Biological Psychology 91 (2012) 212220

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Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

Adult attachment and emotional processing biases: An Event-Related Potentials

(ERPs) study
Orrie Dan a,1 , Sivan Raz a,b,,1
a
Department of Psychology, The Center for Psychobiological Research, The Max Stern Academic College of Emek Yezreel, Israel
b
Department of Psychology, Tel Hai College, Israel

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

Article history: Attachment-related electrophysiological differences in emotional processing biases were examined using
Received 11 January 2012 Event-Related Potentials (ERPs). We identied ERP correlates of emotional processing by comparing ERPs
Accepted 7 June 2012 elicited in trials with angry and neutral faces. These emotional expression effects were then compared
Available online 23 June 2012
across groups with secure, anxious and avoidant attachment orientations. Results revealed signicant
interactions between attachment orientation and facial expression in mean amplitudes of the early C1
Keywords:
(5080 ms post-stimulus) and P1 (80120 ms post-stimulus) ERP components. Signicant differences in
Adult attachment
C1 and P1 mean amplitudes were found at occipital and posterior-parietal channels in response to angry
Event-Related Potentials (ERPs)
Facial expressions
compared with neutral faces only within the avoidant attachment group. No such differences were found
Emotional processing bias within the secure or anxious attachment groups. The present study underscores the usefulness of the ERP
methodology, as a sensitive measure for the study of emotional processing biases in the research eld of
attachment.
2012 Elsevier B.V. All rights reserved.

1. Introduction characterized by a lack of attachment security, a strong need for

Attachment theory (Bowlby, 1973, 1982) focuses on how early
experiences with primary caregivers inuence behavior and emo-
tion regulation, as well as on how attachment-relevant stimuli are
perceived and interpreted later in life (e.g., Bowlby, 1982; Hazan
and Shaver, 1987; Spangler and Zimmermann, 1999; Stern, 1985;
Suslow et al., 2009). Differences in attachment style may predict
selective biases in attention toward certain types of emotional
information from the external environment (e.g., Edelstein and
Gillath, 2008; Feeney et al., 1994; Tucker and Anders, 1999). Early
experiences with attachment gures are also assumed to affect
the development and maturation of the brain and to have long-
lasting effects on brain structures and brain function (Schore, 1994).
Indeed, attachment-related differences in brain function have been
reported in several fMRI studies (e.g., Buchheim et al., 2006; Coan
et al., 2006; Gillath et al., 2005; Lemche et al., 2006; Vrticka et al.,
2008; Warren et al., 2010).
Adult attachment is best conceptualized using two dimensions:
anxiety and avoidance (Bartholomew and Horowitz, 1991; Brennan
et al., 1998; Mikulincer and Shaver, 2007). Attachment anxiety is
Corresponding author at: Department of Psychology, The Center for Psychobio-
logical Research, The Max Stern Academic College of Emek Yezreel, Israel.
Tel.: +972 546634301; fax: +972 46423618.
E-mail address: sivanr@yvc.ac.il (S. Raz).
1
These authors contributed equally to this work.
closeness, worries about relationships, and fear of being rejected.
Some evidence indicates that adults with an anxious attachment
style tend to exhibit hyper-vigilance in response to emotional facial
expressions (Fraley et al., 2006; Maier et al., 2005; Niedenthal et al.,
2002; Shaver and Hazan, 1993) and heightened cognitive acces-
sibility to attachment-related material (e.g., Gillath et al., 2005;
Mikulincer et al., 2002; Mikulincer and Orbach, 1995). Yet other
ndings suggest that such individuals may be less attentive to this
type of emotional material (Van Emmichoven et al., 2003).
Attachment avoidance is marked by a lack of attachment secu-
rity as well as by compulsive self-reliance and a preference for
emotional distance from others. Bartholomew and Horowitz (1991)
reported that the behavioral patterns shown by individuals with
anxious attachment were the opposite of those exhibited by indi-
viduals with avoidant attachment in almost every respect. Although
avoidant individuals are thought to rely on deactivating or defen-
sive strategies (Fraley et al., 1998, 2000), there is very little direct
evidence for emotional processing biases among avoidant adults.
Avoidant adults may perhaps be less attentive to attachment-
related experiences. Thus, their defense mechanisms may operate
preemptively to limit the amount of information that gets encoded.
Alternately, avoidant individuals may reect less and elaborate
less on the emotional experiences they have encoded. In this case,
defense mechanisms may operate after the fact, or post-emptively,
to suppress or deactivate ideas and memories that have already
been attended to or encoded (Edelstein, 2006; Fraley et al., 1998,
2000).

