Emotional primes modulate the responses to others' pain: an ERP study.

Abstract

Previous event-related potential (ERP) and brain imaging studies have suggested observer responses to others' pain are modulated by various bottom-up and top-down factors, including emotional primes. However, the temporal dynamics underlying the impact of emotional primes on responses to others' pain remains poorly understood. In the present study, we explored effects of negative, neutral, and positive emotional priming stimuli on behavioral and cortical responses to visual depictions of others in pain. ERPs were recorded from 20 healthy adults, who were presented with painful and non-painful target pictures following observation of negative, neutral, and positive emotional priming pictures. ERP analyses revealed that relative to non-painful pictures, differential P3 amplitudes for painful pictures were larger followed by negative primes than either neutral or positive primes. There were no significant differential P3 amplitudes for painful pictures relative to non-painful pictures were found followed neutral and positive emotional primes. These results suggest that negative emotional primes strengthen observers' attention toward others' pain. These results support the threat value of pain hypothesis.

Full text

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Exp Brain Res (2012) 220: 277–286
DOI 10.1007/s00221-012-3136-2




Emotional primes modulate the responses to others’ pain:
an ERP study


Jing Meng • Li Hu • Lin Shen • Zhou Yang •
Hong Chen • Xiting Huang • Todd Jackson




Received: 21 November 2011 /Accepted: 23 May 2012/ Published online: 14 June 2012
Springer-Verlag 2012


Abstract Previous event-related potential (ERP) and
brain imaging studies have suggested observer responses to
others‟ pain are modulated by various bottom-up and top-
down factors, including emotional primes. However, the
temporal dynamics underlying the impact of emotional
primes on responses to others‟ pain remains poorly
understood. In the present study, we explored effects of
negative, neutral, and positive emotional priming stimuli
on behavioral and cortical responses to visual depictions of
others in pain. ERPs were recorded from 20 healthy adults,
who were presented with painful and non-painful target
pictures following observation of negative, neutral, and
positive emotional priming pictures. ERP analyses revealed
that relative to non-painful pictures, differential P3
amplitudes for painful pictures were larger followed by
negative primes than either neutral or positive primes.
There were no significant differential P3 amplitudes for


J. Meng • L. Hu • Z. Yang
Key Laboratory of Cognition & Personality,
Faculty of of Psychological Science, Southwest University, Beibei,
Chongqing 400715, China

L. Shen
College of Mathematics Science, Chonqing Normal University,
Chongqing 400715 , China

H. Chen • X. Huang • T. Jackson ()
Key Laboratory of Cognition & Personality,
Faculty of Psychological Science, Southwest University,
Chongqing 400715, China
H. Chen
e-mail: chenhg@swu.edu.cn
X. Huang
e-mail: xthuang@swu.edu.cn
T. Jackson
e-mail: tjackson173@hotmail.com

painful pictures relative to non-painful pictures were found
followed neutral and positive emotional primes. These
results suggest that negative emotional primes strengthen
observers‟ attention towards others‟ pain. These results
support the threat value of pain hypothesis.


Keywords Pain • Emotion • Priming •
Event-related potentials (ERP) • P3


Introduction

Pain serves as a signal warning us of possible or actual
tissue damage resulting from exposure to noxious stimuli
(e.g., Bonica 1987). Similarly, when observing injury or
pain in another, perceptions of alarm and danger may be
activated to promote escape or other protective responses
(Yamada and Decety 2009; Eccleston and Crombez 1999;
Williams 2002; Decety 2011; Ibáñez et al. 2011). The
“threat value of pain hypothesis” (TVPH) posits observing
others‟ pain is potentially threatening to observers, and
activates an early, threat-detection system instead of
evoking automatic empathic responses (Ibáñez et al. 2011).
According to motivational priming theory, emotions can
be explicated in terms of two motive systems: the appétit-
ive system which is prototypically expressed by behavioral
approach and the aversive system which is prototypically
expressed by behavioral escape and avoidance (Lang et al.
1990). This hypothesis posits that if the appetitive or
aversive motivational system is activated by prime stimuli,
responses to targets that follow are congruent with the
engaged motivational system is more strongly activated
(Lang 1995). Based on this premise, negative emotional
primes (e.g., unpleasant music, negative emotional pic-
tures) increase subjective perceptions of pain while

