Neuropsychologia 81 (2016) 207–218
Contents lists available at ScienceDirect
Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
Neural correlates of processing “self-conscious” vs. “basic” emotions
Michael Gilead a,n,1, Maayan Katzir b,1, Tal Eyal b, Nira Liberman a
a
b
School of Psychological Sciences, Tel-Aviv University, Ramat-Aviv, Tel-Aviv 69978, Israel
Department of Psychology, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel
art ic l e i nf o
a b s t r a c t
Article history:
Received 17 June 2015
Received in revised form
9 December 2015
Accepted 14 December 2015
Available online 18 December 2015
Self-conscious emotions are prevalent in our daily lives and play an important role in both normal and
pathological behavior. Despite their immense significance, the neural substrates that are involved in the
processing of such emotions are surprisingly under-studied. In light of this, we conducted an fMRI study
in which participants thought of various personal events which elicited feelings of negative and positive
self-conscious (i.e., guilt, pride) or basic (i.e., anger, joy) emotions. We performed a conjunction analysis
to investigate the neural correlates associated with processing events that are related to self-conscious
vs. basic emotions, irrespective of valence. The results show that processing self-conscious emotions
resulted in activation within frontal areas associated with self-processing and self-control, namely, the
mPFC extending to the dACC, and within the lateral-dorsal prefrontal cortex. Processing basic emotions
resulted in activation throughout relatively phylogenetically-ancient regions of the cortex, namely in
visual and tactile processing areas and in the insular cortex. Furthermore, self-conscious emotions differentially activated the mPFC such that the negative self-conscious emotion (guilt) was associated with a
more dorsal activation, and the positive self-conscious emotion (pride) was associated with a more
ventral activation. We discuss how these results shed light on the nature of mental representations and
neural systems involved in self-reflective and affective processing.
& 2015 Elsevier Ltd. All rights reserved.
Keywords:
Self
Emotion
mPFC
dACC
dlPFC
Self-control
Pride
Guilt: Anger
Joy
1. Introduction
The self-conscious emotions acknowledged in contemporary
psychological theories are guilt, shame, embarrassment, and pride
(Tangney, 2003; Tracy and Robins, 2004). These emotions are
prevalent in daily life (Hofmann et al., 2013), and are involved in
various psychopathologies. For example, exaggerated feelings of
guilt play a dominant role in depression (e.g., O’Connor et al.,
2002), shame is crucially involved in social-avoidance (e.g., Lutwak
and Ferrari, 1997), and pride is a dominant emotion in narcissism
(Tracy et al., 2009). In light of this, furthering our understanding of
the psychological and biological mechanisms that play a role in the
processing of self-conscious emotions is an immensely important
and clinically significant task.
Despite the involvement of self-conscious emotions in pathological
and normal behavior, only a handful of neuroimaging studies have
directly addressed this important topic. The goal of the current study
was, accordingly, to investigate the neural correlates of processing
positive and negative self-conscious vs. non-self-conscious emotions,
sometimes referred to as “basic emotions” (Tracy and Robins, 2007).
n
Corresponding author.
E-mail address: [email protected] (M. Gilead).
1
Equal contribution.
http://dx.doi.org/10.1016/j.neuropsychologia.2015.12.009
0028-3932/& 2015 Elsevier Ltd. All rights reserved.
How might the neural substrates that are involved in processing self-conscious emotions differ from those involved in processing non-self-conscious emotions? To begin addressing this
question we will turn to carefully examine the psychological
processes that distinguish basic and self-conscious emotions, and
then review neural literature that addressed related questions.
1.1. Psychological differences between self-conscious and basic
emotions
Self-conscious emotions differ from non-self-conscious (i.e.,
basic) emotions in several respects. In what follows we discuss two
of the main differences. The most straight-forward distinction
between self-conscious and basic emotions pertains to the object
that is at the center of the emotional appraisal: for self-conscious
emotions, this object is the self, for basic emotions it is not. Selfconscious emotions involve self-awareness, self-evaluation, and a
consideration of how the self is being evaluated by others, to a
greater extent than basic emotions (Baldwin and Baccus, 2004;
Leary, 2007; Tracy and Robins, 2004; Tangney, 2003). In light
of this, one might predict that processing self-conscious
emotions will activate neural substrates involved in self-reflection
(e.g., Kelley et al., 2002) and mentalizing (e.g., Mitchell et al.,
2005; Denny et al., 2012), namely, the medial Pre-Frontal Cortex
(mPFC).
208
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
The second main distinction pertains to the goals associated
with the emotion; self-conscious emotions are associated with
high-order goals, and play an important role in adaptive social
behavior such as moral behavior (Tangney et al., 2007), cooperation (Dorfman et al., 2014), and self-regulation (Eyal and Fishbach,
2010; Giner-Sorolla, 2001). To illustrate the latter, self-conscious
emotions are believed to direct behavior towards long-term goals,
and hence, play an important role in regulating self-control conflicts, i.e., conflicts between a long-term goal that offers large yet
delayed benefits and a short-term temptation that offers smaller
yet immediate benefits (Williams and DeSteno, 2008; ZemackRugar et al., 2007). Consistent with this line of theorizing, recent
research has shown that self-conscious emotions such as pride and
guilt are associated with adherence to long-term goals and the
exertion of self-control, whereas emotions such as joy, excitement,
sadness and frustration are associated with pursuit of short-term
goals and succumbing to temptations (Eyal and Fishbach, 2010;
Giner-Sorolla, 2001; Hofmann and Fisher, 2012; Mukhopadhyay
and Johar, 2007; Williams and DeSteno, 2008; Zemack-Rugar et al.,
2007). For example, in recent studies, we have found that compared to a positive emotion that is not self-conscious (i.e., joy),
priming pride improved self-control (Katzir et al., 2010, see also
Katzir et al., 2015). Considering that the brain areas commonly
associated with conflict resolution are the dorsal Anterior Cingulate Cortex (dACC) and lateral-dorsal prefrontal cortex (e.g., Botvinick et al., 2004; Cole and Schneider, 2007; Hare et al., 2009;
MacDonald et al., 2000; Ochsner et al., 2012; Kerns et al., 2004),
the processing of self-conscious (vs. basic) emotions may be expected to recruit these regions.
1.2 Past research on neural substrates of self-conscious emotions
Several past studies investigated the neural substrates of a specific self-conscious emotion. These studies often (but not always)
reported activations in the medial prefrontal cortex: Shin et al.
(2000) compared the processing of guilt-evoking vs. neutral scenarios and found activation within the anterior temporal poles,
anterior cingulate gyrus, and left anterior insular cortex/inferior
frontal gyrus. Moll et al. (2007) conducted a study on moral emotions that included guilt and anger, but did not report the results of
a comparison between the two. Kedia et al. (2008) conducted a
study on moral emotions in which they compared guilt-evoking
trials to anger evoking trials and to compassion-evoking trials. Their
results showed that emotional (vs. non-emotional) trials activated
the dorsal mPFC, insula, amygdala, and the temporo-parietal junction—but there were no significant differences in activation between the different emotion categories. Basile et al. (2011) compared guilt to sadness and anger and found greater activation
within the mPFC and the cingulate gyrus in the guilt condition.
Somerville et al. (2013) induced self-evaluation by making participants believe they are being watched by a peer through a camera,
and discovered heightened engagement of the mPFC in adolescence
(relative to childhood) that persists into adulthood. Finally, Fourie
et al. (2014) induced feelings of guilt in the context of race relations,
and found activations in the ACC, anterior insula, the mPFC, posterior cingulate cortex, and the precuneus.
Studies that focused on the neural substrates of a single positive self-conscious emotion did not observe activations in the
medial prefrontal cortex. Takahashi et al. (2008) compared the
neural correlates of processing pride as compared to joy, and
discovered that pride was associated with activation of two regions involved in mentalizing tasks (the superior temporal sulcus
and temporal poles) but not in the mPFC. Another study (SimonThomas et al., 2012) contrasted the processing of pride with
compassion, and discovered activation in the posterior cingulate
cortex.
The studies outlined above investigated a single self-conscious
emotion, and contrasted it with non-emotional states, or basic
emotions. Thus, these studies were not in a position to tap into the
correlates of self-conscious emotions over and above emotionspecific content. However, five previous studies looked at neural
correlates that are associated with more than one self-conscious
emotion. Once again, these studies often reported activations in
the mPFC: Wagner et al. (2011) investigated the unique neural
correlates of guilt processing as compared with two closely related
emotions, sadness and shame. They found that guilt was associated with greater activation of the mPFC as compared to sadness
and shame. Takahashi et al. (2004) compared feelings of guilt and
embarrassment to a non-emotional control; once again, they discovered activation in the mPFC as well as in the superior temporal
sulcus. Michl et al. (2014) replicated the paradigm from Takahashi
et al. (2004) but did not find mPFC activation for the guilt
condition. However, Burnett et al. (2009) compared guilt and
embarrassment to basic emotions (disgust and fear) and replicated
Takahashi et al.'s (2004) findings.