0301-0511/$ see front matter 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.biopsycho.2012.06.003
 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220
In this two-dimensional space, the secure style is a region
where both anxiety and avoidance are low. Secure individuals
show neither of these biases and exhibit balanced and moderate
responses to emotional information and events (Shaver and Hazan,
1993).
Despite theoretical claims and considerable evidence that indi-
vidual differences in attachment security provide a foundation for
emotional perception (Sroufe et al., 2005), surprisingly few stud-
ies have investigated the specic neural mechanisms underlying
these patterns. Most of the literature integrating attachment and
neuroscience is theoretical rather than empirical, and studies of the
neural circuitry associated with attachment are quite rare (Coan,
2008).
The aim of the present study was to identify patterns of
behavioral responses and brain activity during emotion percep-
tion among adults with differing attachment representations. More
specically, we sought to explore the interaction effects between
attachment anxiety and avoidance and the initial neural changes
associated with automatic attention to emotional facial expres-
sions.
Electroencephalogram-Event Related Potentials (EEG-ERPs), a
technique used to investigate the temporal brain dynamics of atten-
tive processing at ne temporal resolution, was the method of
choice. Since evaluation of emotional faces seems to occur as early
as 100 ms following stimulus presentation (Halgren et al., 2000; Liu
et al., 2002), we focused on the early C1 and P1 ERP components.
ERP dot-probe studies with healthy adults have shown emotion-
related modulation in the C1 component time locked to the faces
display (Pourtois et al., 2004) and in the P1 component time locked
to target onset (Pourtois et al., 2004; Santesso et al., 2008). The C1
component (50100 ms post-stimulus) is the rst ERP component
triggered by the appearance of a stimulus in the visual eld and is
thought to be pre-attentive and independent of spatial attention
(Clark and Hillyard, 1996; Foxe and Simpson, 2002; Fu et al., 2005;
Hillyard and Anllo-Vento, 1998; Stolarova et al., 2006). C1 has been
found to be more intense in displays containing threatening faces
than in displays containing non-threatening faces (Pourtois et al.,
2004). It has been suggested that the modulation of C1 by the emo-
tional valence of the cue display on the dot-probe task could be the
consequence of an interaction between the primary visual cortex
and the subcortical limbic structures responsible for the detection
of threats (Pourtois et al., 2004; Stolarova et al., 2006). The P1
component, an early sensory component peaking around 100 ms
post-stimulus, may constitute an index of mobilization of auto-
matic attentional resources (see review in Hopnger and Mangun,
2001). Carreti et al. (2004) reported that automatic attention (P1)
is initially captured by negative pictures rather than by those that
are positive or non-emotional. According to these researchers, the
fact that negative stimuli mobilize attentional resources as early as
105 ms post-stimulus is probably a manifestation of the negativity
bias.
To the best of our knowledge, only two ERP studies have
examined the relations between attachment orientation and facial
emotional perception (Fraedrich et al., 2010; Zhang et al., 2008).
Another ERP study used emotional pictures from the IAPS as stim-
uli (Zilber et al., 2007). All of these studies reported relatively late
ERP (N170 and later) differences between attachment orientations.
In the present study, we sought to identify ERP correlates of
emotional face-processing by comparing early ERPs (C1 and P1)
elicited in trials using angry and neutral faces. Emotional expres-
sion effects were then compared across groups with secure, anxious
and avoidant attachment orientations. The perception of angry
faces may be suitable for studies of attachment, since such facial
expressions signal social disapproval and threat and the violation of
social rules or expectations (Averill, 1983; hman, 1986; Santesso
et al., 2008). In healthy populations, a processing bias toward
213
threat-related (angry) faces has been demonstrated in visual search
tasks using both schematic (Eastwood et al., 2001; Fox et al., 2000)
