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Anxiety, Stress, & Coping: An


International Journal
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Assessing the role of spatial


engagement and disengagement of
attention in anxiety-linked attentional
bias: a critique of current paradigms
and suggestions for future research
directions
a a b
Patrick J.F. Clarke , Colin MacLeod & Adam J. Guastella
a
School of Psychology , The University of Western Australia ,
Crawley , WA , 6009 , Australia
b
Brain & Mind Research Institute, University of Sydney , Sydney ,
NSW , 2050 , Australia
Accepted author version posted online: 09 Nov 2011.Published
online: 05 Dec 2011.

To cite this article: Patrick J.F. Clarke , Colin MacLeod & Adam J. Guastella (2013) Assessing the
role of spatial engagement and disengagement of attention in anxiety-linked attentional bias: a
critique of current paradigms and suggestions for future research directions, Anxiety, Stress, &
Coping: An International Journal, 26:1, 1-19, DOI: 10.1080/10615806.2011.638054

To link to this article: http://dx.doi.org/10.1080/10615806.2011.638054

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Anxiety, Stress, & Coping, 2013
Vol. 26, No. 1, 119, http://dx.doi.org/10.1080/10615806.2011.638054

Assessing the role of spatial engagement and disengagement of attention


in anxiety-linked attentional bias: a critique of current paradigms and
suggestions for future research directions
Patrick J.F. Clarkea*, Colin MacLeoda and Adam J. Guastellab
a
School of Psychology, The University of Western Australia, Crawley, WA 6009, Australia;
b
Brain & Mind Research Institute, University of Sydney, Sydney, NSW 2050, Australia
(Received 4 July 2011; final version received 1 November 2011)
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A considerable volume of research has demonstrated an anxiety-linked atten-


tional bias characterized by selective processing of threat stimuli. The last decade
has seen growing interest in identifying the precise attentional mechanisms which
underlie such selective processing to advance both theoretical and etiological
models of anxiety. This research has particularly focused on the roles of spatial
engagement and disengagement of attention. The relative contribution of these
attentional components to selective processing of threat in anxious individuals
remains unclear however. Moreover, we argue here that many of the tasks
employed to examine these mechanisms, may not be capable of indexing the
attentional processes that they claim to measure. In this article, we provide a
methodological review, critically evaluating the adequacy of previous tasks
employed to measure biased attentional engagement and disengagement. Based
on a number of concerns raised about the ability of such tasks to differentiate
these component attentional processes, we detail three task criteria that we believe
are essential to be confident that a task will accurately index biased attentional
engagement with, and disengagement from threat in anxious participants.
Keywords: anxiety; biased attention; attentional engagement; attentional
disengagement

Introduction
Individuals who are vulnerable to anxious mood demonstrate an attentional bias
favoring the processing of threatening stimuli, compared to participants less
susceptible to anxiety. A recent meta-analysis concluded that the threat-related
bias in anxious individuals is an exceedingly consistent research finding that ‘‘cannot
be reduced to insignificance in the next 11,339 studies, even if those studies yielded
only null results’’ (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van
Ijzendoorn, 2007, p. 15). It is now accepted that this preferential threat bias is part of
the cognitive architecture of anxiety and the development of interventions which
directly modify threat biases have further demonstrated its critical role in maintain-
ing anxiety (Hakamata et al., 2010). The robustness of the relationship between
biased attention and anxiety has highlighted the importance of moving the focus of
cognitive bias research from establishing the presence of this relationship, to

*Corresponding author. Email: patrick.clarke@uwa.edu.au


# 2013 Taylor & Francis
2 P.J.F. Clarke et al.

illuminating the attentional mechanisms which contribute to selective attention in


anxiety (Bar-Haim et al., 2007). Of central importance to this issue is the need to
establish whether attentional selectivity in anxiety results from preferential attention
engagement with emotionally threatening stimuli, or from selective difficulty
disengaging attention from such information once it has been identified.
The last decade has seen increasing interest in discriminating the roles of biased
attentional engagement and disengagement in anxiety-linked attentional bias.
Researchers have developed a number of attention assessment tasks in an attempt
to measure these processes. In a recent review of attentional bias research, Cisler and
Koster (2010) highlighted that a growing body of research which posits support for
the hypothesis that anxious individuals have difficulty disengaging attention from
threat. However, while it provides a useful summary of recent empirical data, and the
conclusions drawn by the researchers on the basis of these, it did not seek to critically
evaluate the methodological limitations of the tasks used to generate these findings.
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The absence of such critical evaluation in recent reviews and in the wider literature
has led to conclusions based on tasks which may not be truly capable of accurately
indexing the constructs that they are intended to measure. We argue that research
paradigms recently adopted to differentiate biased engagement and disengagement
of spatial attention in anxiety do not adequately isolate and index these attentional
processes and potentially compromise the conclusions derived from studies which
have employed these tasks.
In the following critique, we define the relevant attentional constructs and discuss
why identifying the relative contributions of each to selective attention in anxiety is
of considerable theoretical and applied importance. We briefly review how those
measures which originally revealed the presence of anxiety-linked selective atten-
tional cannot serve to differentiate between biased attentional engagement and
disengagement, before providing a detailed critique of recently adopted research
paradigms. Finally, we conclude by detailing three key criteria that we suggest
researchers should adhere to when developing measures of attentional engagement
and disengagement and, provide examples of how these may be met, by describing
the types of experimental paradigms that can fulfill these criteria.

