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Biological Psychology 91 (2012) 212220

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

(ERPs) study
Orrie Dan a,1 , Sivan Raz a,b,,1
Department of Psychology, The Center for Psychobiological Research, The Max Stern Academic College of Emek Yezreel, Israel
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
(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
2012 Elsevier B.V. All rights reserved.

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

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

0301-0511/$ see front matter 2012 Elsevier B.V. All rights reserved.
O. Dan, S. Raz / Biological Psychology 91 (2012) 212220 213

In this two-dimensional space, the secure style is a region threat-related (angry) faces has been demonstrated in visual search
where both anxiety and avoidance are low. Secure individuals tasks using both schematic (Eastwood et al., 2001; Fox et al., 2000)
show neither of these biases and exhibit balanced and moderate and real (Horstmann and Bauland, 2006; Williams et al., 2005) face
responses to emotional information and events (Shaver and Hazan, stimuli.
1993). In general, we hypothesized that attachment orientation would
Despite theoretical claims and considerable evidence that indi- interact with behavioral and ERP patterns in response to angry
vidual differences in attachment security provide a foundation for facial expressions, compared with neutral expressions. More
emotional perception (Sroufe et al., 2005), surprisingly few stud- specically, we hypothesized (following Edelstein, 2006; Fraley
ies have investigated the specic neural mechanisms underlying et al., 2000) that in order for attachment-avoidant individuals to
these patterns. Most of the literature integrating attachment and apply deactivating/defensive strategies, they must rst attend to
neuroscience is theoretical rather than empirical, and studies of the the valence of a face stimulus and must very quickly differentiate
neural circuitry associated with attachment are quite rare (Coan, emotional faces from neutral ones. Therefore, we expected process-
2008). ing bias reected in longer RTs, as well as differential (i.e., greater)
The aim of the present study was to identify patterns of C1 and P1 amplitudes in response to angry compared to neutral
behavioral responses and brain activity during emotion percep- faces within the avoidant group. In contrast, at these very early
tion among adults with differing attachment representations. More stages of information processing, attachment-anxious individuals
specically, we sought to explore the interaction effects between may be equally attentive and hyper-vigilant to all kinds of faces
attachment anxiety and avoidance and the initial neural changes in the environment. We therefore expected anxious individuals to
associated with automatic attention to emotional facial expres- have the same RTs as well as the same C1 and P1 amplitudes in
sions. response both to angry and to neutral faces. In other words, we
Electroencephalogram-Event Related Potentials (EEG-ERPs), a hypothesized that avoidant rather than anxious individuals would
technique used to investigate the temporal brain dynamics of atten- show an early processing bias towards emotional faces.
tive processing at ne temporal resolution, was the method of
choice. Since evaluation of emotional faces seems to occur as early 2. Methods
as 100 ms following stimulus presentation (Halgren et al., 2000; Liu
2.1. Participants
et al., 2002), we focused on the early C1 and P1 ERP components.
ERP dot-probe studies with healthy adults have shown emotion- Participants were 50 undergraduate students (32 females), mean age
related modulation in the C1 component time locked to the faces 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
display (Pourtois et al., 2004) and in the P1 component time locked
allocated to three attachment groups. Those with low scores both on avoidance and
to target onset (Pourtois et al., 2004; Santesso et al., 2008). The C1 anxiety scales were allocated to the secure group (n = 17; 11 females). Those with
