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Contents lists available at ScienceDirect

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

Top-down and bottom-up factors in threat-related perception and

attention in anxiety
Tamara J. Sussman, Jingwen Jin, Aprajita Mohanty ∗
Department of Psychology, Stony Brook University, United States

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

Article history: Anxiety is characterized by the anticipation of aversive future events. The importance of prestimulus
Received 14 September 2015 anticipatory factors, such as goals and expectations, is well-established in both visual perception and
Received in revised form 10 August 2016 attention. Nevertheless, the prioritized perception of threatening stimuli in anxiety has been attributed
Accepted 17 August 2016
to the automatic processing of these stimuli and the role of prestimulus factors has been neglected. The
Available online xxx
present review will focus on the role of top-down processes that occur before stimulus onset in the
perceptual and attentional prioritization of threatening stimuli in anxiety. We will review both the cog-
Keywords:
nitive and neuroscience literature, showing how top-down factors, and interactions between top-down
Top-down
Endogenous and bottom-up factors may contribute to biased perception of threatening stimuli in normal function
Threat perception and anxiety. The shift in focus from stimulus-driven to endogenous factors and interactions between
Prestimulus processes top-down and bottom-up factors in the prioritization of threat-related stimuli represents an important
Attention conceptual advance. In addition, it may yield important clues into the development and maintenance of
Amygdala anxiety, as well as inform novel treatments for anxiety.
Anxiety © 2016 Elsevier B.V. All rights reserved.
Sensory cortex
Prefrontal cortex
Perceptual bias
Attentional bias

1. Introduction stimuli shown rapidly in a stream of images are identified more

Emotional stimuli require rapid adaptive responses, such as
avoidance of threat or approach towards a rewarding stimulus. To
allow for these swift behavioural responses, our perceptual and
attentional system prioritizes emotional stimuli over stimuli that
are relatively unemotional in nature. Spiders, snakes and angry
faces are hypothesized to belong to a special class of stimuli that
are perceptually prioritized due to their importance for survival
(Brosch, Pourtois, & Sander, 2010; New, Cosmides, & Tooby, 2007;
Seligman, 1971). Empirical research supporting this view shows
that spiders and snakes are detected more rapidly than mush-
rooms and flowers (Ohman, Flykt, & Esteves, 2001) and. angry faces
are detected faster than neutral faces (Hansen & Hansen, 1988;
Horstmann, 2007). Saccadic eye movements orient more quickly to
images of threatening compared to neutral faces and body postures
(Bannerman, Milders, de Gelder, & Sahraie, 2009). Threatening
∗ Corresponding author at: Department of Psychology, Stony Brook University,
Stony Brook, NY 11794, United States.
E-mail address: aprajita.mohanty@stonybrook.edu (A. Mohanty).
accurately than neutral stimuli (Anderson, 2005). While positive
stimuli may also be associated with similar perceptual benefits, the
effects tend to be smaller than those elicited by threatening stimuli
(Carretie, Mercado, Tapia, & Hinojosa, 2001; Dijksterhuis & Aarts,
2003; Smith, Cacioppo, Larsen, & Chartrand, 2003; Stefanics, Csukly,
Komlosi, Czobor, & Czigler, 2012; Sussman, Weinberg, Szekely,
Hajcak, & Mohanty, 2016).
The facilitated perception of threatening stimuli has been
attributed to bottom-up processing driven by the physical charac-
teristics or evolutionary significance of these stimuli (Bannerman
et al., 2009; Ohman et al., 2001). In line with this view, research
in affective neuroscience has centered on examining the neural
pathways that promote ‘automatic’ perception of emotional stim-
uli (Fox, 2002; Mendez-Bertolo et al., 2016; Vuilleumier & Pourtois,
2007). It is hypothesized that threatening stimuli are prioritized
due to a processing bias (Bar-Haim, Lamy, Pergamin, Bakermans-
Kranenburg, & van, 2007; Cisler, Bacon, & Williams, 2009). This
processing bias is not measured directly, and instead is inferred
from accuracy and reaction time differences between the detec-
tion of threatening compared to neutral stimuli. Depending on the
design of the task, the threat bias is hypothesized to facilitate detec-

http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
0301-0511/© 2016 Elsevier B.V. All rights reserved.

Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
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2 T.J. Sussman et al. / Biological Psychology xxx (2016) xxx–xxx
tion of threatening stimuli in visual search and dot-probe-like tasks
or impede performance when threatening stimuli distract from the
task at hand (Mathews & MacLeod, 1994; Ohman et al., 2001). Here,
we explore the possibility that in addition to processing biases that
occur coincident with stimulus presentation, prioritized percep-
tion of threatening stimuli in normal function and anxiety may be
attributed to prestimulus biases.
The idea that prestimulus biases impact threat-perception is
consistent with research indicating that the process of perception
starts prior to an encounter with a stimulus, and with research
demonstrating that perception is guided by top-down factors such
as goals and expectations (Bacon & Egeth, 1994; Itti & Koch, 2001).
For example, both implicit and explicit prestimulus cues improve
target perception (Chen & Zelinsky, 2006; Wolfe, Butcher, Lee,
& Hyle, 2003). Similarly, in day-to-day life, we often use both
implicit and explicit emotional information to guide our percep-
tion, for example, while scanning for spiders in an uninhabited
room filled with cobwebs. These anticipatory search behaviors,
aimed at rapidly detecting sources of potential reward or threat, are
deployed in a wide range of situations from driving on a highway to
navigating social gatherings. Prestimulus biases may be of partic-
ular importance in anxiety, as dispositional anxiety is associated
with overestimation of the likelihood and cost of future nega-
tive events (Aue & Okon-Singer, 2015; Grupe & Nitschke, 2013).
The importance of top-down processes in anxiety has also been
demonstrated by studies showing that threat-related cues impact
subsequent perception differently depending on type of anxiety
(Sussman, Szekely et al., 2016).
In the present review we first discuss the current affec-
tive neuroscience literature on exogenous, ‘bottom-up’ factors in
understanding perceptual and attentional biases towards threaten-
ing stimuli, both in normal function and in anxiety. While research
has examined the role of top-down factors that are non-emotional
in nature (for e.g., searching for matching Gabor patches) and their
interaction with bottom-up processing of emotional stimuli (for
e.g., task-irrelevant emotional faces in the background), very few
studies have examined top-down factors that are themselves emo-
tional in nature (e.g., cues indicating an upcoming threatening face)
and their effect on perception. Hence, we discuss conceptual and
methodological issues in the research literature that arise from an
exclusive focus on bottom-up factors in understanding prioritized
perception of threatening stimuli. We then discuss the importance
of endogenous, emotion-related ‘top-down’ factors, such as expec-
tations and prior knowledge regarding threat, in guiding basic
human perception. We also discuss emerging evidence that under-
scores the importance of endogenous processing in the perceptual
prioritization of threatening stimuli both in normal function and in
anxiety. Finally, we highlight the importance of shifting the empha-
sis from stimulus-driven to top-down mechanisms as well as their
interaction with bottom-up mechanisms in the study of the percep-
tual prioritization of threatening stimuli both in normal function
and in anxiety (Mohanty & Sussman, 2013).
