Eye gaze is a powerful and compelling social cue. It can be rapidly detected (Senju and Hasegawa 2005
) allowing discrimination of complex emotions (Baron-Cohen et al. 1997
) and intentions (Senju and Johnson 2009a
). Direct gaze also signals that another person can see out, and this belief in seeing something has been linked to mentalizing (Teufel et al. 2010a
). A variety of studies suggest that comprehension of gaze and responses to gaze may be different in autistic people (Senju and Johnson 2009a
). Recently, it has been found that typical adults prefer viewing faces with direct gaze to those with averted gaze, while no such preference is seen in autism (Dubey et al. 2015
). However, it is not yet clear if differences in gaze preference in autism are related to processing the gaze as a physical eye-shape, or to differences in the belief of whether others can see something. The present paper uses a novel paradigm to explore these different possibilities.
Models of Gaze Processing
Current models of gaze processing suggest two possible neurocognitive responses to the gaze of another person—a basic alerting mechanism and a more elaborate perceptual mentalizing process. The basic alerting mechanism is believed to be implemented by a sub-cortical pathway, whereby an image of a pair of eyes activates the superior colliculus, pulvinar and amygdala (Senju and Johnson 2009b
), and directs attention towards the eyes (Senju and Hasegawa 2005
). It is thought that this pathway has an evolutionary meaning, since in many non-human species direct gaze signals threat from a predator (Emery 2000
). In humans, neuroimaging studies indicate that the subcortical regions modulate, in turn, the recruitment of the social brain network (e.g. superior temporal sulcus, medial prefrontal cortex), which modulates the processing of contextual social information (Senju and Johnson 2009b
). Overall, the subcortical mechanism operates rapidly and seems to function in the same way for all stimuli which match the basic features of a pair of eyes. Thus, we could describe this attentional gaze processing as being driven by an ‘eye-shape’, regardless of whether that is a photo, a schematic drawing or a live person.
More recently, research has also begun to uncover how people process gaze as a form of perceptual mentalizing. It is important to distinguish perceptual mentalizing from the audience effect. Perceptual mentalizing is the attribution of perceptual states to other people about whether they can or cannot see something
(Teufel et al. 2010a
). Instead, the audience effect refers to changes in behaviour that happen under the belief that other people can specifically see me
(Hamilton and Lind 2016
). Substantial research has investigated the audience effect, showing that the belief in being seen modulates emotional arousal (Myllyneva and Hietanen 2015
), eye gaze directed at the observer (Gobel et al. 2015
; Laidlaw et al. 2011
), and prosocial behaviour (Izuma et al. 2009
). However, only few studies have looked at how perceptual mentalizing influences social information processing.
For instance, Teufel et al. (2010b
) found that gaze cueing effects are driven by perceptual mentalizing. Participants saw videos of an actor wearing obscured goggles with different coloured frames, and were told that one pair of goggles was transparent whereas the other was opaque; participants were also told that the videos were live streamed from an adjacent room. Results showed that the gaze cueing effect was greater in valid trials (i.e. trials where actor’s gaze and target are on the same side) only for the transparent goggles. This suggests that the gaze cueing effect was strongly influenced by the attribution of meaningful mental states to the confederate, and that this only happened when the confederate could see through the goggles (see Nuku and Bekkering 2008
for a similar study).
In another study, Furlanetto et al. (2016
) showed that perceptual mentalizing also influences visual perspective taking. In each trial participants first saw the words ‘YOU’ or ‘SHE/HE’ on the screen, then a digit, and finally an avatar looking towards the right or left wall of a room (created with a virtual reality software). Each wall had a number of dots that ranged from 0 to 2. Participants had to judge whether the digit was consistent with the number of dots that themselves (‘YOU’) or the avatar (‘SHE/HE’) could see, respectively. Crucially, this task was combined with the goggles paradigm designed by Teufel et al. (2010b
): the avatar was wearing obscured goggles that participants believed to be either transparent or opaque. They found that reaction times were slower when the avatar was wearing transparent goggles, suggesting that participants took the perspective of the avatar only when they knew the avatar could see the dots through the goggles.
