Enhanced visuomotor processing of phobic images in blood-injury-injection fear

https://doi.org/10.1016/j.janxdis.2014.02.001Get rights and content

Highlights

  • Phobic images accelerate information processing in blood-injury-injection (BII) participants.

  • Enhanced processing already occurs in the fastest visuomotor responses.

  • Results contradict recent studies observing no information processing bias of phobic stimuli in BII phobia.

  • Results show that information processing of phobic stimuli in this type of phobia is comparable to other specific phobias (e.g., animal phobia).

Abstract

Numerous studies have identified attentional biases and processing enhancements for fear-relevant stimuli in individuals with specific phobias. However, this has not been conclusively shown in blood-injury-injection (BII) phobia, which has rarely been investigated even though it has features distinct from all other specific phobias. The present study aims to fill that gap and compares the time-course of visuomotor processing of phobic stimuli (i.e., pictures of small injuries) in BII-fearful (n = 19) and non-anxious control participants (n = 23) by using a response priming paradigm. In BII-fearful participants, phobic stimuli produced larger priming effects and lower response times compared to neutral stimuli, whereas non-anxious control participants showed no such differences. Because these effects are fully present in the fastest responses, they indicate an enhancement in early visuomotor processing of injury pictures in BII-fearful participants. These results are comparable to the enhanced processing of phobic stimuli in other specific phobias (i.e., spider phobia).

Introduction

In recent years, numerous studies demonstrated that information processing of phobic stimuli is enhanced in individuals with animal phobias. For instance, motor responses are faster and visual search times are lower for phobic stimuli as compared to neutral ones (e.g., Lipp and Waters, 2007, Öhman et al., 2001). Additionally, an involuntary orientation of attention toward phobic stimuli is frequently reported (Mogg and Bradley, 2006, Rinck and Becker, 2006, for reviews see Mogg and Bradley, 1998, Williams et al., 1997). For instance, the studies by Mogg and Bradley (2006) and by Rinck and Becker (2006) suggest that phobic stimuli capture attention. While there is wide agreement about the existence of an attentional bias toward phobic stimuli, it is less clear what the exact attentional mechanisms are. Several studies suggest that an initial, involuntary orientation toward phobic images is followed by intentional avoidance (Derakshan et al., 2007, Mogg and Bradley, 2006, Rinck and Becker, 2006), but many of the currently employed paradigms are not precise enough to distinguish between automatic capture of attention and rapid modulation by top-down processes. For example, Bardeen and Orcutt (2011) as well as Peers and Lawrence (2009) demonstrated that top-down mechanisms, such as attentional control, can influence the bottom-up orientation to threat stimuli within the first 100–200 ms of processing. Beside the interpretation that attention is drawn toward phobic or threat-relevant stimuli, there is also some evidence that the bias might result from disengagement difficulties away from those stimuli in fearful individuals (cf. Amir et al., 2003, Fox et al., 2002, Gerdes et al., 2008). Despite these open questions, all these studies agree that phobic or threat-relevant stimuli benefit from some form of processing enhancement over the time-course of the first half second of processing. In this paper, we are interested specifically in the enhanced ability of phobic stimuli to drive fast motor responses, such as keypress responses performed under time pressure.

Many studies show enhanced processing of fear-relevant material in a great variety of phobias and anxiety disorders, but few studies directly compared participants with different types of anxiety disorders. Öhman et al. (2001) asked non-anxious control, spider phobic, and snake phobic participants in a visual search task to search for pictures of spiders or snakes in grid-pattern arrays of flower and mushroom pictures, or vice versa. They found that fear-relevant pictures of spiders and snakes were found more quickly than neutral pictures by all three groups, with even faster responses to phobic stimuli in the two phobic groups (also cf. Teachman et al., 2001, Wenzel and Holt, 1999).