component (50100 ms post-stimulus) is the rst ERP component low scores on the avoidance scale and high scores on the anxiety scale were allo-
triggered by the appearance of a stimulus in the visual eld and is cated to the anxious group (n = 17; 11 females) and, those with high scores on the
thought to be pre-attentive and independent of spatial attention 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
(Clark and Hillyard, 1996; Foxe and Simpson, 2002; Fu et al., 2005;
a prior history of neurological or psychiatric disorders. All of them gave informed
Hillyard and Anllo-Vento, 1998; Stolarova et al., 2006). C1 has been consent. The experiment was approved by the academic committee of the Yezreel
found to be more intense in displays containing threatening faces Valley College.
than in displays containing non-threatening faces (Pourtois et al.,
2004). It has been suggested that the modulation of C1 by the emo- 2.2. Assessment of attachment
tional valence of the cue display on the dot-probe task could be the
One to two weeks before the ERP experiment, 363 undergraduate students
consequence of an interaction between the primary visual cortex completed a Hebrew version of the Experiences in Close Relationships (ECR) scale
and the subcortical limbic structures responsible for the detection (Brennan et al., 1998). This self-report questionnaire assesses individual differences
of threats (Pourtois et al., 2004; Stolarova et al., 2006). The P1 on the two major dimensions of adult attachment style: avoidance of intimacy and
component, an early sensory component peaking around 100 ms 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
post-stimulus, may constitute an index of mobilization of auto-
down), as does the Anxiety scale (e.g., I worry about being abandoned). Each item is
matic attentional resources (see review in Hopnger and Mangun, rated on a 7-point scale ranging from 1 (not at all) to 7 (very much). This two-
2001). Carreti et al. (2004) reported that automatic attention (P1) dimensional perspective for representing attachment relationships is considered
is initially captured by negative pictures rather than by those that the gold-standard in self-report measures of adult-attachment (Brennan et al.,
1998; Mikulincer and Shaver, 2007). In the current study, internal consistencies
are positive or non-emotional. According to these researchers, the
were = 0.86 for the anxiety and = 0.83 for the avoidance subscales.
fact that negative stimuli mobilize attentional resources as early as
105 ms post-stimulus is probably a manifestation of the negativity 2.3. Stimuli
To the best of our knowledge, only two ERP studies have Photographs of faces of 20 different individuals, 10 male and 10 female, were
examined the relations between attachment orientation and facial 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
emotional perception (Fraedrich et al., 2010; Zhang et al., 2008).
or neutral. Each actor presented both angry and neutral faces and each face was
Another ERP study used emotional pictures from the IAPS as stim- presented four times, resulting in a total of 160 stimuli (divided into four blocks
uli (Zilber et al., 2007). All of these studies reported relatively late of 40 trials each). All trials began with a 1000 ms xation display (white cross on
ERP (N170 and later) differences between attachment orientations. 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)
In the present study, we sought to identify ERP correlates of
of 1000 ms. The experiment began with a short practice block which contained neu-
emotional face-processing by comparing early ERPs (C1 and P1) tral and angry faces corresponding to those presented in the experimental blocks.
elicited in trials using angry and neutral faces. Emotional expres- Participants were allowed a rest period after the practice block. In the experimental
sion effects were then compared across groups with secure, anxious session, targets were displayed with equal probability and their presentation was
and avoidant attachment orientations. The perception of angry randomized between trials.