2. Bottom-up processes influencing the perception of
emotional stimuli
The human visual system is constantly bombarded with infor-
mation. The limited capacity of this system makes it impossible
to process all incoming information (Tsotsos, 1990). As a result,
stimuli entering the visual field compete for neural representa-
tion (Desimone & Duncan, 1995; Tsotsos, 1997). To deal with this
overwhelming excess of information, the visual system biases the
competition between stimuli towards preferential representation
of the most relevant stimuli (Desimone & Duncan, 1995). This
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
biasing process is a function of two mechanisms: a bottom-up, sen-
sory driven mechanism that selects stimuli based on their physical
salience, and a top-down mechanism with variable selection cri-
teria, which selects stimuli based on expectations, knowledge and
goals. Unlike top-down mechanisms, bottom-up mechanisms are
thought to operate by automatically shifting resources to salient
visual stimuli. For example, stimuli that create a local disconti-
nuity in the visual environment, such as abrupt occurrence of a
new object (Jonides & Yantis, 1998), sudden motion and looming
(Abrams & Christ, 2003; Franconeri & Simons, 2003), and luminance
contrast changes (Enns, Austen, Di Lollo, Rauschenberger, & Yantis,
2001) are given more priority.
Similarly, emotional stimuli are considered another class of
stimuli that are hypothesized to be processed in a bottom-up man-
ner. For example, in visual search arrays, snakes and spiders are
detected faster than flowers and mushrooms (Ohman et al., 2001);
and angry faces are detected faster and more efficiently than neu-
tral and happy faces (Eastwood, Smilek, & Merikle, 2001; Tipples,
Atkinson, & Young, 2002). Threatening faces are also processed ear-
lier and receive more perceptual elaboration compared to other
facial expressions (Schupp et al., 2004). Furthermore, saccadic reac-
tion times are faster towards an emotional compared to neutral
faces and body postures (Bannerman et al., 2009), as well as towards
emotional compared to neutral scenes (Nummenmaa, Hyona, &
Calvo, 2009). Similarly, negative words are detected more accu-
rately (Dijksterhuis & Aarts, 2003; Nasrallah, Carmel, & Lavie, 2009)
and more quickly (Dijksterhuis & Aarts, 2003) than positive words.
Attentional probes appearing in the same location as threatening
faces are detected faster than probes appearing in the opposite
location (Armony & Dolan, 2002; Mogg & Bradley, 1999; Pourtois,
Grandjean, Sander, & Vuilleumier, 2004).
It is hypothesized that emotional stimuli are prioritized due to
their salience, as proposed by appraisal, constructivist and, dimen-
sional theories of emotion (Barrett, 2006; Brosch et al., 2010;
Ellsworth & Scherer, 2003; Russell, 2003), or their physical char-
acteristics, as demonstrated by perceptual prioritization of shapes
associated with threats (Larson, Aronoff, Sarinopoulos, & Zhu, 2009;
Larson, Aronoff, & Stearns, 2007). For example, in one study, par-
ticipants were asked to detect and rate the valence of a discrepant
threatening, happy or neutral schematic face in arrays of other-
wise identical faces (Lundqvist & Ohman, 2005). The schematic
faces were manipulated such that three, two or one feature(s)
of the schematic face conveyed emotion. Results showed better
visual search performance for more negatively rated faces, even
if only one feature conveyed emotion, indicating that the threat-
ening meaning of the face drives improved detection (Lundqvist &
Ohman, 2005). On the other hand, researchers have hypothesized
that the search advantage of threatening compared to neutral faces
may be due to features such as upturned lip corners, open eyes, or
frowning that can be discriminated from neutral features (Calvo
& Nummenmaa, 2008; Larson et al., 2007). This could be because
of the salience of the threat-related features, resulting from their
association with the holistic facial expression they come from (e.g.,
Cave & Batty, 2006), or because of physical differences between
features of threatening vs neutral faces regardless of emotional
meaning. Finally, some researchers have hypothesized that it is the
configuration of threatening facial features, such as shape and posi-
tioning of the mouth relative to nose and eyes that aids visual search
(Calder, Young, Keane, & Dean, 2000; Carey & Diamond, 1977),
others have concluded that specific features are responsible for
improved detection (Calvo & Nummenmaa, 2008), and some stud-
ies have presented results supporting both positions (Lundqvist,
Esteves, & Ohman, 2004).
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3. Neural mechanisms involved in bottom-up
threat-perception
At the neural level, the bottom-up processing of emotional stim-
uli is believed to be mediated via the amygdala and its interactions
with the visual cortices (Cisler & Koster, 2010; Dolan, 2002; Ohman,
2002, 2005). For example, results from studies using backward
masking paradigms suggest that fearful faces activate the amygdala
in the absence of conscious awareness (Morris, Ohman, & Dolan,
1998; Whalen et al., 1998). Using an event-related fMRI paradigm
in which subjects fixated on a central cue and matched either
two fearful or neutral faces or two houses presented eccentrically,
Vuilleumier and colleagues examined the hypothesis that emo-
tion and voluntary attention reflect distinct influences that do not
interact (Vuilleumier, Armony, Driver, & Dolan, 2001; Vuilleumier,
Richardson, Armony, Driver, & Dolan, 2004). They found that while
activity in the fusiform gyrus (FG), which is known to respond
strongly to faces, was modulated by voluntary attention, amyg-
dala responses to fearful faces were not (Vuilleumier et al., 2001).
Bottom-up appraisal of emotional stimuli is also associated with
greater connectivity between the amygdala and limbic regions,
such as the anterior cingulate cortex (Comte et al., 2014).
The amygdala is thought to quickly detect relevant stim-
uli, including threatening stimuli (Cunningham & Brosch, 2012;
Sander, Grafman, & Zalla, 2003), via a neural pathway, sometimes
referred to as the ‘low road,’ that passes through the superior
colliculi and the thalamus, that does not require cortical input
(LeDoux, 2000), and carries low-spatial frequency information.
This theory has been supported by evidence demonstrating that
low spatial frequency images of fearful faces produce more amyg-
dala activation than fearful images displayed with high spatial
frequency (Vuilleumier, Armony, Driver, & Dolan, 2003) and by
evidence that emotional faces can be processed in the absence of
awareness in a subject with a lesioned striate visual cortex (de
Gelder, Vroomen, Pourtois, & Weiskrantz, 1999). Recent evidence
using human intracranial electrophysiological data showed fast
amygdala responses, beginning as early as 74-ms after the onset
of fearful, but not neutral or happy, facial expressions (Mendez-
Bertolo et al., 2016). The latency of fear responses in amygdala was
much shorter than their latency in the visual cortices and relied on
low spatial frequency information. However, this theory has been
challenged by a competing model, positing that during the pro-
cessing of emotional visual stimuli, the amygdala’s primary role is
to coordinate cortical function and detect salient stimuli (Pessoa &
Adolphs, 2010). This model (discussed in greater detail below) has
been supported by evidence demonstrating that emotional faces
only produce greater amygdala activity when faces are actively
attended to (Pessoa, Kastner, & Ungerleider, 2002), and by evi-
dence that rapid fear detection can rely on high spatial frequency
information, suggesting involvement of cortical visual areas (Stein,
Seymour, Hebart, & Sterzer, 2014).
After the amygdala evaluates incoming information as threat-
ening, it can boost processing in other brain regions, such as
the sensory cortices, via re-entrant feedback (Vuilleumier, 2005).
Hence, exogenously-driven perceptual prioritization of threat-
related information is hypothesized to involve visual processing
modulated by re-entrant feedback signals from the amygdala
(Anderson & Phelps, 2001; Davidson, 2002; Ohman et al., 2001;
Ohman, 2005; Vuilleumier & Pourtois, 2007). Since the amygdala
both receives inputs from all sensory modalities and projects to
numerous cortical and subcortical areas, it is well positioned to
influence a number of processes and behaviors (Fox, Oler, Tromp,
Fudge, & Kalin, 2015; Freese & Amaral, 2009; Holland & Gallagher,
1999). Supporting the theory that this rich connectivity is used
during threat perception is evidence that lesions in the human
amygdala lead to less activation of the FG when viewing fearful
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
3
faces compared to healthy controls and participants with hip-
pocampal lesions (Vuilleumier et al., 2004) and also lead to less
activation in the inferior temporal cortex, a region crucial for visual
recognition, in monkeys (Hadj-Bouziane et al., 2012). Furthermore,
greater connectivity between the amygdala and sensory regions
has been found during threat perception (Lim, Padmala, & Pessoa,
2009; Morris, Friston et al., 1998; Pessoa, Gutierrez, & Ungerleider,
2002). These empirical results support claims of quick and auto-
matic processing of salient stimuli, and provide an amygdala-based
mechanism by which threat stimuli could be perceptually priori-
tized.