Components of movement in spatial attention


The components of attentional movement have been thoroughly described by past
researchers, though their role in biased attention to threat has been largely ignored
until quite recently. Orienting of attention can be decomposed into three critical
component processes (Posner, 1980; Posner & Petersen, 1990). Attentional ‘‘engage-
ment’’ refers to the selection and preferential processing of a specific stimulus or
location. The process of ‘‘shifting’’ involves the movement of attention. ‘‘Disengage-
ment’’ refers to the withdrawal of attention via the cessation of selection and
preferential processing of a stimulus. Thus, when a new stimulus or location is
selected for processing, attention is first disengaged from the current object of focus,
and a shift then occurs before attention then engages with the new stimulus or
location. In this article, we use the terms attentional engagement and attentional
disengagement in line with these precise meanings.
Posner (1980) developed an attentional cueing paradigm to assess these specified
components of visual attention. In this task, attention is initially directed to the left
Anxiety, Stress, & Coping 3

or right of a central fixation point via the brief presentation of a cue, such as the
brightening of one area of a screen. On the majority of trials (80%), the
cue accurately predicts the location of a to-be-identified target (valid trials), while
on the remaining trials the target appears in the location opposite the initial cue
(invalid trials). Using this task, Posner, Inhoff, Friedrich and Cohen (1987) found
that targets were detected faster on valid trials, as compared to invalid trials. Slowing
on invalid trials was attributed to costs of having to disengage from the cued
location, and engage with the target appearing in the opposite location. In
considering the discrete components which contribute to orienting of attention as
described by Posner, it is readily apparent that biased attention to threatening
material could be affected by selectivity operating within either, or both the
engagement and/or disengagement process. With reference to anxiety-linked selective
processing of threat, we here use the term biased attentional engagement to
specifically describe the rapid orientation of attention to a threat stimulus due to
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its enhanced ability to ‘‘capture’’ or ‘‘draw’’ attention. Conversely, we use the term
biased attentional disengagement to describe delayed withdrawal of attention from a
threat stimulus due to its ability ‘‘hold’’ attention.
The question of whether biased attentional engagement and/or disengagement
underpin selective attentional response to threat in anxiety is important for a number
of theoretical and applied reasons. While most theoretical models implicate the role
of selective attention in anxiety, few make specific predictions about the role of
attentional engagement and disengagement. Beck’s schema model, for example
(Beck, 1976; Beck & Clark, 1997; Beck, Emery, & Greenberg, 2005), predicts that
high trait anxious individuals will exhibit an attentional preference for stimuli which
are emotionally threatening in tone, but makes no predictions about the contribu-
tions of attentional engagement and disengagement. Williams, Watts, MacLeod, and
Mathews’ (1997) integrative processing model is perhaps one of the few cognitive
models that does implicate one of these specific attentional mechanisms, albeit
indirectly. This model of emotional vulnerability proposes that high trait anxiety is
associated with highly integrated representations of threatening information. Such
integrated representations will lead to partial matches in the environment activating
the entire representation. Williams et al.’s model specifically predicts that this will
lower the threshold for detecting anxiety-congruent information in individuals more
vulnerable to anxious mood, resulting in rapid detection of threatening material.
Unlike Beck’s, this model thereby implicates biased attentional engagement, through
rapid detection and preferential processing of threat stimuli.
The theoretical models outlined earlier share in common the premise that
selective attention to threat causally mediates anxiety vulnerability. Consistent with
this, experimental procedures designed to induce an attention bias toward or away
from threat stimuli by systematically manipulating attentional processing has been
shown to affect vulnerability to experience anxious mood in response to a stressor
(Eldar, Ricon, & Bar-Haim, 2008; MacLeod, Rutherford, Campbell, Ebsworthy, &
Holker, 2002; Mathews & MacLeod, 2002). Such attention manipulation tasks,
originally developed to test this causal account of the relationship between
attentional bias and anxiety, are now also showing considerable applied potential
in remediating pathological anxiety. A number of studies have now demonstrated
that completing a computer task which encourages selective processing of neutral
rather than threat stimuli a number of times, over several days or weeks, can
4 P.J.F. Clarke et al.

significantly attenuate anxiety symptoms (cf. Hakamata et al., 2010; MacLeod,


Koster, & Fox, 2009). Clearly, the demonstrated therapeutic benefit of attention
modification procedures highlights the importance of determining whether biased
spatial attention to threat in anxiety reflects enhanced attentional engagement with,
or impaired disengagement from, threatening information. When the nature of the
attentional bias that sustains anxiety vulnerability is clearly established, then this
particular aspect of attentional selectivity can become the key target for therapeutic
change, within interventions that attempt to remediate dysfunctional anxiety through
the direct modification of attentional bias.

Two dominant approaches to the measurement of anxiety-linked attentional bias


A comprehensive description of tasks that have been used to examine biased
attention in anxiety can be found in recent reviews of this research literature (e.g.,
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Cisler & Koster, 2010; Yiend, 2010). Here we will briefly discuss two of the more
dominant methods used to assess biased attention, using these as exemplars to
illustrate the difficulties associated with distinguishing biased attentional engagement
from biased attentional disengagement. Specifically, we consider the emotional
Stroop task (Mathews & MacLeod, 1985) and attentional probe tasks (MacLeod,
Mathews, & Tata, 1986), which have been instrumental in establishing the presence
of selective attention for threat in anxious individuals.
The emotional Stroop task typically involves presenting individual threat and
neutral stimulus words in colored text to participants who differ in anxiety
vulnerability. Longer color-naming latencies for words of a specific valence are
taken to indicate selective processing of the semantic content of these words. The
consistent observation that both highly anxious and clinically anxious individuals is
disproportionately slow to color-name threat as compared to neutral words (e.g.,
Egloff & Hock, 2001; Mathews & MacLeod, 1985; Rutherford, MacLeod, &
Campbell, 2004) has been taken as evidence that such individuals selectively attend
to the content of more threatening stimuli.
Findings from the Emotional Stroop task can be equally attributed to a bias in
either attentional engagement with, or disengagement from the content of threat
stimuli. A biased attentional engagement account of the effect would maintain that
anxious individuals preferentially engage attention with the content of negative
words, resulting in longer latencies to color-name threat words. Alternatively, a
biased attentional disengagement account would maintain that anxious and non-
anxious individuals may both equally engage attention with the content of
threatening material initially, but anxious individuals have particular difficulty
then disengaging attention from stimulus meaning to process the text color, resulting
in longer color-naming latencies.
The attentional probe paradigm was designed to provide a measure of spatial
attention and overcome critical limitations of the emotional Stroop task (MacLeod
et al., 1986). Because the emotional Stroop presents only a single threat or neutral
word on any trial, it is possible that the observed effects could be explained by
behavioral freezing in the presence of threat for anxious individuals, which operates
independently of any attentional bias. This alternative possibility suggests that even
when individuals who differ according to anxiety vulnerability devote equivalent
attention to threatening stimuli, they differ in the extent to which this invokes
Anxiety, Stress, & Coping 5

