Processing of social threats in adolescents with autism spectrum disorders

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Eye-region fixation

In sections 1.1 and 1.2, I stressed the general inattention and absence of spontaneous orientation towards salient social stimuli in ASD, such as the eye-region of the interlocutor. This has been reported in the literature from the first definitions of autism, is found in young children with ASD and in this section I will explain how it influences participants’ performance.
A failure to engage in appropriate eye-contact and an indifference to the faces of others are characteristic of ASD from the first description of their symptomatology (Kanner, 1943) and reduced attention to others’ eyes is evident from approximately 2-6 months of age in infants who are later diagnosed with ASD (Jones & Klin, 2013). Individuals with ASD present reduced or deviant fixation patterns to the eyes of others (Corden, Chilvers, & Skuse, 2008; Pelphrey et al., 2002; Senju & Johnson, 2009; Spezio, Adolphs, Hurley, & Piven, 2007) and enhanced attention to the mouth region instead (Klin, Jones, Schultz, Volkmar, & Cohen, 2002). Spezio, Adolphs, Hurley, & Piven, (2007) used the “Bubbles” technique to occlude different areas of the same face in order to create different stimuli and then assessed which information each of the two different groups use when they judge emotions from the face accurately. They found that while the TD group used information from the eyes, the ASD group used information from the mouth. Similarly, Grossman & Tager-Flusberg, (2008) assessed the ability of adolescents with and without autism to implicitly process facial expressions of emotions or lip-read words mimed by the same stimuli, both when the eyes of the stimuli were masked and unmasked. The TD group performed better in the emotion task and worse in the word task in the unmasked condition, when they could extract information from the eyes. However, emotion accuracy of the ASD group was comparable across the masked and unmasked conditions (see Figure 8) suggesting that collection of information from the eyes is not prioritised in this group.
Figure 8 : Performance of the ASD (left) and TD (right) groups in both the masked (bullet) and unmasked (square) conditions from Grossman & Tager-Flusberg, (2008). The bottom dot line represents the chance level.
At the same time there is a part of the literature that presents doubts regarding the deviant social attention or gaze in ASD. Some report no group differences at all while others report differences only in areas of the face that surround specifically the eyes, in experimental conditions which are complex, i.e. gaze following (Fletcher-Watson, Leekam, Benson, Frank, & Findlay, 2009; Freeth, Chapman, Ropar, & Mitchell, 2010). Recently an exhaustive study with a large sample size (N = 81) disentangled this by investigating social attention of individuals with ASD using three different visual exploration paradigms; one static, one dynamic or one interactive (Chevallier et al., 2015). The total time spent fixating to the eye-region of others depended on the task for the ASD group and meaningful group differences appeared when tasks became interactive and thus more ecological, suggesting that reduced social attention is indeed characteristic of this group at least in the most realistic, ecologically valid paradigms, in which we are most interested. This is in line with past findings in ASD that favour a failure to adjust one’s level of attention to social stimuli as a function of the stimulus’ changes in saliency (Birmingham, Cerf, & Adolphs, 2011; Horlin et al., 2013). Importantly, total fixation duration is positively correlated with the activation of the fusiform gyrus and the amygdala in response to faces (Dalton et al., 2005). Hypoactivation of FG and hyperactivation of the amygdala has been widely reported in ASD in response to threatening social and emotional cues and the authors proposed that the variation in eye-region fixation could account for this variation in activity in response to faces (Dalton et al., 2005). This suggests reduced responses to faces and heightened emotional responses to gaze fixations in ASD. These findings put forward three suggestions: 1) individuals with ASD do not find mutual gaze pleasant, 2) their gaze fixation duration pattern is associated with their ability to process faces and 3) there are no deficits in the ability to orient to these features but rather deficits in the spontaneity or prioritisation of this orientation. Similarly a lack of spontaneity/prioritisation to engage in social interaction or social tasks, rather than an inability to perform the tasks themselves, could underlie observed behavioural deficits in ASD.