Importantly, all of these studies examined only negative emotions. In light of that, further research is still warranted in order to
fully capture the construct of self-conscious emotions, as it also
pertains to positive self-evaluation, namely, a sense of pride. The
importance of this point is further highlighted by the fact that
whereas negative self-conscious emotions often activated the
mPFC (e.g., Takahashi et al., 2004; Burnett et al. 2009; Wagner
et al., 2011), the two studies that examined the processing of pride
did not report activations within this region (Takahashi et al.,
2008; Simon-Thomas et al., 2012).
Two previous studies included within their design a positive and
a negative self-conscious emotion. However, they did not compare
self-conscious to non-self-conscious emotions: Roth et al. (2014)
compared the processing of a negative self-conscious emotion
(shame/guilt) to a positive self-conscious emotion (pride) and a
non-emotional control. Comparing self-conscious emotions vs. no
emotion (i.e., a condition in which participants waited for a distracting picture to appear) resulted in widespread activation across
the cortex. Comparing pride to guilt and shame resulted in greater
activation in widespread regions including the left superior frontal
gyrus, left ventral mPFC, middle and posterior cingulate cortex, the
inferior temporal gyrus, inferior parietal gyrus, the left caudate
body and left lateral thalamus. The reverse contrast (guilt and
shame vs. pride) did not result in significant differences. In Roth et
al.'s study, the focus of investigation was the processing of guilt as
compared to pride; in light of this, it did not include basic-emotion
conditions to allow researchers to distinguish between self-conscious and non-self-conscious affective processing. Zahn et al.
(2009) conducted a study on social-moral emotions wherein they
compared the processing of events that elicit the social emotions of
guilt, pride, gratitude and anger. Their results showed that participants’ reports of feeling pride during the task were correlated with
activity in the septum, and feelings of guilt were correlated with
activity in the subgenual ACC. When the researchers looked at the
neural activity during pride trials (vs. guilt, gratitude and anger)
they found activation in the vmPFC, the ventral tegmental area, and
the parahippocampal gyrus; there were no significantly stronger
activations for guilt (compared with pride, gratitude, and anger).
Similarly to Roth et al.'s (2014) study, in this study as well, the focus
of investigation was not self-conscious emotions, therefore, it did
not directly address the question of whether there are neural substrates that subserve self-conscious (but not basic) emotions, irrespective of the dimension of valence.
Thus, at the current stage of investigation, further work is
needed in order to uncover the neural substrates that subserve
self-conscious emotions—above and beyond emotion-specific and
valence-specific processes.
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
2. The current study
209
approved by the Institutional Review Board of the Sourasky
Medical Center, Tel-Aviv.
In order to investigate the neural correlates of processing
events that elicit positive and negative self-conscious emotions,
we chose four prototypes of self-conscious and basic emotions:
pride (self-conscious, positive), guilt (self-conscious, negative), joy
(basic, positive) and anger (basic, negative). Based on theoretical
and empirical distinctions between self-conscious and basic
emotions, we generated the following predictions and research
questions:
(i) Given past work (Eyal and Fishbach, 2010; Giner-Sorolla,
2001; Hofmann and Fisher, 2012; Katzir et al., 2010; Shimoni et al.,
2016; Williams and DeSteno, 2008; Zemack-Rugar et al., 2007) on
the role of self-conscious emotions in self-control, we predicted
that processing self-conscious emotions should activate areas related
to self-control, namely, the ACC and lateral-dorsal prefrontal cortex
(e.g., Botvinick et al., 2004; Cole and Schneider, 2007; Hare et al.,
2009; MacDonald et al., 2000; Ochsner et al., 2012; Kerns et al.,
2004).
(ii) Given the inconclusive neural findings reviewed above, we
were specifically interested to see whether both positive and negative self-conscious emotions activate the region previously implicated in self-referential processing, namely, the mPFC (e.g., Denny
et al., 2012; Mitchell et al., 2006).
Furthermore, we were interested in two exploratory hypotheses concerning activation within the mPFC: extant evidence
shows that the mPFC is divided into a dorsal region which is more
strongly activated in reflection upon others, and a ventral region
which is more strongly associated with self-reflection (Denny
et al., 2012; Mitchell et al., 2006). Consequently, as a secondary
goal of the current study, we wanted to see whether the specific
self-conscious emotions—i.e., guilt and pride—differentially rely
upon these two sub-regions. Additionally, past research shows
that the dorsal mPFC is involved both in thinking of future events
and recollection of the past (e.g., Addis et al., 2007) whereas the
ventral mPFC is more active when participants imagine (vs. remember) events (Addis et al., 2009). In light of this, as a secondary
goal of the current study, we were interested in whether activity
within this region differs when processing emotional events which
occurred in the past, as opposed to events that are imagined to
occur in the future.
2.1. Method
2.1.1. Participants
Twenty right-handed participants (14 women, average age 25.9
years, range 21–33 years) from Tel-Aviv University participated in
the experiment. They were all native Hebrew speakers, none had a
history of neurological or psychiatric disorders, and all had normal
or corrected-to normal vision. One participant was excluded from
the final analysis due to excessive motion. They gave written
consent prior to taking part in the experiment. The study was
2.1.2. Materials
We created the stimuli based upon a pre-test. First, based on
face validity, we compiled a list of 96 events (24 per emotion category) which we suspected might evoke a sense of guilt, pride,
anger, and joy. Each event was described in general terms and a
few examples of specific possible instantiations followed. For example: “Neglecting to speak to someone close for a long time (a
friend; parent; sibling)”.
These scenarios were rated by thirty-eight participants (33 females,
2 unknown, average age 23.11 years, range 19–26 years) who answered two questions concerning each item: (i) whether it is likely
that they would find themselves in the circumstance described in the
course of the next five years (by making a “yes”/“no” response); (ii)
whether such an event is typically associated with feelings of guilt,
pride, anger, joy or some other emotion (by selecting one of the five
options). Based upon participants’ responses we selected 16 events for
each emotion that were likely to occur, and were typically associated
with a specific emotion. Specifically, for each emotion category, we
selected stimuli such that across all items in the category: (i) more
than 90% of participants said it is likely that they would find themselves in these situations; (ii) at least 60% of participants categorized
the stimuli according to our designated classification.
Chi-squared tests indicated that participants classified guilt
stimuli as being associated with guilt more often than not, χ2
(1,38)¼4.90, p ¼.026; pride stimuli as being associated with pride
more often than not, χ2 (1,38)¼5.35, p ¼.020; anger stimuli as
being associated with anger more often than not, χ2 (1,38)¼5.35,
p¼ .020; joy stimuli as being associated with joy more often than
not, χ2 (1,38)¼26.34, p o.001 (Table 1).
The first pre-test was meant to help generate a set of events
that are common experiences for participants, and that participants label as being associated with one of the four emotions. In
order to make sure that the behavioral procedure (described below) elicits the corresponding emotion, we conducted a second
pre-test. Twenty-four participants (16 females, average age 25.00
years, range 21–30 years) performed the experimental procedure
with the exceptions that (1) they performed it individually in front
of a computer rather than inside the scanner, and therefore their
neural activation was not recorded, and (2) following each block of
the experimental procedure (i.e., a series of 4 questions from the
same emotion, see below) they provided four responses to indicate
the degree to which they feel the four emotions (anger, guilt, joy,
and pride) on a 5 point scale (1-low, 5-high).
The results indicated that the experimental procedure successfully elicited the target emotions. Specifically, participants reported feeling more intense pride following pride blocks than joy
blocks, F(1,23)¼34.00, po .001, ηp2 ¼ .60, and more intense joy
following joy blocks than pride blocks, F(1,23) ¼15.92, p o.001,
ηp2 ¼ .41. They also reported feeling more intense anger following
Table 1
Pre-test data – Average (across stimuli) of number of participants (out of 38) who reported that the stimulus elicits a given emotion. SDs in parentheses.
Stimulus classification
Reported emotion
Guilt
Guilt
Pride
Anger
Joy
24.5
0.12
0.125
0.18
Pride
(6.86)
(0.34)
(0.34)
(0.40)
0.5
24.81
0.18
0.12
(0.73)
(7.07)
(0.54)
(0.34)
Anger
Joy
1.18
0.18
24.81
0.06
0.56
8.56
0.18
32.87
(1.37)
(0.54)
(6.63)
(0.25)
Other
(0.81)
(6.61)
(0.40)
(4.22)
11.25
4.31
12.68
3.94
(6.78)
(3.77)
(6.52)
(4.75)
210
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
Table 2
Pre-test data – Average (across block type) of intensity ratings of each emotion
following the 4 types of emotion blocks (anger, guilt, joy, and pride). SEs in
parentheses.
