
To tease apart the influence of explicit perception on
the changes in Chinese pictograph pleasantness induced
by the priming stimulus, the (Greenwald et al. 1995) logic
was adopted. It was reasoned that the sensitivity in detect-
ing the position of the prime (without identifying it) could
be considered as a direct measure of implicit stimuli pro-
cessing ([Ddirect
′ ]), while the Chinese pictograph ‘judgment’
could be considered as an indirect measure. More specifi-
cally, for the [Ddirect
′ ] computation, the coherent response
with respect to the priming stimulus as ‘correct responses,’
i.e., ‘dislike’ judgment on the Chinese pictograph in cor-
respondence to the painful condition and ‘incorrect’ as the
incongruent rating, i.e., ‘dislike’ judgment after a pleasant
prime. Thus, the [Ddirect
′ ] measure was used as a depend-
ent variable and the [Ddirect
′ ] as the predictor in a regression
analysis. If the intercept was shown to be statistically above
zero when accounting for the direct measure, it could be
said that the indirect measure effect could not be explained
entirely by the explicit perception of the stimulus (Green-
wald et al. 1995).
Since it was found that the pleasant and neutral prim-
ing effects did not differ at the subliminal level, the analysis
was applied only to the pleasant and painful conditions. The
pleasant stimuli were chosen because arousal is controlled
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Exp Brain Res (2015) 233:2373–2382
for, regarding the neutral condition. Finally, the pleasant-
ness ratings differed significantly from chance (t29 = 3.685,
p = .001). Coherent with predictions, it was found that the
intercept term of the dependent variable (AMP measure
sensitivity) was significantly greater than zero (t28 = 6.702,
p < .001), whereas the slope of the direct measure was not
different from zero (β = −.084, t = −4.51, p = .655). This
linear regression analysis of the relationship between the
signal detection sensitivity indices for direct and indirect
measures (Fig. 4) demonstrates that implicit cognition (the
priming effect) is independent from explicit cognition con-
cerning the detection of the stimulus position (Greenwald
et al. 1995).
Scan paths and pupillary reactivity
Two areas of interest (AOI) were drawn to delimit the left
and right side of the screen respecting the fixation cross
(Left and Right AOIs). Only a central rectangle (subtend-
ing beyond two horizontal visual angles) around the fixa-
tion cross has been excluded. The number of fixations that
occurred in each AOI (Glascher and Adolphs 2003) was
then assessed. An index was created, subtracting from the
number of fixations falling on the side of the screen where
the stimulus was presented (congruent), and the number of
fixations occurring on the opposite AOI (incongruent), for
each of the three conditions. A one-way repeated-measures
ANOVA was then run on this index. It was considered that,
if participants were completely unaware of the suppressed
stimuli’s occurrence, the number of fixations falling in each
of the two screen windows should be equal overall. Results
confirm this assumption, since the number of fixations did
not differ across conditions (F2,60 = .48, p = .57, η2 = .02).
Moreover, to test whether differential autonomic reactiv-
ity was triggered by the different suppressed primes, data
from an assessment of pupil dilation were divided into two
time windows: early and late, according to the time point.
Each time point was compared with the previous through
paired t testing (Azevedo et al. 2012). This analysis showed
Exp Brain Res (2015) 233:2373–2382 2379

larger autonomic reactivity from 800 ms after stimuli onset

onwards (all ps <.001, Bonferroni-corrected for the number
of time points).
A one-way repeated-measures ANOVA on pupil dila-
tion with the suppressed priming condition as a factor,
focused on the late window (last 600 ms), was performed.
No significant effect was found (F2,62  = .152, p  = .820,
η2 = .005).
In order to check whether pupil dilation was related to
the AMP, the two measures were correlated. Since the neu-
tral and pleasure conditions did not differ significantly in
the subliminal phase, the following analyses focused only
Fig. 5  Scatter plot with regression line fit showing the relationship
on the pleasant and painful conditions, coherently with between the empathic trait, measured by the empathic concern sub-
what was done in the AMP phase. Finally, the AMP meas- scale of the IRI, and pupil diameter during the implicit presentation
ures were mean centered in order to better interpret results. of painful faces with respect to the pleasant priming
Correlation analyses (Pearson’s r) showed a trend toward
a negative relationship between the autonomic response
and the affective misattribution caused by the occurrence This analysis allowed for an exploration of the extent
of the painful (vs. pleasant) suppressed primes (r = −.36, to which trait empathy is accounted for by pupil dila-
p = .08). tion during the painful (vs. pleasant) subliminal stimuli
This suggests that the more the participants’ autonomic presentation.
system was engaged by a painful compared with a pleasant The backward regression revealed that EC significantly
stimulus, the less they liked the Chinese pictograms when predicted pupil dilation (β = .54, p = .004), accounting for
preceded by a subliminal painful prime. nearly 30 % of the variance (F1,28 = 10.155, p = .004).