However, Soares, Esteves, Lundquist, and Öhman (2009) reported that spider-fearful participants were specifically faster in detecting spiders compared to fear-relevant but non-phobic snakes and to neutral targets in a visual search task. In contrast, snake-fearful participants showed no differences in performance between snakes and fear-relevant but non-phobic spider pictures. We observed a similar asymmetry in a response priming study with spider-fearful, snake-fearful, and non-anxious control participants (Haberkamp, Schmidt, & Schmidt, 2013). Participants were presented with target images of spiders, snakes, flowers, or mushrooms, and had to decide as quickly as possible whether the target was an animal or non-animal by pressing one of two keys. Target images were preceded by prime images from the same four categories that could either prime the correct or incorrect response, thereby speeding or slowing responses to the target (response priming effect; Vorberg, Mattler, Heinecke, Schmidt, & Schwarzbach, 2003). In the group of spider-fearful participants, only spider pictures had a strong influence on motor responses, leading to fast response times and large priming effects. In contrast, in snake-fearful participants, enhanced processing of phobic material was less pronounced and extended not only to snake but also to spider images.

Such results suggest that information processing might differ in different types of specific phobias. Within the class of specific phobias, there is one type that especially differs from other specific phobias; that is blood-injury-injection (BII) phobia. In BII phobia, individuals experience an extreme and irrational fear of blood, injuries, or of receiving an injection or an invasive medical procedure (Öst, 1992). The prevalence rate is approximately 3.5% (Bienvenu & Eaton, 1998), and women are affected twice as often as men (Hamm, 2006). This phobia lends itself to investigation due to three reasons: (1) BII phobia has distinct features that distinguish it from all other specific phobias (e.g., experience of nausea and fainting in phobic situations; experiencing not only fear but also disgust,1 e.g., Koch et al., 2002, Schienle et al., 2005); (2) few studies have investigated the speed of information processing in individuals with BII phobia compared to the large number of studies focusing on animal and social phobia; (3) those studies that did produced mixed results. Thus, it remains unclear whether BII-fearful individuals exhibit enhanced information processing and a bias similar to that in other phobias.

Let us look at the peculiarities of BII phobia in some more detail. First of all, up to 70% of BII phobics report a history of fainting due to a marked drop in blood pressure, heart rate, or both when confronted with their phobic stimuli (i.e., blood or injections) (Öst, 1992). In contrast, in other specific phobias (e.g., animal phobia), exposure typically triggers sympathetic reactions, for instance, panic-related symptoms like sweating, trembling, and an increased heart rate and blood-pressure (Antony, Brown, & Barlow, 1997). Furthermore, individuals with BII phobia frequently avoid medical procedures, which might lead to serious health implications (Öst, 1992). Therefore, Armstrong, Hemminger, and Olatunji (2013) argue that research should contribute to develop more effective treatments for BII-fearful individuals. According to these authors, one promising area is that of studying vigilance in BII-fearful individuals since the early attentional bias may contribute to the increased distress when they are confronted with a phobic stimulus (Weierich, Treat, & Hollingworth, 2008).

Even though an attentional bias favoring phobic stimuli is a core feature of other specific phobias, the evidence for such a bias in BII fear is equivocal. For example, Sawchuk et al. (1999) used a modified Stroop task to compare semantic information processing in BII phobic and non-phobic control participants. Ten medical (e.g., “injection”), 10 disgust (e.g., “vomit”), 10 negative (e.g., “lonely”), and 10 neutral words (e.g., “spoon”) were randomly presented in black, blue, green, or red. The authors measured color-naming latencies in BII phobics and control participants for medical and disgust words and found no difference between the two groups. In particular, BII phobics were not slowed in naming the color of phobic words, indicating that their attention was not distracted by the phobic word. In line with these findings, Wenzel and Holt (1999) showed in a dot-probe task that individuals with BII phobia did not exhibit an attentional bias toward their phobic stimuli (i.e., the phobic group responded similarly fast to the probe regardless of whether it was presented at the location of a phobic or a neutral word). However, both studies are limited by the fact that they used lexical stimuli which might not be strong enough to elicit an attentional bias in BII-fearful participants (Armstrong et al., 2013). Additionally, the modified Stroop task has recently received some criticism, with some authors suggesting that the task is not suitable to measure information processing biases for emotional words (Algom et al., 2004, McKenna and Sharma, 2004, Weierich et al., 2008; for a critical review of the modified Stroop task in PTSD cf. Kimble, Frueh, & Marks, 2009; also see Bardeen & Orcutt, 2011).

