The effect of fear on attentional processing in a sample of healthy females

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Abstract

The present experiment examines the effect of fear on efficiency of three attention networks: executive attention, orienting and alerting, in a healthy female sample. International Affective Picture System (IAPS) images were used to elicit both a fear response and a non-emotional response in 100 participants. During the emotion manipulation, participants performed a modified version of the Attention Network Test (ANT). Results showed enhanced executive attention in the fear condition compared to the control condition. Specifically, during a fear experience participants were better able to inhibit irrelevant information resulting in faster response times to a target. There was no effect of fear on orienting while the effect of fear on alerting was inconclusive. It is suggested that enhanced executive attention in fear-eliciting situations may function to focus attention on a potentially threat-related target, thus facilitating subsequent rapid responding.

Introduction

Fear is an emotional response to danger characterized by an appraisal of physical or psychological harm. It activates defensive behavior (e.g., immobility or fight-flight) and a repertoire of psychophysiological responses to deal with a threatening situation (Frijda, 1986). Much previous research on the relationship between fear and attentional processing has focused on the effect of anxiety on attentional orienting towards threatening stimuli or selective attention for threatening stimuli (e.g., threatening faces or words). For instance, studies have shown that high anxious individuals are faster to orient attention towards threat (Mogg and Bradley, 1999a, Mogg and Bradley, 1999b), slower to disengage attention from threat (Fox et al., 2001, Georgiou et al., 2005) and show enhanced selective attention for threatening stimuli (Williams, Mathews, & MacLeod, 1996).

Fewer studies have specifically examined the effect of a fear experience on attentional processing of non-emotional information. However, such studies are important as they shed light on whether emotional experience influences an individual's performance of common non-emotional tasks. Many everyday activities such as searching for an object can be non-emotional in nature. An important question is whether experience of fear-related states facilitates or impairs attention during the performance of such activities.

There is indirect evidence for a relationship between high arousal emotional states and enhanced selective attention. In a classic paper, Easterbrook (1959) argued that emotional arousal reduces the range of cues that an individual processes, resulting in a sharpening of attention in a central location and impairments in the processing of peripherally located stimuli. Such reduction in cue utilization can facilitate or impair performance depending on task requirements. For instance, a reduction in the range of cues utilized enhances performance in tasks where irrelevant cues need to be ignored. In contrast, in tasks that require the use of a wider range of cues for optimal performance (e.g., creative problem solving or divergent thinking), a reduction in cue utilization is likely to impair performance. This suggests that high arousal negative affective states such as fear are likely to reduce cue utilization, narrow scope of attention and consequently enhance selective attention.

Drawing on the work of Easterbrook (1959), Derryberry and Reed (1998) examined the effect of state and trait anxiety on attentional focus. A global–local task was used to assess attentional focus (Navon, 1977). Participants were presented with a composite stimulus that consisted of small letters arranged to form a large letter. They were instructed to identify either the small letters (local focus) or the large letters (global focus). Faster RTs to global in comparison to local targets indicated global focus and broadened scope of attention. In contrast, relatively faster RTs to local targets reflected local focus and narrowed scope of attention. Positive and negative motivational conditions were created by presenting the task within a game where points were to be gained or lost. In two experiments high trait anxious participants showed enhanced attentional focusing during negative games. Derryberry and Reed argued that trait anxiety leads to focused attention by facilitating local perceptual information during negative motivational states.

Taking account of Easterbrook (1959) and Derryberry and Reed (1998), Fredrickson (1998) proposed the broaden-and-build theory which posits that positive emotions broaden scope of attention, whereas negative emotions have the opposite effect. To assess the effect of emotions on breadth of attention, Fredrickson and Branigan (2005) also used a global–local visual processing task. Their paper-based task required participants to judge which of two comparison figures were most similar to a target figure. For example, in one of the trials, the target figure was a triangle composed of three squares. Two comparison figures were simultaneously presented below the target: (i) a triangle composed of three squares (the overall shape matched the global form of the target) and (ii) a square composed of four triangles (the local components of the comparison figure matched the local components of the target). Choosing the triangle composed of three squares was taken to represent a global processing bias and broadened scope of attention, as the choice is made based on the global form of the target. In contrast, choosing the square composed of triangles was believed to reflect a local processing bias, and narrowed scope of attention. Fredrickson and Branigan did not find an effect of fear or anxiety on attentional narrowing, but suggested that their version of the global–local task may have been too insensitive to measure changes in breadth of attention.