behavioral freezing. Indeed a recent study by Mogg, Holmes, Garner, and Bradley
(2008) demonstrated just this, revealing that when no movement of attention is
required reaction times were significantly slower for high trait anxious individuals as
compared to those with low trait anxiety, when presented with threatening stimuli
within an already attended locus. The attentional probe task overcomes this problem
by presenting both threat and neutral stimuli on each trial, thus controlling for any
general slowing in the presence of threat, as threat stimuli are present on every trial.
This paradigm involves the simultaneous presentation of the threat and neutral
stimulus on a computer screen for a brief duration (e.g., 500 ms). The distribution of
attention is inferred from the pattern of latencies to identify a small probe that
appears in the locus of either the threat or neutral stimulus, after the initial display is
terminated. Shorter latencies to identify probes appearing in the locus of one
stimulus category suggest attention to this type of stimulus. Results from studies
employing the attentional probe task have consistently shown that individuals more
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vulnerable to anxiety are faster to identify probes appearing in the locus of threat as
compared to neutral stimuli (Mogg, Philippot, & Bradley, 2004; Musa, Lepine,
Clark, Mansell, & Ehlers, 2003; Tata, Leibowitz, Prunty, Cameron, & Pickering,
1996).
Although the attentional probe task provides convincing evidence that anxious
individuals show selective alignment of spatial attention with threatening stimuli, a
bias in either attentional engagement or attentional disengagement can equally well
account for the findings observed using this task. If anxiety is characterized by
selective engagement with threatening material then this would result in shorter
latencies to identify probes in their vicinity due to preferential orienting of attention
to this locus. If anxiety is characterized by biased attentional disengagement, then
anxious individuals will initially engage attention equally often with either the
threatening or neutral stimuli, but, will be less likely to move attention away from the
locus of initially attended stimuli when it is threatening. This increased tendency to
remain in the locus of threatening material will result in shorter latencies to detect
probes appearing in the same spatial locus, relative to probes appearing in the
opposite location (i.e., in the vicinity of neutral stimuli). Therefore, as with results
from the emotional Stroop task, the findings from the attentional probe task may be
explained either in terms of biased attentional engagement with, or disengagement
from, threat in anxious individuals.

Attempts to dissociate biased engagement and disengagement of spatial attention in


anxiety
It is now accepted that past experimental paradigms do not have the capacity to
clarify whether selective attention in anxiety is associated with biased attentional
engagement or disengagement. This has led to a number of attempts to discriminate
these component processes through the development of new experimental tasks. In
the following we briefly review a number of methodological approaches developed to
examine biased attentional engagement and disengagement in anxiety, describing the
experimental findings, and conclusions that have been drawn on the basis of these. Of
these different experimental approaches, the modified version of Posner et al.’s (1987)
attentional cueing task has been by far the most widely used. Because this task has
been most consistently used by studies attempting to differentiate biased attentional
6 P.J.F. Clarke et al.

engagement and disengagement, and consequently has made the most significant
impact on this research area, our critique places particular focuses on evaluating the
methodological adequacy of this paradigm. However, we also consider other recent
experimental approaches that have attempted to distinguish these dimensions of
biased spatial attention and consider their strengths and limitations also.
Fox Russo, Bowles, and Dutton (2001) were among the first to employ a variant
of Posner’s attentional cueing paradigm in an attempt to discriminate biased
attentional engagement and disengagement among anxious individuals. The
structure of this task was such that, on each trial, a threatening or neutral stimulus,
acting as a directional cue, was presented to the right or left of a central fixation
point for a brief duration. The display is then cleared, and a probe was presented in
the same or opposite screen position to this valenced cue. On the majority of trials,
the cue predicted the location of the probe (valid trials), while the remaining trials
presented the probe in the opposite location to the threatening and neutral
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cue stimuli (invalid trials). They found that on trials where the probe appeared
opposite the initial emotional stimulus, participants who were higher in state anxiety
were slower to identify targets when this initial stimulus was threat-related. No
differences were observed across groups in speed to identify probes appearing in the
same location as this emotional stimulus. Based on these findings, the authors
concluded that that the presence of threatening information influences the
disengagement process in anxious individuals, resulting in slowing to relocate
attention away from threatening stimuli once it has been identified, rather than an
increased tendency to initially orient attention toward such stimuli (Fox et al., 2001).
A number of subsequent studies have obtained similar findings using this
paradigm to compare participants who differ in trait anxiety (see Figure 1 for
example of the common format of this attentional cueing task). It has been shown
that high trait anxious individuals are disproportionately slow to identify probes
appearing in the screen position opposite the location of an initially presented single
threat stimulus (either words or faces; Fox, Russo, & Dutton, 2002; Koster, Crombez,
Verschuere, Van Damme, & Wiersema, 2006b; Yiend & Mathews, 2001). This pattern
of findings has also been observed for individuals with social phobia who show
disproportionate slowing to respond to probes appearing opposite initially exposed
single social threat words as compared to neutral words (Amir, Elias, Klumpp, &
Przeworski, 2003). While the pattern of findings from this task has been consistent
across these studies, it is important to recognize that this pattern does not, in
fact, require the conclusion that anxious participants display biased attentional

