By combining binocular suppression technique and a probe detection paradigm, we investigated attentional bias to invisible stimuli and its gender difference in both high trait anxiety (HTA) and low trait anxiety (LTA) individuals. As an attentional cue, happy or fearful face pictures were presented to HTAs and LTAs for 800 ms either consciously or unconsciously (through binocular suppression). Participants were asked to judge the orientation of a gabor patch following the face pictures. Their performance was used to measure attentional effect induced by the cue. We found gender differences of attentional effect only in the unconscious condition with HTAs. Female HTAs exhibited difficulty in disengaging attention from the location where fearful faces were presented, while male HTAs showed attentional avoidance of it. Our results suggested that the failure to find attentional avoidance of threatening stimuli in many previous studies might be attributed to consciously presented stimuli and data analysis regardless of participants' gender. These findings also contributed to our understanding of gender difference in anxiety disorder.

Introduction

Generalized anxiety disorder (GAD) is an anxiety disorder that is characterized by excessive, uncontrollable and often irrational worry about everyday things, which is disproportionate to the actual source of worry [1]. To study its psychopathology, researchers usually adopted patients with generalized anxiety disorder as clinical sample and individuals with high trait anxiety as subclinical sample [2]. Recently, studying subclinical or non clinical population was recommended for the convenient participant recruitment and the exclusion of factors of medicine and therapy.

Cognitive theories about generalized anxiety disorders propose that patients or HTA individuals have cognitive vulnerabilities at the level of attentive processing of threat that may maintain anxiety, and may even lead to the development of clinical anxiety disorders [3], [4]. Several studies [5], [6] have suggested that the attentional system of anxious individuals may be abnormally sensitive to threat-related stimuli in the environment, leading to an even more pronounced processing bias in favor of threat-related stimulation than is observed in non-anxious individuals. The role of the attentional bias played in the development and maintenance of anxious disorders has been studied for about two decades [7]. Mogg and Bradley [8] proposed the “vigilance-avoidance” pattern to interpret the cognitive processing in anxious populations. HTA individuals initially attend to threat, but this is often followed by attentional avoidance of threat. This pattern of vigilance and avoidance is hypothesized to maintain anxiety [9].

Researchers usually used a dot-probe detection paradigm [10] to investigate the attentional bias in high trait anxiety population. In this paradigm, participants were exposed to a word pair or a picture pair on a computer screen, which included one threatening and one neutral word/picture. After the exposure, a dot (the probe) appeared in the location of one of the words/pictures. Participants were instructed to press a button as fast as possible to indicate the detection of the probe. For a short presentation of the stimulus pair (i.e. 500 ms), anxious participants were faster or more accurate to detect the probe when it was in the location of the threatening stimulus [5], [11], [12]. They exhibited attentional vigilance towards threatening stimuli. However, for a long presentation of the stimulus pair (i.e. 1250 ms or 1500 ms), no attentional effect was found in both HTA and LTA groups [5], [12]. This is not consistent with the “vigilance-avoidance” pattern proposed by Mogg and Bradley [8] because they predicted attentional avoidance of threatening stimuli with a long presentation. There are two potential reasons to explain the absence of attentional avoidance in previous studies: consciousness manipulation and gender difference in anxiety disorders. Our study aimed to address these two issues.

Many studies have demonstrated that attentional bias could be induced by an unconsciously presented cue [13]. For example, emotional Stroop task with backward masking was widely used in this field and researchers consistently found that HTAs exhibit attentional bias to threatening materials at subconscious level [14]–[16]. However, one drawback of backward masking is that this technique cannot render a stimulus invisible for a long presentation, thus is not suitable for test the “vigilance-avoidance” proposal.

This drawback can be overcome by another psychophysical method – binocular rivalry. When two incompatible pictures are presented to the two eyes that cannot be merged to a single visual percept, binocular rivalry occurs. Observer's perception switches back and forth between the two incompatible pictures, that is, they compete for perceptual dominance [17]. Some factors could boost the strength of one rival picture over another, such as high-contrast, brighter stimulus, moving contours, densely contoured, and stimuli presented in dominant eye [18]. Accordingly, the ‘stronger’ competitor enjoys an advantage in overall perceptual dominance. Jiang et al. [19] took advantage of binocular rivalry to study the effect of invisible images on the distribution of spatial attention. In their study, high contrast dynamic noise was presented to the dominant eye, and a meaningful picture was presented to the non-dominant eye. Because of the strong inter-ocular suppression by the dynamic noise, subjects were completely unaware of the meaningful picture. They found that a 800 ms presentation of invisible pictures could result in attentional bias and the bias was dependent on subjects' gender. This experimental paradigm is also call binocular suppression because of the imbalance of the strength of the two competing stimuli. In our study, we will use binocular suppression to render images invisible for a long presentation and investigate attentional bias at unconscious level.

We suspect that the failure to find attentional avoidance of threatening stimuli in many previous studies might be, at least partially, attributed to data analysis regardless of participants' gender. Many researches have indicated that there are gender differences in attention to and appraising of threat, which means females are more sensitive to threat-related cues than males and tend to overestimate the level of danger [20], [21]. McClure et al. [22] also found that orbitofrontal cortex and amygdala were selectively activated to unambiguous threatening stimuli in adult women but not men. What's more, some researches interested in gender differences in anxiety disorders [23]–[25] have shown that female suffer anxiety disorder much more frequently than male [11], [26], [27]. Waters and Valvoi [28] also proposed that there might be different ways for anxious and non-anxious girls to regulate their attention towards threatening faces. Thus, we proposed that there might be gender differences in the attentional bias to threatening cues and taking this variable into account may help us reconsider the “vigilance-avoidance” proposal. However, there was almost no study investigating the gender difference of anxious population with a cognitive approach. Only some researches in neurotic and high-defensive population had made such attempts. For example, the studies by Osorio et al. [29] and Jansson et al. [30] revealed that the relationship between neuroticism or defensiveness and attentional bias is affected by gender. It is likely that some gender effect on attentional bias may occur in high trait anxiety individuals.

In addition, many previous studies on attentional bias used an unbalanced gender ratio. For example, Koster et al. [7] recruited high trait anxiety participants with a gender ratio of female to male as 16 ∶ 6. Another ERP study about anxious individuals' perception of emotional faces used 8 female and 2 male [31]. The majority of female in researches might have led to a biased conclusion for the overall anxious population. The other aim of our study is to clarify the gender difference issue in attentional bias in high trait anxiety individuals, which has been ignored previously.

In summary, the main object of our study is to examine attentional bias and its gender difference at unconscious level for both HTA and LTA individuals. We predict that, at unconscious level, only HTA females might exhibit an attentional bias towards fearful faces.