Block type
Guilt
Anger
Pride
Joy
Intensity of affect
Guilt
Anger
Pride
Joy
2.98
1.71
1.57
1.53
2.23
2.88
1.69
1.58
2.49
2.36
3.97
3.26
2.77
2.77
3.95
4.42
(0.35)
(0.24)
(0.22)
(0.21)
(0.35)
(0.39)
(0.26)
(0.24)
(0.26)
(0.27)
(0.31)
(0.32)
(0.27)
(0.24)
(0.30)
(0.33)
anger blocks than guilt blocks, F(1,23) ¼16.46, p o.001, ηp2 ¼ .42,
and more intense guilt following guilt blocks than anger blocks, F
(1,23)¼52.08, p o.001, ηp2 ¼.69 (see Table 2).
We also wanted to make sure that differences between selfconscious and basic emotions do not reflect differences in the
degree of social interaction in the chosen eliciting events. To that
end, two independent judges coded the degree to which each of
the chosen 16 events entailed a social interaction on a 0–2 scale,
(0-“no social interaction”; 1-“might involve social interaction”; 2“definitely involves social interaction”). Inter-rater reliability was
high (r ¼ .87). The emotion category involving the least amount of
social interaction was guilt (M¼ 1.18), followed by joy (M¼1.37),
pride (M¼ 1.50), with anger being the most socially-interactive
emotion (M¼ 1.75). Thus, on average, ratings of social interaction
for self-conscious emotions (M¼1.34) were not higher than those
of basic emotions (M ¼1.56).
2.1.3. Behavioral procedure
Participants were carefully instructed and trained on the task
prior to entering the scanner. The training was repeated verbatim
inside the scanner. The items used for the training session were
taken from a different pool of sentences than the main task. Participants answered the emotion-eliciting questions by pressing a
key on a response box with their index and middle left hand fingers. Stimuli were presented with Presentation version 14.9
(Neurobehavioral Systems, CA, USA). Each question was presented
on screen for 6000 milliseconds.
The experiment consisted of two consecutive sessions, each
lasting 9 min and 14 s. We presented the stimuli in a blocked
design. Each block contained a series of 4 questions from the same
temporal perspective and emotion, and was succeeded by a 10
seconds fixation (Fig. 1). Each session contained 2 blocks from each
of the 8 conditions (created by crossing the 4 emotions with the
2 temporal perspectives). We fully-randomized the order of experimental blocks, and of stimuli in each block. In total, each
participant answered all 128 questions (16 questions from each of
the 8 block types).
In the actual experiment, we made participants recollect or
imagine the emotion-eliciting events by asking them whether it is
possible that each event would happen to them sometime in the
next-five years and whether they have experienced an event like
this sometime in the preceding five years. Participants were cued
before each block with the appropriate temporal perspective (future/past). On each experimental trial, participants saw the emotion eliciting statement (e.g., “Neglecting to speak to someone
close for a long time [a friend; parent; sibling]). On each experimental trial, participants responded whether the event happened
to them or is likely to occur by choosing “yes” or “no” buttons. The
list of stimuli contained 128 questions: 16 events per emotion
category 4 emotion types: guilt, pride, anger and joy) 2 temporal perspectives (past vs. future). The complete list of stimuli is
provided in Appendix A.
2.1.4. Imaging procedure
Whole-brain T2*-weighted EPI functional images were acquired
with a GE 3-T Signa Horizon LX 9.1 echo speed scanner (Milwaukee,
WI). 264 volumes were acquired (TR¼2000 ms, 200 mm FOV, 64 64
matrix, TE¼ 35, 35 pure axial slices, 3.15 3.15 3.5 mm3 voxel size,
no gap). Slices were collected in an interleaved order. At the beginning
of each scanning session, 5 additional volumes were acquired, to allow
for T1* equilibration (they were not included in the analysis). Before
the experiment, high-resolution anatomical images (SPGR; 1 mm sagittal slices) were obtained. Head motion was minimized by using
cushions arranged around each participant’s head, and by explicitly
guiding the participants prior to entering the scanner. Imaging data
were preprocessed and analyzed using SPM5 (Wellcome Department
of Cognitive Neurology, London). A slice-timing correction to the first
slice was performed followed by realignment of the images to the first
image. Next, data were spatially normalized to an EPI template based
upon the MNI305 stereotactic space. The images were then resampled
into 2-mm cubic voxels, and finally smoothed with an 8-mm FWHM
isotropic Gaussian kernel. The general linear model was used for statistical analyses. Eight regressors (one for each stimulus condition)
were used to model the effects of interest; each consisted of a boxcar
function convolved with a standard hemodynamic response function.
Two additional regressors were included in the model to account for
session-specific low-frequency effects. Based on our design parameters, SPM’s optimal high-pass filter cutoff was determined using
Design Magic high-pass filter optimization tool (developed by Matthijs
Vink; http://www.ni-utrecht.nl/downloads/d_magic) and was set at
272. We computed the second-level analyses (in which participants
were treated as random effects) using one-sample t-tests. Significant
regions of activation were identified using a threshold of po.001 with
a cluster size threshold of 74 voxels, corresponding to a threshold
Fig. 1. An example block (Self-conscious, Negative, Past). Example items are translated from Hebrew (complete list of stimuli available in Appendix A). The experiment
consisted of 8 block types (created by crossing the variables: Past/Future Self-conscious/Basic Positive/Negative). Each block contained four questions all of which
meant to elicit a specific emotion. Each question was presented for 6 s.
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
of po.05, corrected for multiple comparison, as assessed through
Monte Carlo simulations implemented in Matlab (Slotnick et al., 2003).
We ran 1000 iterations of the simulation using the pre-defined
parameters of our design, and the smoothness parameter as estimated
in SPM.
In order to investigate the neural correlates of self-conscious
and basic emotions, regardless of emotion-specific content, we
searched for regions that were activated for both positive and
negative emotions. The Self-conscious 4Basic emotions conjunction analysis (Guilt 4Anger)∩(Pride 4Joy) was implemented by
running the contrast of Guilt 4Anger (at a threshold of 0.031)
inclusively masked with the contrast of Pride 4Joy (at a threshold
of 0.031). Similarly, the Basic 4Self-conscious conjunction analysis
was implemented by running the contrast of Anger4Guilt inclusively masked with the contrast of Joy4 Pride, using the same
thresholds. Since both contrasts are orthogonal, with a cluster size
of 74 voxels, this analysis tests against the conjunction null at
p o.05, corrected.
2.2. Results
2.2.1. Behavioral results
Participants indicated that they have experienced or are likely
to experience the emotion-eliciting events on 93.82% of trials.
There were no significant differences in ratio of yes and no responses between the different emotions. There was no significant
difference in response latencies for negative self-conscious (guilt)
and negative basic (anger) emotion questions, F(1,18) ¼ 1.18,
p ¼.202. Participants responded more quickly to the positive-valence basic emotion questions (joy; M ¼2164 ms, SD ¼509 ms)
than to the positive self-conscious emotion questions (pride;
M ¼2312 ms, SD ¼453 ms), F(1,18) ¼ 6.94, p ¼.016,2 ηp2 ¼ .30. Participants also generally responded more quickly to positive
(M ¼2238 ms, SD ¼466 ms) compared to negative emotion questions (M¼ 2564 ms, SD ¼544 ms), F(1,18) ¼27.00, po .001, ηp2 ¼ .61.
Furthermore, there was a significant interaction between Temporal
Perspective and Emotion Type, F(1,18) ¼5.41, p ¼.030 (See Table 3),
such that participants responded more slowly to self-conscious
emotions than to basic emotions when thinking of the future, F(1,
18) ¼ 10.54, p ¼.004, ηp2 ¼.40, but not when thinking of the past, F
(1, 18) ¼1.96, p ¼.177. There were no other significant effects.
2.2.2. Imaging data
2.2.2.1. Temporal perspective. Temporal perspective did not have a
significant main effect, nor did it interact with any of the other
independent variables. Therefore, we collapsed all of our analyses
across this variable.
2.2.2.2. Self-conscious emotions (Guilt 4 Anger)∩(Pride 4Joy). As
predicted, processing self-conscious emotions activated frontal
regions associated with cognitive control: a region within the
mPFC extending to the dACC, and within a lateral-dorsal prefrontal
region (see Fig. 2 and Table 4).
2.2.2.3. Basic emotions (Anger 4Guilt)∩(Joy 4Pride). Processing
basic emotions activated regions associated with embodied experience, namely, regions associated with visual-spatial perception and imagery (left superior occipital gyrus and bilateral
2
The correlates of self-conscious and basic emotions were identified using
conjunction analyses which pin-pointed significant differences in neural activation
that were evident for both the positive and negative emotions. Because there were
no differences in response latencies for anger and guilt trials, the difference in
response latencies between joy and pride cannot account for our findings regarding
the neural correlates of self-conscious and basic emotions.
