Biological Psychology 88 (2011) 188–195
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Biological Psychology
jo ur nal homep age : www.elsevier.com/locate/biopsycho
Neural activation during the processing of ambiguous fearful facial expressions:
An ERP study in anxious and nonanxious individuals
Tahl I. Frenkel
∗
, Yair Bar-Haim
The Adler Center for Research in Child Developmental and Psychopathology, Department of Psychology, Tel Aviv University, Tel Aviv 69978, Israel
a r t i c l e i n f o
Article history:
Received 27 December 2010
Accepted 1 August 2011
Available online 16 August 2011
Keywords:
Anxiety
ERP
Threat-processing
Attention bias
Face-processing
a b s t r a c t
Event-related brain potentials (ERPs) were recorded from anxious and nonanxious participants during
performance on a fear detection task. Sequential presentation of gradually increasing fear cues from
neutral to fearful allowed an examination of anxiety-related differences in the neural activation patterns
corresponding to participants’ overt detection of fear in ambiguous stimuli as well as the activation pat-
terns corresponding to stages of fear processing preceding overt fear detection. While centro-parietal Late
Positive Potential (LPP) amplitude of nonanxious participants was significantly modulated by increases
in stimulus fear intensity preceding overt fear detection, no such LPP sensitivity was detected in anx-
ious participants. Additionally, anxiety group differences as well as emotion related modulation were
found for earlier ERP components (P1, P2 and EPN). These findings reveal an anxiety-related dissociation
between the early and late processing stages of threat processing. Implications are discussed in light of
existing theories of cognitive biases in anxiety.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
Behavioral research has documented anxiety-related differ-
ences in the classification of ambiguous threat-related facial
expressions (e.g., Richards et al., 2002). Based on such findings,
biased processing of ambiguously threatening facial cues has been
implicated as an etiologic and maintaining factor in anxiety (e.g.,
Mathews and Mackintosh, 2000; Mathews and MacLeod, 2002;
Mathews et al., 2007; Wilson et al., 2006).
Here we examine the neural correlates of anxiety-related dif-
ferences in the fear detection process. Specifically, event-related
potentials (ERPs) were recorded during a fear detection task in
which interpolated face stimuli were gradually unfolding from
neutral, through mildly fearful, and up to moderately fearful
expressions which eventually elicited an overt detection of fear.
As such, the study design allowed neural activation to be examined
both at the time of overt fear detection, and during the processing
of fears’ precursors in slightly less fearful stimuli not yet eliciting
overt detection of fear.
Previous studies have employed a variety of emotional facial
expressions as threat-related stimuli, for instance angry (e.g., Bar-
Haim et al., 2005; Fox et al., 2002; Horley et al., 2003, 2004; Kolassa
∗
Corresponding author. Tel.: +972 3 6405465; fax: +972 3 6409547.
E-mail address: tahlfren@post.tau.ac.il (T.I. Frenkel).
et al., 2009; Mogg et al., 2004; Mueller et al., 2009; Richards et
al., 2002; Wilson and MacLeod, 2003), fearful (Fox, 2002; Holmes
et al., 2008; Richards et al., 2002), disgust (Gilboa-Schechtman
et al., 1999; Mansell et al., 1999). While some facial expressions
are thought to be highly relevant for specific types of anxiety such
as disgusted faces for socially anxious individuals (Amir et al.,
2010; Cobb et al., 2005), or to elicit specific threat cues (e.g., an
angry face in a frontal presentation), fearful faces are thought to
signal the presence of a diffuse/unknown danger in the immedi-
ate environment thus, serving as a threatening stimulus that is
generally effective across a wide range of contexts. Indeed, neu-
roimaging research indicates that fearful faces elicit the strongest
fear-circuitry response (e.g., Dolan and Vuilleumier, 2003). Thus,
here we examine anxiety-related differences in the fear detection
process.
Threat detection in faces is comprised of several stages of infor-
mation processing that can be grossly divided into early processes
such as stimulus encoding and selective allocation of attention,
and late strategic processes reflecting sustained motivated atten-
tion and stimulus interpretation. In attempt to provide further
information on the time course and neural correlates of these, the
present study focused on the examination of both early and late
ERP components that are thought to differentially reflect these dis-
tinct cognitive processes. Specifically, early ERP components such
as the attention-related P1 (e.g., Batty and Taylor, 2003; Eimer and
Holmes, 2002, 2007; Holmes et al., 2003; Streit et al., 2003) and P2
0301-0511/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.biopsycho.2011.08.001