In addition to evidence of an amygdala-driven bottom-up pro-
cessing of salient stimuli, studies suggest that a ventral network,
comprising the temporoparietal junction (TPJ) and the ventral
frontal cortex (VFC), helps to reorient attention to salient incom-
ing sensory information outside the current focus of processing
(Corbetta & Shulman, 2002). This network is recruited by infre-
quent or unexpected events that are salient; for e.g., invalidly cued
targets in the Posner task or oddballs. Studies show that during top-
down attentional guidance activity in TPJ is suppressed (Shulman,
Astafiev, McAvoy, d’Avossa, & Corbetta, 2007; Shulman et al., 2003;
Todd, Fougnie, & Marois, 2005) and in the presence of salient non-
targets stimulus activity in TPJ increases (Geng & Mangun, 2011).
Hence, the TPJ and VFC function like circuit breakers that shift
the focus to salient but task-irrelevant stimuli, even in case of
emotional stimuli (Dolcos & McCarthy, 2006). These studies sug-
gest additional bottom-up stimulus-driven mechanisms by which
threats could be perceptually prioritized, and demonstrate a possi-
bility of interactions between top-down and bottom-up processes
via a brain network that is sensitive to both kinds of processing.
4. The influence of anxiety on bottom-up threat-perception
While anxiety is typically conceptualized as an anticipatory
response to future threatening events, fear is typically thought of
as the response to an immediate threat (Davis, Walker, Miles, &
Grillon, 2010; Grupe & Nitschke, 2013; LeDoux, 2015). Neverthe-
less, perceptual processing in anxiety is typically conceptualized
as driven by bottom-up processes (Mathews & MacLeod, 1994;
Ohman et al., 2001). Empirical studies examining perception of
threatening stimuli in anxious individuals, like the studies that
examine these phenomena in healthy individuals, tend to utilize
tasks that exogenously drive perception and attention through
the use of unanticipated or task-irrelevant stimuli. Common tasks
employed to study this phenomenon present emotional stimuli
that ‘pop out’ amongst non-emotional stimuli (Fox et al., 2000;
Ohman et al., 2001), are peripheral to fixation (Mogg & Bradley,
1999), appear rapidly in stream of images (Arend & Botella, 2002),
or are irrelevant to the task at hand (Williams, Mathews, &
MacLeod, 1996).
Experimental results suggest that compared to healthy controls,
individuals with clinical anxiety (Klumpp & Amir, 2009; Mogg,
Millar, & Bradley, 2000; Ohman et al., 2001), dispositional anxi-
ety (Eysenck, Derakshan, Santos, & Calvo, 2007; Mogg & Bradley,
1999; Richards, French, Johnson, Naparstek, & Williams, 1992), and
experimentally induced anxiety (Lim & Pessoa, 2008; Robinson,
Letkiewicz, Overstreet, Ernst, & Grillon, 2011) detect or orient
towards threatening stimuli more quickly. Other studies have
found no difference in the initial orientation to threat, but have
demonstrated that individual differences in anxiety increase dwell
time and the time required to disengage from a threatening stim-
ulus (Fox, Russo, Bowles, & Dutton, 2001; Yiend & Mathews,
2001). However, there is some empirical evidence demonstrat-
ing that anxiety can both facilitate engagement with threatening
stimuli and slow disengagement with threatening stimuli (Koster,
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Verschuere, Crombez, & Van Damme, 2005; Shackman, Maxwell,
McMenamin, Greischar, & Davidson, 2011), suggesting that anx-
iety influences both earlier and later sensory processes involved
in threat perception. Finally, recent studies of soldiers experi-
encing acute stressors, such as combat, show that avoidance of
threat, rather than a bias towards threats predicts subsequent PTSD
symptoms (Wald, Shechner et al., 2011; Wald, et al., 2011). These
studies suggest that situationally induced anxiety may influence
the relationship between orientation to threat and future anxiety
symptoms.
The well-documented, bidirectional relationship between
attentional biases to threat and anxiety (Van Bockstaele et al.,
2014) has led to the development of cognitive-bias modification of
selective attention (CBM-A), a procedure with demonstrated thera-
peutic promise, and Attention Bias Modification Treatment (ABMT),
a treatment for anxiety. Both of these techniques are based on cog-
nitive behavioural models positing that cognitive biases can lead to
anxiety disorders, and therefore altering attentional biases could
subsequently reduce anxiety symptoms. Reviews of both CBM-A
and Attention Bias Modification (ABM) have shown these proce-
dures reduce anxiety symptoms and vulnerability to anxiety in
adults (MacLeod & Clarke, 2015; MacLeod & Mathews, 2012) and in
children (Eldar et al., 2012). Furthermore, meta-analyses of stud-
ies examining the impact of CBM and ABMT on anxiety symptoms
has demonstrated that these treatments are effective (Hakamata
et al., 2010; Hallion & Ruscio, 2011). A meta-analysis of the efficacy
of ABMT on clinical anxiety demonstrated that more patients who
received this treatment no longer met diagnostic criteria compared
to patients in control conditions (Linetzky, Pergamin-Hight, Pine, &
Bar-Haim, 2015).
Different types of anxiety (e.g. dispositional vs situationally
induced) can interact, impacting perceptual biases for threatening
images. For example, anxiety induced by an upcoming examination
increased a pre-existing tendency for those higher in dispositional
anxiety to respond more rapidly to targets following a threaten-
ing stimulus (MacLeod & Mathews, 1988). Similarly, in individuals
high in trait-anxiety, a negative mood manipulation led to greater
interference from anxiety-related words on an emotional Stroop
task (Richards et al., 1992). However, some studies have found a
different pattern of interaction. For example, while participants
high in trait anxiety responded more slowly to threatening words
on an emotional Stroop task − indicating that attention had been
captured by these threatening distractors − under stress, trait anx-
iety no longer influenced response times (Mogg, Mathews, Bird, &
Macgregor-Morris, 1990). A subsequent study suggests that while
transient stressors may wash out differences between high and low
anxious individuals, chronic stressors exaggerate the differences in
attention attributed to trait anxiety (Mogg, Bradley, & Hallowell,
1994). Therefore, paying attention to the type of stressor at hand
could resolve the differences between studies that find that induced
anxiety either increases or decreases threat biases.
Overall, clinical, dispositional and situationally induced anxiety
are associated with faster detection of threatening stimuli. This per-
ceptual prioritization of threat in anxiety is attributed to attentional
capture by the stimulus or automatic processing of threaten-
ing stimuli (Ohman et al., 2001; Robinson, Charney, Overstreet,
Vytal, & Grillon, 2012; Robinson et al., 2011). Studies that exam-
ined brain activity while unanticipated or task-irrelevant stimuli
exogenously drive perception and attention demonstrate increased
amygdala and visual cortical activity for feared stimuli in anxi-
ety (Lipka, Miltner, & Straube, 2011; Straube, Mentzel, & Miltner,
2005). It is hypothesized that these perceptual enhancements
share similarities with exogenous stimulus-driven mechanisms
and are mediated via amydalar feedback into visual sensory regions
(Pourtois, Schettino, & Vuilleumier, 2013).