and real (Horstmann and Bauland, 2006; Williams et al., 2005) face
stimuli.
In general, we hypothesized that attachment orientation would
interact with behavioral and ERP patterns in response to angry
facial expressions, compared with neutral expressions. More
specically, we hypothesized (following Edelstein, 2006; Fraley
et al., 2000) that in order for attachment-avoidant individuals to
apply deactivating/defensive strategies, they must rst attend to
the valence of a face stimulus and must very quickly differentiate
emotional faces from neutral ones. Therefore, we expected process-
ing bias reected in longer RTs, as well as differential (i.e., greater)
C1 and P1 amplitudes in response to angry compared to neutral
faces within the avoidant group. In contrast, at these very early
stages of information processing, attachment-anxious individuals
may be equally attentive and hyper-vigilant to all kinds of faces
in the environment. We therefore expected anxious individuals to
have the same RTs as well as the same C1 and P1 amplitudes in
response both to angry and to neutral faces. In other words, we
hypothesized that avoidant rather than anxious individuals would
show an early processing bias towards emotional faces.
2. Methods
2.1. Participants
Participants were 50 undergraduate students (32 females), mean age
23.58 3.31 years, selected on the basis of their attachment scores from the Experi-
ences in Close Relationships (ECR) scale (Brennan et al., 1998). The participants were
allocated to three attachment groups. Those with low scores both on avoidance and
anxiety scales were allocated to the secure group (n = 17; 11 females). Those with
low scores on the avoidance scale and high scores on the anxiety scale were allo-
cated to the anxious group (n = 17; 11 females) and, those with high scores on the
avoidance scale and low scores on the anxiety scale were allocated to the avoidant
group (n = 16; 10 females). All the participants where healthy and none of them had
a prior history of neurological or psychiatric disorders. All of them gave informed
consent. The experiment was approved by the academic committee of the Yezreel
Valley College.
2.2. Assessment of attachment
One to two weeks before the ERP experiment, 363 undergraduate students
completed a Hebrew version of the Experiences in Close Relationships (ECR) scale
(Brennan et al., 1998). This self-report questionnaire assesses individual differences
on the two major dimensions of adult attachment style: avoidance of intimacy and
interdependence, and anxiety about rejection and abandonment. The Avoidance
scale contains 18 Likert-type items (e.g., I prefer not to show a partner how I feel deep
down), as does the Anxiety scale (e.g., I worry about being abandoned). Each item is
rated on a 7-point scale ranging from 1 (not at all) to 7 (very much). This two-
dimensional perspective for representing attachment relationships is considered
the gold-standard in self-report measures of adult-attachment (Brennan et al.,
1998; Mikulincer and Shaver, 2007). In the current study, internal consistencies
were = 0.86 for the anxiety and = 0.83 for the avoidance subscales.
2.3. Stimuli
Photographs of faces of 20 different individuals, 10 male and 10 female, were
used as stimuli. All faces were taken from a standard set of pictures of facial affect,
the NimStim face stimulus set (Tottenham et al., 2002). Facial expression was angry
or neutral. Each actor presented both angry and neutral faces and each face was
presented four times, resulting in a total of 160 stimuli (divided into four blocks
of 40 trials each). All trials began with a 1000 ms xation display (white cross on
a black background) followed by 500 ms of the target faces (angry or neutral) dis-
play. Following target display the screen went blank for an inter-trial interval (ITI)
of 1000 ms. The experiment began with a short practice block which contained neu-
tral and angry faces corresponding to those presented in the experimental blocks.
Participants were allowed a rest period after the practice block. In the experimental
session, targets were displayed with equal probability and their presentation was
randomized between trials.
2.4. Procedure
Participants were seated in a comfortable chair in a dimly lit room at a distance
of 80 cm from a 19 computer screen. They were instructed to focus their gaze on the
214 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220