Thus, these studies show that perceptual mentalizing itself modulates how we process social information from eye gaze. Here, we aim to test the relationship between perceptual mentalizing and social motivation, and whether this relationship is different in autism.
Gaze and Social Interaction in Autism
People with the Autism Spectrum Condition (ASC) show persistent difficulties in social interactions (DSM-5; Diagnostic and Statistical Manual of Mental Disorders 5th Ed. 2013
) including the processing of eye gaze. Eye tracking studies suggest autistic people make fewer fixations on the eyes of actors in a movie (Klin et al. 2002
), though this effect is reduced for static photos of faces (Chevallier et al. 2015
). They have also difficulties in understanding the social meaning of gaze duration and gaze direction, and show abnormal recruitment of brain areas that process this information (Georgescu et al. 2013
; Senju et al. 2005
). At the same time, there is evidence suggesting that autistic people might be less susceptible to the belief in being seen (audience effect): for instance, they do not seem to increase prosocial behaviour when other people are observing them (Cage et al. 2013
; Izuma et al. 2011
). However, no previous research has yet addressed perceptual mentalizing in autism. Thus, it is not yet clear if differences in responsiveness to gaze in autism are due to changes in the subcortical gaze-attention mechanism, or due to differences in perceptual mentalizing about whether others can see something. The present paper investigates this issue, in relation to the measurement of motivation.
Recently, it has been suggested that typical adults find social stimuli and social interactions inherently rewarding, possessing an inbuilt social motivation, but that this motivation might be reduced in autism (Chevallier et al. 2012
). For instance, autistic participants self-report diminished enjoyment in social situations when compared to typical ones (Chevallier et al. 2011
). At the neural level, they activate reward-related brain areas (e.g. ventral striatum) significantly less than typical people, specifically in response to social reward (Scott-Van Zeeland et al. 2010
; see also; Delmonte et al. 2012
and; Kohls et al. 2013
). Chevallier et al. (2012
) distinguish three levels of social motivation. First, social orienting
happens when we give attentional priority to social stimuli rather than non-social; second, there is social seeking
when we make an effort to get social stimuli because we like them (i.e. we want them because we find them inherently rewarding); finally, social maintaining
refers to the development of strategies to enhance relationships with others (e.g. be viewed as likeable, cooperative, etc.). For the scope of the present study we will focus on social seeking.
A number of studies have found ways to measure social seeking behaviour. For example, people will sacrifice a small monetary reward to view a genuine smile (Shore and Heerey 2011
), and will press a key repeatedly to see attractive people (Hayden et al. 2007
). A new measure of social seeking behaviour has been recently developed, which attempts to quantify how much effort people will make to seek out social stimuli. In this Choose-A-Movie (CAM) paradigm, participants are presented on each trial with two coloured boxes and know that (for example) the orange box contains movies of people, while the green box contains movies of household objects. They can chose which box to open and thus which movie category to watch on each trial. To encourage careful decision making, on each trial there are a number of locks on each box (one, two or three locks), and to open a box with three locks participants must press a key and wait for that lock to open three times. This imposes a small but noticeable effort cost on that box, compared to a box with one lock. Thus, participants must trade-off their preference to view a particular movie against the effort involved in viewing it. Results show that they do just that (Dubey et al. 2015
). More critically, the data show that typical adults prefer to view direct gaze video-clips to averted gaze video-clips and object video-clips. Conversely, autistic individuals prefer object clips to direct or averted gaze, and have a weak preference for averted gaze over direct gaze.