211
Table 3
Behavioral Results. RTs (SDs in parentheses) in milliseconds by Valence of emotion,
Emotion Type and Temporal Perspective.
Negative
Self-conscious
(Guilt)
Future 2635 (598)
Past
2571 (662)
Positive
Basic (Anger) Self-conscious
(Pride)
Basic (Joy)
2499 (556)
2550 (509)
2130 (475)
2197 (578)
2347 (499)
2277 (464)
parahippocampal gyrus) and somatosensation (right postcentral
gyrus). Furthermore, basic emotions activated a region of the left
insula, which was found in previous studies to be activated in
emotional processing and interoception (e.g., Stein et al., 2007;
Zaki et al., 2012) (see Fig. 2 and Table 4).
2.2.2.4. Guilt4 Other emotions. Guilt-evoking questions were associated with widespread activation throughout the cortex (most
prominently in the dorsomedial and lateral PFC) in the right lateral
orbitofrontal cortex and in subcortical regions (most prominently
in the caudate nucleus and thalamus) (see Fig. 3 and Table 4).
2.2.2.5. Pride4Other emotions. Pride-evoking questions were associated with activation of regions involved in self-referential
processing and reward, namely, the ventromedial prefrontal cortex
extending to the orbitofrontal cortex (see Fig. 3 and Table 4).
2.2.2.6. Anger4 Other emotions. Anger-evoking questions were
associated with activation of the left temporo-parietal junction
and superior temporal sulcus (see Fig. 3 and Table 4).
2.2.2.7. Joy4Other emotions. Joy-evoking questions were associated with activation of the bilateral superior occipital gyrus (see
Fig. 3 and Table 4).
2.2.2.8. Interpersonal 4Non-interpersonal emotions. Processing the
social emotions (i.e., anger, guilt, & pride) compared to non- social
emotions (i.e., joy) recruited regions involved in social-cognition,
namely the medial prefrontal cortex, precuneus and temporoparietal junction. Further activations included the cerebellum and
left lateral prefrontal cortex (see Table 4).
2.2.2.9. Valence. Similarly to previous behavioral and neural studies which have shown an asymmetry between positive and negative valence (Baumeister et al., 2001), we observed robust
and widespread activations throughout cortical and sub-cortical
regions associated with negative emotions, whereas positive
emotions were not associated with significant activation (see
Table 4).
2.2.2.10. ROI analysis. We defined as regions of interest the two
clusters associated with processing self-conscious emotions (the
mPFC extending to the ACC, and the lateral-dorsal prefrontal
cluster), and the five regions associated with processing basicemotions. We extracted parameter estimates from each ROI on a
subject-by-subject basis using MarsBaR v.042 (Brett et al., 2002).
We conducted a Valence (Negative, Positive) Type (Self-conscious, Basic) repeated measured ANOVA on the mean beta values
of each of the seven ROIs. None of the regions displayed an interaction of Valence and Type, max F(1,18) ¼1.26, p¼ .276. In the
mPFC, there was greater activity for self-conscious (vs. basic)
emotions, F(1,18) ¼15.32, p ¼.001, and for negative (vs. positive)
valence, F(1,18) ¼18.96, p o.001; In the left middle frontal gyrus,
there was greater activity for self-conscious (vs. basic) emotions, F
212
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
Fig. 2. Sagittal view of the brain showing neural activity associated with self-conscious and basic emotions. Activations are shown at a threshold of p o.05 (corrected). For
activation foci see Table 4.
(1,18) ¼16.88, p o.001, and for negative (vs. positive) valence, F
(1,18) ¼38.13, po .001.
In the left insula, there was greater activity for basic (vs. self-conscious) emotions, F(1,18)¼12.65, p¼.002, and for positive (vs. negative) valence, F(1,18)¼5.31, p¼ .034; In the left parahippocampal gyrus
there was greater activity for basic (vs. self-conscious) emotions, F
(1,18)¼15.62, po.001; In the right parahippocampal gyrus there was
greater activity for basic (vs. self-conscious) emotions, F(1,18)¼ 13.04,
p¼ .002; In the left superior occipital gyrus, there was greater activity
for basic (vs. self-conscious) emotions, F(1,18)¼10.40, p¼.005; In the
right postcentral gyrus there was greater activity for basic (vs. selfconscious) emotions, F(1,18)¼11.79, p¼.003. There were no other
significant differences.
negative emotions. Self-conscious emotions were associated with
activation within the mPFC extending to the dACC and within the
lateral-dorsal prefrontal cortex. We also observed that self-conscious emotions differentially activated regions within the mPFC
such that the negative self-conscious emotion (guilt) was associated with a dorsal activation, and the positive self-conscious
emotion (pride) was associated with activation of the ventral
mPFC. The cluster co-activated by both types of self-conscious
emotions was located somewhere in between the ventral and
dorsal sub-regions. We did not find significant activations associated with temporal perspective. Overall, we believe that these
results might shed light on the neural basis and phenomenology of
self-reflective and affective processing. We now turn to discuss
each of our main findings.
3. Discussion
3.1. Self-conscious emotions and self-regulation
In the present study participants thought of various personal
events which elicited feelings of self-conscious or basic positive or
As predicted, we found that processing of self-conscious emotion, regardless of their valence, activated the dACC and the
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
213
Table 4
Regions identified in the whole brain analysis. All activations are below a threshold of p o .001 and a cluster extent of 74 voxels (FWE-corrected, p o .05).
Contrast
Region
Coordinates
Self-consious 4Basic
Frontal
Significance level
x
y
z
Z-score
Voxels
L
Medial Prefrontal Cortex
Middle Frontal Gyrus
8
38
46
14
36
46
3.74
3.02
325
109
Occipital
Parietal
Insula
L
R
L
R
L
Parahippocampal Gyrus
Parahippocampal Gyrus
Superior Occipital gyrus
Postcentral Gyrus
Insula
28
14
46
64
50
38
50
80
16
6
24
6
32
30
8
3.63
2.46
3.08
3.01
2.72
434
146
199
279
89
Sub-lobar
Frontal
R
Caudate
Inferior Frontal Gyrus
Dorsomedial Prefrontal Cortex
Inferior Frontal Gyrus
Inferior Frontal Gyrus
Fusiform Gyrus
Precuneus
Lingual Gyrus
Inferior Semi-Lunar Lobule
Uvula
8
58
6
52
46
48
42
14
24
22
8
26
16
20
38
38
64
86
80
80
8
14
68
8
14
8
42
2
38
24
5.24
5.14
4.91
4.78
4.6
4.41
4.04
3.5
4.54
3.8
3545
769
2602
2278
220
207
782
113
209
238
Ventromedial Prefrontal Cortex
2
62
24
4.67
278
Basic 4Self-consious
Temporal
Guilt 4Other
Temporal
Parietal
Occipital
Cerebellum
L
R
L
L
R
L
R
Pride 4 Other
Frontal
Anger4 Other
Temporal
L
L
Temporo-Parietal Junction
Superior Temoral Sulcus
40
52
60
6
26
28
4.38
4.3
792
250
Occipital
R
L
Superior Occipital Gyrus
Superior Occipital Gyrus
40
36
84
86
32
36
4.69
3.71
215
125
Dorsomedial Prefrontal Cortex
Inferior Frontal Gyrus
Middle Frontal Gyrus
Middle Frontal Gyrus
Temporo-Parietal Junction
Precuneus
Inferior Semi-Lunar Lobule
Inferior Semi-Lunar Lobule
8
50
38
34
50
2
22
26
52
26
10
52
64
62
80
80
28
10
50
8
18
38
44
42
4.98
3.98
3.95
3.87
4.55
4.25
3.87
3.82
2894
611
572
87
1422
733
85
93
Middle Frontal Gyrus
Superior Frontal Gyrus
Inferior Frontal Gyrus
Middle Temporal Gyrus
Inferior Temporal Gyrus
Pyramis
42
2
42
50
52
20
10
40
30
64
8
86
52
52
18
20
28
32
5.27
5.21
4.99
5.17
4.76
4.82
3354
3970
691
2951
283
4571
Joy4Other
Social 4Non-social
Frontal
Temporal
Parietal
Cerebellum
Negative4 Postive
Frontal
Occipital
Temporal
Cerebellum
Positive4Negative
Non identified
L
L
L
L
L
R
L
R
L
L
L
lateral-dorsal prefrontal cortex. Much research shows that the
dACC and the lateral-dorsal prefrontal cortex are involved in effortful cognitive control (e.g., Cole and Schneider, 2007; Hare et al.,
2009; Ochsner et al., 2012). Specifically, it has been suggested that
the dACC is involved in monitoring cognitive conflict (e.g., Botvinick et al., 2004) and that lateral-dorsal regions are involved in
implementation of control over conflict (MacDonald et al., 2000).