The limitations of the modified Stroop task were overcome in a series of experiments that were conducted more recently by Buodo and colleagues. In their eye-tracking study, BII-fearful and control participants were shown phobic, positive emotional, and neutral pictures (Buodo, Sarlo, Codispoti, & Palomba, 2006). The authors measured free viewing times and event-related potentials (ERPs). The eye-tracking results revealed no clear pattern of visual avoidance in BII-fearful participants: Even though these participants spent less time looking at blood pictures when compared to control participants (between-groups comparison), they did not spend less time looking at blood pictures compared to the other picture categories (within-group comparison). Thus, phobic pictures were not specifically shunned by BII-fearful individuals. Additionally, the ERPs amplitudes of BII-fearful participants revealed neither an increase indicating an attentional bias toward the phobic stimuli nor a decrease indicating avoidance of the phobic stimuli. The authors concluded that BII-fearful individuals show no vigilance-avoidance pattern.

In a follow-up study, the authors measured magnetoencephalography (MEG) activity in BII-fearful and non-anxious control participants in response to phobic and non-phobic pictures (Buodo, Peyk, Junghöfer, Palomba, & Rockstroh, 2007). They found a higher activation in BII-fearful participants for the two picture categories of phobic and neutral stimuli, but not specifically for phobic pictures. Again, they interpreted these findings as evidence that phobic stimuli are not preferentially processed by BII-fearful individuals.

However, there is also evidence that BII phobia is associated with a vigilance-avoidance pattern. Tolin, Lohr, Lee, and Sawchuck (1999) used a viewing paradigm and showed that BII phobics avoided viewing injection images compared to non-anxious controls and spider phobics. Mogg, Bradley, Miles, and Dixon (2004) found the same effect for BII-fearful participants in a visual dot-probe task. In addition, the authors showed that an intentional avoidance was preceded by an initial vigilance for phobic stimuli. Finally, two studies by the group of Buodo and colleagues contradicted the group's earlier results. Buodo, Sarlo, and Munafò (2010) investigated the N2pc component of ERPs – which is assumed to reflect processes of spatial attention – in BII-fearful and non-anxious control participants and found an attentional bias followed by visual avoidance. Subsequent, Sarlo, Buodo, Devigili, Munafò, and Palomba (2011) induced cognitive-emotional sensitization in BII-fearful participants by repeatedly presenting the same pictures of blood and mutilation, randomly interspersed with neutral images. They observed an early attentional bias, indicated by larger early N100 potentials, in the group of BII phobics compared to controls, followed by attentional avoidance reflected in smaller late positive potentials.

There is even one study that reports an attentional bias but not in line with the vigilance-avoidance theory. In an eye-tracking study by Armstrong et al. (2013), BII-fearful participants showed a robust vigilance-avoidance pattern. But even though BII-fearful participants oriented their attention more often to injection images and avoided them subsequently compared with non-anxious control participants, they did not attend to those images more frequently compared to other emotional images. These results imply that BII-fearful individuals respond more vigorously to emotional images per se, but not specifically to phobic images.

In sum, the existence of a processing bias for phobic stimuli in BII phobics is equivocal. Here, we provide further evidence for enhanced processing for phobic images in BII phobia. We measured behavioral data by using a response priming paradigm (Klotz and Wolff, 1995, Vorberg et al., 2003, also cf. Schmidt, Haberkamp, & Schmidt, 2011). This paradigm focuses on rapid and automatic information processing and was successfully applied in a previous study with spider- and snake-fearful participants (Haberkamp et al., 2013, Schmidt et al., 2011a). In a typical response priming task, participants are asked to classify a target stimulus as quickly and accurately as possible by pressing either the left or the right button. For instance, participants are required to press one button if the target shows an injured body part, and the other button if it shows an uninjured body part. The target stimulus is preceded by a prime stimulus that is either assigned to the same response, speeding the response to the target (consistent prime), or it is assigned to the opposite response, slowing the response to the target and provoking response errors (inconsistent prime). The difference in response time or error rate between trials with consistent and inconsistent primes is called the response priming effect and increases with increasing stimulus-onset asynchrony (SOA) between prime and target (Vorberg et al., 2003). We have argued (Schmidt et al., 2011a, Schmidt et al., 2006, Vath and Schmidt, 2007) that response priming is based on visuomotor feedforward sweeps triggered by the primes and targets, i.e., neuronal activation progressing quickly enough from visual to motor areas to remain essentially devoid of intracortical feedback (Lamme & Roelfsema, 2000). We propose that feedforward sweeps elicited by primes and targets traverse the visuomotor system in strict sequence, leading to a motor conflict when the two stimuli are mapped to different responses (rapid-chase theory of response priming).