Target presentation + Target presentation +

Kill Fail
Emotional cue + Emotional cue +
Kill Fail

Initial fixation + Initial fixation +

Validly cued trial Invalidly cued trial

Figure 1. Example of the typical format of valid and invalid trials in the modified attentional
cueing task. Example shows threat stimuli only.
Anxiety, Stress, & Coping 7

disengagement from threat. Several issues compromise the capacity of this


attentional cueing paradigm to dissociate biased attentional engagement from biased
attentional disengagement, and these are considered in turn in the following section.
A subsequent task developed by Fox, Mathews, Calder, and Yiend (2007) used an
alternative design involving endogenous cueing in an attempt to measure anxiety-
linked differences in attentional ‘‘orienting’’ (i.e., attentional engagement) and
attentional ‘‘holding’’ (i.e., disengagement). In this study, participants are presented
with a central face depicting emotional expressions which have either forward facing,
or averted eye gaze (to the left or the right). A subsequent probe is presented to the
left or right of the central face with equal frequency on each trial. The results
obtained from this task indicated that high trait anxious individuals were faster to
identify probes appearing in the same direction as the eye gaze of fearful faces and
slower to respond to facial expressions depicting anger when eye-gaze faced forward.
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The authors concluded that attention is more likely to be ‘‘held’’ by an angry


expression but more likely to be spatially ‘‘guided’’ by a face expressing fear. While
the results of this study are certainly interesting, as with the modified attentional
cueing task, there are problems drawing firm conclusions from these findings
regarding biased attentional engagement and disengagement, as we now will shortly
discuss.
We are aware of at least two other research paradigms that purportedly examine
biased attentional engagement and disengagement of spatial attention in anxiety. The
first is a slight variant of the traditional attentional probe task. This task, initially
employed by Koster, Crombez, Verschuere, and De Houwer (2004), employed
equivalent trials to those delivered in the original probe task, where threat-neutral
stimulus pairs are presented followed by probes in the locus of either stimulus.
However, the task includes neutralneutral stimulus pairs, also followed by probes in
either screen location. Results from this task indicate that anxious participants
generally show slower response latencies to identify probes that replace the neutral
stimuli within threat-neutral stimulus pairs, than to probes that replace neutral
stimuli within neutralneutral pairs. On the basis of these findings, investigators have
concluded that the attentional bias shown by such participants consequently must
reflect impaired attentional disengagement from threat stimuli (Koster et al., 2004;
Koster, Crombez, Verschuere, & De Houwer, 2006a; Salemink, van den Hout, &
Kindt, 2007).
A final approach which some research claims may index biased attentional
engagement and disengagement, employs a standard visual search task design in
which participants are required to identify either target neutral words within an array
of threat words, or target threat words within an array of neutral words (Pineles,
Shipherd, Mostoufi, Abramovitz, & Yovel, 2009; Pineles, Shipherd, Welch, & Yovel,
2007). When individuals with either a high or low prevalence of posttraumatic stress
disorder symptoms have been compared on this task, those with high posttraumatic
stress disorder (PTSD) symptoms are slower to identify neutral targets within an
array of threat stimuli, while no consistent difference is observed in latencies to
identify threat targets within an array of neutral stimuli. The slowing to identify
neutral targets embedded within a number of threat items has been taken to indicate
that individuals with high PTSD symptoms have selective difficulty disengaging
attention from threat stimuli.
8 P.J.F. Clarke et al.

We believe that each of these approaches to measuring biased engagement and


disengagement of spatial attention contain methodological confounds that limit the
conclusions that can be drawn on the basis of such experimental methodologies. The
following considers these problems, highlighting thematic issues which potentially
impact on a number of these tasks.

Potential confounds with tasks assessing biased attentional engagement and


disengagement
Defining biased attentional engagement and disengagement
While some experimental papers provide definitions of attentional engagement and
disengagement to clearly communicate their intended meaning of the terms, this is by
no means a consistent feature of research in this area. The absence of this can result
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in the loose application of these terms which are applied to experimental measures
that are not in fact able to index these attentional processes. The problem with this is
perhaps most clearly illustrated in research employing visual search tasks to examine
biased attentional engagement and disengagement (Pineles et al., 2007, 2009). A
fundamental problem with the conclusions derived from these tasks is that the
authors equate difficulty disengaging attention from threat with ‘‘interference’’
without justifying why these processes are assumed to be equivalent. Specifically, the
authors suggest that slowing to identify neutral targets embedded within an array of
threat distracters necessarily implicates biased attentional disengagement from
threat. That is, slowing to respond must be the result of delayed disengagement
from threatening stimuli. There is no reason to assume, however, that biased
attentional engagement would not interfere with the task of identifying a neutral
target in the presence of threat distracters. If anxious individuals are more likely to
engage with one or multiple threat distracter items, then this will in turn slow their
responses to identify a neutral target. As discussed with regard to the results from the
emotional Stroop, it is entirely possible that an attentional engagement bias could
cause interference with a primary task of processing a neutral target in the presence
distracting threatening information.
Thus, while the results of studies employing such visual search tasks may
justifiably attribute longer response latencies to interference, whether such inter-
ference is the result of biased attentional engagement with or biased attentional
disengagement from threatening material cannot be derived from such an experi-
mental design. The findings derived from research employing visual search task
methodologies do not appear to warrant the conclusion that selective attention is
characterized by delayed disengagement. The issue of conflating the two distinct
issues of interference effects and biased attentional disengagement is but one of a
number of issues which cast doubt on conclusions drawn regarding the roles of
component attentional processes in anxiety on the basis the majority of methodo-
logical approaches employed to date.

The use of an emotional cue to secure attention


A key issue with the modified attentional cueing task (Fox et al., 2001, 2002) is the
use of an emotional stimulus to serve the two incompatible functions of equivalently
Anxiety, Stress, & Coping 9

securing attention, and differentiating an attentional response to valenced stimuli.