faces may be suitable for studies of attachment, since such facial

2.4. Procedure
expressions signal social disapproval and threat and the violation of
social rules or expectations (Averill, 1983; hman, 1986; Santesso Participants were seated in a comfortable chair in a dimly lit room at a distance
et al., 2008). In healthy populations, a processing bias toward 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
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- 3.1.2. Error rates
ity, mean amplitudes for the pre-selected C1 (5080 ms), P1 (80120 ms) and N170 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.
The peak amplitude approach to ERPs analyses revealed an overall similar pat- Follow-up contrasts within each attachment group showed that
tern of results (albeit somewhat less pronounced in some instances) as the mean error rates on trials with angry faces were higher (6.03% 1.42)
amplitude approach both for the C1 and P1 components. compared to error rates on trials with neutral faces (4.19% 1.42)
Analysis of differences in latency to peak amplitude (on both C1 and P1) in for the anxious attachment group, t(16) = 2.68, p = 0.017, 2 p = 0.31
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-
(Fig. 2b). This difference was not found for the avoidant (p = 0.29)
actions. Latency values are therefore not reported. or secure (p = 0.24) attachment groups.
O. Dan, S. Raz / Biological Psychology 91 (2012) 212220 215

(a) 640 signicant Emotion Group interaction effect, F(2,45) = 4.08,

p = 0.02, 2 p = 0.15. This two-way interaction was subsumed under
620 Neutral 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
580 regions were combined to create a single occipito-parietal region
RT (ms)

for post hoc analysis. To explicate the three-way interaction,

560 Follow-up comparisons (t-tests) between P1 mean amplitudes
540 for angry and neutral faces were conducted for each attach-
ment group at the left, midline and right locations. Analyses for
520 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-
480 pared with neutral faces (0.98 V 0.89; 0.60 V 0.88)
Secure Avoidant Anxious 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
(b) 9
anxious (ps = 0.80; 0.88) or secure (ps = 0.31;0.17) attachment
Angry groups (Fig. 5a and b). There were no signicant differences in
8 response to angry compared with neutral faces on right channels
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,
2 p = 0.001) or Emotion Group interaction (F(2,45) = 0.93, p = 0.40,
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)
and Emotion Group Region (F(2,45) = 0.26, p = 0.77, 2 p = 0.01)
interactions were non-signicant as well.
Secure Avoidant Anxious

Fig. 2. Mean reaction times (a) and mean percent of errors (b) on trials with angry
4. Discussion
and neutral faces for the secure, avoidant and anxious attachment groups.
The aim of the present study was to examine behavioral and
early ERP correlates of emotional face-processing within adults of
3.2. Electrophysiological data
different attachment orientations. We identied ERP correlates of
emotional face-processing by comparing ERPs elicited on trials with
Grand-averaged ERPs to angry and neutral faces by attachment
angry and neutral faces. These emotional expression effects were
group at left, midline and right channels are presented in Fig. 3. Two
then compared within and across the secure, anxious and avoidant
participants from the anxious attachment group were excluded
attachment groups.
from ERP analyses due to excessive artifacts in the EEG data (In both
The current electrophysiological results, consistent with ear-
cases more than 85% of the segments were bad due to equipment
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;
3.2.1. C1 (5080 ms post face stimulus onset) Pourtois et al., 2004, 2005; Santesso et al., 2008). In contrast, C1
The omnibus ANOVA revealed a main effect of Emotion (5080 ms) amplitude was more pronounced (more negative) in
such that C1 amplitude was greater (more negative) for neu- response to the neutral rather than to the angry faces. However,
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- cal signicance only within the avoidant group and not within the
sumed under a signicant Emotion Attachment Group interac- anxious or secure groups. While individuals with secure and espe-
tion effect, F(2,45) = 5.02, p = 0.011, 2 p = 0.18. Neither Location cially anxious attachment orientations had the same ERP reaction
(left/midline/right) nor Region (occipital/posterior-parietal) inter- to both angry and neutral faces, individuals with avoidant attach-
acted with attachment group. To explicate the Emotion Group ment showed an early ERP differentiation between the emotional
interaction, separate follow-up comparisons (t-tests) between C1 and neutral faces.
mean amplitudes for angry and neutral faces were conducted To our knowledge, the current study is among the rst ERP
for each attachment group. Signicant differences in C1 ampli- studies to examine emotional processing biases in relation to
tude in response to angry (0.04 V 0.14) relative to neutral adult attachment. Emotional processing bias effects have been
(-1.50 V 0.57) faces were observed only within the avoidant extensively studied in the context of anxiety disorders. As such,
attachment group, t(15) = 2.53, p = 0.02, 2 p = 0.30 and not in the this literature provides a broader framework for interpreting
anxious (p = 0.76) or secure (p = 0.60) attachment groups (Fig. 4). our results. Several authors have suggested that the attentional
system of anxious individuals may be abnormally sensitive to
3.2.2. P1 (80120 ms post face stimulus onset) threat-related stimuli in the environment, leading to an even more
The omnibus ANOVA revealed a main effect of Emotion pronounced processing bias in favor of threat-related stimulation
such that angry faces produced greater (more positive) P1 than is observed in non-anxious individuals. Such preferential
amplitude (1.55 V 0.28) than neutral faces (0.88 V 0.35), attention towards threatening information has been assigned
F(1,45) = 8.15, p = 0.007, 2 p = 0.15. In addition, analysis revealed a 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
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-

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

of 0.37 between attachment anxiety and the STAI-T, while the
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)
were evident only within the avoidant group. It is possible that only