The involvement of cognitive-control regions in the processing
of self-conscious emotions is consistent with the view according to
which the function of self-consciousness is to allow flexible and
complex control of behavior (e.g., Anderson, 1983). More specifically, self-conscious emotions can help us manage conflicts between phylogenetically-ancient hedonic value (the taste of burger
and fries), and phylogenetically-novel, socially-constructed values
(being thin, not hurting animals). Supporting this idea, recent
behavioral work suggests that both negative (Zemack-Rugar et al.,
2007) and positive (Eyal and Fishbach, 2010; Katzir et al., 2010;
Shimoni et al., 2016; Williams and DeSteno, 2008) self-conscious
emotions lead people to exert greater degrees of self-control. For
example, in recent studies, we (Katzir et al., 2010, 2015) have
shown that thinking of pride- (vs. joy-) evoking events facilitates
self-control, as evident in (1) more successful inhibition on an
anti-saccade task (performance on which is known to rely on the
dACC and lateral-dorsal prefrontal cortex, e.g., Klein et al., 2007;
Pierrot-Deseilligny et al., 2003), and (2) reduced congruency effect
on a switching task (reduced congruency effect indicates better
conflict resolution which is known to rely on the dACC and lateraldorsal prefrontal cortex, Kerns et al., 2004). Thus, the current work
joins this previous behavioral evidence in highlighting the role of
self-conscious emotions in heightened self-control.
The finding that self-conscious emotions, irrespective of valence, activate medial frontal regions is also consistent with extant
neuropsychological literature that examined the behavior of individuals with medial frontal cortex lesions (e.g., Sturm et al.,
214
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
Fig. 3. Sagittal view of the brain showing neural activity associated with specific emotions. Activations are shown at a threshold of p o .05 (corrected). For activation foci see
Table 4.
2013; Beer et al., 2003; 2006; Moll et al., 2011; Krajbich et al.,
2009). This work documented brain-lesioned individuals' reduced
affect in response to guilt-, shame-, and embarrassment-evoking
situations. The current findings, which implicate medial frontal
regions also in positive self-conscious affect, raise the possibility
that frontal-lesioned individuals should also be deficient in their
ability to feel a sense of pride, even when their behavior justly
warrants it. This prediction, to the best of our knowledge, has not
been directly tested, and should be investigated in future work.
3.2. Self-conscious emotions and self-related processing
Our results show that affective self-processing was associated
with activation of the mPFC. This region was previously shown to
be involved in the cognitive aspects of self-reflective processing,
namely, in processing knowledge about the self (e.g., Kelley et al.,
2002) and in processing the mental states of the self and others
(Mitchell et al., 2005). Past research has consistently shown that
negative self-conscious emotions activate the mPFC (e.g.,
Takahashi et al., 2004; Burnett et al., 2009; Wagner et al., 2011).
The current study joins a study by Zahn et al. (2009) in showing
that feelings of pride activate the mPFC. However two previous
studies that examined the processing of pride did not report activations within this region (Takahashi et al., 2008; Simon-Thomas
et al., 2012).
It is likely that methodological differences between the current
study and the studies by Takahashi et al. (2008) and Simon-Thomas et al. (2012) produced these diverging findings. In Takahashi
et al.'s study participants read sentences describing pride-related
events (e.g., “I graduated from the most prestigious university); in
Simon-Thomas et al.'s study participants observed pride-related
images (e.g., images of graduation). It is possible that the stimuli in
these studies were not sufficiently self-relevant, and therefore did
not produce sufficiently strong feelings of pride. This possibility
should be studied in future research comparing different approaches for the elicitation of self-conscious emotions.
Extensive findings show that within the mPFC, a meaningful
distinction may be made between the dorsal region, which is more
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
strongly activated when thinking of other people, and the ventral
region, which is associated with thinking about the self and close
others (e.g., Denny et al., 2012; Mitchell et al., 2006). Interestingly,
our results also exhibited a distinction between the ventral and
dorsal mPFC, wherein guilt was associated with more dorsal activation, and pride was associated with ventral activation.
The association between the ventral mPFC and pride is consistent with recent work (Chavez and Heatherton, 2015) showing
that the individuals' level of self-esteem (which can be seen as a
sustained feeling of pride) is correlated with structural integrity
and functional connectivity between the ventral mPFC and subcortical regions involved in processing rewards (i.e., the ventral
striatum). These findings, alongside with the current research,
may suggest that the differential involvement of the ventral mPFC
in self- (vs. other-) focused processing could be related to its role
as part of a network of regions that subserve positive-affective
processing (e.g., Brown et al., 2011; Liu et al., 2011).
However, it remains possible that guilt and pride differentially
activate the ventral and dorsal mPFC because they differ in the
degree of self- and other-related processing. Guilt is often related
to moral considerations; in such cases it likely entails the representation of both a moral agent (the self) and a moral patient
(the other; Gray et al., 2012; e.g., I feel guilty because I hurt them).
Although feelings of pride often involve the perspective of others
(e.g., I bet they are proud of me), it is also common to feel pride
irrespective of the consideration of others (e.g., I am proud of
myself for accomplishing this). Thus, future research should attempt to carefully disentangle the involvement of representations
of self and others in feelings of guilt and pride, and thereby may
help shed light on the nature of the functional distinction between
the ventral and dorsal mPFC.
An additional observed distinction between the dorsal and ventral
mPFC is that the dorsal mPFC is involved both in thinking of future
events and recollection of the past (e.g., Addis et al., 2007) whereas the
ventral mPFC is more active when participants imagine (vs. remember) events (e.g., Addis et al., 2009). Contrary to our expectation,
in the current investigation we did not find significant differences in
activation for future and past events in the mPFC (or within any other
brain region). Although surprising, this null finding is consistent with
much previous research suggesting that the neural systems which
allow us to imagine future worlds and to recollect the past substantially overlap (e.g., Schacter et al., 2007; Buckner and Carroll,
2007); thus, it is likely that any differences between future- and pastoriented processing may have been too subtle to be detected in the
current paradigm.
Finally, much literature shows that many psychopathologies
are associated with dis-regulated activity of the medial prefrontal
cortex. For example, research shows that the vmPFC is hypoactivated in post-traumatic stress disorder (Shin and Liberzon, 2010)
and hyperactivated in obsessive-compulsive disorder (e.g., Sturm
et al., 2013). In contrast, the dmPFC was found to be hypoactivated
during reward-seeking among heavy drinkers (e.g., Bogg et al.,
2012). The finding whereby the dmPFC is associated with guilt
whereas the vmPFC is associated with pride may help in developing a more refined model of the link between dysregulated selfconscious affective processing, psychopathology, and mPFC disregulation. For example, our findings may suggest that interventions that apply repeated transcranial magnetic (rTMS) in order to
treat depressive and manic states (e.g., Pallanti et al., 2014), may
benefit from targeting the dmPFC and vmPFC, respectively.
3.3. Self-conscious vs. social emotions
Self-conscious emotions are believed to have developed as an
adaptation to the complex social organization of the ancient human
societies (Dunbar, 1998), and are central in motivating socially
215
appropriate and desired behaviors (e.g., Tangney et al., 2007). In light
of this, it is unsurprising that self-conscious emotions are also necessarily “social emotions”. Many aspects of the self are socially constructed, in that they pertain to a valuation that is dependent upon
social norms (e.g., “I am smart/stupid relative to my peers”, “I am a
moral/immoral person”). Indeed, much research shows that there is
substantial overlap between the brain regions involved in processing
social information and self-relevant information (e.g., Mitchell et al.,
2005). This convergence was also evident in our study, wherein selfconscious emotions, once again, activated the mPFC.
However, it is important to note that self-conscious emotions
and social-emotions are not one and the same. An emotion can be
inherently inter-personal without requiring any self-focus or selfreflection; for example, anger is clearly an inter-personal emotion
in that it is typically directed towards other people, yet it does not
require much self-reflection. Indeed, contrasting the widely acknowledged “inter-personal emotions” (i.e., guilt, pride, anger)
with a non- inter-personal emotion (joy) revealed activation
within a network of regions involved in social-cognition, which
includes the precuneus, the posterior superior temporal sulcus
(pSTS) extending to the temporo-parietal junction and to the
temporal pole, as well as activation within the mPFC (Van Overwalle and Baetens, 2009).
These findings are consistent with those of several other studies investigating the correlates of inter-personal and non-interpersonal emotions (e.g., Britton et al., 2006; Frewen et al., 2011).