Thus, participants with higher affective empathy tended
Questionnaires to have a stronger autonomic reaction to the painful com-
pared to the pleasant stimuli (Fig. 5).
Means for each questionnaire are shown in Table S2 in the
Supplemental Material available online. A backward mul-
tiple regression analysis with the three measured empathic Discussion
traits and autonomic reactivity in subliminal painful ver-
sus pleasant or neutral stimuli condition was performed This study demonstrated that implicitly seeing a person
(Table 2). receiving painful, neutral or pleasant touches can elicit an
affectively congruent response in the onlooker. This effect
is indexed by likeability ratings of a neutral target, which
turn out to be lower following the subliminal presentation
Table 2  Summary of backward regression analysis for variables pre- of painful facial expressions compared with pleasant and
dicting trait empathy
neutral expressions. That the effect of AMP was found with
Variable B SE B Beta F both subliminal and visible stimuli is in keeping with previ-
ous studies (Murphy and Zajonc 1993; Payne et al. 2005).
Step 1 4.829*
A completely novel result is that even in the implicit
 EC .238 .072 .551**
perception CFS condition, both categories of suppressed
 PT −.131 .079 −.275
stimuli (pleasant and painful) influenced the likeability rat-
 PD .065 .074 .148
ings. This may contradict previous findings showing that
Step 2 6.913**
only negative primes can affect the observers’ responses
 EC .247 .071 .572**
in strong masking paradigms (Almeida et al. 2013). Inter-
 PT .133 .079 −.281
estingly, the Almeida’s et al. (2013) explanation of selec-
Step 3 10.155**
tive effect of negative primes relied on the possibility that
 EC .235 .074 .545**
under CFS, the affective content is processed by subcorti-
Multiple regression analysis, R  = .24, for Step 1; R2 = .23 for Step 2;
2 cal regions, e.g., the superior colliculus and pulvinar nuclei.
R2 = .21 for Step 3 These link the retina to the amygdale and handle threat
EC empathic concern, PT perspective taking, PD personal distress signals (LeDoux 2003; Tamietto et al. 2012). In contrast,
* p < .05; ** p < .005 present results show that empathy for pleasure also exerts

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some influence on the way in which people react to the
environment. In fact, in our study, the pleasantness rat-
ings differed significantly from chance level (50 %). For
this reason, a point of merit of here might be the evidence
that the face-preferring ventral temporal stream is not com-
pletely disrupted during CFS. One possible way of explain-
ing why the modulatory effect of pleasurable priming
stimuli was found in this study but not in Almeida’s et al’s
(2013), may depend on participants’ shorter exposure to the
masked stimuli (1400 vs. 200 ms, respectively). Since neg-
ative stimuli (i.e., anger) are connected to a faster braking
suppression under CFS (Yang et al. 2007), it is not surpris-
ing that pleasantness requires more time to be processed.
A further possible explanation for this seeming discrepancy
may be based upon the longer time allotted to participants
to make the like versus dislike choice toward pictographs
(2000 vs. 150 ms). Indeed, global affective reactions are
generally more immediate and less under voluntary control
(Murphy and Zajonc 1993).
Studies indicate that inducing changes of arousal states
through subliminal stimuli could have greater effects on
affective misattribution (e.g., Murphy and Zajonc 1993).
One possible mechanism for this seemingly counterin-
tuitive effect is that being aware of the source of arousal
may allow one to implement down regulation mechanisms
(Schachter and Singer 1962).
In keeping with previous studies (e.g., Murphy and
Zajonc 1993), the data demonstrate that the emotional con-
tent influenced responses regardless of awareness. Also
demonstrated is that it is almost impossible to avoid the
priming influence, both during subliminal and supraliminal
images presentations (Murphy and Zajonc 1993). Payne
et al. (2005) found an effect also when the prime picture
was entirely visible to the subject for 1500 ms. Tellingly,
the misattribution effect induced by supraliminal, long-
lasting stimuli was not statistically different from when
the prime presentation lasted only 75 ms. It is important to
emphasize that the sparse and ambiguous qualities of the
target pictograph may be key for the above results. Indeed,
as participants had only 150 ms to judge the pictographs, it
is unlikely that they would have enough resources to down
regulate the evoked emotion (Payne et al. 2005). A similar
effect might have occurred in this study where, in spite of
the explicit instruction to ignore the primes, pictograph rat-
ings were influenced by the type of prime in both the sub-
liminal and supraliminal presentation conditions.
