Detecting and reacting to potential threats in the environment is an essential skill for survival. Emotional information that indicates threat in the environment, such as a fearful or angry face, confers perceptual and attentional advantages compared to neutral information (Carretié, 2014; Pourtois et al., 2013; Vuilleumier, 2005): Emotional information enhances visual sensitivity (Phelps et al., 2006; Fox et al., 2000), potentiates effects of attention on visual sensitivity (Ferneyhough et al., 2013; Bocanegra and Zeelenberg, 2009; Bocanegra and Zeelenberg, 2011a; Bocanegra and Zeelenberg, 2011b; Ohman et al., 2001; Lundqvist and Ohman, 2005) and on appearance (Barbot and Carrasco, 2018), and gains preferential access to awareness (Amting et al., 2010; Yang et al., 2007; Milders et al., 2006; Hedger et al., 2015). The advantages of emotional information extend to actions. Eye (Bannerman et al., 2009a; Bannerman et al., 2009b; Bannerman et al., 2010; Nummenmaa et al., 2009) - or pointing (Valk et al., 2015) movements towards emotional –especially threat-related stimuli– are facilitated, whereas saccades away from these are delayed (Belopolsky et al., 2011; Kissler and Keil, 2008). Further, emotional information influences gaze trajectories, that is directly guides eye movements. Usually, people’s eyes are attracted more towards emotional than neutral faces (Mogg et al., 2007; Kret et al., 2013a; Kret et al., 2013b), yet, sometimes gaze is repelled from threat-related –angry or fearful– faces (Hunnius et al., 2011; Becker and Detweiler-Bedell, 2009; Schmidt et al., 2012).

Remarkably, the recognition of a face’s emotional expression does not require awareness of the face. (Some authors refer to ‘awareness’ and ‘consciousness’ interchangeably; in line with a recent review on the dissociations of perception and eye movements for neutral stimuli (Spering and Carrasco, 2015), we use the term awareness and operationally define it as the ability to make an explicit perceptual report). Cortically blind individuals are able to correctly ‘guess’ the emotions of faces they cannot see (de Gelder et al., 2005; de Gelder et al., 1999; Pegna et al., 2005; Tamietto et al., 2009; Bertini et al., 2013; Striemer et al., 2017). In neurologically intact observers, emotional — especially threat-related — information they remain entirely unaware of, is prioritized over neutral information (Hedger et al., 2016), facilitates visual discrimination (Bertini et al., 2017), and alters subsequent perceptual (Almeida et al., 2013) and discrimination judgments differentially for the unseen emotion (Zhan and de Gelder, 2018). Emotional stimuli observers are unaware of also elicit physiological reactions, for example changes in skin conductance (Esteves et al., 1994), facial muscle activity and pupil dilation (Tamietto et al., 2009), and activate subcortical structures, for example the amygdala, pulvinar, basal ganglia and superior colliculus (Tamietto and de Gelder, 2010; Jiang and He, 2006; Troiani et al., 2014; Troiani and Schultz, 2013), as well as cortical structures (Pessoa and Adolphs, 2010). Furthermore, suppressed emotional stimuli influence oculomotor response times; when observers saccade towards color patches to report a mask’s color, saccades initiation is slower departing from masked angry faces than from masked happy faces (Terburg et al., 2012). Despite this evidence indicating perceptual and attentional advantages, it is unknown whether suppressed emotional information can also directly guide actions or whether we have to become aware of the threat before we can act upon it.

Eye movements are the ideal testing ground for the relation between suppressed emotional information and actions, as recent evidence has shown that eye movements and visual awareness for neutral stimuli can be dissociated (Spering and Carrasco, 2015). Whether and how oculomotor actions are guided by unaware emotional information can be investigated by suppressing stimuli from awareness while measuring eye movements. The dissociation of eye movements and visual awareness reflects situations in which the direction of eye movements change in response to particular visual features, such as orientation or motion direction, even though observers are unable to report these features because they are not aware of them (Spering and Carrasco, 2015; Spering and Carrasco, 2012; Spering et al., 2011; Rothkirch et al., 2012; Glasser and Tadin, 2014; Kuhn and Land, 2006; Simoncini et al., 2012; Tavassoli and Ringach, 2010). In other words, suppressed neutral stimuli determine the trajectory of eye movements in the absence of awareness. Moreover, visual attention can modulate the processing of neutral stimuli and the eye movements they elicit even when observers are unaware of them (Spering and Carrasco, 2012).