The claim that an emotionally valenced stimulus acting as a directional cue to a
subsequent probe target (appearing in either the same or opposite screen position)
can be used to discriminate both biased attentional engagement and disengagement
rests on two clearly incompatible assumptions about the use of such an emotional
cue. A necessary assumption for the measurement of individual differences in biased
attentional disengagement is that the abrupt onset of any single stimulus necessarily
must recruit initial attention, regardless of its emotional tone or participants’
emotional disposition. If this is indeed the case, however, then the task cannot be
represented as an adequate means of assessing individual difference in attentional
engagement with emotional information, because the task will not permit such
individual differences to emerge. The alternative assumption is that the onset of a
single stimulus does permit individual differences in attentional engagement with this
stimulus. If this is indeed the case, then it follows that the attentional disengagement
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measure will be confounded with any such initial differences in attentional


engagement bias. That is, any initial differences in attentional engagement with the
emotional cue will affect subsequent response latencies to probes appearing opposite
the cue, meaning that what are taken to be individuals differences in attentional
disengagement bias may instead result from individual differences in attentional
engagement bias.
Problems with the use of an emotional cue to secure attention become further
apparent when considering the issue of changes in the cue validity ratios in the
modified attentional cueing task. Some researchers who have adapted Posner’s
attentional cueing task to examine anxiety-linked attention to threat have maintained
the integrity of the original valid/invalid trial distinction by ensuring that the initial
stimulus remained genuinely predictive of subsequent probe position (e.g., Fox et al.,
2001). In these studies, the position of the initial emotional stimulus was also the
location of the subsequent probe on the majority of trials (valid trials), while probes
appeared in the opposite screen position on fewer trials (invalid trials). It is
noteworthy, however, that many later studies simply eliminated this probability
difference, such that probes appeared in the same or opposite location to the initial
valenced stimulus with equal frequency (e.g., Fox et al., 2002; Koster et al., 2006b;
Yiend & Mathews, 2001). When the probability of the probe occurring in the same or
different locus as the initial stimulus is at chance, the task essentially is exactly the
same as the original attentional probe task (MacLeod et al., 1986), except that single
threat or neutral stimuli are exposed on each trial, rather than pairs that each contain
both a threat and a neutral stimulus, prior to the probe’s appearance.
Eliminating the predictive value of the cue within this paradigm, while
maintaining that it still will reveal individual differences in attentional disengagement
bias, necessarily requires the assumption that the cue will continue to draw initial
attention. In the original form of the modified attentional cueing task (Fox et al.,
2001, 2002), the cue was expected to draw initial attention because of its predictive
value (that is, because it provided a participant with a probabilistic indication of
where the final target would appear). When removing the predictive value of the cue
the assumption changes from the perhaps more reasonable position that the
emotional cue will equivalently secure attention because it predicts the location of
a to-be-identified target; to the more tenuous assertion that the emotional cue will
equivalently secure attention because any abrupt stimulus onset in the visual field will
10 P.J.F. Clarke et al.

equivalently draw attention. While it may be that the abrupt onset of a single stimulus
will draw attention to some degree, the critical requirement for measuring biased
attentional engagement and disengagement in anxiety using this paradigm is that this
stimulus must draw attention equivalently, regardless of its emotional valence, for
both high and low anxious individuals, despite their known difference in attentional
preference for negative valenced stimuli. We are aware of no research that has
systematically investigated whether changing the predictive value of an emotionally
valenced cue stimulus will affect the degree to which it draws initial attention, in
participants who differ in anxiety vulnerability. Hence, assumptions about the
capacity of a single emotional stimulus to draw initial attention not only are
inconsistent, but are untested.

The influence of non-attentional processes on reaction time measures


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A number of tasks designed to measure biased attentional engagement and


disengagement may be compromised by non-attentional processes, such as a general
slowing of reaction-time (i.e., freezing) for anxious individuals in the presence of
threat stimuli. Such a non-attentional effect could influence results on many of the
tasks employed in the attempt to assess biased attentional engagement and
disengagement, including the modified attention cueing task (Fox et al., 2001,
2002), the eye-gaze endogenous cueing task (Fox et al., 2007) and the modified
variant of the attentional probe task (Koster et al., 2004; Koster et al., 2006a;
Salemink et al., 2007). Recall that the potential influence of non-attentional
behavioral freezing in the presence of threat was a major criticism of the emotional
Stroop task, which led to the adoption of the original attentional probe
methodology. Specifically, because the emotional Stroop task presented single
stimuli that were either threatening or not, the general influence of non-attentional
behavioral freezing in the presence of threat for anxious participants could account
for their slowing to color name threat words, without the need to implicate
attentional selectivity. The attentional probe task overcame this problem by
presenting threat and non-threat word pairs, thereby ensuring that threat was
present on every trial, and so eliminated any confound between non-attentional
behavioral freezing in the presence of threat, and response latency effects due to
attentional selectivity.
However, a number of the experimental tasks recently adopted to assess biased
attentional engagement and disengagement lose this methodological advantage by
returning to single stimulus presentations, reintroducing the very confound that the
original probe task was designed to eliminate. The confounding influence of this
becomes evident when you consider the potential consequences of anxious
participants displaying both non-attentional behavioral freezing in the presence of
threat, and increased attentional engagement with threat. On the modified
attentional cueing task, the effect of biased attentional engagement alone would
result in speeded latencies to probes in the same locus as single threat rather than
neutral words (valid trials), without producing any difference between the latencies
for probes appearing in the opposing screen locus from these two word types (on
invalid trials). However, non-attentional behavioral freezing in the presence of threat
would mean that latencies would be slowed when a threat word, rather than a neutral
word, appeared on-screen. The net result of overlaying these two effects would be
Anxiety, Stress, & Coping 11

that anxious participants could display equivalent response latencies for probes
appearing in the same locus of the threat and neutral words (combining the speeding
to probes in the locus of threat produced by their engagement bias, with their
behavioral response freezing in the presence of threat). These anxious participants
would, however, show longer latencies for probes appearing opposite threat words
rather than neutral words (as now their behavioral response freezing in the presence
of threat would not be offset by any benefit from their attentional engagement bias).
Thus, the possibility of non-attentional behavioral response freezing in the presence
of threat, among anxious participants, prevents spatial cueing tasks from distin-
guishing engagement bias from disengagement bias. Therefore, the pattern of effects
that researchers have obtained, which has been construed as evidence that anxious
participants show no enhanced attentional engagement with threat, and instead
display impaired attentional disengagement from such information (Fox et al., 2001,
2002; Koster et al., 2006b; Yiend & Mathews, 2001), could instead reflect only their
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enhanced attentional engagement with threat, coupled with general behavioral