In addition to the behavioral evidence, autonomic
reactivity shows that subliminally presented facial
expressions predicts the behavioral outcome of affec-
tive misattribution, triggered by the implicitly processed
primes. Specifically, the more the participants were
implicitly aroused (as indexed by pupillary dilation)
by the display of a face receiving a slap, the less likely
13
Exp Brain Res (2015) 233:2373–2382
they were to judge the following Chinese pictograph as
pleasant. Importantly, pupil reactivity as a function of the
subliminal exposure to painful versus neutral and pleas-
ant stimuli is predicted by EC (but not by the other IRI
subscales). This suggests that such empathic reactivity is
modulated by particular individual dispositions toward
affective empathy. This result militates in favor of data
suggesting dispositional empathy plays a role in the reac-
tion to pain in others (Avenanti et al. 2009). Crucially,
this effect is present whether or not the pain is explic-
itly perceived by the onlooker. Results did not show dif-
ferences in pupil dilation across conditions. Neverthe-
less, a strong negative association was reported between
the autonomic system activity (pupil diameter) and the
AMP effect. As expected, the greater influence of the
negative prime, manifested through lower likeability rat-
ings relative to pleasant stimuli, corresponds to stronger
pupil reactivity. Furthermore, empathic concern seems
to linearly predict pupil dilation occurring for the pain-
ful facial expression condition as opposed to the pleasant
condition. Such a result is in line with previous studies
(Bradley et al. 2008; Partala and Surakka 2003), showing
that greater affective empathy is associated with a larger
autonomic (sympathetic) response.
Allowing that it has been clearly demonstrated that pupil
diameter increases for highly arousing stimuli, existing data
about the relationship between valence and pupil reactiv-
ity are controversial. Studies of unconscious perception of
stimuli in patients with phenomenal blindness due to uni-
lateral destruction of the visual cortex found greater pupil
responses to fearful than happy bodies and faces (Tamietto
and de Gelder 2009). This effect suggests that fear is more
effective in inducing an arousal response.
However, it has also been suggested that the increase in
pupil diameter is always present when processing emotion-
ally engaging, supraliminal stimuli, regardless of hedonic
valence (Bradley et al. 2008). That a strong general effect
of negative or positive subliminal primes was not found
may be accounted for by a variety of factors including the
experimental sample or the strength of the primes. Impor-
tantly, however, differences in autonomic reactivity to the
painful versus pleasant stimuli were predicted by EC. This
result suggests that people with high empathic traits are
more aroused by the exposure to painful stimuli, even if
they are presented subliminally.
Since the diameter of the pupil is generally affected
by changes in illumination, color and movement, it is in
principle possible that flickering stimuli influences pupil
response. It is worth noting, however, that finding differ-
ences depending on the priming condition should at least
partially rule out mere flickering effects and that the gen-
eral level of brightness was stable during the entire video
presentation.
Exp Brain Res (2015) 233:2373–2382 2381
A possible limitation of the present study deserves dis-
cussion. First, the paradigm does not allow us to directly
test whether the AMP finding can be due to empathic reac-
tivity per se. It is in principle possible that the affective
misattribution effect is at least partially due to the mere
valence of the prime (painful = negative, pleasant = posi-
tive). Secondly, there is no correlation between AMP and
EC. Therefore, a direct role of empathic personality traits
on the behavioral-dependent variable cannot be demon-
strated. On the other hand, although the behavioral-depend-
ent variable does not seem to be related to empathic dis-
position (measured by the EC), the physiological variable
(i.e., pupil dilation) does. This finding provides preliminary
evidence in favor of involuntary empathic reactivity to the
perception of pain and pleasure in others. Future studies on
the neural systems underpinning the processes herein inves-
tigated are warranted, in order to unveil the possible link
between the AMP effect driven by exposure to suppressed
painful (vs. pleasant and neutral) stimuli and empathic
reactivity. It is worth noting that studies on the neural
mechanisms involved in this implicit process could help
in disentangling the emotional aspect of painful and pleas-
ant stimuli perception, from a more sophisticated affective
reaction related to empathy. Neuroimaging studies sug-
gest that observation of painful stimuli may induce differ-
ent patterns of brain activity within the network coding the
empathic response. For example, the affective-motivational
and the sensorimotor components of empathy for pain
seem associated with insular and cingulate cortices (Payne
et al. 2005) and with the precentral and postcentral cortices
(Avenanti et al. 2005), respectively. Therefore, it would be
interesting to assess how these areas are influenced by the
subliminal perception of stimuli depicting others experi-
encing pain or pleasure. It would also be potentially impor-
tant to explore the link between subliminal perception and
the ability to empathize, in individuals with deficits in such
ability, for example, people on the autistic spectrum or who
have alexithymia (Bird et al. 2010). Thus, future studies
could be aimed at exploring, in neurotypical and autistic
people, whether different nodes of the empathic or emo-
tional network are recruited by painful and pleasant social
versus nonsocial stimuli presented subliminally.
Acknowledgments  This work was funded by the EU Informa-
tion and Communication Technologies Grant (VERE Project, FP7-
ICT-2009-5, Prot. Num. 257695) and the Italian Ministry of Health
(Grant RF-2010-2312912).
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