Response priming can measure rapid information processing of visual primitives (e.g., grouping principles, Schmidt & Schmidt, 2013) and can compare motor activation with aspects of conscious perception (Ansorge et al., 2011, Mattler, 2007, Schmidt and Vorberg, 2006, Vorberg et al., 2003). It was also successfully applied to investigate the processing of natural images which have been shown to be classified very rapidly (Kirchner and Thorpe, 2006, VanRullen and Thorpe, 2001). For instance, Schmidt and Schmidt (2009) asked participants to classify natural target images into animals and objects by means of speeded pointing responses. They demonstrated not only that primes are able to influence the pointing trajectory, but that the initial movement is controlled exclusively by the prime, which determines the finger's initial flight-path independent of the actual target. In contrast, later phases of the movement are controlled by the target (cf. Schmidt et al., 2006). This pattern of strictly sequential response control by primes and targets lends strong support to the idea that response priming is based on sequential visuomotor feedforward sweeps, even when natural images are involved. Response priming should thus be suitable for measuring basic processing characteristics for BII-relevant stimuli like pictures of harmed and unharmed body parts. It has the additional advantage that strategic response biases (which are common in fearful individuals) are not likely to influence the results. In addition, we can analyze the fastest responses of the participants to confirm a strong prediction of rapid-chase theory: Priming effects should be fully present in the fastest responses and not increase any further in slower responses (Haberkamp et al., 2013, Schmidt and Schmidt, 2014).

We chose to employ images of small injuries plus control images of unharmed body parts. These pictures of small injuries represent phobic stimuli for BII-fearful participants, but merely fear-relevant stimuli for the non-anxious control participants. The control pictures represent neutral stimuli for both groups. We assumed that highly arousing pictures of severe mutilations would also evoke strong reactions in the control participants, so that possible differences between them and the BII-fearful group would be difficult to detect. In contrast, minor injuries, which are frequently encountered in everyday life, should elicit strong emotional reactions only in the BII-fearful participants but not in control participants. In the present experiment, one prime and one target were presented in rapid sequence, and participants classified the targets as quickly as possible by pressing one button for injury pictures and another button for non-injury (neutral) pictures. We hypothesized that the BII-fearful participants would show enhanced processing of the injury pictures. This will be expressed in larger priming effects by injury as compared to neutral primes (within-group comparison) or as compared to non-anxious control participants (between-groups comparison). In addition, there should be faster responses to injury targets as compared to neutral targets (within-group and between-groups comparisons).

Section snippets

Methods

Participants. Fifty-one participants took part in the experiment, recruited through the University of Kaiserslautern. All of them were naïve to the purpose of the study. We specifically asked for participants who rated themselves as being highly afraid of blood, injuries, and injections, or neither of these. All participants were screened for fear of blood, injury and injections before the experiment started. For this purpose, we applied two blood-injury-injection-questionnaires (German version

Results

We first analyze the influence of the primes on response times in the two groups and link the effect to the influence of the targets on overall response times. Second, we test whether the influences of primes and targets are fully present in the fastest responses (i.e., in the 2nd and 3rd deciles of the response time distribution).

Influence of the primes on response times. Response times for the two groups (controls and BII fear) and prime types (injured vs. unharmed body parts) are displayed

Discussion

Overall, we found robust response priming effects for each of the two prime categories in the two groups of non-anxious control and BII-fearful individuals. In all experimental conditions (except one, but see below), inconsistent trials led to slower response times and more errors compared to consistent ones. These findings are in line with previous results from the image classification literature (e.g., Bacon-Macé et al., 2007, Kirchner and Thorpe, 2006; for a review see Fabre-Thorpe, 2011) as

Author note

This work was supported by the German Research Foundation (DFG), grant Schm1671/1 to T.S. We especially thank Nicole Reinert, Marie Salzmann, and Dessislava Todorova for data collection. For a profound revision of an earlier manuscript version, thanks to Shanley Allen, Filipp Schmidt, and Andreas Weber. Furthermore, we thank our student assistants Peter Kohl and Miriam Neumann.

References (73)

  • M.D. Koch et al.