Furthermore, they are somewhat consistent with two previous
studies which investigated self-conscious emotion processing (e.g.,
Guilt – Takahashi et al., 2004; Pride – Takahashi et al., 2008). Our
findings further suggest that the superior temporal sulcus and
precuneus activation evident in previous studies on guilt and pride
might be related to the social interaction that is inherent to these
emotions rather than the “self-referential” aspects of self-conscious emotions. In fact, our results show that pSTS activation was
most markedly associated with emotions of anger, which is an
inter-personal, but not a self-conscious emotion.
3.4. Basic emotions and embodied experience
It is argued that self-conscious and basic emotions are likely to
differ with regards to the abstractness of mental representations
that they typically rely upon (Karsh and Eyal, 2015; Agerström
et al., 2012). The self-construct is an entity that has concretephysical properties (e.g., “I have blonde hair”), as well as immaterial properties (e.g., “I am an honest person”; “I am greedy”)
that rely on an abstract-symbolic representational medium. In
contrast, basic emotions are believed by some to exist in animals
and infants, and thus may precede the emergence of abstractsymbolic thought (e.g., Izard et al., 1995). Consequently, basic
emotions may rely to a greater extent upon phylogenetically and
ontogenetically earlier-developed, modality-specific systems, that
do not necessarily employ abstract mental representations,
whereas self-conscious emotions are likely to rely on the phylogenetically-novel prefrontal cortex, which is involved in the processing of more abstract mental representations (e.g., Badre et al.,
2010; Mian et al., 2014; Straube et al., 2013; Cole et al., 2011; Tanji
et al., 2007; Wang et al., 2010; But see, for example, Barrett, 2006,
for an approach according to which all human emotion relies on
abstract mental representation).
Our results show that processing basic emotions (i.e., anger and
joy) compared with self-conscious emotions, resulted in activation
throughout relatively phylogenetically and ontogenetically earlierdeveloped regions of the cortex, namely in visual and tactile
processing areas (i.e., occipital cortex, somatosensory cortex, and
parahippocampal gyrus) and in the insular cortex. Notably,
whereas self-conscious emotions recruited the frontal cortex, no
216
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
frontal activations were evident for basic-emotion processing (as
compared to self-conscious emotions). These findings are consistent with the idea according to which self-conscious emotions
are a relatively recent adaptation (Demoulin et al., 2004), whereas
basic emotions originate early in our evolutionary ancestry (Ekman, 1992).
Furthermore, these findings are consistent with somatic (e.g.,
the James-Lange approach, e.g., Lang, 1994) and embodied (e.g.,
Niedenthal, 2007) theories of emotion which stress the importance of bodily states in emotional experience. However, they
also imply that the association between somatic and emotional
states is particularly relevant to basic emotions, and that selfconscious emotions may be more abstract and dis-embodied in
nature.
3.5. Concluding comments
Research in recent years has begun to delineate the neural
systems that are involved in the processing of self-related information (e.g., Mitchell et al., 2006) and the processing of affectively laden stimuli (e.g., Lindquist et al., 2012). However, research
that attempts to understand the neural systems involved in the
processing of self-conscious emotions has been surprisingly scarce.
By situating our investigation within a broader theory of the
functionality of self-conscious emotions, the current study addressed a major gap in the research into self-conscious emotions,
and provided an important piece of evidence for this cumulative
endeavor. Of course, much more research into the affective component of self-processing is clearly warranted, as it may shed light
on the age-old mystery of self-reflection, as well as provide a more
refined framework for understanding and treatment of
psychopathologies.
Acknowledgments
This work was supported by Grants from The Israel Science
Foundation to Nira Liberman (Grant no. 92/12) and to Tal Eyal
(Grant no. 923/09), by the I-CORE Program of the Planning and
Budgeting Committee and The Israel Science Foundation (Grant
no. 51/11) and by a research Grant from the Israeli Foundation
Trustees to Maayan Katzir (Fund for Doctoral Students no. 30).
Michael Gilead is financially supported by fellowships from the
Fulbright and Rothschild Foundations.
Appendix A: Stimuli
The Appendix presents the 16 stimuli used for each emotion.
Although each stimulus appeared both in the future condition and
in the past condition, for brevity, we present in this appendix the
stimuli either in their past form or in their future form.
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
References
Addis, D.R., Pan, L., Vu, M.A., Laiser, N., Schacter, D.L., 2009. Constructive episodic
simulation of the future and the past: distinct subsystems of a core brain
network mediate imagining and remembering. Neuropsychologia 47 (11),
2222–2238. http://dx.doi.org/10.1016/j.neuropsychologia.2008.10.026.
Addis, D.R., Wong, A.T., Schacter, D.L., 2007. Remembering the past and imagining
the future: common and distinct neural substrates during event construction
and elaboration. Neuropsychologia 45 (7), 1363–1377. http://dx.doi.org/
10.1016/j.neuropsychologia.2006.10.016.
Agerström, J., Björklund, F., Carlsson, R., 2012. Emotions in time: Moral emotions
appear more intense with temporal distance. Social Cognition 30 (2), 181–198.
http://dx.doi.org/10.1521/soco.2012.30.2.181.
Anderson, J.R., 1983. The Architecture of Cognition. Lawrence Erlbaum Associates,
Inc., Hillsdale, NJ, England.
Badre, D., Kayser, A.S., D’Esposito, M., 2010. Frontal cortex and the discovery of
abstract action rules. Neuron 66 (2), 315–326. http://dx.doi.org/10.1016/j.
neuron.2010.03.025.
Baldwin, M.W., Baccus, J.R., 2004. Maintaining a focus on the social goals underlying self-conscious emotions. Psychol. Inq., 139–144.
Barrett, L.F., 2006. Are emotions natural kinds? Perspectives on Psychological
217
Science 1 (1), 28–58. http://dx.doi.org/10.1111/j.1745-6916.2006.00003.x.
Basile, B., Mancini, F., Macaluso, E., Caltagirone, C., Frackowiak, R.S.J., Bozzali, M.,
2011. Deontological and altruistic guilt: evidence for distinct neurobiological
substrates. Hum. Brain Mapp. 32 (2), 229–239. http://dx.doi.org/10.1002/
hbm.21009.
Baumeister, R.F., Bratlavsky, E., Finkenauer, C., Vohs, K.D., 2001. Bad is stronger than
good. Review of General Psychology 5, 323–370.
Beer, J.S., Heerey, E.A., Keltner, D., Scabini, D., Knight, R.T., 2003. The regulatory
function of self-conscious emotion: insights from patients with orbitofrontal
damage. J. Personal. Soc. Psychol. 85 (4), 594.
Beer, J.S., John, O.P., Scabini, D., Knight, R.T., 2006. Orbitofrontal cortex and social
behavior: integrating self-monitoring and emotion-cognition interactions. J.
Cogn. Neurosci. 18 (6), 871–879. http://dx.doi.org/10.1162/jocn.2006.18.6.871.
Bogg, T., Fukunaga, R., Finn, P.R., Brown, J.W., 2012. Cognitive control links alcohol
use, trait disinhibition, and reduced cognitive capacity: Evidence for medial
prefrontal cortex dysregulation during reward-seeking behavior. Drug and Alcohol Dependence 122 (1-2), 112–118. http://dx.doi.org/10.1016/j.
drugalcdep.2011.09.018.
Botvinick, M.M., Cohen, J.D., Carter, C.S., 2004. Conflict monitoring and anterior
cingulate cortex: an update. Trends in cognitive sciences 8 (12), 539–546.
Brett, M., Anton, J.-L., Valabregue, R., Poline, J.B., 2002. Region of interest analysis
using the MarsBar toolbox for SPM 99. Neuroimage 16, S497.
Britton, J.C., Phan, K.L., Taylor, S.F., Welsh, R.C., Berridge, K.C., Liberzon, I., 2006.
Neural correlates of social and nonsocial emotions: an fMRI study. Neuroimage
31 (1), 397–409. http://dx.doi.org/10.1016/j.neuroimage.2005.11.027.
Brown, S., Gao, X.Q., Tisdelle, L., Eickhoff, S.B., Liotti, M., 2011. Naturalizing aesthetics: brain areas for aesthetic appraisal across sensory modalities. Neuroimage 58 (1), 250–258. http://dx.doi.org/10.1016/j.neuroimage.2011.06.012.
Buckner, R.L., Carroll, D.C., 2007. Self-projection and the brain. Trends in Cognitive
Sciences 11 (2), 49–57. http://dx.doi.org/10.1016/j.tics.2006.11.004.
Burnett, S., Bird, G., Moll, J., Frith, C., Blakemore, S.J., 2009. Development during
adolescence of the neural processing of social emotion. J. Cogn. Neurosci. 21 (9),
1736–1750. http://dx.doi.org/10.1162/jocn.2009.21121.
Chavez, R.S., Heatherton, T.F., 2015. Multimodal frontostriatal connectivity underlies individual differences in self-esteem. Soc. Cogn. Affect. Neurosci. 10 (3),
364–370. http://dx.doi.org/10.1093/scan/nsu063.