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
Other studies have demonstrated that very early sensory pro-
cessing is boosted in clinically anxious individuals (Knott et al.,
1994), and in children higher in dispositional anxiety (Woodward
et al., 2001). Threatening stimuli have been shown to activate the
amygdala more for anxious than non-anxious subjects, in clinical,
dispositional and experimentally induced anxiety (Bishop, Duncan,
& Lawrence, 2004; Calder, Ewbank, & Passamonti, 2011; Etkin &
Wager, 2007; Etkin et al., 2004; Larson, Ruffalo, Nietert, & Davidson,
2005). However, the amygdala does not work in isolation. A recent
study demonstrated that under threat of shock, greater functional
connectivity between the amygdala and the dorsolateral prefrontal
cortex (DLPFC) predicted faster threat detection, and was positively
associated with trait anxiety (Robinson et al., 2012). Other studies
have found that individuals with anxiety disorders had less func-
tional connectivity between the amygdala and the DLPFC compared
to healthy controls while resting or viewing threatening faces (Birn
et al., 2014; Prater, Hosanagar, Klumpp, Angstadt, & Phan, 2013).
Furthermore, in one study, the connectivity between DLPFC and
amygdala correlated negatively with measures of social anxiety
(Prater et al., 2013). Together, these studies suggest that different
kinds of anxiety influence the relationship between the amygdala
and the frontal cortex in distinct ways.
While the literature describing the impact of anxiety on per-
ception consistently demonstrates a bias for threatening stimuli,
precisely when this bias comes into play remains unclear. Since one
of the core features of anxiety is a tendency to make inaccurate pre-
dictions regarding the likelihood and costs of future negative events
(Grupe & Nitschke, 2013), the effect of anxiety on threat perception
may start before stimulus presentation and may involve top-down
factors such as goals, expectations and prior knowledge. Therefore,
to gain a complete understanding of how anxiety impacts threat
detection, it is necessary to examine the impact of top-down pro-
cessing on threat perception in anxiety.
5. Conceptual and methodological issues regarding
research on bottom-up factors effecting perception
Overall, studies of psychological and neural mechanisms
involved in perception of emotional stimuli have reinforced the
view that emotional salience-related, bottom-up effects are invol-
untary and not under the control of attention (Vuilleumier & Driver,
2007). However, this research raises methodological issues.
First, the majority of studies examining the influence of emo-
tional stimuli on attention have used tasks in which emotional
stimuli appear unexpectedly, such as modifications of a peripheral
or exogenous cuing task (Armony & Dolan, 2002; Holmes, Green, &
Vuilleumier, 2005; Keil, Moratti, Sabatinelli, Bradley, & Lang, 2005;
Mogg & Bradley, 1999; Mogg, McNamara et al., 2000; Stormark
& Hugdahl, 1996, 1997). The dot probe paradigm is a very com-
monly used task in which both a threatening and neutral stimulus
are presented simultaneously and peripherally, and one of them
is followed by an attentional probe (Holmes et al., 2005; Mogg &
Bradley, 1999; Mogg, McNamara et al., 2000). A facilitated response
to probes that appear at the same location of threat information
(valid trial), in comparison with responses to probes at the oppo-
site location of threat information (invalid trial), is interpreted as
vigilance for threat.
Secondly, bottom-up processing of emotional stimuli has been
shown to interact with top-down factors such as goals and task-
relevance. While bottom-up processing of emotional stimuli is
adaptive when they are relevant to our well-being, it is equally
adaptive to ignore these stimuli and stay task-focused when they
pose no danger. Hence, adaptive behavior requires constant inter-
action between top-down goals and bottom-up processing. Studies
using paradigms in which emotional stimuli are task-irrelevant
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hypothesize that emotional stimuli distract from the task at hand
because they are processed automatically, leading to impaired task-
relevant performance. For example, task-irrelevant emotional faces
slow reaction times (Vuilleumier et al., 2001) and decrease accuracy
(McHugo, Olatunji, & Zald, 2013). The presentation of emotional
stimuli exogenously or as distractors in experimental paradigms
has contributed to the view that emotional stimuli are processed
involuntarily in a bottom-up manner and are immune to the effect
attention or cognitive control.
However, studies also show that strong as it may be, bottom-up
processing of an emotional stimulus is also susceptible to top-down
control. For example, happy and threatening facial expressions
have been shown to capture attention when they are the tar-
get of search but not when they are in opposition to task goals
(Hahn & Gronlund, 2007; Williams, Moss, Bradshaw, & Mattingley,
2005). This indicates that in addition to stimulus characteristics,
top-down goals guide the efficiency of emotional facial expression
search. Similarly, reward and punishment can modulate bottom-
up capture of attention (Engelmann & Pessoa, 2007) and distractor
inhibition (Della Libera & Chelazzi, 2006). For more detailed cov-
erage on the interaction between top-down goals and bottom-up
processing of emotional stimuli we would refer readers to more
comprehensive reviews on this topic by Aue, Chauvigne, Bristle,
Okon-Singer, & Guex, 2016; Pessoa, 2009; Pessoa & Ungerleider,
2005 and Pessoa et al., 2002; Pessoa, Gutierrez et al., 2002.
Neural evidence also indicates that bottom-up subcortical pro-
cessing of emotional stimuli is susceptible to top-down control.
For example, amygdala and its influence on the visual cortex, is
impacted by top-down factors like task-context and attentional
control (Pessoa & Adolphs, 2010; Pessoa, 2008). Amygdala response
is modulated via top-down input from prefrontal brain regions
during emotional conflict (Etkin, Egner, Peraza, Kandel, & Hirsch,
2006) and reappraisal (Ochsner, Bunge, Gross, & Gabrieli, 2002;
Ochsner et al., 2004; Phan, Wager, Taylor, & Liberzon, 2004); for
a review see (Ochsner & Gross, 2005). While some studies have
argued that amygdala response to threatening stimuli is indepen-
dent of voluntary attention (e.g. Vuilleumier et al., 2001), these
studies tend to use tasks in which threatening stimuli are presented
in an unexpected manner, and have not examined the contributions
top-down factors, such as those implemented via projections from
the prefrontal cortex to the amygdala. Hence, Pessoa and Adolphs
(2010) propose an alternative model, which underlines the numer-
ous connections between the prefrontal cortex, the visual cortex,
the amygdala and other subcortical structures, and posits that the
amygdala is primarily involved in the coordination of cortical pro-
cessing rather than just the detection of threat.
The interaction between bottom-up emotional processing and
top-down factors also plays an important role in anxiety as outlined
by the attentional control theory (Eysenck et al., 2007). This theory
posits that trait anxiety increases the attention given to threatening
stimuli and impairs attentional control. In other words, trait anxi-
ety impairs top-down guidance of attention and boosts bottom-up
processes related to threat detection. More specifically, according
to attentional control theory, trait anxiety impairs the efficiency
with which non-threatening stimuli are processed, rather than
always impacting performance. This is consistent with studies that
found that accuracy (Calvo, Eysenck, Ramos, & Jimenez, 1994; Ikeda,
Iwanaga, & Seiwa, 1996; Markham & Darke, 1991) or reaction
time was not negatively impacted by anxiety (Bishop et al., 2004;
Compton et al., 2003; Whalen et al., 1998). Attentional control the-
ory also posits that the impact of trait anxiety on performance is
exacerbated as demands on the executive control increase (Ashcraft
& Kirk, 2001; Eysenck, 1985).