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278 Exp Brain Res (2012) 220: 277–286

and positive emotional valences (“Appendix”). Arousal
level (negative: 4.725 ± 0.39, neutral: 4.726 ± 0.35,
positive: 4.717 ± 0.36; F(2, 57) = 0.004, P = 0.997), image
size, definition, and luminance level of pictures were
matched across priming conditions.
Target stimuli consisted of 120 digital color pictures
showing people‟s hands, forearms, or feet in painful or
non-painful situations (60 pictures each). All situations
depicted familiar events that occasionally happen in
everyday life. Examples of painful pictures included a hand
cut by a knife and a foot stabbed by a syringe. Non-painful
target pictures corresponded to those shown in “painful”
depictions without any nociceptive component. Examples
of non-painful pictures included a hand using a knife to cut
vegetables and a foot touched by a pencil. Target pictures
were shot from angles that promoted first-person
perspectives. Luminance, contrast, and color were matched
between painful and non-painful pictures, as illustrated in
Fig. 1. Based on 9-point Likert scales, pain intensity
(1 = no sensation, 4 = pain threshold, 9 = unbearable
pain), emotional valence (1 = very unhappy, 9 = very
happy), and arousal (1 = extremely peaceful, 9 = extre-
mely exciting) of painful and non-painful pictures were
assessed by 70 undergraduate students. In addition,
subjective reports of implied motion were assessed by 49
undergraduate students based on a 9-point Likert scale
between “1 = no motion at all” and “9 = extremely rapid
motion”. The descriptive statistics of painful and non-
painful pictures in each dimension were summarized in
Table 1. All target pictures were the same in three emotional
priming conditions.
Each picture (including prime and target pictures) was
9 × 6.76 cm (width × height) and 100 pixels per inch.


positive emotional primes may reduce pain perception
(see Villemure and Bushnell 2002).
A burgeoning literature has used pictures or video clips
with depictions of human body parts in pain (e.g., Ibáñez et
al. 2011; Minio-Paluello et al. 2006; Decety et al. 2010;
Fan and Han 2008; Avenanti et al. 2010) or painful facial
expressions (e.g., Yamada and Decety 2009; Han et al.
2009) to explore potential influences and mechanisms
associated with observer responses to others‟ pain.
However, few of these studies have examined the impact of
emotional primes on responses to others‟ pain. In one
subliminal affective priming study, participants were
presented with faces expressing varying intensities of pain
and happiness after first
subliminally-presented “likable” and “dislikable” affective
words. The authors reported a greater tendency to judge
pain in other people following negative words than neutral
or positive words (Yamada and Decety 2009). The authors
concluded that this pattern reflected the activation of a
primitive threat-defensive system that enhanced observers‟
vigilance for pain stimuli.
To date, no event-related potentials (ERP) research has
evaluated temporal dynamic features of cortical responses
for others‟ pain following exposure to emotional pictures
having different valences. In the current study, we explored
the impact of the negative, neutral, and positive emotional
primes on brain responses to depictions of injury and pain in
others using ERP. Based on the TVPH and motivational
priming theory, we hypothesized exposure to negative
emotional priming stimuli
threat-detection system and result in greater allocation of
mental resources to depictions of others‟ pain than would
positive or neutral primes.


Materials and methods

Participants

Twenty healthy undergraduate students (10 men, 10
women) from Southwest University (SWU), Chongqing,
China, participated in the study as paid volunteers. All
participants were right-handed, aged between 18-23 years
(M = 21.4 years, SD = 1.23 years), had normal/cor-
rected-to-normal vision, and an absence of neurological
conditions. This study was approved by the SWU research
ethics committee.

Stimuli

Priming stimuli were emotional pictures from the Interna-
tional Affective Picture System (IAPS) (Lang et al. 1999),
and included 20 pictures each depicting negative, neutral,


being presented with
would activate the


Fig. 1 Illustration of the painful and non-painful pictures. The left
panel shows examples of painful pictures. The right panel shows
examples of non-painful pictures.

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Exp Brain Res (2012) 220: 277–286 279




Participants were seated in an acoustically isolated room at a
viewing distance of 100 cm from the computer screen. The
horizontal and vertical visual angles were both below 6°.