freezing in the presence of threat.
The same problem applies to the endogenous cueing task of Fox et al. (2007),
which employs central emotional stimuli with either forward facing or averted eye
gaze (to the left or the right). This study found that high trait anxious individuals
were faster to identify probes appearing in the same direction as the eye gaze of
fearful faces and slower to respond to facial expressions depicting anger when eye-
gaze faced forward. It is entirely possible, however that angry faces with forward
facing gaze are more threatening than fearful faces with averted gaze. Thus, these
angry faces may not ‘‘hold’’ attention in anxious participants as claimed, but may
simply serve more effectively to elicit these participants’ greater behavioral freezing
in the presence of threatening stimuli, thus slowing their response latencies on these
trials.
This failure to take account of anxiety-linked non-attentional behavioral freezing
in the presence of threat also compromises conclusions drawn on the basis of the
alternative variant of the attentional probe described earlier (Koster et al., 2004b;
Koster, et al., 2006b; Salemink et al., 2007). As will be recalled, this task employs
neutralneutral stimulus pairs in addition to the threat-neutral stimulus pairs of the
original task. On the basis of the observation that anxious participants show slower
response latencies to probes that replace the neutral stimuli within threat-neutral
stimulus pairs, than to probes that replace neutral stimuli within neutralneutral
pairs, investigators have concluded that their attentional bias consequently must
reflect impaired attentional disengagement from threat stimuli (Koster et al., 2004;
Koster, 2006a; Salemink et al., 2007). However, such longer response latencies can
just as readily be accounted for by anxiety-linked non-attentional behavioral freezing
in the presence of threat. Hence, there is no justification for inferring from this
observed effect that the anxiety-linked attentional bias necessarily reflects their
difficulty disengaging attention from such information. Yet, this problem has gone
largely unrecognized, even within recent literature reviews, which continue to
represent such findings as evidence of impaired attentional disengagement from
threat in anxiety (Cisler & Koster, 2010; Yiend, 2010).
The problems associated with interpreting findings from the modified attentional
cueing task, given its failure to take account of non-attentional behavioral freezing in
the presence of threat for anxious individuals, was nicely demonstrated in an elegant
12 P.J.F. Clarke et al.

experiment by Mogg, Holmes, Garner, and Bradley (2008). These researchers


compared probe discrimination latencies for individuals who differed in anxiety
vulnerability using the modified attentional cueing task. Critically, they included an
additional condition designed to directly assess, and correct for non-attentional
behavioral freezing in the presence of threat, where no movement of attention was
required. In this condition, threat and neutral stimuli were presented centrally with
the probe appearing in this same central locus. Mogg et al. (2008) revealed that, when
participants were presented with threat stimuli within an already attended locus
(where no spatial shift in attention was required), high trait anxious participants, but
not low trait anxious participants, were significantly slowed in identifying probes.
The probe discrimination latencies observed on trials that replicated past versions of
the modified attentional cueing paradigm (e.g., Fox et al., 2001; Yiend & Mathews,
2001) were consistent with previous findings derived from this task, showing that
anxious participants were slower to respond to probes appearing opposite threat
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rather than neutral stimuli, but were not faster to respond to probes appearing in the
same locus as threat rather than neutral stimuli. Interestingly, when response
latencies from trials where no movement in attention was required were used to
corrected for the behavioral freezing observed in the presence of threat, the pattern of
results instead suggested that anxious individuals were relatively faster to respond to
probes appearing in the same locus as threat as opposed to neutral stimuli, but were
not slowed in their responses to probes appearing opposite the location of
threatening rather than neutral cues. Thus, Mogg et al.’s (2008) study clearly
demonstrates that longer response times to probes appearing opposite threat stimuli
cannot be confidently attributed to difficulty disengaging attention from these threat
stimuli. Their findings suggest that when non-attentional behavioral freezing in the
presence of threat is accounted for, anxious participants display enhanced attentional
engagement with threat stimuli.
While Mogg et al.’s (2008) study clearly demonstrates the interpretive difficulties
that can result from confounding non-attentional behavioral freezing in the presence
of threat and selective attentional response to threat, it does not conclusively resolve
the question of whether biased attentional engagement or disengagement underpins
the selective attentional preference for threat in anxious individuals. As the authors
point out, it cannot confidently be assumed that non-attentional behavioral freezing
in the presence of threat necessarily must be additive with effects resulting from
attentional selectivity. We concur with Mogg et al. that there is a need to further
improve upon their methodology.

Proposed task criteria for measuring biased attentional engagement and disengagement
in anxiety
Based on the reviewed limitations of the cognitive-experimental tasks used to date,
and guided by our discussion of how these limitations may be attenuated, we propose
three criteria that an experimental task should fulfill, to effectively yield valid
measures of biased attentional engagement and disengagement. One obvious
criterion is that the task must control for non-attentional behavioral freezing in the
presence of threat. Without a means of accounting for this effect, differences in
responding to task stimuli cannot be attributed with confidence to either biased
attentional engagement or disengagement.
Anxiety, Stress, & Coping 13

There are at least two methods to control for behavioral freezing in the presence
of threat. One, as demonstrated by Mogg et al. (2008), involves the inclusion of
control trials where threat and neutral stimuli are presented within an attended locus
and no spatial movement of attention is required. The response latencies on these
trials provide a measure of the degree to which individual participants exhibit a
general behavioral freezing in the presence of threat, and this effect can then be
statistically removed from effects observed when attention is required to move,
providing a corrected measure of attentional orienting. As highlighted by Mogg et al.
(2008), however, this method may not be ideal as it assumes that behavioral freezing
effects are additive with the patterns of speeding or slowing resulting from biased
attentional selectivity. Another method of controlling for non-attentional behavioral
freezing in the presence of threat would be to simultaneously display both
threatening and neutral stimuli on every trial. This removes the need for separate
control trials as threat stimuli are always present.
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A second criteria that we consider essential for the adequate differentiation of


biased attentional engagement with and disengagement from threat, is that a task
should always include a means of equivalently securing attention on a predetermined
initial focus, before allowing subsequent attentional movement, either toward
attentionally distal emotional stimuli, or away from attentionally proximal emotional
stimuli. For measures of biased attentional engagement, attention initially should be
equivalently secured on emotionally neutral information, before assessing relative ease
to shift attention to instead process differentially valenced information. For measures
of biased attentional disengagement, attention initially should be equivalently
secured on emotionally valenced information, before assessing relative ease to shift
attention away from this information. Ideally, a means of assessing whether initial
attention has been successfully secured as required should be included in the task.
Our third and final criterion is that once initial attention has been secured, the
task must enable assessment of the ease with which attention then can be shifted in
relation to emotionally valenced information. Thus, the task must include a means
of assessing the relative ease with which such shifts occur under conditions where
emotionally valenced information is located proximally to or distally from
the original focus of attention. While none of the tasks previously described meet
these criteria, we believe that they could readily be imported into a number of
existing paradigms. In the following section, we consider how cognitive-experimental
methodologies previously used to assess anxiety-linked attention could potentially be
adapted to differentially assess biased attentional engagement with threat and biased
attentional disengagement from threat, by incorporating these criteria.