face stimuli to be presented in the center of the screen, and then to identify the sex of
the target. They were required to press 1 on the response box with their right hand
if the target was a male and 2 if it was a female. Subjects were naive with respect
to the specic questions investigated; it was an implicit emotional task. Participants
were asked to refrain from making eye movements throughout the session. It was
emphasized that they could perform the task without having to move their eyes.

2.5. EEG/ERP recording; data acquisition

EEG was recorded continuously using a 64-channel HydroCel Geodesic Sen-

sor Net, Net Amps 300 amplier, and Net Station, Version 4.2, software (Electrical
Geodesics Inc, Eugene, OR) at 250 Hz with 0.1 Hz high-pass and 100 Hz low-pass
ltering. Electrode impedances were maintained below 60 k. All channels were
referenced to Cz during acquisition.
After acquisition, in an off line processing, the continuous EEG was re-
referenced to an average reference, ltered with a 130 Hz band-pass lter
and segmented by condition into 900 ms stimulus-locked epochs from 100 ms
pre-stimulus to 800 ms post-stimulus. Epochs contaminated with vertical eye move-
ments (eye blinks; 140 V) and horizontal eye movement (55 V) artifacts as
identied by computerized algorithm and veried by visual inspection, were elim-
inated. In addition, a recording segment was marked bad if it contained more than
10 bad channels. Individual bad channels were replaced on a segment-by-segment
basis with spherical spline interpolation. After artifact correction, an average of
77.62% of the 160 trials was retained in the analyses. The mean number of artifact-
free trials per condition was 61.19 2.47 for angry faces and 63 2.41 for neutral
faces.
Averaged ERP data were baseline corrected and re-referenced into an average
reference frame. Only trials in which the face target was classied correctly were
entered into the average. The exclusion of inaccurate responses resulted in the loss of
additional 3.5% of data. All stimulus presentation and behavioral response collection Fig. 1. Layout of the electrode array and the electrodes chosen for analysis.
was controlled by a PC computer running E-prime 2.0 software (Psychology Software
Tools Inc., PA).
(120180 ms) ERP components at occipital (35, 37, 39) and posterior-parietal (31 &
2.6. Target-evoked ERP components 33, 34 & 36, 38 & 40) channels were analyzed with a four-way repeated measures
multivariate analysis of variance (mixed-design ANOVA). Emotion (angry/neutral),
Our focus was on an a priori hypothesis related to the rst negative (C1) and Location (left/midline/right) and Region (occipital/posterior-parietal) were the
positive (P1) voltage deections in the ERP occurring after target onset. Both C1 within-subject factors and Attachment Group (secure/avoidant/anxious) was the
and P1 are known to be modulated by attention (see Santesso et al., 2008; Miller between-subjects factor. Follow-up paired sample t-tests were used to breakdown
and Tomarken, 2001) and to have an occipitalparietal distribution (Pourtois et al., interaction effects. For the sake of brevity, only effects involving the factors Emotion
2004; Clark et al., 1995; Andersson et al., 2004). Following inspection of the grand and Group are reported in detail.
mean ERPs, we decided to quantify the mean amplitude of the C1 and P1 compo- For both the behavioral and electrophysiological analysis, signicance levels
nents within two specied latency windows (centered on the components peak): were adjusted using the GreenhouseGeisser correction when needed (the degrees
5080 ms post-stimulus (C1) and 80120 ms post-stimulus (P1). The mean ampli- of freedom indicated in the text are always those before the GreenhouseGeisser
tude is a traditional and well accepted approach to ERP analysis which has been correction). In all the post hoc comparisons, the Bonferroni correction was applied
used in many studies investigating early ERPs in response to emotional faces (e.g., where appropriate and only signicant results were reported. Numeric results are
Bar-Haim et al., 2005; Eldar et al., 2010; Pourtois et al., 2004; Rellecke et al., 2011; presented as mean SEM in both text and gures.
Santesso et al., 2008; Stolarova et al., 2006).2 , 3 C1 and P1 mean amplitudes were
quantied over three occipital scalp locations: left channel (35), midline channel
(37; Oz) and right channel (39) and over three posterior-parietal scalp locations: 3. Results
left channels (average of channels 31 & 33), midline channels (average of channels
34; Pz & 36) and right channels (average of channels 38 & 40). For the electrode
3.1. Behavioral measures
array, see Fig. 1. For completeness, we additionally analyzed the mean amplitude of
the ERP N170 component (120180 ms) which is known to be modulated by faces
display (e.g., Bentin et al., 1996; Eimer, 1998, 2000; Jeffreys, 1989). It was suggested 3.1.1. Reaction time (RT)
that the N170 component may have specicity and differential sensitivity to human Repeated measures ANOVA revealed a main effect of Emo-
faces as opposed to animal faces or other animate and inanimate nonface stimuli tion, F(1,47) = 11.35, p = 0.002, 2 p = 0.19. RTs on trials with angry
(Bentin et al., 1996).
faces were longer (553.99 ms 14.06) than on trials with neutral
2.7. Data analysis faces (543.46 ms 12.74). The Emotion Group interaction effect
was also signicant F(2,47) = 7.97, p = 0.001, 2 p = 0.25. Follow-up
2.7.1. Behavioral data contrasts within each attachment group showed slower RTs on
To examine group differences in reaction times (RTs) and in accuracy (per- trials with angry faces (602.65 ms 28.59) relative to trials with
cent of errors), Repeated Measures ANOVA (Analysis of Variance) was conducted
with Emotion (angry/neutral) as within-subject factor and Attachment Group
neutral faces (573.53 ms 24.01) within the avoidant attachment
(secure/avoidant/anxious) as between-subjects factor. Follow-up paired sample t- group, t(15) = 4.75, p = 0.0001, 2 p = 0.60, but not within the anxious
tests were used to breakdown interaction effects. (p = 0.91) or secure attachment groups (p = 0.21) (Fig. 2a).