However, it is not yet clear why autistic people show differences in their motivation to view direct gaze stimuli. Many differences in gaze processing have been reported in autism, such as gaze comprehension (Baron-Cohen et al. 1997
) and attentional cueing from gaze (Senju and Johnson 2009a
). These effects could be explained by differences in a basic sub-cortical mechanism sensitive to eye-shapes. Autistic individuals also show differences when attributing mental states to others (Baron-Cohen et al. 1985
; Senju et al. 2009
), and seem to be less sensitive to the presence of other people observing them (Cage et al. 2013
; Izuma et al. 2011
). This suggests that differences in response to direct gaze might reflect differences in perceptual mentalizing capacities. In the present study, we contrast these two hypotheses in the context of social motivation. Our task also allows us to distinguish whether differences in social motivation are due to active avoidance of eye gaze and social information or passive omission of these cues (Corden et al. 2008
; Senju and Johnson 2009a
The Present Study
The present study aimed to dissociate responses to eye-shapes, presumably processed by a subcortical mechanism (Senju and Johnson 2009a
), and responses to the belief that another person can see something, presumably related to perceptual mentalizing (Teufel et al. 2010a
). To test responses to eye-shapes, we contrasted videos of an actress with empty sunglasses (no lenses) to videos of the actress wearing normal sunglasses. To test responses to the belief that others can see, we adopted the manipulation of Teufel et al. (2010b
), where participants believed the actress can see through one set of sunglasses (normal sunglasses, e.g. those with blue frames) but cannot see through the other (opaque sunglasses, e.g. those with red frames). We counterbalanced which frame colour was linked to each belief (can see or cannot see) across participants. To complete our 2 × 2 factorial design, we created videos of the actress wearing sunglasses with paper eyes glued over the lenses—typical eye-shapes are present in this manipulation, but the actress cannot see through. This set of stimuli gave a complete 2 × 2 factorial design with levels Belief in seeing (Belief, B+ and B−) and Eye-shape (Eyes, E+ and E−); sample stimuli from each cell are shown in Table 1
Factorial design used for the video categories and sample screenshots of the video-clips
Belief in being seen (B)
Empty sunglasses (B+E+)
Normal sunglasses (B+E−)
Paper-eyes sunglasses (B−E+)
Opaque sunglasses (B−E−)
Taking these four social video-clips, we used the Chose-A-Movie task to measure which movie participants preferred to view. Expanding on the design by Dubey et al. (2015
), we gave participants a choice of all four movies on each trial, with variable numbers of locks to manipulate effort. Our primary outcome measure was the percentage of trials on which participants chose each movie. Note that we did not attempt to persuade participants that these videos represented a live-feed of another person from another room. We took this decision for three reasons. First, we wanted to specifically test the effect of perceptual mentalizing (belief that someone can see something
) on social motivation. Second, we wanted to remain close to the procedure of Dubey et al. (2015
), where there was no live-feed manipulation. Third, it is not very plausible to have a live-feed of the same person wearing multiple different sets of sunglasses at very short notice. Thus, our experimental design addresses perceptual mentalizing in a non-interactive way: participants know that they are not in an online interaction with the actress.
Based on our hypotheses, we can make several predictions. First, if typical participants prefer attributing perceptual mental states because they have no difficulties in further social information processing, they should choose to view stimuli with empty and normal sunglasses (B+ conditions, actress can see through) over stimuli with paper-eyes and opaque sunglasses (B− conditions, actress cannot see through). Second, if autistic people show reduced social motivation because they are not sensible to eye-shapes, they will show no difference in preference for E+ and E− conditions. However, if autistic individuals actively avoid eye-shapes, they should prefer videos with normal and opaque sunglasses (E− conditions, eyes not visible) to videos with empty and paper-eyes sunglasses (E+ conditions, eyes visible). Third, if autistic people show reduced social motivation due to difficulties in attributing a perceptual mental state to the actress, they should show no difference in preference for B+ and B− conditions. If they attribute perceptual mental states but are less motivated to engage because of difficulties in further processing of this or other social information, they should prefer videos with opaque and paper-eyes sunglasses (B− conditions) to videos of empty and normal sunglasses (B+ conditions). Systematic group differences should be reflected in Group × belief and group × eyes interactions. Because the paper-eyes sunglasses are a slightly odd stimulus with low ecological validity, the strongest test of the claim that beliefs about whether someone can see impact on social motivation comes from examining the conditions where participants cannot see the eyes of the actress but their belief about whether or not she can see through is manipulated. Thus, the Group X Belief interaction was also examined including only the E− conditions, that is, normal sunglasses (B+E−) and opaque sunglasses (B−E−).