Finally, in addition to evidence indicating that emotional
bottom-up factors constantly interact with top-down factors,
research increasingly shows that top-down factors play a vital role
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
5
in perception (Barrett & Simmons, 2015; Summerfield & de Lange,
2014). Perceptual decision-making is heavily influenced by factors
that occur prior to physical encounter with the stimulus, such as,
expectations regarding what is contextually relevant or likely. This
is exemplified by faster and more accurate recognition of objects
that occur in familiar contexts (Bar, 2004; Brattico, Naatanen, &
Tervaniemi, 2002; Enns & Lleras, 2008), hence, a loaf of bread is
identified more accurately than a drum in the kitchen (Palmer,
1975). More recently, research is showing that emotional top-down
factors can also influence perception (e.g., Sussman et al., 2016;
Sussman, Szekely et al., 2016). In the brain, top-down factors such
as expectation, context, attention, and learning have been shown
to influence amygdala activity. The amygdala is one of the most
highly connected regions of the brain and shows connectivity con-
sistent with that of a ‘hub’ region (Barbas, 1995; Stephan et al.,
2000; Swanson, 2003; Young, Scannell, Burns, & Blakemore, 1994)
indicating that it is well situated to influence processing in other
regions.
In summary, while much has been learned regarding the
bottom-up factors involved in the perceptual prioritization of
emotional stimuli, increasing evidence is showing that 1) studies
examining attentional and perceptual biases for emotional stim-
uli have largely utilized paradigms that capitalize on the use of
bottom-up processes, 2) bottom-up perception and related neu-
ral mechanisms are sensitive to top-down influence, 3) top-down
factors play a critical role in human visual perception. Together,
these lines of evidence underscore the importance of examining the
role of top-down prestimulus biases in the prirotized perception of
threatening stimuli.
6. Top-down guidance of perception
In contrast to bottom-up processes, top-down processes are
endogenous and driven by contexts or goals. According to the
top-down perspective, visual perception involves a process of
hypothesis testing in which predictive perceptual models are
proposed based on prior knowledge and incoming sensory infor-
mation is compared to these predicted models (Gregory, 1968;
Summerfield et al., 2006). Therefore, past knowledge and expe-
rience create expectations of what is relevant or likely, helping
facilitate the speed and accuracy of subsequent perceptual judg-
ments. This expectation takes the form of predictive neural
representations that may be based on perceptual templates that
consist of important discriminating features (Neisser, 2014) used
to aid stimulus recognition.
These predictive representations are implemented via two
important top-down mechanisms: 1) by an attention-related pri-
oritization of stimulus processing based on the relevance of the
stimulus to goals and 2) by an expectation-related interpretation
of stimulus based on the likelihood of encountering an antici-
pated stimulus (Summerfield & de Lange, 2014; Summerfield et al.,
2006). The function of top-down attention is to allocate cognitive
resources based on the relevance or salience of a stimulus given the
current context. Common manipulations of attention by top-down
processes include spatial attention, feature-based attention, and
object-based attention (Kanwisher & Wojciulik, 2000). For exam-
ple, prior knowledge of the target stimulus location enhances the
detection of stimuli at the attended location (Carrasco, Ling, & Read,
2004; Posner, Snyder, & Davidson, 1980), even when attention is
‘covert’ (i.e. in the absence of saccades to attended locations). Sim-
ilarly, top-down spatial biasing towards the location reduces the
distracting effects of salient stimuli at other locations (Theeuwes,
1991; Yantis & Jonides, 1984). In contrast to attention, the effect
of expectation is often studied by manipulating the likelihood of
the occurrence of a stimulus. Studies have robustly demonstrated
that responses to visual stimuli are facilitated by the conditional
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probability of occurrence in a given context. Objects are recog-
nized more quickly in a context in which they are likely to be
found (Gold & Shadlen, 2007; Heekeren, Marrett, & Ungerleider,
2008). Research also demonstrates that objects in familiar or pre-
dictable contexts are recognized faster and more accurately than
objects seen in unpredictable contexts (Bar, 2004; Brattico et al.,
2002; Enns & Lleras, 2008); for example, a loaf of bread is iden-
tified more accurately than a drum in the kitchen (Palmer, 1975).
Additionally, humans integrate and weigh prior knowledge about
likelihood and uncertainty in combination with current sensory
information in perceptual decision-making following Bayes’ the-
orem (Bach & Dolan, 2012). In contrast, unexpected visual objects
in a complex scene are often detected more slowly and with more
errors (Biederman, Mezzanotte, & Rabinowitz, 1982).
7. Top-down guidance of perception by emotional cues
While threatening stimuli can take us by surprise, we often
detect these stimuli within contexts or following cues that indi-
cate an upcoming threat. Implicit and explicit environmental cues
direct us to stimuli that are relevant or likely given the context,
subsequently improving perception. For example, a context such
as a dense forest path in Colorado can create expectations of see-
ing a bear, or an overt cue, such as a sign warning that a floor was
recently washed, encourages us to look for slippery spots, resulting
in faster detection of the expected stimulus. Emotional and moti-
vational top-down factors (e.g. searching for threat or anticipating
reward) have been shown to influence target detection. When emo-
tional stimuli are task-relevant, in other words, when they are
prioritized both by top-down and bottom-up processes, detection
of these stimuli are improved. For example, happy and threaten-
ing facial expressions are prioritized when they are the target of
search, but not when they are in opposition to task goals, (Hahn
& Gronlund, 2007; Williams et al., 2005). Furthermore, cues indi-
cating an upcoming threat-related perceptual decision improve the
sensitivity and speed of subsequent perceptual decisions (Sussman
et al., 2016; Sussman, Szekely et al., 2016), specifically in case of
subsequent fearful faces (Sussman, et al., 2016). These studies indi-
cate that, in addition to stimulus characteristics, emotion-related
top-down goals guide the efficiency of facial expression search, and
can improve target detection.
Top-down processes could improve threat perception by guid-
ing attention to a spatial location, or to a specific feature. For
example, on a visual search task, cues correctly predicting the
spatial location and threat value of faces improved reaction time;
performance improved both when spatial cues were accurate and
when cues accurately predicted an angry face, demonstrating that
endogenous processes related to both spatial and feature-based
attention can enhance threat detection (Mohanty, Egner, Monti,
& Mesulam, 2009). Additionally, on a cued word identification
task, emotional words were more accurately identified than neutral
words, while emotional distractors had no impact on performance,
suggesting that when directed to looking for a specific emotional
stimulus via cues, perceptual processing of that emotional stim-
ulus is enhanced (Zeelenberg, Wagenmakers, & Rotteveel, 2006).
The arousal-biased competition theory suggests a mechanism by
which top-down processes may perceptually prioritize emotional
stimuli. It posits that emotional cues increase arousal, biasing selec-
tive attention toward perception of the stimuli relevant to the goal
at hand (Mather & Sutherland, 2011).
8. Brain mechanisms of top-down guidance of perception
After sensory information hits the retina it is processed in hier-
archically organized regions with increasing level of abstractness
and complexity before a percept is formed (Deco & Rolls, 2004;
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
Tanaka, 1996). Downstream (higher order) brain regions feed infor-
mation back to upstream (lower order) regions, influencing how
information is processed. These feedback projections outnumber
the feedforward projections in most stages of the hierarchy, and
therefore are likely to have a major influence on the processing of
incoming information (Angelucci et al., 2002). Since attention and
expectation are two top-down influences that may play a crucial
role in perceptual biases towards threatening stimuli, this review
will focus on these two factors.
Top-down modulation of perception impacts most known
stages of visual information processing, even in brain regions that
process basic visual information, such as V1 (Li, Piech, & Gilbert,
2006; Motter, 1993; Roelfsema, Lamme, & Spekreijse, 1998). In fact,
top-down modulation has been found to occur even before the sen-
sory information reaches the cortex in the subcortical region of
lateral geniculate nucleus (McAlonan, Cavanaugh, & Wurtz, 2008;
O’Connor, Fukui, Pinsk, & Kastner, 2002); for review see (Gilbert
& Li, 2013). Top-down modulation is more obvious in extrastri-
ate areas (V2/V3 and V4) (McAdams & Maunsell, 1999; Nienborg &
Cumming, 2009), and in the medial (Womelsdorf, Anton-Erxleben,
& Treue, 2008) and ventral visual streams (Chelazzi, Miller, Duncan,
& Desimone, 1993). The effect of attention and expectation on visual
cortical activity prior to stimulus onset has been demonstrated
in multiple human studies (Esterman & Yantis, 2010; Peelen, Fei-
Fei, & Kastner, 2009; Stokes, Thompson, Nobre, & Duncan, 2009;
Summerfield et al., 2006). For example, using a cued face/house
discrimination task, one study demonstrated increase of blood-
oxygen-level dependent (BOLD) signal in object-category-specific
visual cortical areas during expectation (Esterman & Yantis, 2010).