2.7.2. Statistical ERP analysis

To assess the relationship between attachment representation and brain activ-
ity, mean amplitudes for the pre-selected C1 (5080 ms), P1 (80120 ms) and N170
2
The peak amplitude approach to ERPs analyses revealed an overall similar pat-
tern of results (albeit somewhat less pronounced in some instances) as the mean
amplitude approach both for the C1 and P1 components.
3
Analysis of differences in latency to peak amplitude (on both C1 and P1) in
response to angry and neutral faces within each of the attachment groups, as well
as between groups, revealed no signicant Emotion or Group main effects or inter-
actions. Latency values are therefore not reported.
3.1.2. Error rates
Repeated measures ANOVA revealed a signicant Emo-
tion Attachment Group interaction effect, F(2,47) = 3.30, p = 0.04,
2 p = 0.12 with non-signicant Emotion or Group main effects.
Follow-up contrasts within each attachment group showed that
error rates on trials with angry faces were higher (6.03% 1.42)
compared to error rates on trials with neutral faces (4.19% 1.42)
for the anxious attachment group, t(16) = 2.68, p = 0.017, 2 p = 0.31
(Fig. 2b). This difference was not found for the avoidant (p = 0.29)
or secure (p = 0.24) attachment groups.
 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220
(a) 640
Angry
620 Neutral
***
600
580
RT (ms)
560
540
520
500
480
Secure Avoidant Anxious
(b) 9
Angry
8 response to angry compared with neutral faces on right channels
Neutral
7 (Fig. 5c).
6 **
% of errors
5 3.2.3. N170 (120180 ms post face stimulus onset)
4 No signicant main effect of Emotion (F(1,45) = 0.05, p = 0.83,
3 2 p = 0.04) related to the N170 component were observed.
2 The Emotion Group Location (F(4,90) = 1.64, p = 0.17, 2 p = 0.07)
1
0
Secure Avoidant Anxious
Fig. 2. Mean reaction times (a) and mean percent of errors (b) on trials with angry
and neutral faces for the secure, avoidant and anxious attachment groups.
3.2. Electrophysiological data
Grand-averaged ERPs to angry and neutral faces by attachment
group at left, midline and right channels are presented in Fig. 3. Two
participants from the anxious attachment group were excluded
from ERP analyses due to excessive artifacts in the EEG data (In both
cases more than 85% of the segments were bad due to equipment
failure).
3.2.1. C1 (5080 ms post face stimulus onset)
The omnibus ANOVA revealed a main effect of Emotion
such that C1 amplitude was greater (more negative) for neu-
tral faces (0.60 V 0.23) than for angry faces (0.13 V 0.11), in the present study, those P1 and C1 patterns reached statisti-
F(1,45) = 3.98, p = 0.05, 2 p = 0.09. This main effect was sub-
sumed under a signicant Emotion Attachment Group interac-
tion effect, F(2,45) = 5.02, p = 0.011, 2 p = 0.18. Neither Location
(left/midline/right) nor Region (occipital/posterior-parietal) inter-
acted with attachment group. To explicate the Emotion Group
interaction, separate follow-up comparisons (t-tests) between C1
mean amplitudes for angry and neutral faces were conducted
for each attachment group. Signicant differences in C1 ampli-
tude in response to angry (0.04 V 0.14) relative to neutral
(-1.50 V 0.57) faces were observed only within the avoidant
attachment group, t(15) = 2.53, p = 0.02, 2 p = 0.30 and not in the
anxious (p = 0.76) or secure (p = 0.60) attachment groups (Fig. 4).
3.2.2. P1 (80120 ms post face stimulus onset)
The omnibus ANOVA revealed a main effect of Emotion
such that angry faces produced greater (more positive) P1
amplitude (1.55 V 0.28) than neutral faces (0.88 V 0.35),
F(1,45) = 8.15, p = 0.007, 2 p = 0.15. In addition, analysis revealed a
215
signicant Emotion Group interaction effect, F(2,45) = 4.08,
p = 0.02, 2 p = 0.15. This two-way interaction was subsumed under
a three-way interaction effect of Emotion Group Location,
F(4,90) = 6, p = 0.0001, 2 p = 0.21. Since there were no main effects
or interactions involving Region, occipital and posterior-parietal
regions were combined to create a single occipito-parietal region
for post hoc analysis. To explicate the three-way interaction,
Follow-up comparisons (t-tests) between P1 mean amplitudes
for angry and neutral faces were conducted for each attach-
ment group at the left, midline and right locations. Analyses for
both the left and midline locations revealed signicant differ-
ences in P1 amplitude in response to angry faces (1.15 V 0.52;
1.09 V 0.62 on left and midline channels, respectively) com-
pared with neutral faces (0.98 V 0.89; 0.60 V 0.88)
within the avoidant attachment group, t(15) = 2.77, p = 0.014,
2 p = 0.34; t(15) = 2.83, p = 0.013, 2 p = 0.35, but not in the
anxious (ps = 0.80; 0.88) or secure (ps = 0.31;0.17) attachment
groups (Fig. 5a and b). There were no signicant differences in
2 p = 0.001) or Emotion Group interaction (F(2,45) = 0.93, p = 0.40,
and Emotion Group Region (F(2,45) = 0.26, p = 0.77, 2 p = 0.01)
interactions were non-signicant as well.
4. Discussion
The aim of the present study was to examine behavioral and
early ERP correlates of emotional face-processing within adults of
different attachment orientations. We identied ERP correlates of
emotional face-processing by comparing ERPs elicited on trials with
angry and neutral faces. These emotional expression effects were
then compared within and across the secure, anxious and avoidant
attachment groups.
The current electrophysiological results, consistent with ear-
lier studies, indicated that emotional faces triggered an increased
early positivity (P1; 80120 ms) relative to neutral faces (Batty
and Taylor, 2003; Carreti et al., 2004; Pizzagalli et al., 1999;
Pourtois et al., 2004, 2005; Santesso et al., 2008). In contrast, C1
(5080 ms) amplitude was more pronounced (more negative) in
response to the neutral rather than to the angry faces. However,
cal signicance only within the avoidant group and not within the
anxious or secure groups. While individuals with secure and espe-
cially anxious attachment orientations had the same ERP reaction
to both angry and neutral faces, individuals with avoidant attach-
ment showed an early ERP differentiation between the emotional
and neutral faces.
To our knowledge, the current study is among the rst ERP
studies to examine emotional processing biases in relation to
adult attachment. Emotional processing bias effects have been
extensively studied in the context of anxiety disorders. As such,
this literature provides a broader framework for interpreting
our results. Several authors have suggested that the attentional
system of anxious individuals may be abnormally sensitive to
threat-related stimuli in the environment, leading to an even more
pronounced processing bias in favor of threat-related stimulation
than is observed in non-anxious individuals. Such preferential
attention towards threatening information has been assigned
a prominent role in the etiology and maintenance of anxiety
216 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220