Angry and fearful faces convey different types of threat, and elicit different reactions under awareness. Fearful faces indicate a potential indirect threat in the environment of the fearful person without indicating the source of the threat, suggesting more information is needed to appraise the situation (Davis et al., 2011). This ambiguity leads to increased amygdala activation (Whalen et al., 2013), heightens visual attention to the seen fearful stimulus location (Phelps et al., 2006; Ferneyhough et al., 2013) and attracts eye movements that enable detailed processing of the face and its environment (Mogg et al., 2007). Angry faces indicate direct threats (a person with an angry expression looking directly at the observer) leading to avoidance (Schmidt et al., 2012; Marsh et al., 2005) or freezing (Roelofs et al., 2010) responses. When looking at angry faces observers show a stronger startle reflex (Springer et al., 2007), stronger activation of the torso muscles (Huis In 't Veld et al., 2014), widening of the pupils (Kret et al., 2013b), and higher activation in brain areas associated with defense preparation (Williams et al., 2005; Pichon et al., 2009; Kret et al., 2011) than when looking at fearful faces. Threat processing is considered to evolve along two distinctive neuronal pathways, a fast sub-cortical and a slower cortical route (LeDoux, 1998). There is some evidence that fear information, relative to anger information, may be preferentially processed along the fast, subcortical route (Luo et al., 2007). This rich body of research suggests differential processing of fear and anger under awareness. Yet, when observers are presented with unmasked angry and fearful faces, both attract (Mogg et al., 2007; Kret et al., 2013a) or repel (Hunnius et al., 2011; Becker and Detweiler-Bedell, 2009) their attention and eye gaze equally strongly. Of note, there is only circumstantial evidence for distinct effects of emotional faces in the absence of awareness: Fearful faces have preferential access to awareness (Yang et al., 2007; Milders et al., 2006; Troiani et al., 2014; Jusyte et al., 2015), whereas angry faces remain suppressed longer (Jusyte et al., 2015; Zhan et al., 2015), both compared to neutral faces presented during continuous-flash suppression (CFS).

Our study had two goals: (1) To test whether threat-related emotional stimuli can guide eye movements in the absence of visual awareness. Were suppressed emotional faces to guide eye movements, their trajectory would depend on the location of the emotional stimuli. (2) To test whether these oculomotor actions in the absence of awareness are distinct for different threat-related facial emotions. Were threat-related emotional information to guide eye-movements, the trajectories could be similar or differential, that is depend on the nature of the threat, direct — angry faces — or indirect — fearful faces.

We investigated these critical open questions by assessing whether different threat-related stimuli can direct oculomotor actions in the absence of awareness, as indicated by objective and subjective measures, and whether those actions are similar or differential by contrasting eye movements elicited by angry faces and fearful faces.

We rendered emotional faces unaware using continuous flash suppression (Tsuchiya and Koch, 2005; Fang and He, 2005). Low contrast face stimuli located in one of four quadrants of the visual display were presented to the non-dominant eye and a high contrast flickering mask was presented to the dominant eye (Figure 1). As such, the viewer is only aware of the flickering mask, but not of the stimulus presented to the non-dominant eye. In this way, continuous flash suppression suppresses stimuli for up to several seconds, enabling the measurement of eye movements in the absence of awareness (Rothkirch et al., 2012; Madipakkam et al., 2016).

Figure 1

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To investigate the extent to which the different emotional facial expressions are processed and whether they affect eye movements differentially, we used two negative-valence expressions, fearful faces, indicating an indirect threat in the environment, and angry faces, indicating a direct threat from the depicted person. We also used neutral faces to control for the effects of face stimuli on eye movements that are unrelated to threat. To rule out the possibility that eye movements could have been simply triggered by low-level visual features (e.g., contrast differences between the eye and mouth regions), we also presented the same stimulus set upside down, as done in previous studies (Phelps et al., 2006; Bocanegra and Zeelenberg, 2009; Barbot and Carrasco, 2018) (Figure 1).