** 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
-1.5 detection or discrimination of emotionally signicant stimuli and a
Neutral subsequent higher-level, conscious, processing of emotional facial
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
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:
Vuilleumier, 2005; Vuilleumier and Pourtois, 2007), enabling the
rapid detection of emotional stimuli. More specically, an early

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
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
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

addition, the differences in P1 amplitude in response to angry and
0 neutral faces within the avoidant group were observed only at left
Secure Avoidant Anxious
and midline scalp locations. Analysis of P1 differences at the right
channels revealed a similar pattern to the one described for the left
-1 and midline channels, however, these differences did not reach sta-
tistical signicance. This laterality-related nding is tangential to
-1.5 the main focus of the current study and further work is required to
Fig. 5. Mean amplitude of the P1 component (80120 ms) in response to angry and
explore this seemingly hemispheric asymmetry in the context of
neutral faces on left (a) midline (b) and right (c) channels within the secure, avoidant attachment.
and anxious attachment groups. 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
group. They concluded that in PTSD there may be a reduced disappointment, disapproval or threat. Individuals with avoidant
capacity to discriminate between threat and non-threat stimuli attachment strategies are reluctant to confront relational tensions
relative to controls, as neutral stimuli are perceived as ambigu- and unwilling to deal with partners distress and are, therefore,
ous and therefore potentially as threatening as angry faces. This characterized by a deactivation of their attachment behavioral
notion may also explain why attachment anxiety was not cor- system which leads to a down-regulation of interpersonally expe-
related with processing bias towards angry faces in the present rienced emotions (Bartholomew and Horowitz, 1991; Suslow et al.,
study. It seems that further study is needed to specify the inu- 2009). For example, in an fMRI study, Suslow et al. (2009) found
ence of anxiety on early ERP components triggered by emotional that attachment avoidance was inversely related to responses of
expressions. the primary somatosensory cortex to masked sad faces. They sug-
Nonetheless, it is important to state that trait anxiety and gested that reduced generation of somatosensory representations
attachment anxiety are not necessarily correspondents. For exam- could reect the neural basis of habitual deactivating strategies of
ple, Van Emmichoven et al. (2003) reported that only 29% of attachment. Niedenthal et al. (2002) has suggested that avoidant
anxiety disorder outpatients were classied as having attachment defensive strategies are the product of a secondary, more effortful
anxiety (preoccupied), whereas 43% were classied as having strategy occurring later in the information-processing sequence.
attachment avoidance (dismissive). In a much larger sample 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 when using an implicit task, where the participants are told to
them to inhibit attention to those threats at later stages of respond to the gender of the presented face. Related, another poten-
processing. tial issue within the study involves the gender of participants.4
It might be proposed that in order to apply such higher order Since females comprised the majority of participants in the cur-
deactivating strategies one must rst attend to and very quickly rent study (64%) the generalizability may be limited here. Third, the
discriminate between neutral and emotional attachment-related polarity of the C1 component may be sensitive to upper and lower
stimuli. In light of the present study results, we suggest that early visual eld effects (Clark et al., 1995) and typically studies assess-
attentive, non-conscious, discriminative, brain mechanisms may ing C1 effects compensate for this by presenting stimuli in either
function more efciently in participants with avoidant, compared the upper or lower visual eld (e.g., Pourtois et al., 2004). How-
with anxious or secure, attachment styles allowing them to later ever, in the present study face images were presented centrally.
ignore and avoid negative thoughts and feelings. This may partly explain the relatively low C1 amplitudes elicited in
In the current study the N170 ERP to face stimuli was not mod- most conditions (with the exception of C1 amplitude in response to
ulated by emotional valence nor did it interact with attachment neutral faces in the avoidant group). Nevertheless, there are recent
orientation. This is consistent with others who reported that N170 reports on C1 effects with centrally presented emotional stimuli