Fig. 3. Grand averaged ERPs to angry and neutral faces at left (a; average of channels 31, 33, 35) midline (b; average of channels 34, 36, 37) and right (c; average of channels
38, 39, 40) scalp locations for the secure, avoidant and anxious attachment groups.

disorders and PTSD (for reviews see Bar-Haim et al., 2007; Buckley P1 in response to emotional faces in high-anxious individuals,
et al., 2000; Karl et al., 2006). the time window dened as P1 was later than in the present
In light of this it may seem odd that, in the present study, individ- study. For example, in Holmes et al. (2008) P1 = 120150; in Li
uals with anxious attachment orientation did not differ in their ERPs et al. (2008) P1 = 145175. Felmingham et al. (2003) reported no
in response to angry compared with neutral faces. Theoretically, ERP differences between angry and neutral faces within a PTSD
anxious individuals should be especially attentive to attachment-
related information; however, this hypothesis has received only 0.5
limited empirical support. There is some evidence that attach-
ment anxious adults are vigilant to emotional facial expressions
(Fraley et al., 2006) and show heightened cognitive accessibility of 0
attachment-related material (e.g., Gillath et al., 2005; Mikulincer
*
et al., 2002; Mikulincer and Orbach, 1995). However, other ndings
-0.5
suggest that anxious individuals are less attentive to threatening
material (Van Emmichoven et al., 2003). Secure Avoidant Anxious
C1 modulation by threat stimuli has been observed in previ-
v

-1
ous ERP studies of non-selected populations (Pourtois et al., 2004;
Stolarova et al., 2006). However, there are relatively few studies Angry
examining links between anxiety and early ERP sensory compo- -1.5 Neutral
nents such as the C1 and P1 in response to expressive faces. Of
those conducted, only one (Eldar et al., 2010) reported a more
prominent C1 (60105 ms) in high vs. low anxious participants in -2
response to angry faces (but not in response to happy or neutral
faces). Effects of anxiety on P1 amplitude have been reported by
some groups (e.g., Holmes et al., 2008; Li et al., 2008) but not oth- -2.5
ers (e.g., Bar-Haim et al., 2005; Eldar et al., 2010; Holmes et al.,
Fig. 4. Mean amplitudes of the C1 component (5080 ms) in response to angry and
2009). Moreover, of those who did report a more pronounced neutral faces within the secure, avoidant and anxious attachment groups.
 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220 217

(a) 3 (n = 515), Wei et al. (2003) reported a signicant correlation

LeftChannels
of 0.37 between attachment anxiety and the STAI-T, while the
2.5
correlation between attachment avoidance and the STAI-T reached
2 0.39.
1.5 As stated above, processing biases towards angry faces (in the
P1 component) and towards neutral faces (in the C1 component)
1
were evident only within the avoidant group. It is possible that only
v

0.5
** avoidant participants may have the capacity to distinguish or differ-
0 entiate between threat and non-threat stimuli at such early stages
of information processing. It has been suggested (Adolphs et al.,
-0.5 Secure Avoidant Anxious
2003; Eimer and Holmes, 2007) that the processing of facial expres-
-1 sions consist of two distinct stages: an initial rapid, automatic
Angry
-1.5 detection or discrimination of emotionally signicant stimuli and a
Neutral subsequent higher-level, conscious, processing of emotional facial
-2
expression for the strategic control of thought and action, as well as
for the production of concomitant feeling states. The initial, atten-
(b) 2.5 Midline Channels tive, processing is reected in the early differential ERP components
such as the C1 and P1. The mechanisms underlying such early
2
components have been linked to visual processing of emotional
1.5 stimuli on the basis of rather coarse visual features. These are sup-
posed to be processed via a fast magnocellular route (for reviews:
1
Vuilleumier, 2005; Vuilleumier and Pourtois, 2007), enabling the
rapid detection of emotional stimuli. More specically, an early
v