We determined full suppression of visual awareness based on subjective visibility ratings, whose validity we verified for each observer using objective measures. This verification is essential as subjective measures alone could reflect criterion rather than discriminability differences (Hedger et al., 2016; Sterzer et al., 2014). After each trial, participants (a) judged the location and emotional expression of the face stimulus and (b) rated its visibility (Figure 2). We analyzed only those trials in which subjective visibility was zero, and only data from participants’ whose objective performance across trials with subjective zero visibility was at chance level for each of the two tasks, location and emotional expression, matching their subjective impression.

Figure 2

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Despite face stimuli being fully suppressed from awareness, participants moved their eyes towards fearful faces and away from angry faces, compared to neutral faces. Figure 3 shows gaze position relative to the face stimulus as a function of time. Most locations within the display were further away from the face than the fixation point. Thus, the distance between gaze position and face increased for all faces when participants moved their eyes after an initial mandatory fixation period. At ~400 ms after full display was reached, distance of gaze position to fearful faces decreased compared to neutral faces, indicating an orienting of gaze towards fearful faces. In contrast, distance of gaze position to angry faces increased compared to the distance to neutral faces, indicating gaze aversion from angry faces. This pattern of results was not observed with upside-down presented faces. The absence of an effect for upside-down presented faces rules out the possibility that low-level visual features were responsible for the effect observed with upright presented emotional faces, a confound not controlled for in previous studies (Bodenschatz et al., 2018) (Figure 3).

Figure 3 with 1 supplement see all

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To determine the preferentially viewed location for each emotion, we contrasted the spatial distribution of dwell times for upright faces with their upside-down counterparts; the latter provided a suitable baseline as they evoked no emotion-specific eye movements (Figure 3). This dwell time analysis (Figure 4) showed that, observers looked significantly longer towards the location at which an upright fearful face was displayed: dwell times at the target location increased by 57% compared to trials with upside-down presented fearful faces. In contrast, observers looked significantly longer towards an adjacent location when an upright compared to an upside-down angry face was displayed, demonstrating a consistent and lasting gaze aversion from an angry face. No effect emerged for neutral faces.

Figure 4

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We found that in the absence of visual awareness, observers’ eye movements were attracted towards fearful faces and repelled away from angry faces, compared to neutral faces. These novel results revealed that threat-related emotional faces can guide oculomotor actions without entering awareness. Our objective performance measures (Figure 2, red dots) validate the subjective visibility ratings, and together indicate that the emotional faces were suppressed from perceptual awareness. The absence of an effect with upside-down presented angry faces precludes confounds with low-level feature differences between faces of different emotional expressions.

Remarkably, the elicited eye movements were specific to the displayed facial emotion regarding the type of threat it conveyed. These distinct consequences on oculomotor actions demonstrate qualitative processing of the emotional expression, rather than mere detection of emotional stimuli in the absence of awareness. Previous studies on emotional face perception predominantly demonstrated preferential emergence of fearful faces into awareness (Hedger et al., 2016), which could simply indicate unspecific arousal caused by emotional content.

How can emotional stimuli directly guide oculomotor actions in the absence of awareness? For neutral stimuli, dissociations between visual awareness and eye movements, revealing more sensitive processing of information, have been related to the involvement of a fast subcortical retinocollicular pathway (Spering and Carrasco, 2015). Furthermore, processing of unaware emotional visual information has been associated with a subcortical pathway involving the amygdala, pulvinar, and superior colliculus (Tamietto and de Gelder, 2010), as well as structural connections between the amygdala and cortical motor‐related areas (Grèzes et al., 2014). The superior colliculus plays a crucial role in the control of voluntary and involuntary eye movements (Bell and Munoz, 2008). Thus, in the absence of awareness, orienting of eye movements towards and away from emotional faces could be mediated by these subcortical structures, in addition to the potential involvement of a cortical pathway (Pessoa and Adolphs, 2010). A possible mechanism could be that the amygdala assesses facial emotional expression, and the superior colliculus guides eye movements according to a fight, flight, or freeze response.