Example research designs fulfilling the proposed criteria


One method of assessing biased attentional engagement and disengagement is
through the use of eye-tracking. Eye-movement measures of attention are likely to
index more overt orienting of attention whereas cueing and probe tasks may index
covert shifts of attention (cf. Weierich, Treat, & Hollingworth, 2008). However, eye-
movement measures have the advantage that they can be recorded unobtrusively, and
so are compatible with many different types of attentional tasks. An increasing
number of contemporary researchers have access to eye-movement measures, so it is
worth considering how this tool can be used to effectively distinguish the
14 P.J.F. Clarke et al.

contribution made by attentional engagement and disengagement to anxiety-linked


attentional preference for threat. The relative directness of indexing eye-movement
might erroneously be thought to imply that using such measures will readily
distinguish selective attentional engagement from selective attentional disengage-
ment, on any type of attentional task. However, this will be the case only if the task
meets the three criteria outlined earlier.
To accurately measure either biased attentional engagement with or disengage-
ment from emotionally valenced stimuli using eye-movement measures, attention still
must first be equivalently secured within a predetermined initial screen locus. Eye-
gaze measures can enable this to be verified, or by linking task delivery to eye-
movement measures, the trial might progress only once attention initially is fixated
on this required locus. To assess biased attentional engagement, after securing initial
attention in the locus of a non-emotional neutral stimulus, threat or neutral stimuli
could then be presented to attentionally distal screen positions, to assess how the
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valence of this distal information influences the shifting of eye-gaze toward it. A
measure of biased attentional disengagement would instead be achieved by securing
initial attention in the locus of threat or neutral stimuli, then presenting a non-
emotional neutral stimulus to an attentionally distal screen locus, to assess how the
valence of the attentionally proximal information influences the shifting of eye-gaze
away from it.
While a number of previous studies have incorporated eye-gaze measures into
attentional tasks (e.g., Caseras, Garner, Bradley, & Mogg, 2007; Hermans,
Vansteenwegen, & Eelen, 1999; Rohner, 2002), few have attempted to directly index
biased attentional engagement with and disengagement from emotionally valenced
stimuli in anxiety. We are aware of none that have employed the conditions we
propose necessary to adequately assess biased attentional disengagement from
emotional information. However, a few such studies have adopted task conditions
similar to those outlined earlier, to yield measures of biased attentional engagement
with threat (Garner, Mogg, & Bradley, 2006; Mogg, Millar, & Bradley, 2000).
Mogg et al. (2000) incorporated eye-gaze measures into an attentional probe
paradigm comparing the direction of initial eye-movements between groups of
individuals with Generalized Anxiety Disorder (GAD), depression, and controls.
Measures of initial eye-gaze were consistent with the criteria for biased attentional
engagement outlined earlier. Eye tracking was used to subsequently verify that
attention was first secured with a central, emotionally neutral fixation stimulus.
Following initial fixation, paired threat and neutral stimuli were presented to
alternate screen positions. The direction and latency to first fixation provided
measures of the relative ease with which attention is shifted in relation to these
emotionally valenced stimuli. Their results revealed that individuals with GAD
directed attention initially toward threat stimuli on more trials and were faster to
orient toward such stimuli as compared to the other two groups. Because both threat
and neutral stimuli were present on each trial, this study can confidently control for
non-attentional behavioral freezing in the presence of threat. Furthermore, the
finding that GAD participants were more likely, and showed shorter latencies, to
align eye-gaze with threat stimuli cannot be an artifact of non-attentional
behavioural freezing in the presence of threat.
Garner et al. (2006) similarly used eye-gaze measures to compare responses of
high and low socially anxious individuals on an attentional probe task presenting
Anxiety, Stress, & Coping 15

paired emotional (happy or angry faces) and neutral face stimuli. As with Mogg et al.
(2000), Garner et al.’s (2006) measure of biased engagement was derived from trials
where attention was first secured with a central non-emotion fixation stimulus before
assessing individual differences in the direction of first fixation between two stimuli
subsequently presented to different screen positions. High socially anxious partici-
pants initially engaged with emotionally expressive faces more frequently than low
socially anxious participants and had shorter latencies when emotional stimuli were
the object of initial engagement. No difference was observed between groups in the
tendency to engage with either happy or angry faces. It is noteworthy however, that
threatening (angry face) stimuli were not present on all trials. Results could have been
confounded by non-attentional behavioral freezing in the presence of threat on
angry-neutral face trials, which would be absent on happy-neutral face trials. The
additional inclusion of happy-angry face trials would be necessary to permit
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confidence that the absence of between-group differences in engagement with happy