In the mimicry literature, individuals with ASD showed reduced spontaneous facial mimicry in response to happy and angry facial expressions but when asked to voluntary mimic the expression of others they do so successfully (McIntosh, Reichmann-Decker, Winkielman, & Wilbarger, 2006), suggesting that there is mimicking ability in ASD but its automaticity is deficient. Similarly, in a study by Begeer et al., (2006) the ASD group failed to match cards according to their emotional expression only when the matching was implicit and they could choose amongst 3 matching criteria; presence of glasses, presence of moustache and emotional expression. The ASD group spontaneously chose non-social and non-emotional criteria. When however, they were explicitly asked to match the cards according to the emotion all group differences disappeared, suggesting that the abilities are intact but the salience of emotions or their prioritisation might be reduced. Given that this impaired performance is underlined by intact abilities and manifests due to a lack of spontaneous engagement with the social world, then lack of spontaneous orientation specifically to the eye-region would be expected to lead to similar results (impaired performance) in tasks assessing abilities which are however preserved. In cases like these, explicit instruction or use of jitters to direct attention to relevant cues of the social world, in this case the eye-region, should lead to typical performance of the ASD group. In support of that individuals with ASD do not show contagious yawning in response to someone else yawning, which is considered mimicry, but when children with ASD were asked to fixate the eyes of the face stimuli, they yawned equally frequently to the TD group (Senju et al., 2009). In a different study (Rutherford & Krysko, 2008) measuring reflexive attentional shifts in response to gaze direction or head movement direction changes, participants were asked to focus on the fixation point and indicate the location of a target point that would appear and disappear, while ignoring any face images that appeared concomitantly. Following instruction to attend to the fixation cross, and in the absence of a social task (ignore faces), the ASD and TD groups performed similarly, so that the salient social cues, in this case gaze direction change, influenced both groups more than the head movement (see Figure 9). We could argue the possibility that the same is the case in emotion recognition tasks, where ASD participants would fail because they do not spontaneously orient to the eyes, rather than because of an inability to perceive emotions.
Figure 9 : Results from Rutherford & Krysko, (2008) for A) 100ms and B) 800ms stimulus presentation during target appearance. The gaze direction or head movement were either congruent or incongruent with the side in which the target appeared.
In support of this argument, firstly, emotion recognition abilities depend on one’s capacity to focus on relevant information (Kuusikko et al., 2009), secondly attention to eye-region is linked to emotion decoding performance (Bal et al., 2010) and thirdly, eye-tracking findings suggest that people who orient spontaneously to others’ eyes, show greater emotion recognition abilities (Kirchner, Hatri, Heekeren, & Dziobek, 2011). This is particularly important for threatening emotions, such as fear and anger given that these emotions are predominantly expressed in the upper part of the face (Dimberg & Petterson, 2000). Thus individuals with ASD might not decode emotions accurately because they do not spontaneously look at the appropriate features of the face. Specifically in ASD, which is characterised by deviant gaze behaviour, this is highly relevant because the group’s fixation time on the eyes or mouth of the stimulus predicts their emotion recognition performance (see Figure 10 from Kirchner, Hatri, Heekeren, & Dziobek, 2011). Hence, the absence of methodological implementations to intentionally allocate the participants’ attention to relevant social cues could bring individuals with ASD at a disadvantage as compared to their age-matched controls (Chevallier, Kohls, et al., 2012).
Figure 10 : from Kirchner et al., (2011). A) Fixation on the eye-region is a positive predictor of emotion recognition performance in the ASD group and B) fixation to the mouth is a negative predictor of emotion recognition performance in ASD.