    Domain-specific and generalized disgust sensitivity in blood-injection-injury phobia: the application of behavioral approach/avoidance tasks

    Journal of Anxiety Disorders

    (2002)
  • V.A.F. Lamme et al.

    The distinct modes of vision offered by feedforward and recurrent processing

    Trends in Neurosciences

    (2000)
  • S. Lissek et al.

    The strong situation: a potential impediment to studying the psychobiology and pharmacology of anxiety disorders

    Biological Psychology

    (2006)
  • K. Mogg et al.

    A cognitive-motivational analysis of anxiety

    Behaviour Research and Therapy

    (1998)
  • K. Mogg et al.

    Time course of attentional bias for fear-relevant pictures in spider-fearful individuals

    Behaviour Research and Therapy

    (2006)
  • T.C. Monson et al.

    Actors, observers, and the attribution process: toward a reconceptualization

    Journal of Experimental Social Psychology

    (1977)
  • M. Sarlo et al.

    Emotional sensitization highlights the attentional bias in blood–injection–injury phobics: an ERP study

    Neuroscience Letters

    (2011)
  • C.N. Sawchuk et al.

    Exposure to disgust-evoking imagery and information processing biases in blood–injection–injury phobia

    Behaviour Research and Therapy

    (1999)
  • F. Schmidt et al.

    Grouping principles in direct competition

    Vision Research

    (2013)
  • S.C. Soares et al.

    Some animal specific fears are more specific than others: evidence from attention and emotion measures

    Behaviour Research and Therapy

    (2009)
  • D.F. Tolin et al.

    Visual avoidance in specific phobia

    Behaviour Research and Therapy

    (1999)
  • A. Treisman

    The binding problem

    Current Opinion in Neurobiology

    (1996)
  • N. Vath et al.

    Tracing sequential waves of rapid visuomotor activation in lateralized readiness potentials

    Neuroscience

    (2007)
  • U. Ansorge et al.

    No conflict control in the absence of awareness

    Psychological Research

    (2011)
  • American Psychiatric Association [APA]

    Diagnostic and statistical manual of mental disorders, 4th edn. Text Revision (DSM-IV-TR)

    (2000)
  • D. Algom et al.

    A rational look at the emotional stroop phenomenon: a generic slowdown, not a stroop effect

    Journal of Experimental Psychology: General

    (2004)
  • N. Bacon-Macé et al.

    Effects of task requirements on rapid natural scene processing: from common sensory encoding to distinct decisional mechanisms

    Journal of Experimental Psychology: Human Perception and Performance

    (2007)
  • O.J. Bienvenu et al.

    The epidemiology of blood-injection-injury phobia

    Psychological Medicine

    (1998)
  • G. Buodo et al.

    Event-related potentials and visual avoidance in blood phobics: is there any attentional bias?

    Depression and Anxiety

    (2006)
  • G. Buodo et al.

    The neural correlates of attentional bias in blood phobia as revealed by the N2pc

    SCAN

    (2010)
  • W.G. Cochran

    The analysis of variance when experimental errors follow the Poisson or binomial laws

    The Annals of Mathematical Statistics

    (1940)
  • D. Cousineau

    Confidence intervals in within-subject designs: a simpler solution to Loftus and Masson's method

    Tutorials in Quantitative Methods for Psychology

    (2005)
  • N. Derakshan et al.

    Emotional information processing in repressors: the vigilance–avoidance theory

    Cognition and Emotion

    (2007)
  • M. Fabre-Thorpe

    The characteristics and limits of rapid visual categorization

    Frontiers in Psychology

    (2011)
  • E. Fox et al.

    Attentional bias for threat: Evidence for delayed disengagement from emotional faces

    Cognition & Emotion

    (2002)
  • C. Gebhardt et al.

    Die deutsche Version des Multidimensional Blood/Injury Phobia Inventory

    Zeitschrift für Klinische Psychologie und Psychotherapie

    (2010)
  • Cited by (11)

    • Interpreting and responding to ambiguous natural images in spider phobia

      2019, Journal of Behavior Therapy and Experimental Psychiatry
      Citation Excerpt :

      This should increase generalizability of our findings beyond single stimuli. In Study 1, we use a response priming task which measures rapid visuomotor information processing (e.g., Klotz & Neumann, 1999; Klotz & Wolff, 1995), and was previously applied to study visuomotor processing in fearful individuals (Haberkamp & Schmidt, 2014; Haberkamp, Schmidt, & Schmidt, 2013). In Study 2, we use a go/no-go task (e.g., Delorme, Richard, & Fabre-Thorpe, 2010; Fabre-Thorpe, 2011; Thorpe, Fize, & Marlot, 1996) to gather further information on the visuomotor processing of briefly presented morphed images.