was not sensitive to emotional facial expressions, as no system- (e.g., Rellecke et al., 2011; Stolarova et al., 2006; Yang et al., 2011).
atic differences in N170 amplitudes or latencies were observed for Future studies may control for this possible involvement of stimuli
emotional as compared to neutral faces (Eimer et al., 2003; Eimer spatial presentation. Finally, the current study used an adult attach-
and Holmes, 2007; Pourtois et al., 2004; Santesso et al., 2008). Oth- ment self-report questionnaire (the ECR). Future studies could use
ers have reported, however, larger N170 amplitudes for emotional additional tools such as the Adult Attachment Inventory to validate
compared with neutral faces, especially with regard to fearful faces the attachment classication.
(Batty and Taylor, 2003; Blau et al., 2007; Carlson and Reinke, 2010; In conclusion, the present study represents an important pre-
Krombholz et al., 2007). liminary investigation of early attentive brain mechanisms in
As to the behavioral results of the current study, consistent the research eld of adult attachment. Our results revealed that
with our hypothesis, analysis of behavioral data revealed Emo- attachment orientation in adulthood may inuence the percep-
tion Group interactions in both RTs and accuracy (percent of tion of facial expressions in different ways. It demonstrates that
errors). Participants with avoidant attachment orientation reacted attachment-related differences/interactions in emotional expres-
more slowly following displays of angry faces compared with neu- sions processing emerge at a very early stage of stimulus analysis.
tral faces. Such difference was not found for the secure or anxious Moreover, our data give support to the proposal (Maier et al., 2005;
groups. In contrast, the percent of errors was higher following dis- Niedenthal et al., 2002; Sonnby-Borgstrm and Jonsson, 2004) that
plays of angry faces compared to neutral faces only within the perceptual biases, which operate at those very early stages of
anxious group but not within the secure or avoidant groups. The information processing, may allow avoidant individuals to quickly
fact that avoidant individuals reacted more slowly to the angry identify potential sources of threat that, given additional time and
faces may reect a more cautious processing style which possi- resources, can subsequently be avoided. In other words, it may be
bly led to less distraction/interference and hence fewer errors in suggested that, at this early perceptual level, vigilant rather than
identifying the gender of the face. These results are in line with defensive style is characteristic of avoidant attachment orienta-
others (e.g., Cooper et al., 2009; Edelstein and Gillath, 2008) who tion. The present study also underscores the usefulness of the ERP
reported reduction in interference for emotional stimuli among methodology, as a sensitive measure for the study of emotional
avoidant attached participants. Conversely, anxious individuals processing biases in the research eld of attachment.
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. Adolphs, R., Tranel, D., Damasio, A.R., 2003. Dissociable neural systems for recogniz-
The present study has some limitations. First, we used only two ing emotions. Brain and Cognition 52, 6169.
types of faces (neutral and angry) since we were mainly inter- Andersson, F., Etard, O., Denise, P., Petit, L., 2004. Early visual evoked potentials are
modulated by eye position in humans induced by whole body rotations. BMC
ested in exploring early (attentive) ERPs elicited in response to Neuroscience 5, 35.
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Bar-Haim, Y., Lamy, D., Glickman, S., 2005. Attentional bias in anxiety: a behavioral
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We tested gender-related differences in mean amplitude of the C1 and P1 com-
face. This may have some unintended consequences in preparing ponents in response to angry and neutral faces at occipital and posterior-parietal
the ready state differentially across subjects and angry versus neu- locations. Analysis (t-tests) revealed no signicant differences between male and
tral faces. It is possible that ERP patterns would have been different female subjects. C1: occipital channels: t(46) = 0.46, p = 0.64; t(46) = 1.35, p = 0.20
had participants been instructed to respond to the emotionality of for angry and neutral faces, respectively, posterior-parietal channels: t(46) = 0.28,
p = 0.78; t(46) = 1.42, p = 0.17 for angry and neutral faces, respectively. P1: occipi-
the face. Behavioral and ERP effects related to the gender of the tal channels: t(46) = 0.76, p = 0.45; t(46) = 0.61, p = 0.54 for angry and neutral faces,
face stimuli were not investigated in the current study. However, respectively. Posterior-parietal channels: t(46) = 0.46, p = 0.65; t(46) = 1.05, p = 0.30
this may be an important objective for future studies particularly for angry and neutral faces, respectively.
O. Dan, S. Raz / Biological Psychology 91 (2012) 212220 219

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