Experimental procedure

All participants signed an informed consent form before
participating in the experiment. Prior to the experiment, all
participants were told that the computer screen would
present a series of prime stimuli (negative, neutral, and
positive emotional pictures) and target stimuli (painful and
non-painful pictures), and they were instructed to respond
with a key-press only to target stimuli. Specifically, in each
trial, participants were instructed to judge subjective pain
intensities in response to painful and non-painful target
stimuli using 9-point Likert scale (1 = no sensation,
4 = pain threshold, and 9 = unbearable pain).
In order to rule out the ERP contribution of prime stimuli,
two kinds of trials (Prime+Target trials and Prime-only
trials) were used. In Prime+Target trials, a priming stim-
ulus was presented for 200 ms, followed by a 200 ms blank
screen prior to the onset of a target stimulus. The target
stimulus remained on screen until a response was made, or
for a 3 s maximum. In Prime-only trials, which were served
as the baseline condition, a prime stimulus was presented
for 200 ms, followed by a blank screen for 1,000 ms.





Participants were instructed to simply wait for the next trial.
The inter-trial interval was randomly varied between 1,000
ms and 2,000 ms (Fig. 2). The number of Prime-only trials
(180) was equal to the number of trials for painful (180) and
non-painful (180) target conditions. Electrophysiological
activities recorded from Prime-only trials were subtracted
from ERPs recorded from Prime+Target trials. Results of
these subtractions were considered to reflect pure electro-
physiological activity related to target stimuli and were
labeled “target-related activity”.
The experiment was comprised of three blocks. For
each block, 180 trials were delivered. The sequence of
Prime +Target trials and Prime-only trials were pseudo-
random, with presentation of the prime-only condition
never occurring on three consecutive trials.

ERP recording

Electroencephalography (EEG) data were recorded from
64 scalp sites using tin electrodes mounted in an elastic cap
(brain Products). The electrode at the right mastoid was
used as a reference, and electrode on the medial frontal
aspect was used as a ground electrode. Vertical electro-
oculograms (EOGs) were recorded supra and infra-orbi-
tally at the left eye. Horizontal EOGs were recorded as the
left versus right orbital rim. EEG and EOG activity was

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280 Exp Brain Res (2012) 220: 277–286




amplified with a DC~100Hz bandpass and continuously
sampled at 500Hz. All electrode impedances were main-
tained below 5 kΩ.

Data analysis

Behavioral data - pain intensity ratings and reaction times
(RTs) - were calculated for each participant in each
condition. Two within-participants factors--Prime type
(negative, neutral, positive) and Target type (painful,
non-painful)--were included for two-way repeated-
measures analysis of variance (ANOVA).
EEG data were pre-processed and analyzed using Matlab
7.0 (MathWorks, US) and EEGLAB toolbox (Delorme and
Makeig 2004). EEG signals passed through an off-line
0.01-30 Hz band-pass filter. Pre-prime (200 ms) and post-
prime (1,200 ms) segments were extracted from the EEG,
and the whole epoch was baseline-corrected by the pre-
prime interval. For each participant, averaged waveforms for
Prime-only trials were subtracted from averaged waveforms
of Prime+Target trials, resulting in corrected target–related
ERPs not confounded by Prime-related activity (Fig. 3).
Obtained single-trial ERP waveforms were then epoched from
pre-target (200 ms) to post-target (800 ms), and baseline-
corrected using a 200 ms pre-target interval.
For the purposes of selecting electrodes for further data
analysis, a preliminary point-by-point two-way repeated-
measure ANOVA (Boly et al. 2011) was conducted with
Prime type and Target type as repeated factors for each
electrode. The criteria for inclusion of electrodes for further
analysis were as follows: (1) statistical differences were
considered significant at p < 0.001 (uncorrected), and (2) the
significant area included at least three adjacent significant
electrodes. In addition, as considering the lateralization, the
following electrodes were included for further statistical
analysis: FC3, C3, CP3, P3 (four left sites); FCz, Cz,
CPz, Pz (four midline sites); FC4, C4, CP4, P4 (four
right sites). Mean amplitude values were obtained from
each grand averaged peak. A four-way repeated-measures
ANOVA was conducted for each component. The four
ANOVA factors were Prime type, Target type, Region (left,
midline, right), and Electrode. Degrees of freedom for the
F-ratio were corrected according to the Greenhouse-Geisser
method. Statistical differences were considered significant at
p < 0.05. The post-hoc analyses were corrected according to
Bonferroni correction with considered significant at p < 0.01.
To investigate whether electrophysiological activity
elicited by painful/non-painful target stimuli were related to
pain intensity when participants were primed with different
emotional pictures, Spearman rank correlation was calcu-
lated between pain intensity ratings and ERP amplitudes at
various scalp regions. Correlations were considered sig-
nificant at p < 0.05.