Despite this, support for the narrowing hypothesis can be taken from Gasper and Clore (2002). Using a global–local paradigm, these researchers found evidence for an influence of negative affect on breadth of attention, though their study focused on positive and negative mood in general, as opposed to fear in particular. Although interesting, studies of general negative affective states do not distinguish between diverse negative emotional states; a discrete emotions approach which involves eliciting fear in a lab setting is necessary to examine whether fear influences selective attention. With this in mind, the present study involves eliciting fear response in participants. A primary goal is to determine whether or not the experience of fear influences selective attention to a non-emotional target.

Previous research has also considered the relationship between anxiety and various forms of attentional orienting to threatening stimuli (e.g., Broomfield and Turpin, 2005, Calvo and Avero, 2005, Fox et al., 2001, Mogg and Bradley, 2002). Orienting includes shift and disengagement forms of attentional processing (Posner & Petersen, 1990). Experimental studies investigating the effect of anxiety on attentional orienting to threatening stimuli have shown that anxious individuals are more likely to gaze longer at intensely negative face stimuli (Mogg, Garner, & Bradley, 2007), have a stronger tendency to orient attention towards subliminally presented threat-related faces (Mogg and Bradley, 1999a, Mogg and Bradley, 2002), and demonstrate increased dwell time on threatening stimuli (Amir et al., 2003, Fox et al., 2001, Georgiou et al., 2005, Yiend and Matthews, 2001). Fewer studies have investigated whether a fear experience influences orienting irrespective of the valence of the information that is being attended. In one study Compton, Wirtz, Pajoumand, Claus, and Heller (2004) examined the relationship between baseline mood state (i.e., with no emotion manipulation) and performance on an orienting task. Individuals low in positive affect were slower to covertly shift their attention.1 However, there was no relationship between negative affect and orienting. In normal populations, baseline levels of negative affect are generally low; therefore relationships between negative affect and attentional processing variables are likely to be weak or nonexistent. Studies which explicitly focus on the effect of a fear experience on attentional orienting to neutral stimuli are more useful in examining whether fear or anxiety-related states influences orienting. Consequently, a second goal of the current study is to examine the effect of fear induced in a lab setting on attentional orienting to non-emotional stimuli.

A third form of attention – alerting attention – is an important but under studied aspect of attention research in general (Raz & Buhle, 2006). Alerting attention (or phasic alerting) reflects the individual's ability to mobilize their attentional resources in response to an impending stimulus (Posner and Fan, 2004, Posner and Rothbart, 2007). Unsurprisingly, given the general lack of empirical work on alerting, there is little research on the relationship between emotion and alerting. Yet, from a theoretical perspective, there is much to suggest that the experience of fear will enhance the efficiency of the alerting network. Fear increases the readiness of the individual to respond appropriately in the presence of danger. A fear response is characterized by avoidance related action tendencies (Frijda, 1986) and is associated with physiological changes which prepares the individual to respond to an impending threat (e.g., Stemmler, Heldmann, Pauls, & Scherer, 2001). Bearing this in mind, it is reasonable to suggest that the experience of fear will also be associated with increased alerting, or enhanced mobilization of attentional resources, in response to a potential threat. There is some evidence for this – Dennis, Chen, and McCandliss (2007) reported a positive relationship between state anxiety and alerting attention. Similarly, Compton et al. (2004) reported a positive association between negative affect and alerting. However, a link between fear or anxiety-related states and alerting has not been found in other studies (Dennis and Chen, 2007a, Dennis and Chen, 2007b). Given the mixed findings relating to fear, anxiety and alerting attention, further research is clearly required. A further goal of this study is to examine the relationship between a fear experience and alerting attention.