Cole, M.W., Etzel, J.A., Zacks, J.M., Schneider, W., Braver, T.S., 2011. Rapid transfer of
abstract rules to novel contexts in human lateral prefrontal cortex. Front. Hum.
Neurosci. 5, 13. http://dx.doi.org/10.3389/fnhum.2011.00142.
Cole, M.W., Schneider, W., 2007. The cognitive control network: Integrated cortical
regions with dissociable functions. Neuroimage 37 (1), 343–360. http://dx.doi.
org/10.1016/j.neuroimage.2007.03.071.
Demoulin, S., Leyens, J.P., Paladino, M.P., Rodriguez-Torres, R., Rodriguez-Perez, A.,
Dovidio, J.F., 2004. Dimensions of “uniquely” and “non-uniquely” human
emotions. Cogn. Emotion 18 (1), 71–96. http://dx.doi.org/10.1080/
02699930244000444.
Denny, B.T., Kober, H., Wager, T.D., Ochsner, K.N., 2012. A meta-analysis of functional neuroimaging studies of self- and other judgments reveals a spatial
gradient for mentalizing in medial prefrontal cortex. J. Cogn. Neurosci. 24 (8),
1742–1752.
Dorfman, A., Eyal, T., Bereby-Meyer, Y., 2014. Proud to cooperate: The consideration
of pride promotes cooperation in a social dilemma. Journal of Experimental
Social Psychology 55, 105–109.
Dunbar, R.I.M., 1998. The social brain hypothesis. Evol. Anthropol. 6 (5), 178–190.
Ekman, P., 1992. An argument for basic emotions. Cognition and Emotion 6 (3-4),
169–200. http://dx.doi.org/10.1080/02699939208411068.
Eyal, T., Fishbach, A., 2010. The Motivation-emotion Matching Hypothesis. BenGurion University of the Negev, Israel (unpublished manuscript).
Frewen, P.A., Dozois, D.J.A., Neufeld, R.W.J., Densmore, M., Stevens, T.K., Lanius, R.A.,
2011. Neuroimaging social emotional processing in women: fMRI study of
script-driven imagery. Social Cognitive and Affective Neuroscience 6 (3),
375–392. http://dx.doi.org/10.1093/scan/nsq047.
Fourie, M.M., Thomas, K.G.F., Amodio, D.M., Warton, C.M.R., Meintjes, E.M., 2014.
Neural correlates of experienced moral emotion: an fMRI investigation of
emotion in response to prejudice feedback. Soc. Neurosci. 9 (2), 203–218. http:
//dx.doi.org/10.1080/17470919.2013.878750.
Giner-Sorolla, R., 2001. Guilty pleasures and grim necessities: affective attitudes in
dilemmas of self-control. J. Personal. Soc. Psychol. 80 (2), 206–221.
Gray, K., Young, L., Waytz, A., 2012. Mind perception is the essence of morality.
Psychol. Inq. 23 (2), 101–124. http://dx.doi.org/10.1080/1047840x.2012.651387.
Hare, T.A., Camerer, C.F., Rangel, A., 2009. Self-control in decision-making involves
modulation of the vmPFC valuation system. Science 324 (5927), 646–648.
Hofmann, W., Fisher, R.R., 2012. How guilt and pride shape subsequent self-control.
Soc. Psychol. Personal. Sci. 3 (6), 682–690.
Hofmann, W., Kotabe, H., Luhmann, M., 2013. The spoiled pleasure of giving in to
temptation. Motiv. Emotion 37 (4), 733–742. http://dx.doi.org/10.1007/
s11031-013-9355-4.
Izard, C.E., Fantauzzo, C.A., Castle, J.M., Haynes, O.M., Rayias, M.F., Putnam, P.H.,
1995. The ontogeny and significant of infants facial expressions in the first
9 months of life. Dev. Psychol. 31 (6), 997–1013. http://dx.doi.org/10.1037/
0012-1649.31.6.997.
Karsh, N., Eyal, T., 2015. How the Consideration of Positive Emotions Influences
Persuasion: The Differential Effect of Pride Versus Joy. Journal of Behavioral
Decision Making 28 (1), 27–35.
Katzir, M., Eyal, T., Meiran, N., Kessler, Y., 2010. Imagined positive emotions and
inhibitory control: the differentiated effect of pride versus happiness. J. Exp.
218
M. Gilead et al. / Neuropsychologia 81 (2016) 207–218
Psychol.-Learn. Memory Cogn. 36 (5), 1314–1320. http://dx.doi.org/10.1037/
a0020120.
Katzir, M., Ori, B., Eyal, T., Meiran, N., 2015. Go with the flow: How the consideration
of joy versus pride influences automaticity. Acta psychologica 155, 57–66. http:
//dx.doi.org/10.1016/j.actpsy.2014.12.003.
Kedia, G., Berthoz, S., Wessa, M., Hilton, D., Martinot, J.L., 2008. An agent harms a
victim: a functional magnetic resonance imaging study on specific moral
emotions. J. Cogn. Neurosci. 20 (10), 1788–1798. http://dx.doi.org/10.1162/
jocn.2008.20070.
Kelley, W.M., Macrae, C.N., Wyland, C.L., Caglar, S., Inati, S., Heatherton, T.F., 2002.
Finding the self? An event-related fMRI study. J. Cogn. Neurosci. 14 (5),
785–794. http://dx.doi.org/10.1162/08989290260138672.
Kerns, J.G., Cohen, J.D., MacDonald III, A.W., Cho, R.Y., Stenger, V.A., Carter, C.S.,
2004. Anterior Cingulate Conflict Monitoring and Adjustments in Control. Science 303 (5660), 1023–1026. http://dx.doi.org/10.1126/science.1089910.
Klein, T.A., Endrass, T., Kathmann, N., Neumann, J., von Cramon, D.Y., Ullsperger, M.,
2007. Neural correlates of error awareness. Neuroimage 34 (4), 1774–1781.
http://dx.doi.org/10.1016/j.neuroimage.2006.11.014.
Krajbich, I., Adolphs, R., Tranel, D., Denburg, N.L., Camerer, C.F., 2009. Economic
games quantify diminished sense of guilt in patients with damage to the prefrontal cortex. J. Neurosci. 29 (7), 2188–2192. http://dx.doi.org/10.1523/
jneurosci.5086-08.2009.
Lang, P.J., 1994. The varities of emotional experience – a meditation of James-Lange
theory. Psychol. Rev. 101 (2), 211–221. http://dx.doi.org/10.1037/
0033-295x.101.2.211.
Leary, M.R., 2007. Motivational and emotional aspects of the self. Annu. Rev. Psychol. 58, 317–344.
Lindquist, K.A., Wager, T.D., Kober, H., Bliss-Moreau, E., Barrett, L.F., 2012. The brain
basis of emotion: a meta-analytic review. Behav. Brain Sci. 35 (3), 121–143.
http://dx.doi.org/10.1017/s0140525x11000446.
Liu, X., Hairston, J., Schrier, M., Fan, J., 2011. Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional
neuroimaging studies. Neurosci. Biobehav. Rev. 35 (5), 1219–1236. http://dx.
doi.org/10.1016/j.neubiorev.2010.12.012.
Lutwak, N., Ferrari, J.R., 1997. Shame-related social anxiety: replicating a link with
various social interaction measures. Anxiety Stress Coping 10 (4), 335–340.
http://dx.doi.org/10.1080/10615809708249307.
MacDonald, A.W., Cohen, J.D., Stenger, V.A., Carter, C.S., 2000. Dissociating the role
of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control.
Science 288 (5472), 1835–1838.
Mian, M.K., Sheth, S.A., Patel, S.R., Spiliopoulos, K., Eskandar, E.N., Williams, Z.M.,
2014. Encoding of rules by neurons in the human dorsolateral prefrontal cortex.
Cereb. Cortex 24 (3), 807–816. http://dx.doi.org/10.1093/cercor/bhs361.
Michl, P., Meindl, T., Meister, F., Born, C., Engel, R.R., Reiser, M., Hennig-Fast, K.,
2014. Neurobiological underpinnings of shame and guilt: A pilot fMRI study.
Social Cognitive and Affective Neuroscience 9 (2), 150–157. http://dx.doi.org/
10.1093/scan/nss114.
Mitchell, J.P., Banaji, M.R., Macrae, C.N., 2005. The link between social cognition and
self-referential thought in the medial prefrontal cortex. J. Cogn. Neurosci. 17 (8),
1306–1315. http://dx.doi.org/10.1162/0898929055002418.
Mitchell, J.P., Macrae, C.N., Banaji, M.R., 2006. Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron 50 (4),
655–663. http://dx.doi.org/10.1016/j.neuron.2006.03.040.