and angry stimuli is not due to any more general effect of behavioral freezing in the
presence of threat.
Other eye-movement studies have also failed to find evidence of anxiety-linked
differences in attentional engagement with and disengagement from threat. Research
by Derakshan and Koster (2010) using a visual search task design found no evidence
to suggest that high trait anxious individuals exhibit facilitated orienting of eye gaze
toward threat stimuli, or show delayed disengagement of eye-gaze from threat
stimuli. The absence of such effects was also revealed in a subsequent study using a
similar design (Berggren, Koster, & Derakshan, in press). While these studies
included differentially valenced stimuli on all trials, they did not seek to equivalently
align initial eye-gaze with either emotional stimuli (to measure subsequent biased
disengagement) or non-emotional stimuli (to measure biased engagement) making
clear interpretation of attentional engagement and disengagement effects more
difficult.
While eye-movement technology may be compatible with experimental tasks that
meet our three methodological criteria for dissociating biased attentional engage-
ment with and disengagement from threat information, it certainly is not a requisite.
It is equally possible to envisage variants of the attentional probe task, amended in
ways that fulfill these criteria. Consistent with the criteria outlined earlier, to assess
selective attentional engagement with emotional information, such an attentional
probe task variant would need to equivalently secure initial attention on a non-
emotional, perhaps meaningless, stimulus. For example, participants could be
induced to attend to the locus where a meaningless letter string appears, by requiring
them to discriminate the identity of an initial probe stimuli very briefly exposed in
this locus immediately prior to the appearance of the non-word. Correct responding
to this probe would provide assurance that attention initially was thus secured.
Threat or non-threat words could be exposed in an opposing screen locus, therefore
appearing distally from the initial focus of attention. Relative latency to process
target probes appearing in the vicinity of these distal threatening or neutral stimuli,
compared to probes that instead appear in the initially attended screen locus, would
reveal the relative speed to engage attention with each type of emotional stimulus.
Such an experimental design controls for any behavioral freezing in the presence of
threat, because the speed of attentional engagement with each type of emotional
16 P.J.F. Clarke et al.

stimuli will be revealed by comparing the latency to process probes that appear in
each screen locus when this type of emotional information is present on the screen.
To instead index biased attentional disengagement from emotional information
using such an amended probe task, attention would need to be initially secured on
emotionally valenced stimuli, while non-threatening meaningless stimuli would be
presented in an attentionally distal screen region. Relative latency to process target
probes appearing in the vicinity of these non-threatening meaningless stimuli,
compared to probes in the originally attended screen locus, then would reveal relative
speed to disengage attention from the emotional information. Again, such a task
could control for the possibility of behavioral freezing in the presence of threat,
because the measures of attentional disengagement from each type of emotional
stimuli come from comparing the latencies to process probes in differing screen loci
when this type of information is present on-screen. This is just one example of a task
which could, in principle, incorporate the task criteria outlined earlier to assess
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biased attentional engagement and disengagement. We are not aware of any research
which has to date sought to investigate these component attentional processes in
anxiety using such a task. However, similar variants of the attentional probe task,
which tightly control both the initial and final locus of attention on each trial, and so
enable assessment of relative speeds to move attention toward and away from
emotional information, may provide greater confidence that the task is indeed
isolating and indexing the attentional processes of interest. Whether such tasks prove
to be successful, and whether the pattern of observed effects will cleanly differentiate
these two candidate types of anxiety-linked attentional bias remains an issue for
future research to determine.
The focus of this review, and indeed the focus of virtually all research to date that
has investigated biased attentional engagement and disengagement in anxiety, has
been restricted to the consideration of the movement of spatial attention. While
spatial attention is of considerable importance to understanding the theoretical and
applied value of anxiety-linked information processing biases, such research should
not be conducted at the expense of research examining non-spatial shifts of
attention. Measuring non-spatial shifts in attentional engagement and disengage-
ment poses a different set of challenges from the measurement of spatial attention.
For example, rather than equivalently securing initial attention in a particular spatial
locus, such methods would instead be concerned with securing initial attention to an
emotional or non-emotional facet of information in a single locus. The task would
then require movement of attention between alternative dimensions of the informa-
tion in this single locus, rather than between alternative stimuli in spatially separate
loci. Given that the emotional Stroop task involves the presentation of stimuli which
contain the dimensions of structural form (color) and semantic content (word
meaning), it is conceivable that variants of this task could differentiate biased
attentional engagement and disengagement, when participants shift attention
between alternative dimensions of a single stimulus.
One recent study has employed an experimental design that involves such non-
spatial shifts in attention in an attempt to modify patterns of attentional engagement
and disengagement. Hirsch et al.’s (2011) task required that participants either
initially attend to the structure of a word (identify if the word is in upper or lower
case letters) before shifting attention to its semantic content, or else initially attend to
its semantic content (by identifying if it is positive or negative) before then shifting
Anxiety, Stress, & Coping 17

attention to its structure. By varying contingencies, Hirsch et al. sought to induce


either reduced attentional engagement with threatening semantic content, or increase
attentional disengagement from threatening semantic content, and found that only
the former attentional manipulation served to influence subsequent worry.
As can be seen, quite different methods can potentially be used to distinguish the
roles of biased attentional engagement with, and biased attentional disengagement
from, threatening information in anxious participants. However, we contend that the
value of such tasks will depend upon them meeting three key criteria. They must
control for the possibility of general non-attentional behavioral freezing in the
presence of threat, and ensure that such an effect would not be confounded with the
resulting measures of selective attentional engagement and disengagement. They
must initially secure attention, to an equivalent degree across participants, on a
predetermined focus. In addition, they must assess both differences in the subsequent
shifting of attention toward threatening and neutral information, when the original
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attentional focus contains non-emotional information, and differences in the shifting


of the attention toward non-emotional information, when the original attentional
focus contains threatening or neutral information.
In conclusion, we believe that there is great potential to adapt tasks previously
used to demonstrate only a general anxiety-linked attentional preference for threat,
in a manner that could enable them separately assess anxiety-linked attentional
engagement with threat, and attentional disengagement from threat. However, we
also argue that the methodological approaches most widely employed to date for this
purpose have been compromised by limitations that preclude their capacity to
differentiate these two types of attentional selectivity. Here, we have attempted to
provide a detailed methodological review of these tasks, not only to highlight their
associated problems, but also to propose three key criteria, which we argue should be
met by attentional tasks to permit adequate measurement of selective attentional
engagement with, and disengagement from, threatening information in anxiety. We
hope that these ideas motivate further enquiry and assist researchers to develop novel
and innovative methodologies which will further our presently limited understanding
of the respective contributions made by each of these attentional mechanisms to the
well-established attentional preference for threat shown by anxious individuals.

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