Anticipation increases prestimulus neuronal activity in sensory
and decision-related neurons (Kastner, Pinsk, De Weerd, Desimone,
& Ungerleider, 1999; Ress, Backus, & Heeger, 2000; Summerfield
& de Lange, 2014). For example, studies show that neurons in
the inferior temporal lobe that encode the expected stimulus
show increased activation following a predictive cue (Erickson &
Desimone, 1999). Similarly, neurons in medial temporal lobe (sen-
sitive to object motion) are activated prior to a predicted motion
stimulus (Albright, 2012; K. Sakai & Miyashita, 1991). Prestimulus
BOLD signal in extrastriate visual cortex is associated with sub-
sequent decisions regarding whether subjects report seeing the
Rubin’s vase illusion as a face or a vase (Hesselmann, Kell, Eger,
& Kleinschmidt, 2008), and face-related cues elicit increased BOLD
signal in fusiform face area (FFA) prior to face stimulus onset (Bar
et al., 2001; Esterman & Yantis, 2010; Puri, Wojciulik, & Ranganath,
2009). In a random dot classification task, BOLD signal in motion
sensitive visual cortex prior to stimulus onset predicts the subject’s
response (Hesselmann, Kell, & Kleinschmidt, 2008). Another study
examining the prestimulus oscillatory activity over motor cortex
found that both endogenous expectation (without explicit cue) and
expectation induced by explicit cues biases the starting point of
decision-related activity before the accumulation of sensory evi-
dence (de Lange, Rahnev, Donner, & Lau, 2013).
Studies examining the ensemble activity patterns of BOLD signal
have shown that top-down attention to a target activates target-
specific representations in shape-sensitive visual areas (Peelen
et al., 2009), and brain regions involved in olfactory perception
(Zelano, Mohanty, & Gottfried, 2011), indicating a preparatory bias
favoring the attended stimulus over competing ones.
Increased prestimulus activity may reflect increased attention
prior to stimulus onset, thereby improving subsequent detection
(Hesselmann, Sadaghiani, Friston, & Kleinschmidt, 2010). Alter-
natively, according to sequential sampling models of perceptual
decision-making, like the drift diffusion model (Ratcliff & Smith,
2004; Ratcliff, 1978), increases in prestimulus activity may reflect a
bias or shift in the starting point for evidence accumulation towards
a specific decision boundary, or may reflect a change in the rate of
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evidence accumulation (Summerfield & de Lange, 2014). Behav-
iorally, studies have shown that a predicted stimulus is associated
with faster reaction time, higher accuracy, and higher perceptual
sensitivity compared to unpredicted stimuli (Bar, 2004; Geisler,
2008; Polat & Sagi, 1994).
In addition to sensory areas, top-down modulation of visual
processing involves prefrontal and parietal areas. For example,
top-down biasing of attention in space involves a network of
frontoparietal regions that include the intra-parietal sulcus in
the posterior parietal cortex (PPC) and the frontal eye fields
(FEF), the anterior cingulate cortex and supplementary motor area
(ACC/SMA), and the thalamus and superior colliculus (Corbetta
& Shulman, 2002; Gitelman et al., 1999; Kastner, De Weerd,
Desimone, & Ungerleider, 1998; Kastner et al., 1999; Mesulam,
1981, 1999; Reynolds, Chelazzi, & Desimone, 1999). This spatial
attention network is hypothesized to form an integrated search
template combining the spatial coordinates and the relevance of
the anticipated stimulus to bias visual neurons in preparation
for the search process (Egner, 2008; Gottlieb, 2007; Thompson
& Bichot, 2005). Brain regions involved with assessing the moti-
vational value of a stimulus include neurons in the inferior
parietal lobule and the intra-parietal sulcus (Bushnell, Goldberg,
& Robinson, 1981; Mountcastle, Lynch, Georgopoulos, Sakata, &
Acuna, 1975; Sugrue, Corrado, & Newsome, 2004) and limbic
regions such as amygdala (Pessoa et al., 2002; Pessoa, Gutierrez
et al., 2002; Vuilleumier & Driver, 2007). However, whether these
regions communicate is unclear. The cingulate gyrus may be a con-
duit for information on motivational salience used by the spatial
attention network (Mesulam, Van Hoesen, Pandya, & Geschwind,
1977), as the limbic parts of the cingulate gyrus send projec-
tions to frontoparietal regions and posterior cingulate neurons
signal reward outcomes associated with eye movements (McCoy,
Crowley, Haghighian, Dean, & Platt, 2003) and preferences guiding
visual orienting (McCoy & Platt, 2005).
9. Brain mechanisms of top-down guidance of perception
by emotional cues
While most studies have focused on the brain mechanisms
of bottom-up perception of emotional stimuli, newer evidence
is beginning to uncover the brain circuitry that is involved
in top-down guidance by emotional information. In one study,
endogenous guidance of attention was manipulated by predic-
tive cues offering both probabilistic information related to the
location of a subsequently presented stimulus, and information
regarding the emotional salience of that stimulus (Mohanty et al.,
2009). Spatially valid cues enhanced target detection. In addition,
cues accurately predicting angry face targets were associated with
faster responses than uninformative cues, indicating an endoge-
nous mediation of improved target detection, driven by emotional
cues. Functional imaging showed that prior to the stimulus pre-
sentation, spatially informative cues activated the frontoparietal
spatial attention network including the intra-parietal sulcus and
FEF, as well as FG. Cues predicting angry faces also activated brain
regions associated with emotional processing, including limbic
areas, such as the amygdala. Additive effects of spatial and emo-
tional cueing were identified in the intra-parietal sulcus, FEF and
FG indicating that cues activate regions involved in directing spatial
attention prior to arrival of the threat are activated in preparation.
These regions also had increased connectivity with the amygdala
following angry face cues. This study demonstrates that prestimu-
lus threat-related cues elicit amygdala input to the spatial attention
network and inferotemporal visual areas, thereby facilitating threat
detection.
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
7
Separate from the effects of attention, expectations regarding
upcoming targets can enhance their perception (Summerfield &
Egner, 2009). According to the ‘predictive coding’ theory, rather
than passively absorbing sensory input, the brain actively predicts
what is coming, generating a prestimulus template against which
observed sensory information is matched (Summerfield et al.,
2006; Zelano et al., 2011). In an fMRI study in which human subjects
decided whether visual objects were faces or not, predictive neural
representations related to faces were reported in medial prefrontal
cortex (mPFC; Summerfield et al., 2006). Interestingly, perceptual
decisions about faces were associated with an increase in top-down
connectivity from the mPFC to face-sensitive visual cortices, includ-
ing FFA, consistent with the idea that the prefrontal cortex codes
for the predicted representations and sends top-down signals that
guide the sensory regions in collecting relevant evidence to make
the perceptual decision. Using multivariate pattern (MVP) analy-
ses of prestimulus ensemble patterns, another study showed that
target-specific ensemble patterns emerge prior to encountering the
target stimulus in the orbitofrontal cortex (OFC) and in sensory
cortices. Furthermore, these prestimulus patterns reliably predict
subsequent behavioural performance (Zelano et al., 2011).