Attention can be viewed as an umbrella term for various forms of psychological phenomena (Styles, 2006). A consensus is now emerging that attention is best viewed in terms of at least three functionally and neuro-anatomically distinct networks. These are known as executive attention, alerting and orienting (Posner and Rothbart, 2007, Raz and Buhle, 2006). The Attention Network Test (ANT), based on the flanker and exogenous cueing paradigms, has been developed to test the efficiency of these three networks (Fan, McCandliss, Sommer, Raz, & Posner, 2002). Executive attention (selective attention) is the ability to focus on a relevant target and to inhibit irrelevant information in order to facilitate the production of an appropriate response. In the ANT, lower executive attention scores reflect less interference from irrelevant distracters indicating enhanced selective attention. Alerting reflects an individual's ability to increase and maintain response readiness in preparation for an impending stimulus. Alerting attention functions to maintain vigilance throughout task performance and is assessed by comparing reaction times to a cued target with reaction times to an uncued target (Sturm & Willmes, 2001). The cue serves as a warning signal and indicates that a target (e.g., an arrow) is about to appear. A higher alerting score generally indicates faster mobilization of attentional resources in preparation for the impending target. Orienting is concerned with the ability to covertly shift attention to a cued spatial location. In the ANT it is manipulated by presenting a cue indicating where in space an individual should attend, thereby motivating the individual to direct their attention to that location. The ANT assesses the shift aspect of orienting (as opposed to engagement or disengagement).

To date, as far as we are aware, the attention network test has only been used in two studies to examine the relationship between emotion and attention. Dennis, Chen, and McCandliss (2008) used a modified ANT to examine anxiety and attentional biases for threat, and found a positive relationship between state anxiety scores and alerting attention. In another study, Dennis and Chen (2007b) found that exposure to sad and fearful faces resulted in enhanced orienting and executive attention, but an association between both trait and state anxiety and alerting was not found. Given the mixed findings relating to anxiety and attention network performance, further research is clearly required.

The purpose of the present research was to examine the effect of fear on the efficiency of three distinct forms of attentional processing – alerting, orienting and executive attention. Participants were exposed to fear-eliciting and neutral images while they performed a modified version of the Attention Network Test. Performance of participants during the fear condition (where ANT trials were interspersed with fear-related images) was compared with their performance in a control condition (where trials were interspersed with neutral images).

There were two main hypotheses: (i) fear will facilitate executive attention. Specifically, when experiencing fear, individuals will be faster to identify a target, and inhibit irrelevant adjacent stimuli. This is based on previous theory and some evidence that negative emotions narrow attention (Derryberry and Reed, 1998, Derryberry and Tucker, 1994, Easterbrook, 1959, Gasper and Clore, 2002), potentially reflecting enhanced selective attention. (ii) Fear will enhance alerting attention. This is based predominately on theoretical perspectives suggesting that fear facilitates the mobilization of attention resources, thus facilitating subsequent responding to an impending, potentially threatening stimulus. We did not have a specific hypothesis relating to fear and orienting.

As a secondary objective, the effect of trait fear group (high fear or low fear) on the efficiency of each attention network was explored.

Section snippets

Participants

In total, 100 female student participants completed this experiment in return for course credit or a small financial reward (£4.20). An all-female sample was used as previous studies have shown that females sometimes display greater vigilance for threat-related information than males (e.g., Dickie and Armony, 2008, Williams et al., 2005), thus maximizing the likelihood that the fear manipulation would be effective. The mean age of participants was 20.13 years (SD = 3.14). 62% were from the UK,

Data-analysis

Median reaction times (RTs) for each cue type (no, double, center, spatial) and flanker type (congruent, incongruent) were calculated for each participant – both at an overall level (i.e., irrespective of emotion condition) and for each condition (within the fear and neutral conditions). Alerting, orienting, and executive attention scores were calculated as follows (see Fan et al., 2002 for details):

  • Executive attention (cost) = RT incongruent trials  RT congruent trials (baseline). Lower executive

Discussion

This experiment is the first to examine the effect of a lab-induced fear experience on three attention networks – executive attention, alerting and orienting. Fear and state anxiety were found to enhance executive attention. There was no effect of fear on alerting or orienting; however, a trend towards a correlation between trait anxiety and overall alerting was revealed. Results of the fear group analysis (high fear versus low fear) did not yield any significant findings.

In support of our

Conclusion

The present study shows that fear enhances executive attention irrespective of target valence. When experiencing fear, individuals are better able to inhibit irrelevant information resulting in faster reaction times to a neutrally valenced target. We suggest that in healthy individuals, enhanced executive attention in a fear-eliciting situation may function to focus attention on a potentially threat-related target and facilitate subsequent rapid responding.

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