0.5 **
detection of emotional relevance in the C1 window might be based
0 on a rapid association of the stimulis visual features with some
emotional signicance in primary visual cortex (Rellecke et al.,
-0.5 Secure Avoidant Anxious
2011). The P1 effects have been attributed to enhanced sensory
-1 encoding in visual brain areas as a result of feedback from emo-
tion evaluation centers (e.g., amygdala) in the brain, following the
-1.5
rapid perceptual detection of a motivationally signicant stimulus
(Vuilleumier and Pourtois, 2007). The nding of a more pronounced
(c) 2.5 RightChannels C1 in response to neutral (vs. angry) faces within the avoidant group
was contrary to our initial assumption. However, this assumption
2
was based mainly on reports on individuals with high vs. low trait
1.5 anxiety in the absence of reports on attachment-related anxiety or
avoidance. It might be that for avoidant individuals emotional neu-
1 tral faces bare some special relevance compared with anxious or
secure attached individuals. This should be further investigated. In
v

0.5
0 neutral faces within the avoidant group were observed only at left
Secure Avoidant
-0.5
-1
-1.5
Fig. 5. Mean amplitude of the P1 component (80120 ms) in response to angry and
neutral faces on left (a) midline (b) and right (c) channels within the secure, avoidant
and anxious attachment groups.
group. They concluded that in PTSD there may be a reduced
capacity to discriminate between threat and non-threat stimuli
relative to controls, as neutral stimuli are perceived as ambigu-
ous and therefore potentially as threatening as angry faces. This
notion may also explain why attachment anxiety was not cor-
related with processing bias towards angry faces in the present
study. It seems that further study is needed to specify the inu-
ence of anxiety on early ERP components triggered by emotional
expressions.
Nonetheless, it is important to state that trait anxiety and
attachment anxiety are not necessarily correspondents. For exam-
ple, Van Emmichoven et al. (2003) reported that only 29% of
anxiety disorder outpatients were classied as having attachment
anxiety (preoccupied), whereas 43% were classied as having
attachment avoidance (dismissive). In a much larger sample
addition, the differences in P1 amplitude in response to angry and
Anxious
and midline scalp locations. Analysis of P1 differences at the right
channels revealed a similar pattern to the one described for the left
and midline channels, however, these differences did not reach sta-
tistical signicance. This laterality-related nding is tangential to
the main focus of the current study and further work is required to
explore this seemingly hemispheric asymmetry in the context of
attachment.
According to Mikulincer and Shaver (2003), people using
avoidant strategies to regulate social interactions tend to avoid
negative emotional states that demand attachment-system acti-
vation. Negative facial expressions (such as angry faces) signal
disappointment, disapproval or threat. Individuals with avoidant
attachment strategies are reluctant to confront relational tensions
and unwilling to deal with partners distress and are, therefore,
characterized by a deactivation of their attachment behavioral
system which leads to a down-regulation of interpersonally expe-
rienced emotions (Bartholomew and Horowitz, 1991; Suslow et al.,
2009). For example, in an fMRI study, Suslow et al. (2009) found
that attachment avoidance was inversely related to responses of
the primary somatosensory cortex to masked sad faces. They sug-
gested that reduced generation of somatosensory representations
could reect the neural basis of habitual deactivating strategies of
attachment. Niedenthal et al. (2002) has suggested that avoidant
defensive strategies are the product of a secondary, more effortful
strategy occurring later in the information-processing sequence.
Thus, perhaps avoidant individuals can identify potential sources
218 O. Dan, S. Raz / Biological Psychology 91 (2012) 212220
of threat very quickly at a perceptual level, which then allows
them to inhibit attention to those threats at later stages of
processing.
It might be proposed that in order to apply such higher order
deactivating strategies one must rst attend to and very quickly
discriminate between neutral and emotional attachment-related
stimuli. In light of the present study results, we suggest that early
attentive, non-conscious, discriminative, brain mechanisms may
function more efciently in participants with avoidant, compared
with anxious or secure, attachment styles allowing them to later
ignore and avoid negative thoughts and feelings.
In the current study the N170 ERP to face stimuli was not mod-
ulated by emotional valence nor did it interact with attachment
orientation. This is consistent with others who reported that N170
was not sensitive to emotional facial expressions, as no system-
atic differences in N170 amplitudes or latencies were observed for
emotional as compared to neutral faces (Eimer et al., 2003; Eimer
and Holmes, 2007; Pourtois et al., 2004; Santesso et al., 2008). Oth-
ers have reported, however, larger N170 amplitudes for emotional
compared with neutral faces, especially with regard to fearful faces
(Batty and Taylor, 2003; Blau et al., 2007; Carlson and Reinke, 2010;