Fig. 3 Illustration of ERP waves of Prime + Target trials, Prime-
only trials, and the corrected Target-related ERP waves in each
condition at Cz.

Results

Behavioral data

Mean pain intensity ratings and RTs in all conditions are
summarized in Table 2. The ANOVA for pain intensity
showed a significant main effect for Target type
[F(1,19) = 417.91, p < 0.001], indicating painful pictures
were rated as significantly more painful than non-painful
pictures. No other main effect or interaction was found for
pain intensity.
The ANOVA for RT revealed a significant main effect
for Prime type [F(2,38) = 8.47, p = 0.001]; post hoc
analysis indicated that RTs were significantly longer for
targets followed by positive emotional prime than negative
[F(1,19) = 17.04, p = 0.001] and neutral [F(1,19) = 9.44,
p = 0.006] emotional primes. The main effect of Target
type [F(1,19) = 9.95, p = 0.005] indicated RTs were

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Exp Brain Res (2012) 220: 277–286 281



significantly longer for painful pictures than for non-
painful pictures. Notably, these main effects were qualified
by a significant Prime type × Target type interaction
[F(2,38) = 17.02, p < 0.001], indicating RT differences
between painful and non-painful pictures were larger fol-
lowing negative emotional primes than following neutral
[F(1,19) = 8.87, p = 0.008] or positive [F(1,19) = 28.53,
p < 0.001] emotional primes.

Electrophysiological data

Scalp topographies and ERP average waveforms related to
painful and non-painful targets in each emotional priming
condition are shown in Figure 4. In the three emotional
priming conditions, target-related ERPs displayed a neg-
ative component from 90 ms to 150 ms (N1) over the
frontal-central area, a positive wave from 200 to 250 ms
(P2) over the central area, and a negative deflection from
230 to 300 ms (N2) over the frontal region, followed by a
positive component from 350 ms to 450 ms (P3) and a late
latency positive deflection from 500 to 700 ms (LPC) over
the posterior parietal area.
N1 A main effect was found for Target type
[F(1,19) = 6.64, p = 0.018] in this time window. Relative
to non-painful pictures, painful pictures elicited a more
positive ERP deflection. The effect for Region was
also significant [F(2, 38) = 17.32, p < 0.001]; post hoc
analysis revealed ERP amplitudes in the midline region
(-2.04 ± 0.34 µV) were more negative than in the left
[1.58 ± 0.31µV; F(1,19) = 21.92, p < 0.001] and right
[1.61 ± 0.30µV; F(1,19) = 35.159, p < 0.001] regions,
which did not differ from one another [F(1,19) = 0.072,
p = 0.792].
P2 The main effect for Target type [F(1,19) = 7.50,
p = 0.013] indicated that painful pictures elicited a more
positive ERP component than non-painful pictures. Post
hoc analyses of the significant Region effect [F(2,
38) = 6.91, p = 0.004] indicated ERP amplitudes in the
midline region (-2.34 ± 0.96 µV) were more negative
than in the left [-1.16 ± 0.76µV; F(1,19) = 8.60,
p = 0.009] and right [-1.22 ± 0.71µV; F(1,19) = 9.73,
p = 0.006] regions, which did not differ from each other
[F(1,19) = 0.037, p = 0.850].