Why did participants look towards fearful faces, but avert their gaze away from angry faces, in the absence of awareness? As mentioned in the Introduction, under awareness these two threat-related emotions have differential perceptual consequences (Kret et al., 2013b; Marsh et al., 2005; Springer et al., 2007; Huis In 't Veld et al., 2014) and may be mediated by different neural pathways (Luo et al., 2007). In the absence of awareness, before this study, there had been only circumstantial evidence for differential processing of angry and fearful faces according to the time they take to break into awareness (Yang et al., 2007; Milders et al., 2006; Troiani et al., 2014; Jusyte et al., 2015; Zhan et al., 2015). With respect to eye movements, under awareness, both angry and fearful faces have shown to elicit similar eye movement responses, either attraction (Mogg et al., 2007; Kret et al., 2013a) or repulsion (Hunnius et al., 2011; Becker and Detweiler-Bedell, 2009). In the absence of awareness, gaze avoidance from masked angry faces had been demonstrated only indirectly with eyes starting instructed movements towards a response target more slowly in the presence of an angry than a happy face (Terburg et al., 2011). Instead, our results, directly measured with eye tracking, show uninstructed, sustained gaze avoidance to an angry face but sustained gaze attraction to a fearful face, while the faces are entirely suppressed from awareness. Fearful faces are more ambiguous and directing our eyes towards them may be an automatic response to try to gather more information (Bannerman et al., 2009a; Mogg et al., 2007; Davis et al., 2011). In contrast, angry faces pose a direct threat and directing our eyes away from them may be an automatic avoidance response (Davis et al., 2011).

Comparing our finding of differential eye movements in the absence of awareness with the previous findings of similar eye movements under awareness (Mogg et al., 2007; Kret et al., 2013a; Hunnius et al., 2011; Becker and Detweiler-Bedell, 2009) suggest that different factors may influence eye movements under aware and unaware conditions. Across studies, perceptual (Lapate et al., 2016), attentional (Mogg et al., 1994; Fox, 1996) and physiological (Tamietto et al., 2015) effects of emotional information either differ qualitatively or tend to be stronger in the absence than in the presence of awareness (Diano et al., 2017). Moreover, awareness modulates the time course (Liddell et al., 2004) and locus (Tamietto et al., 2015) of neural activations elicited by threat-related information, as well as functional connectivity between the amygdala and pre-frontal areas (Amting et al., 2010; Lapate et al., 2016; Williams et al., 2006). Two different mechanisms might cause threat-related emotions guiding actions differentially in the absence, but not in the presence of awareness: a) the perceived intensity of the threat might be stronger in the absence of awareness (Lapate et al., 2016; Liddell et al., 2004), which in turn may facilitate actions specifically tailored towards the nature of the threat, indirect or direct; b) cognitive mechanisms might suppress automatic actions upon threat-related information only under awareness (Whalen et al., 2013; Mogg et al., 1994), but not in its absence, as in our present findings. Several factors may help overwrite automatic eye movements towards fearful or away from angry faces, ranging from mere adherence to the task instructions (Becker and Detweiler-Bedell, 2009) to regulation of the social communication entailed in holding or averting gaze (Terburg et al., 2011; Emery, 2000; Kendon, 1967).

To conclude, our results provide the first evidence that emotional information humans are unaware of can differentially modulate their eye movements without entering awareness.

Source data and all analyses are available on Github (https://github.com/StephBadde/EyeMovementsSuppressedEmotionalFaces; copy archived at https://github.com/elifesciences-publications/EyeMovementsSuppressedEmotionalFaces).

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Author details

1. Petra Vetter

   1. Department of Psychology, Center for Neural Science, New York University, New York, United States
   2. Department of Psychology, Royal Holloway, University of London, Egham, United Kingdom

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Funding acquisition, Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Contributed equally with

   Stephanie Badde

   For correspondence

   petra.vetter@rhul.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6516-4637

2. Stephanie Badde

   Department of Psychology, Center for Neural Science, New York University, New York, United States

   Contribution

   Data curation, Software, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Petra Vetter

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4005-5503

3. Elizabeth A Phelps

   1. Department of Psychology, Center for Neural Science, New York University, New York, United States
   2. Department of Psychology, Harvard University, Cambridge, United States

   Contribution

   Conceptualization, Resources, Funding acquisition, Writing—review and editing

   Competing interests

   No competing interests declared

4. Marisa Carrasco

   Department of Psychology, Center for Neural Science, New York University, New York, United States

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   marisa.carrasco@nyu.edu

   Competing interests

   Reviewing editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0002-1002-9056

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