Krombholz et al., 2007).
As to the behavioral results of the current study, consistent
with our hypothesis, analysis of behavioral data revealed Emo-
tion Group interactions in both RTs and accuracy (percent of
errors). Participants with avoidant attachment orientation reacted
more slowly following displays of angry faces compared with neu-
tral faces. Such difference was not found for the secure or anxious
groups. In contrast, the percent of errors was higher following dis-
plays of angry faces compared to neutral faces only within the
anxious group but not within the secure or avoidant groups. The
fact that avoidant individuals reacted more slowly to the angry
faces may reect a more cautious processing style which possi-
bly led to less distraction/interference and hence fewer errors in
identifying the gender of the face. These results are in line with
others (e.g., Cooper et al., 2009; Edelstein and Gillath, 2008) who
reported reduction in interference for emotional stimuli among
avoidant attached participants. Conversely, anxious individuals
showed hyper-vigilance to both kinds of faces. They did not pay
closer attention to the angry faces which possibly led to greater dis-
traction/interference and hence higher rate of errors in identifying
the gender of the face.
The present study has some limitations. First, we used only two
types of faces (neutral and angry) since we were mainly inter-
ested in exploring early (attentive) ERPs elicited in response to
negative/threatening emotional stimuli in the general context of
the hypothesized negativity bias. We followed other ERP stud-
ies which focused on the same ERP components as in the current
study and reported a negativity bias in response to angry but not
happy faces in normative and in high anxiety samples (e.g., Eldar
et al., 2010; Santesso et al., 2008). Having said that, in order to
further examine attachment-related differences in early ERP acti-
vation, future studies could include additional facial expressions
such as: sad, fearful and happy.
Second, participants were naive with respect to the specic
questions investigated; it was an implicit emotional task. They were
instructed to respond to the gender of the face (male or female)
rather than to its valence. Hence, their conscious (explicit) atten-
tion was deliberately distracted from the emotional valence of the
face. This may have some unintended consequences in preparing
the ready state differentially across subjects and angry versus neu-
tral faces. It is possible that ERP patterns would have been different
had participants been instructed to respond to the emotionality of
the face. Behavioral and ERP effects related to the gender of the
face stimuli were not investigated in the current study. However,
this may be an important objective for future studies particularly
when using an implicit task, where the participants are told to
respond to the gender of the presented face. Related, another poten-
tial issue within the study involves the gender of participants.4
Since females comprised the majority of participants in the cur-
rent study (64%) the generalizability may be limited here. Third, the
polarity of the C1 component may be sensitive to upper and lower
visual eld effects (Clark et al., 1995) and typically studies assess-
ing C1 effects compensate for this by presenting stimuli in either
the upper or lower visual eld (e.g., Pourtois et al., 2004). How-
ever, in the present study face images were presented centrally.
This may partly explain the relatively low C1 amplitudes elicited in
most conditions (with the exception of C1 amplitude in response to
neutral faces in the avoidant group). Nevertheless, there are recent
reports on C1 effects with centrally presented emotional stimuli
(e.g., Rellecke et al., 2011; Stolarova et al., 2006; Yang et al., 2011).
Future studies may control for this possible involvement of stimuli
spatial presentation. Finally, the current study used an adult attach-
ment self-report questionnaire (the ECR). Future studies could use
additional tools such as the Adult Attachment Inventory to validate
the attachment classication.
In conclusion, the present study represents an important pre-
liminary investigation of early attentive brain mechanisms in
the research eld of adult attachment. Our results revealed that
attachment orientation in adulthood may inuence the percep-
tion of facial expressions in different ways. It demonstrates that
attachment-related differences/interactions in emotional expres-
sions processing emerge at a very early stage of stimulus analysis.
Moreover, our data give support to the proposal (Maier et al., 2005;
Niedenthal et al., 2002; Sonnby-Borgstrm and Jonsson, 2004) that
perceptual biases, which operate at those very early stages of
information processing, may allow avoidant individuals to quickly
identify potential sources of threat that, given additional time and
resources, can subsequently be avoided. In other words, it may be
suggested that, at this early perceptual level, vigilant rather than
defensive style is characteristic of avoidant attachment orienta-
tion. The present study also underscores the usefulness of the ERP
methodology, as a sensitive measure for the study of emotional
processing biases in the research eld of attachment.
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