N2 The main effect for Target type [F(1,19) = 4.97,
p = 0.038] indicated painful pictures elicited smaller
amplitudes than did non-painful pictures. The significant
main effect for Prime type [F(2,38) = 3.59, p = 0.039]
indicated N2 amplitudes for target stimuli were larger
in the negative emotional priming condition (－0.39 ±
0.90 µV) than in the neutral emotional priming condition
[-1.15 ± 0.83 µV; F(1,19) = 7.70, p = 0.012] but not
the positive priming condition [－0.08 ± 0.93 µV; F(1,19)
= 0.71, p = 0.407]. The significant effect for Region [F(2,
38) = 14.98, p < 0.001] revealed more negative ERP
amplitudes in the midline region (－0.68 ± 0.85 µV) than
the left [0.09 ± 0.80µV; F(1,19) = 19.05, p < 0.001] or
right [0.07 ± 0.81µV; F(1,19) = 22.27, p < 0.001]
regions, which did not differ from one another [F(1,19)
= 0.021, p = 0.886].
P3 The main effect of Target type was significant
[F(1,19) = 32.86, p < 0.001]; painful pictures elicited
larger amplitudes than did non-painful pictures. The effect
for Region [F(2, 38) = 8.13, p = 0.002] indicated ERP
amplitudes in the midline region (3.27 ± 1.35 µV) were
smaller than those in left [3.76 ± 1.31µV; F(1,19) =
11.65, p = 0.003] and right [3.94 ± 1.26µV; F(1,19) =
13.36, p = 0.002] regions, which did not differ from one
another [F(1,19) = 0.92, p = 0.349]. The main effect for
Electrode was significant [F(3, 57) = 17.60, p < 0.001].
Table 2 shows descriptive statistics.
More notably, the effect for Prime type × Target type
was significant [F(2, 38) = 4.07, p = 0.033] as well as the
Prime type × Target type × Region interaction [F(4,
76) = 28.29, p = 0.043]. Further analysis revealed inter-
actions between Prime Type and Target type were signif-
icant for midline [F(2, 28) = 4.32, p = 0.026] and left
[F(2, 28) = 4.97, p = 0.019] regions, but not the right
region [F(2, 28) = 2.72, p = 0.086]. The P3 difference
between painful and non-painful pictures in the negative
emotional priming condition (midiline: －3.39 ± 0.58µV;
left: －2.75 ± 0.45µV) were significantly larger than that in
the neutral [midiline: －1.16 ± 0.57µV, F(1, 19) = 6.42,
p = 0.020; left: －0.50 ± 0.62µV, F(1, 19) = 6.99, p =
0.016] and positive [midiline: －2.01 ± 0.52µV, F(1, 19)
= 5.03, p = 0.037; left: －1.65 ± 0.50µV, F(1, 19) =
4.37, p = 0.049] emotional priming conditions. Conversely,

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282 Exp Brain Res (2012) 220: 277–286



































P3 differences between painful and non-painful pictures in
neutral and positive emotional priming conditions was not
significant different [midline: F(1, 19) = 1.19, p = 0.289;
left: F(1, 19) = 2.50, p = 0.130]. Figure 5 illustrates
differential ERP waves between painful and non-painful
pictures in each emotional priming condition.

Correlation between subjective pain intensity and ERP
amplitudes

Averaged amplitudes at P3 time window recorded at Cz
were significantly correlated with subjective pain intensity
ratings of painful pictures when preceded by negative












































emotional primes (r = 0.275, p = 0.043). In contrast, the
correlation between ERP amplitudes and subjective
pain intensity ratings was not significant in the neutral
(r = 0.091, p = 0.289) and positive (r = 0.138, p =
0.198) emotional priming conditions.


Discussion

By analyzing participant responses to painful and non-
painful visual depictions of others following exposure to
negative, neutral, and positive emotional primes, we
demonstrated that emotional primes modulated observers‟

Fig. 4 Painful (left panel) and
non-painful (right panel) target-
related ERP waveforms in
negative, neutral, and positive
emotional priming conditions
recorded at FCz, Cz, CPz, and
Pz. At the bottom, voltage scalp
maps of all peaks in each
condition are shown.

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Exp Brain Res (2012) 220: 277–286 283


Fig. 5 Top: ERP difference waves between painful and non-painful
pictures in the negative (black line), neutral (blue line), and positive
(red line) emotional priming conditions at Cz and CPz. Right-bottom:


behavioral and cortical responses to pictures of others‟ pain.
Larger differential RTs and P3 amplitudes in left-central
areas for painful pictures relative to non-painful pictures
were found following negative emotional primes than
neutral and positive emotional primes. As such, findings
appeared to support predictions based on the TVPH and
motivational priming theory.