In a study that examined the impact of threat compared to
neutral prestimulus cues on brain activity and subsequent perfor-
mance, threat cues increased both cue- and stimulus-related brain
activation and improved subsequent stimulus detection (Sussman
et al., 2016). More specifically, threat cues resulted in a larger late
positive potential (LPP) and in increased superior temporal sul-
cus (STS) activity, both of which are measures of emotional face
processing. In addition, threat cues specifically increased amyg-
dala activity for subsequently presented threatening vs neutral
faces. Furthermore, brain activity, as measured by the LPP and
STS activity, predicted subsequent improvement in the speed and
precision of perceptual decisions about threatening faces. These
results demonstrate how top-down processing elicited by pres-
timulus threat-related cues can enhance subsequent perceptual
decision-making. It has also been hypothesized that this enhance-
ment may be due to arousal-induced release of norepinephrine
into the locus coeruleus leading to increased levels of glutamate
and norepinephrine at the site of the goal-relevant representation,
thereby enhancing the representation of the goal-relevant stimulus
(Mather, Clewett, Sakaki, & Harley, 2015).
Overall, while the neural mechanisms involved in prestimulus
threat-related biases are relatively unexplored, emerging evidence
indicates that top-down factors may impact threat perception both
by changes in prestimulus activity in sensory regions as well as
prestimulus biasing via templates instantiated in higher order
regions (including PPC, FEF, and other prefrontal regions) and inter-
actions of these regions with limbic and sensory regions.
10. Top-down guidance of the perception by emotional
cues in anxiety
Top-down processes may also play a crucial role in the devel-
opment and maintenance of perceptual biases in anxiety disorders.
Anticipation of negative future events is one of the cardinal features
of anxiety. For example, people with anxiety tend to overestimate
both the likelihood of negative events occurring and the cost of
these negative events (Grupe & Nitschke, 2013). Thus, a person with
clinical anxiety or spider-related fear standing in a room with cob-
webs might have higher expectation of spiders being present and
overestimate their dangerousness compared to a non-anxious per-
son in the same room. As a result of this overestimation, anxious
individuals will scan the environment for spiders and will detect
them faster if present. Researchers have proposed that focusing
on the anticipatory phase in anxiety may be an effective strategy
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to determine psychological and neurobiological factors involved in
anxiety development and maintenance (Davis et al., 2010).
According to the ‘uncertainty and anticipation model of anxi-
ety,’ anxiety influences several cognitive processes, two of which
relate directly to threat perception (Grupe & Nitschke, 2013). First,
hypervigilance, or increased attention to threatening information
even before a stimulus is presented can lead to both faster detection
of threatening stimuli and a misinterpretation of neutral stimuli.
For example, anxiety caused by the threat of shock leads to faster
detection of negative stimuli (Robinson et al., 2011), interpretation
of neutral faces as being negative in socially anxious individuals
(Yoon & Zinbarg, 2008) and interpretation of ambiguous intero-
ceptive experiences as being negative in people high in anxiety
sensitivity (Richards, Austin, & Alvarenga, 2001). Second, inflated
estimates of threat probability and the costs of threats can lead to
improved performance (Paulus & Yu, 2012), via overweighting of
low probability events (Mukherjee, 2010).
Recent evidence provides direct support for the view that anx-
iety can improve perception by influencing top-down processes
such as top-down attention. This research shows improvement
in perceptual sensitivity due to prior threat-related information
is dependent on individual differences in trait anxiety and cur-
rent levels of induced anxiety (Sussman, Szekely et al., 2016). In
this study, two groups of participants varying in levels of trait
anxiety (dispositional anxiety) identified degraded emotional and
neutral stimuli in a cued two-alternative forced-choice perceptual
task. One group completed the perceptual tasks in the presence
of the threat of shock (high situationally induced anxiety), while
the other group completed the same task in the absence of threat
of shock (low situationally induced anxiety). Individual differences
in trait anxiety moderated gains in perceptual sensitivity follow-
ing the threat cue, such that higher trait anxiety was associated
with larger gains in perceptual sensitivity in the presence of shock
(Sussman, Szekely et al., 2016) but worse perceptual sensitivity in
the absence of shock. Overall, results from this study demonstrated
that distinct types of anxiety (dispositional and induced) interact
with each other in influencing how prior threat-related informa-
tion is used in a top-down manner to guide perception (Sussman,
Szekely et al., 2016). Prestimulus threat-related information can
influence perception by effecting attention or expectation, both of
which are hypothesized to involve different psychological and neu-
ral mechanisms (Summerfield & de Lange, 2014). The cues in the
aforementioned Sussman, Szekely et al. (2016) indicated what to
look for (threatening or neutral faces) but the cues did not provide
information regarding the likelihood of targets.
Aue and colleagues (2013, 2016) manipulated the probabil-
ity or likelihood of upcoming targets to examine whether threat
expectancy (inflated estimates of threat probability) impacts detec-
tion of a spider or birds in individuals with or without spider fear
(Aue et al., 2016; Aue, Guex, Chauvigne & Okon-Singer, 2013). In
two studies, they manipulated expectancy via a prestimulus cue
telling participants there was a 90% or 50% likelihood of seeing a
spider or a bird. Cues indicating the likelihood of spiders did not
have a significant impact on the speed of spider detection for indi-
viduals with or without spider fear. However, prestimulus cues
regarding the likelihood of seeing a bird on the subsequent trial
lead to observable differences in reaction time, error rates, pupil
diameter and heart rate for both groups of subjects (Aue et al.,
2016; Aue, Guex, Chauvigne & Okon-Singer, 2013). These stud-
ies indicate that top-down manipulation of expectancies does not
impact detection of threatening stimuli the way it affects detec-
tion of non-threatening stimuli. Taken together, the Sussman et al.
(2016, 2016) and Aue et al. (2013, 2016) studies indicate that anxi-
ety is associated with differential utilization of attention but not
probability-related information regarding upcoming threatening
stimuli.
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
Making use of prior threat related information requires the
maintenance of task-relevant representations online in work-
ing memory to match against incoming stimuli (Sreenivasan,
Sambhara, & Jha, 2011). Because emotional representations are
maintained with greater vividness (Bywaters, Andrade, & Turpin,
2004), they may tax working memory resources more than neu-
tral internal representations. Therefore, tasks that require the
maintenance of threat-related information, or that encourage the
unnecessary entry of threat-related information into working
memory may result in deficits for individuals high in trait anx-
iety (Stout, Shackman, & Larson, 2013; Sussman, Szekely et al.,
2016). Trait anxiety is thought to particularly impact the efficiency
on tasks involving the inhibition function (supporting empiri-
cal research includes Calvo & Eysenck, 1996; Fox, 2002; Yiend &
Mathews, 2001), the shifting function (Eysenck et al., 2007; Gopher,
Armony, & Greenshpan, 2000), and, to a certain extent, the updating
function (Duff & Logie, 2001).
Neurally, anxiety is associated with reduced recruitment of
regions involved in top-down control. For example, predictive
representations of upcoming target stimuli are maintained in pre-
frontal regions of the brain, specifically, the dorsal and ventral
medial prefrontal cortex (DMPFC & VMPFC; Summerfield et al.,
2006). Studies show that anxiety is associated with poorer recruit-
ment of DMPFC (Shin et al., 2005) and dorsolateral prefrontal cortex
(DLPFC; Bishop, 2009), possibly contributing to an impaired abil-
ity to maintain and deploy threat-related perceptual templates in
the service of threat perception. In line with this, low trait anxious
individuals have been found to benefit from cues preceding a visual
search task, whereas individuals high in trait anxiety are not able
to use these cues as effectively (Berggren & Derakshan, 2013). In
a recent study, decreased perceptual sensitivity in high trait anx-
iety was observed for threatening but not neutral cues (Sussman,
Szekely et al., 2016). Since the adverse impact of anxiety on per-
formance becomes greater with increasing task demands on the
central executive (Eysenck et al., 2007), it is possible that main-
tenance of a perceptual set for threatening stimuli which might
be more complex may be more demanding than maintaining a
perceptual set for neutral stimuli.