Moll, J., de Oliveira-Souza, R., Garrido, G.J., Bramati, I.E., Caparelli-Daquer, E.M.A.,
Paiva, M., Grafman, J., 2007. The self as a moral agent: Link-ling the neural bases
of social agency and moral sensitivity. Soc. Neurosci. 2 (3–4), 336–352. http:
//dx.doi.org/10.1080/17470910701392024.
Moll, J., Zahn, R., de Oliveira-Souza, R., Bramati, I.E., Krueger, F., Tura, B., Grafman, J.,
2011. Impairment of prosocial sentiments is associated with frontopolar and
septal damage in frontotemporal dementia. Neuroimage 54 (2), 1735–1742.
http://dx.doi.org/10.1016/j.neuroimage.2010.08.026.
Mukhopadhyay, A., Johar, G.V., 2007. Tempted or not? The effect of recent purchase
history on responses to affective advertising. Journal of Consumer Research 33
(4), 445–453.
Niedenthal, P.M., 2007. Embodying emotion. Science 316 (5827), 1002–1005. http:
//dx.doi.org/10.1126/science.1136930.
O’Connor, L.E., Berry, J.W., Weiss, J., Gilbert, P., 2002. Guilt, fear, submission, and
empathy in depression. J. Affect. Disord. 71 (1–3), 19–27. http://dx.doi.org/
10.1016/s0165-0327(01)00408-6.
Ochsner, K.N., Silvers, J.A., Buhle, J.T., 2012. Functional imaging studies of emotion
regulation: a synthetic review and evolving model of the cognitive control of
emotion. Ann. N.Y. Acad. Sci. 1251, E1–24. http://dx.doi.org/10.1111/
j.1749-6632.2012.06751.x.
Pallanti, S., Grassi, G., Antonini, S., Quercioli, L., Salvadori, E., Hollander, E., 2014.
rTMS in resistant mixed states: An exploratory study. J. Affect. Disord. 157,
66–71. http://dx.doi.org/10.1016/j.jad.2013.12.024.
Pierrot-Deseilligny, C., Müri, R.M., Ploner, C.J., Gaymard, B., Demeret, S., RivaudPechoux, S., 2003. Decisional role of the dorsolateral prefrontal cortex in ocular
motor behaviour. Brain: A Journal of Neurology 126 (6), 1460–1473. http://dx.
doi.org/10.1093/brain/awg148.
Roth, L., Kaffenberger, T., Herwig, U., Brühl, A.B., 2014. Brain activation associated
with pride and shame. Neuropsychobiology 69 (2), 95–106. http://dx.doi.org/
10.1159/000358090.
Schacter, D.L., Addis, D.R., Buckner, R.L., 2007. Remembering the past to imagine the
future: The prospective brain. Nature Reviews Neuroscience 8 (9), 657–661.
http://dx.doi.org/10.1038/nrn2213.
Shimoni, E., Asbe, M., Eyal, T., Berger, A., 2016. Too proud to regulate: The differential effect of pride versus joy on children’s ability to delay gratification.
Journal of experimental child psychology 141, 275–282.
Shin, L.M., Dougherty, D.D., Orr, S.P., Pitman, R.K., Lasko, M., Macklin, M.L., Rauch, S.
L., 2000. Activation of anterior paralimbic structures during guilt-related scriptdriven imagery. Biol. Psychiatry 48 (1), 43–50. http://dx.doi.org/10.1016/
s0006-3223(00)00251-1.
Shin, L.M., Liberzon, I., 2010. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35 (1), 169–191. http://dx.doi.org/10.1038/
npp.2009.83.
Simon-Thomas, E.R., Godzik, J., Castle, E., Antonenko, O., Ponz, A., Kogan, A., Keltner,
D.J., 2012. An fMRI study of caring vs self-focus during induced compassion and
pride. Social Cognitive and Affective Neuroscience 7 (6), 635–648. http://dx.doi.
org/10.1093/scan/nsr045.
Slotnick, S.D., Moo, L.R., Segal, J.B., Hart, J., 2003. Distinct prefrontal cortex activity
associated with item memory and source memory for visual shapes. Cogn.
Brain Res. 17 (1), 75–82. http://dx.doi.org/10.1016/s0926-6410(03)00082-x.
Somerville, L.H., Jones, R.M., Ruberry, E.J., Dyke, J.P., Glover, G., Casey, B.J., 2013. The
medial prefrontal cortex and the emergence of self-conscious emotion in
adolescence. Psychological Science 24 (8), 1554–1562. http://dx.doi.org/
10.1177/0956797613475633.
Stein, M.B., Simmons, A.N., Feinstein, J.S., Paulus, M.P., 2007. Increased amygdala
and insula activation during emotion processing in anxiety-prone subjects. Am.
J. Psychiatry 164 (2), 318–327. http://dx.doi.org/10.1176/appi.ajp.164.2.318.
Straube, B., He, Y.F., Steines, M., Gebhardt, H., Kircher, T., Sammer, G., Nagels, A.,
2013. Supramodal neural processing of abstract information conveyed by
speech and gesture. Front. Behav. Neurosci. 7, 14. http://dx.doi.org/10.3389/
fnbeh.2013.00120.
Sturm, V.E., Sollberger, M., Seeley, W.W., Rankin, K.P., Ascher, E.A., Rosen, H.J., Levenson, R.W., 2013. Role of right pregenual anterior cingulate cortex in selfconscious emotional reactivity. Soc. Cognit. Affect. Neurosci. 8 (4), 468–474.
http://dx.doi.org/10.1093/scan/nss023.
Takahashi, H., Matsuura, M., Koeda, M., Yahata, N., Suhara, T., Kato, M., Okubo, Y.,
2008. Brain activations during judgments of positive self-conscious emotion
and positive basic emotion: pride and joy. Cereb. Cortex 18 (4), 898–903.
Takahashi, H., Yahata, N., Koeda, M., Matsuda, T., Asai, K., Okubo, Y., 2004. Brain
activation associated with evaluative processes of guilt and embarrassment: an
fMRI study. Neuroimage 23 (3), 967–974.
Tangney, J. P. (2003). Self-relevant emotions. In M. R. Leary & J. P. Tangney (Eds.),
Handbook of self and identity (pp. 384-400). New York: Guilford Press.
Tangney, J.P., Stuewig, J., Mashek, D.J., 2007. Moral emotions and moral behavior.
Annu. Rev. Psychol. 58, 345–372.
Tanji, J., Shima, K., Mushiake, H., 2007. Concept-based behavioral planning and the
lateral prefrontal cortex. Trends Cogn. Sci. 11 (12), 528–534. http://dx.doi.org/
10.1016/j.tics.2007.09.007.
Tracy, J.L., Cheng, J.T., Robins, R.W., Trzesniewski, K.H., 2009. Authentic and hubristic pride: the affective core of self-esteem and narcissism. Self Identity 8,
196–213. http://dx.doi.org/10.1080/15298860802505053.
Tracy, J.L., Robins, R.W., 2004. Putting the self into self-conscious emotions: a
theoretical model. Psychol. Inq. 15 (2), 103–125.
Tracy, J.L., Robins, R.W., 2007. Self-conscious emotions: where self and emotion
meet. In: The Self in Social Psychology, pp. 187–209.
Van Overwalle, F., Baetens, K., 2009. Understanding others' actions and goals by
mirror and mentalizing systems: a meta-analysis. Neuroimage 48 (3), 564–584.
http://dx.doi.org/10.1016/j.neuroimage.2009.06.009.
Wagner, U., N’Diaye, K., Ethofer, T., Vuilleumier, P., 2011. Guilt-specific processing in
the prefrontal cortex. Cereb. Cortex 21 (11), 2461–2470. http://dx.doi.org/
10.1093/cercor/bhr016.
Wang, J., Conder, J.A., Blitzer, D.N., Shinkareva, S.V., 2010. Neural representation of
abstract and concrete concepts: a meta‐analysis of neuroimaging studies. Hum.
Brain Mapp. 31 (10), 1459–1468.
Williams, L.A., DeSteno, D., 2008. Pride and perseverance: the motivational role of
pride. J. Personal. Soc. Psychol. 94 (6), 1007.
Zahn, R., Moll, J., Paiva, M., Garrido, G., Krueger, F., Huey, E.D., Grafman, J., 2009. The
neural basis of human social values: evidence from functional MRI. Cereb.
Cortex 19 (2), 276–283. http://dx.doi.org/10.1093/cercor/bhn080.
Zaki, J., Davis, J.I., Ochsner, K.N., 2012. Overlapping activity in anterior insula during
interoception and emotional experience. Neuroimage 62 (1), 493–499. http:
//dx.doi.org/10.1016/j.neuroimage.2012.05.012.
Zemack-Rugar, Y., Bettman, J.R., Fitzsimons, G.J., 2007. The effects of nonconsciously
priming emotion concepts on behavior. J. Personal. Soc. Psychol. 93 (6),
927–939.