The implication of ERP waves

Similar to previous ERP studies (e.g., Decety et al. 2010;
Fan and Han 2008; Han et al. 2008), differential cortical
responses were detected between painful and non-painful
portrayals of others in a broad time window from 90 ms to
700 ms. Relative to non-painful pictures, painful pictures
elicited a more positive shift of the ERP waves in these
time windows, which may have been influenced by asso-
ciations with sensory and emotional aspects of pain. First,
because painful stimuli are more novel and important for
survival than non-painful stimuli, they should elicit more
immediate attentional capture and receive more extensive
evaluations (Fan and Han 2008). Second, because there is
an attentional bias for emotionally negative events (Del-
planque et al. 2004; Delplanque et al. 2005; Ito et al. 1998),
more attentional resources should be recruited for painful
than non-painful stimuli. In addition, as the participants
were instructed to judge pain intensity, painful pictures
may be associated with more variability or differentiation
than would non-painful depictions which less relevant to such
evaluations.
Using ERPs to examine temporal dynamics of emotional
primes of cortical responses towards others‟ pain, this study
focused mainly on interactions between Prime type and
Target type. Relative to non-painful pictures, P3

Topographical maps of voltage amplitudes for the painful and non-
painful ERP difference wave in the negative, neutral, and positive
emotional priming conditions at P3 time windows.


amplitudes for painful pictures were larger following
negative emotional primes than neutral and positive emo-
tional primes. Previous ERP studies indicate that task rel-
evance, motivational significance, arousal level and the
influence of these factors on mental resource allocation are
major determinations of P3 processes (Olofsson et al.
2008). In addition, the P3 component over the posterior
parietal area has been linked to late cognitive stimulus
evaluation, which is, to a certain degree, independent of
response selection and execution (Olofsson et al. 2008;
McCarthy and Donchin 1981). Thus, larger differential P3
amplitudes may reflect more extensive evaluations and
mental resources applied to painful pictures following
negative emotional primes than neutral or positive emo-
tional cues. Previous exposure to negative emotional
primes may strengthen observers‟ processing of painful
depictions of others.
Furthermore, recent ERP studies have differentiated
early bottom-up and later top-down stages of processing for
others‟ pain wherein the P3 is considered to be a marker of
top-down attention of the late modulation process (Fan and
Han 2008; Ibáñez et al. 2011). Thus, in our study, emo-
tional primes mainly modulated the top-down controlled
component rather than the relatively automatic bottom-up
component.

The implication of scalp distributions

In accordance with previous ERP studies (e.g., Decety
et al. 2010; Fan and Han 2008; Han et al. 2008), ERP
results evidenced a frontal-central early negative compo-
nent (N1), a positive deflection (P2) over the central area, a
negative component (N2) over the frontal region, and late
latency positive deflections (P3 and LPC) over the

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284 Exp Brain Res (2012) 220: 277–286



posterior parietal area, painful pictures elicited more
positive deflection than non-painful pictures.
More importantly, the late controlled process of detec-
tion of painful stimuli modulated by previous exposure to
emotional cues was salient only over the left-central
regions. Previous studies have indicated affective and
sensory components of processing pain-related information
are coded in different neural nodes in the pain matrix (e.g.,
Rainville 2002). Moreover, this asymmetric activation to
affective and sensory aspects of others‟ pain between the
two cerebral hemispheres has been observed (Minio-Palu-
ello et al. 2006). The cortical right hemisphere is consid-
ered to specialize in emotional processing (see Demaree
et al. 2005) based on fMRI studies reporting several right
brain areas (e.g., right ACC, right AI) involvement in
affective aspects of observing others‟ pain (Morrison et al.
2004; Jackson et al. 2006). However, the left hemisphere
may contribute to processing sensory features of painful
depictions. TMS studies report that the left somatomotor
cortex selectively encodes sensory qualities of others‟ pain
and is strongly inhibited during observation of others‟ pain
(Avenanti et al. 2005; Avenanti et al. 2006). Moreover,
such inhibition correlates with subjective judgments of
sensory rather than emotional pain components (Minio-
Paluello et al. 2006). In the current study, participants were
instructed to consider only sensory qualities of painful or
non-painful pictures (i.e., to judge pain intensities of target
pictures), so the significantly enlarged P3 amplitudes for
painful pictures following negative emotional primes
observed in left-central regions may suggest more evalua-
tion and mental resource allocation to the sensory aspect of
others‟ pain following negative emotional exposure.


General discussion

This study showed that in comparison to neutral and
positive emotional primes, exposure to negative emotional
primes predicted strengthened cortical responses to others‟
pain. The motivational priming hypothesis (Lang 1995)
posits that negative emotions strengthen negative sensory
experiences because the aversive system is activated. This
hypothesis has been supported by studies indicating nega-
tive emotional primes decrease first-hand pain intensity
threshold ratings and increase sensitivity to pain stimuli
(Meagher et al. 2001; Godinho et al. 2006; Kirwilliam and
Derbyshire 2008). Our findings that negative emotional
primes strengthened late cortical responses to painful
depictions of other people was also in accordance with
behavioral research indicating that compared to positive or
neutral emotional cues negative primes are associated with
a more lenient threshold of pain in others (Yamada and
Decety 2009).



