Decomposing unpleasantness: Differential exogenous attention to disgusting and fearful stimuli

Abstract

Negative stimuli have consistently been shown to efficiently attract exogenous attention. Two different types of unpleasant stimuli, disgusting and fearful, sharing similar arousal and valence, are usually employed as a single category. However, since they diverge in several important aspects (biological functionality, associated feelings, and central and peripheral physiological correlates), it may be expected that their potential to capture attention differs. Event-related potentials and behavioral indices were recorded while participants were engaged in a digit categorization task in response to three types of irrelevant, distracting pictures: disgusting, fearful and neutral. Disgusting trials were associated with worse performance than fearful trials in the digit categorization task as revealed by reaction times and number of errors. Moreover, P2-associated cuneus activation and scalp anterior P2 amplitude were greater for disgusting than for fearful distracters. All these indices reveal that, under the experimental conditions employed in the present study, disgusting distracters are more efficient at attracting exogenous attention than are fearful distracters.

Introduction

Negatively arousing visual stimuli have been shown to efficiently attract exogenous attention (also termed automatic or bottom-up attention), as revealed by electrophysiological and behavioral responses to emotional distracters while subjects are engaged in a cognitive task (Carretié et al., 2008, Carretié et al., 2004, Carretié et al., 2009b, Constantine et al., 2001, Doallo et al., 2006, Huang and Luo, 2007, Thomas et al., 2007, Vuilleumier et al., 2001, Yuan et al., 2007). This ability to automatically capture attention has obvious adaptive and evolutionary advantages: the consequences of not detecting a negative event are often much more dramatic than the consequences of ignoring or reacting slowly to neutral or even appetitive stimuli. An important issue is that, in these studies on exogenous attention, negatively arousing stimuli are treated as a single category. In part, this is due to the fact that some of the most prototypical negative stimuli (e.g. spiders or bloody scenes) elicit a mixture of negative emotions (Olatunji and Sawchuk, 2005). Nevertheless, this type of event could be divided into different subcategories.

Fear and disgust are two emotions that share the same emotional valence (negative) and high ability to arouse (higher than that elicited by other negative emotions such as sadness: Russell, 1980). In functional terms, both types of emotion also share the same scope: avoiding the event that is causing, or may cause, displeasure. However, they differ in several respects. First, the subjective feeling associated with each of these two emotional states is clearly different. Second, their biological meaning is also divergent: while disgust is primarily related to contamination (Rozin, 2000), fear facilitates avoidance of a broader type of danger that may cause harm at many levels. Third, they appear to preferentially activate different brain areas. Whereas fear-related stimuli have been reported to mainly activate amygdala, disgusting events preferentially activate the anterior insula when processes other than exogenous attention are explored (see a review in Calder et al., 2001; but see, e.g. Schienle et al., 2006, Stark et al., 2007). Fourth, it has been proposed that, at the peripheral level, disgust is mainly parasympathetically mediated, while fear is a sympathetically mediated process (Levenson et al., 1990).

Therefore, a relevant question that arises once these differences are taken into account is whether disgusting stimuli and fearful stimuli have the same uniform ability to capture attention as previously assumed. Since the main reason why negative stimuli efficiently capture automatic attention is biological, one could contend that threatening and repugnant events, which have diverse biological meaning, should differ in their ability to attract attention. To the best of our knowledge, only two studies, both of a behavioral nature (no physiological responses were recorded), have compared the differences between automatic attention to fearful and to disgusting stimuli. In one of them, the emotional Stroop task was presented to subjects using neutral, threat-related and disgust-related words (Charash and McKay, 2002). While disgust-related words interfered with the cognitive ongoing task to a greater extent than did neutral words, no differences were found between fear-related and neutral words. In the second study (Cisler et al., 2009b), “fear words”, “disgust words” and neutral words were presented to subjects during a cognitive task in which their emotional content was irrelevant. In this case, fear words were found to interfere with the cognitive task more than disgust words. Therefore, although fear- and disgust-related attention differences have been found, the question as to the direction of these differences remains unanswered. Since words tend to be less arousing than other types of visual emotional stimuli (Hinojosa et al., 2009, Keil, 2006, Kissler et al., 2006, Mogg and Bradley, 1998, Vanderploeg et al., 1987), it would be advantageous to obtain additional data using pictorial stimulation.

No studies on brain activity yet exist on the differential ability of fearful and disgusting stimuli to capture attention, although event-related potentials (ERPs) have been shown to be good indices of exogenous attention. More specifically, the P2 component of ERPs shows significant amplitude increments when a negative stimulus automatically attracts attention in a wide variety of tasks (Carretié et al., 2004, Doallo et al., 2006, Huang and Luo, 2007, Thomas et al., 2007, Yuan et al., 2007), in contrast to other components such as late positive potentials, which reflect top-down attention to emotional events (see the review by Olofsson et al., 2008; see also Hajcak et al., 2009). In previous experiments on attention to emotional pictures, P2 has been shown to originate in the visual cortex (Carretié et al., 2001, Carretié et al., 2004). This is an important issue, since Schienle et al. (2006), presenting disgusting and fearful pictures (but not exploring automatic attention: participants were asked explicitly to direct processing resources to pictures), found that maximal disgust > fear differences were produced in visual areas of the brain (fear > disgust was not explored). Stark et al. (2007) also explored brain responses to disgusting and fearful pictures that participants attended to in a top-down fashion. Again, disgust > fear contrasts yielded significant effects in visual areas, along with the insula. Fear > disgust analyses revealed extensive areas of visual cortices as the most sensitive, in statistical terms, to this contrast. Therefore, the role of P2 in automatic attention and its visual cortex origin make this component especially interesting for the scope of this study.

The present experiment was aimed at exploring whether a similar or differential pattern of exogenous attention exists in response to fear- and disgust-related distracters while subjects were engaged in a cognitive task. Both behavioral and neural indices of exogenous attention were recorded. Behavioral measures consisted of reaction times and number of errors in the cognitive task. Automatic capture of attention by distracters is reflected in poorer performance in the ongoing cognitive task. The neural index of attentional capture was P2, which, as explained, has been reported to reflect automatic attention to emotional stimuli. Analyses on this component involved source localization in order to spatially characterize possible experimental effects. Although fearful stimuli have been studied much more than disgusting stimuli in emotional attention research, thus becoming the prototypical negative category, the few existing data comparing both types of unpleasant events suggest that the latter are powerful attracters of exogenous attention. Moreover, some of the most frequently used fearful stimuli, such as threatening animals (e.g. spiders or snakes) or physical injury scenes, may be more associated with disgust than with fear (Olatunji and Sawchuk, 2005), so part of the attentional effect traditionally attributed to “negativity” may have been related to disgust processing. Therefore, we expected behavioral and neural indices of exogenous attention to be significantly modulated by disgustingness of distracters. In line with previous data described above, this disgust modulation of automatic attention could be even greater than fear modulation in several areas of the visual cortex.