Few studies have examined neural mechanisms of threat related
guidance of attention or expectation in anxiety. However, exami-
nation of neural activity at rest or prior to stimulus onset in anxiety
provides clues into potential neural mechanisms. Neuroimaging
studies have demonstrated that the amygdala is more active
for people with anxiety disorders compared to healthy controls
(Furmark et al., 2002; Sakai et al., 2005; Semple et al., 2000), and
for people with a short variant of the 5-HT transported gene com-
pared to individuals homozygous for the long variant (Canli et al.,
2006), when at rest. Anticipatory amygdala and anterior cingulate
cortex activity prior to treatment predicted treatment outcome
8 weeks later (Nitschke et al., 2009). In one experiment, subjects
with social phobia were asked to imagine giving a public speech.
Individuals with social phobia had hyperactivity in limbic and par-
alimbic regions compared to healthy controls (Lorberbaum et al.,
2004). While anticipating giving a public speech, socially anxious
individuals also showed increased limbic activation and decreased
striatal activation (Boehme et al., 2014), as well as reduced func-
tional connectivity between cortical regions involved in emotion
regulation and limbic regions (Cremers et al., 2015). Furthermore,
symptom severity was found to correlate with changes in activa-
tion and connectivity (Boehme et al., 2014; Cremers et al., 2015).
Overall, these studies show greater limbic activity prior to stim-
ulus onset in anxiety suggesting that anxiety may impact threat
perception by changes in prestimulus activity in limbic regions,
possibly leading individuals with anxiety to interpret cues regard-
ing salience and the likelihood of upcoming threatening stimuli
differently than individuals without anxiety. Enhanced perceptual
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sensitivity in threatening contexts, or following threat-related cues
may also be due to enhanced sensory-perceptual functions, which
have been observed in both high trait anxiety and induced anxi-
ety (Robinson, Vytal, Cornwell, & Grillon, 2013). Results from one
study demonstrate that the threat of shock changes neural process-
ing to a sensory-vigilance mode that prioritizes threatening stimuli
(Arnsten, 2009; Shackman et al., 2011). Finally, models of decision-
making suggest a few mechanisms that could drive the perceptual
prioritization of threatening images in anxiety by biasing decisions
towards a threaten response (Sussman, Szekely et al., 2016).
Overall, the role of top-down factors in threat perception in anxi-
ety is not well understood. While greater activity in threat-sensitive
limbic and sensory brain regions at rest and during anticipatory
periods in anxiety suggests a possible mechanism by which threat
perception could be prioritized in anxiety, the impact of anxiety
on top-down attention or expectation of threat is not yet known.
Some empirical evidence supports enhancements in perceptual
sensitivity due to prior threat-related information; however, these
perceptual benefits depend on the type of anxiety. In disposi-
tional anxiety, impairment of top-down mechanisms may make
utilization and maintenance of top-down threat-related informa-
tion harder; whereas this information may be more effectively
utilized in case of clinical and situationally induced anxiety.
11. Conclusion
The perceptual prioritization of threatening stimuli, often
described as a bias for these stimuli, in dispositional, clinical and
induced anxiety has been observed as faster detection of threat-
related stimuli (Lim & Pessoa, 2008; Mogg & Bradley, 1999; Mogg
et al., 2000; Ohman et al., 2001; Robinson et al., 2011), or greater
activation in fear-sensitive brain regions (Bishop et al., 2004; Etkin
et al., 2004; Larson et al., 2005). This perceptual advantage has
generally been studied as a bottom-up phenomenon driven by
the physical characteristics of the threatening stimulus. Because
bottom-up processes were thought to drive the prioritized percep-
tion of threat, experiments designed to study a bias for threatening
stimuli have often relied on tasks that only tested the effects of
exogenous factors. However, top-down processes, such as prior
knowledge, expectations and goals, influence perception (Brosch
et al., 2010; Pessoa & Adolphs, 2010). Furthermore, these endoge-
nous factors are of particular importance in anxiety, which is
characterized by exaggerated and inaccurate estimates of the prob-
ability and costs of future negative events (Grupe & Nitschke, 2013).
Therefore, examining the impact of top-down factors on threat per-
ception in anxiety is a crucial step towards shedding light on how
basic processes of cognition, such as perception, may shape the
development and maintenance of anxiety and related disorders.
Future studies should focus on examining the differential impact
of threat-related top-down and bottom-up mechanisms (e.g., cues
guiding one to look for threatening faces and threatening faces
themselves) on perception and attention. Distinguishing the impact
of prestimulus attention from the impact of prestimulus expec-
tation of seeing a salient target could provide more fine-grained
detail about how top-down factors influence perception in normal
function and in anxiety. Examination of neural and computational
models would help elucidate the mechanisms implementing spe-
cific top-down and bottom-up factors involved in the perceptual
prioritization of emotional stimuli. For example, future studies
could compare pre- and post-stimulus neural representations of
emotional vs neutral stimuli in visual and prefrontal regions of the
brain, allowing us to determine how each contributes to perceptual
prioritization of threat in anxiety. The use of computational models
would allow us to examine the specific mechanisms that contribute
to the perceptual prioritization.
Please cite this article in press as: Sussman, T. J., et al. Top-down and bottom-up factors in threat-related perception and attention in
anxiety. Biol. Psychol. (2016), http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
9
Furthermore, the impact of other types of top-down processes
on threat perception should be examined. For example, since we
typically can infer what kinds of threats and rewards are more
relevant or likely depending on the context we currently inhabit,
exploring the impact of context on threat perception will allow
for more ecologically valid examination of how emotional stimuli
are perceptually prioritized. Some work has been conducted in this
vein. A recent study demonstrated that negative contexts evoked
by recalling a real-life threat (the Boston Marathon Bombings) led
to an increased false alarm rate on a shooting task (Wormwood,
Lynn, Feldman Barrett, & Quigley, 2016). This study demonstrates
that by studying the impact of context, we can add considerably to
our understanding of how threats are perceptually prioritized, and
how neutral stimuli may be misperceived as threatening in day-
to-day life. The interaction of situational contexts (such as the one
described above), and internal contexts, such as anxiety, or other
moods should also be explored to gain a more complete under-
standing of how top-down factors impact perception. While some
research has been done in this area, many questions remain. One
study demonstrated that a fearful mood, induced via film clip, could
speed reaction times over and above the impact of low-level visual
information (LoBue, 2014). However, little is known about how pos-
itive moods impact threat perception, or about how situational and
internal contexts interact in their impact on threat-perception.
Future research should also aim to better isolate the impact of
top-down from bottom-up factors on threat perception, as results
could advance our understanding of how these factors interact to
perceptually prioritize emotional stimuli. Drawing these distinc-
tions is especially crucial when studying the influence of anxiety on
perception, as anxiety is associated with inaccurate estimates of the
likelihood and costs of future negative events (Grupe & Nitschke,
2013). Elucidating how individual differences in anxiety impact
the interaction between top-down and bottom-up factors, both
in terms of behavioural performance and neural processing, could
provide clues about how basic perceptual processes are associated
with clinical symptoms. This, in turn, may provide valuable new
information about how to create new treatments for clinical anxi-
ety, and how to improve existing ones. For example, a recent study
found that delivering an ABMT designed to enhance vigilance for
threat prior to combat exposure protected participants, reducing
post-traumatic stress and depression symptoms following com-
bat (Wald et al., 2016). This demonstrates that acknowledging the
role of top-down processes in anxiety could lead to novel forms of
therapy, some which could even function preventatively.
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