    • Contamination-fear in subclinical obsessive-compulsive disorder: A further proof for no preferential processing of disorder-related stimuli

      2019, Journal of Obsessive-Compulsive and Related Disorders
      Citation Excerpt :

      Neutral images of household aids were assumed to be neutral for both groups. Based on studies demonstrating an attentional bias or preferential processing of OCD-related stimuli (Amir et al., 2009; Cisler & Olatunji, 2010; Lavy et al., 1994; Moritz, Mühlenen, von, Randjbar, Fricke, & Jelinek, 2009; Najmi & Amir, 2010; Tata et al., 1996) and findings of preferential processing of fear-related stimuli in anxiety disorders (Fox et al., 2000; Haberkamp & Schmidt, 2014; Haberkamp et al., 2013; Lipp & Waters, 2007; Öhman et al., 2001), we formulated the following hypotheses: (1) CFr images will be rated as being more unpleasant, arousing, and disgusting by participants with HCF – in contrast to the neutral images of household aids and compared to the LCF group (emotional rating task). ( 2) Response priming effects will occur in both groups for CFr stimuli and neutral images (priming task).

    • We prefer what we fear: A response preference bias mimics attentional capture in spider fear

      2018, Journal of Anxiety Disorders
      Citation Excerpt :

      Thus, testing subclinical spider-fearful individuals might rather underestimate than overestimate the observed response bias. Also, we observed strong effects of feared stimuli in previous studies with subclinical samples in spider as well as blood-injury-injection phobia (cf. Haberkamp & Schmidt, 2014; Haberkamp et al., 2013; Haberkamp & Schmidt, 2015), showing that subclinical samples are sufficient to demonstrate similar effects. In sum, our findings clearly suggest that spider-fearful participants prefer the response option associated with spiders, irrespective of whether this response indicates “spider appeared first” or “spider appeared second”.

    • The DIsgust-RelaTed-Images (DIRTI) database: Validation of a novel standardized set of disgust pictures

      2017, Behaviour Research and Therapy
      Citation Excerpt :

      In clinical research, disgust plays a major role in psychiatric disorders such as contamination-related obsessive-compulsive disorder (OCD) and several specific phobias (e.g. spider phobia or blood-injury-injection phobia; Cisler, Olatunji, Lohr, & Williams, 2009). In recent years, many clinical studies have investigated different aspects of disgust, using various methods to induce this emotion: for example, showing disgust-related videos (e.g. Sawchuk, Lohr, Lee, & Tolin, 1999) or pictures (e.g. Haberkamp & Schmidt, 2014), administering a bitter taste (Eskine, Kacinik, & Prinz, 2011), or using autobiographical recall (Fitzgerald et al., 2004). It has been previously shown that visual material is effective in eliciting specific emotions (Lench, Flores, & Bench, 2011).

    • Interpretative bias in spider phobia: Perception and information processing of ambiguous schematic stimuli

      2015, Acta Psychologica
      Citation Excerpt :

      This effect is even more pronounced in individuals with specific phobias (e.g. Berdica, Gerdes, Pittig, & Alpers, 2014; Gerdes & Alpers, 2014; Haberkamp & Schmidt, 2014; Haberkamp et al., 2013; Lipp & Waters, 2007; Öhman et al., 2001; for a review see Yiend, 2010) and with other anxiety disorders (e.g., social anxiety, Eastwood et al., 2005; Gilboa-Schechtman, Foa, & Amir, 1999). In two recent studies, we investigated rapid information processing by using natural images of neutral, fear-relevant, and phobic stimuli (Haberkamp & Schmidt, 2014; Haberkamp et al., 2013). We found that spider-fearful participants responded faster to phobic target pictures of spiders compared to fear-relevant snakes or neutral flowers and mushrooms.

    View all citing articles on Scopus
    View full text