According to the TVPH (Ibáñez et al. 2011), painful
depictions of other people are a potential threat to
observers, observing painful pictures should activate
the aversive system, thus, the presentation of negative
priming pictures may have primarily activated the aversive
system which, in turn, contributed to the assignment of more
attentional resources and enhanced P3 amplitudes after
observation depictions of others‟ pain. Since participants
were instructed only to consider the sensory aspect of
painful depictions in the present study, responses to sen-
sory-discriminative dimensions of pain in others‟ may have
been amplified by negative emotional primes. However, it
is highly plausible that pictures rated as very painful on a
single item intensity scale would also be appraised as
highly unpleasant on a single item “unpleasantness” scale.
Hence, further research is required to clarify whether per-
ceptions of affective aspects of painful stimuli contribute to
or explain effects of affective primes.
Alternatively, some studies posited that observing
pictures or videoclips of other people in pain may elicit
empathic concern for mental states of others and foster pro-
social responses to support them (Decety and Grezes 2006;
Decety and Lamm 2006). When observing others‟ pain,
the activation of anterior cingulate cortex and insula is also
correlated positively with individual empathy scores
(Singer et al. 2004) and predicts the subsequent costly helping
behavior (Hein et al. 2010). If select behavioral approach
tendencies characteristic of empathic concern predomi-
nated in this study, then it might be expected that cortical
responses to others‟ pain would be strengthened following
positive emotional primes rather than the negative emo-
tional primes. However, there was no significant difference
in cortical responses following neutral and positive emo-
tional primes in the current study. Thus, future studies are
needed to disentangle and clarify how „„threat value‟‟ and
empathic concern processes influence perceptions of oth-
ers‟ pain
Although both the negative priming pictures and the
painful target pictures have negative emotional valences,
ERP results could not be explained by an affective con-
gruency effect. In general, targets are categorized more
quickly and have smaller P3 amplitudes when they are
affectively congruent with primes relative to affectively
incongruent with primes (Bartholow et al. 2009; Ito et al.
1998; Friedman et al. 2001). In this study, painful target
stimuli elicited larger P3 waves following negative primes.
This result was not consistent with affective congruency
effect.
Because emotional priming stimuli used in this research
were selected from the International Affective Picture
System (Lang et al. 2001) and were matched for arousal
levels, observed effects were more likely a function of
emotional valence variations than arousal level differences

Page 9

Exp Brain Res (2012) 220: 277–286 285



in primes. Indeed, previous ERP studies have indicated that
independent of arousal level, emotional valence levels can
influence P3 amplitude (Yuan et al. 2007; Rozenkrants and
Polich 2008).
In summary, the current study showed differential
responses to painful depictions of others occurred when
participants were primed with negative, neutral, and posi-
tive emotional pictures. Relative to non-painful pictures,
late cortical responses to painful pictures were larger fol-
lowing negative emotional primes than neutral and positive
emotional primes. However, this effect was isolated to the
P3 time window in the left-central regions. As such, results
provided some support for extending the threat value of
pain hypothesis as an approach to understanding the
detection of others‟ pain.


Acknowledgements This research was supported by the Funda-
mental Research Funds for the Central Universities (SWU1109084)
and the Key Discipline Fund of the National 211 Project, China
Education Ministry (NSKD08020).


Appendix Identification numbers of IAPS pictures
presented in this study

Negative: 2,276, 2,750, 2,900, 3,160, 3,181, 3,300, 9,007,
9,041, 9,265, 9,280, 9,290, 9,320, 9,330, 9,331, 9,340,
9,415, 9,430, 9,530, 9,561, 9,830.
Neutral: 1,112, 1,945, 2,220, 2,351, 3,5502, 4,001, 4,003,
4,004, 4,005, 4,230, 4,240, 4,279, 4,550, 4,561, 4,613,
4,631, 5,395, 7,211, 7,820, 8,232.
Positive: 1,440, 1,460, 1,590, 1,600, 1,721, 2,310, 2,352,
2,650, 4,610, 5,600, 5,660, 5,820, 5,982, 7,260, 7,430,
7,470, 7,480, 7,580, 8,350, 8,540.



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