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Age, why adolescents?

In the above literature review I focused on emotion processing abilities in children and adolescents with ASD and I presented the most prominent methodological factors that influence their performance. In children emotion processing is mostly assessed using static, high intensity stimuli and the results are based on the recognition accuracy. In adolescents, as we saw the tasks are more refined with different emotion strengths and extra variables such as RTs but still mixed results are reported in adolescent groups. The results in adults, using a variety of different methodologies and variables of interest, are similar (for a comprehensive review see Harms et al., 2010): while some find no group differences when high-functioning adult ASD groups are compared to neurotypical controls (Adolphs, Sears, & Piven, 2001; Rutherford & Towns, 2008), others find that they are deficient in recognising emotions and particularly negative ones (Ashwin, Baron-Cohen, Wheelwright, O’Riordan, & Bullmore, 2007; Corden et al., 2008; Philip et al., 2010; Wallace et al., 2011). In this doctoral work we are interested in development and specifically in perception of threat in adolescents with ASD between the ages of 12 and 17 years old, rather than in children. But why is that?
Firstly, although emotion abilities increase with age, children become experts and can achieve adult levels of emotion interpretation around the age of 11 years old (Custrini & Feldman, 1989; Tonks, Williams, Frampton, Yates, & Slater, 2007). Studies investigating emotions abilities in ASD groups have found that younger children can present intact decoding of pure expressions of emotions, however, when compared to adolescents they might be impaired (Kuusikko et al., 2009). Such age group differences in emotion processing become even more prominent when complex and ambiguous expressions are involved, i.e. ones resulting from blending different emotions (Kuusikko et al., 2009). Thus, investigating adolescents allows for more complex expressions to be used. This means that not only blended but also ambiguous facial expressions of threat can be used, which are more ecological, given that in everyday life people rarely express full intensity emotions. In line with this, investigation of children’s emotion abilities is limited to the analysis of emotion recognition accuracy because tasks have to be simpler (see section 1.3). Working with adolescents, on the other hand, allows for more complex tasks to be used and more variables of interest, such as RTs and physiological measures (eye-tracking, mouse-tacking).
Secondly, in typical development emotion decoding abilities improve with age from childhood throughout adolescence (Thomas, Bellis, Graham, & LaBar, 2007; Vicari, Reilly, Pasqualetti, Vizzotto, & Caltagirone, 2000) in a continuous fashion (Herba & Phillips, 2004). Evidence from neurodevelopmental studies suggests that brain areas responsible for the processing of facial expression of emotion develop throughout late childhood and adolescence, when they start showing corresponding functional differences. The amygdala and the fusiform gyrus for example continue to develop throughout adolescence (Aylward et al., 2005; Schumann et al., 2004; Thomas et al., 2001) and the prefrontal cortex (PFC) is of the last areas to mature (Casey, Giedd, & Thomas, 2000; Casey, Tottenham, Liston, & Durston, 2005). This is highly relevant for the study of emotions and particularly threat in ASD because the amygdala for example is a core area for guiding the individual’s attention to social, biologically relevant stimuli. The amygdala guides attention to the eyes, faces or biological motion (Adolphs & Spezio, 2006) and might be responsible for computing and updating the value of social orienting (Klein, Shepherd, & Platt, 2009). Moreover, it is implicated in the understanding of the significance of information of the face, such as emotions (Aylward et al., 2005) and specifically threatening ones (Adolphs, 2008), which are predominantly expressed using the upper part of the face (Fridlund, 1997). ASD has been characterised by abnormal activation of the amygdala (Hadjikhani, Joseph, Snyder, & Tager-Flusberg, 2007) as compared to TD individuals and by differences in amygdala volume and activation. Importantly, differences are observed between age groups within the ASD group. ASD children have enlarged amygdala volume in comparison to TD children but adolescents with ASD aged 12 to 18 years old do not differ from TD adolescents in amygdala volume (Schumann et al., 2004), and thus allow for better controlled comparisons between groups.
Most importantly, the social brain, which refers to the network behind understanding and interacting with others, undergoes big changes during early adolescence, as individuals show enhanced desire to socialise with others but social exchanges begin to require more sophisticated skills (Howlin, 2003). This is a critical period for the transition from childhood to adulthood with age-specific social, psychological and physical characteristics which are thought to promote independence (Spear, 2000). Neural connections are being remodelled in comparison to childhood because of the PFC development during early adolescence (≈10 years old) with changes in not only goal directed behaviours but also in emotion processing of aversive stimuli (Spear, 2000). This is highly relevant to the present thesis that uses aversive stimuli and focuses on the processing of social threats. Importantly, adolescents offer a better case for studying emotion processing as compared to adults because they show greater connectivity between prefrontal areas (Burnett & Blakemore, 2009), they are more sensitive to emotional ambiguity (Thomas et al., 2001), their frontal activity is modulated by the emotional nature of the stimulus rather than by its attentional demands – which is the case in adulthood – (Blakemore, 2008; Christopher S. Monk et al., 2003) and they show enhanced neural reactivity in response to social threats (Hare et al., 2008). The latter is the case not only in comparison to adults but also to children. Lastly, there are not many symptom improvements related to reciprocal social interaction between adolescence and adulthood in ASD when improvements happen only in the domains of repetitive and restrictive interests (Seltzer, Shattuck, Abbeduto, & Greenberg, 2004).
It appears that age is an important determinant of emotion abilities and adolescence is a developmental period distinct from childhood and adulthood, which allows for more refined and detailed investigation of emotion abilities in typical development and in ASD. Thus, the focus of this doctoral work will be on the perception of threatening emotions in adolescents with ASD.

Section 1.3 conclusion

In the start of this section I presented you with the most dominant account in the literature, proposing a fundamental, generalised deficit in emotion processing in ASD. However, the findings in the literature are mixed and the performance of the ASD group depends on methodological and demographic factors. Such factors include the matched control group, the variables of matching, the age of the participants and so on, all of which contribute to the heterogeneity of findings regarding processing of facial affect in ASD. Moreover, it is important to note that most studies investigated the processing of one facial social cue at a time, which cannot give a full picture of the processing abilities in this group. In real life situations an emotional expression is never presented alone but it is always in context, which might affect and in some cases even enhance the processing of the emotion. The contextual influences on emotion processing in neurotypical individuals and individuals with ASD will be discussed in depth in Chapter 2 where the first experiment of this Ph.D. will be introduced, and emotion processing in adolescents with ASD will be investigated.

Table of contents :

Chapter 1: General Introduction
1.1 Autism spectrum disorders
1.2 Why the face and why in autism? The case of facial expressions of emotion.
1.3 Processing of facial expressions of emotion in autism spectrum disorders
1.3.1 Early studies on emotion processing in children and adolescents
1.3.2 Matching and control group selection
1.3.3 Type of stimuli
1.3.4 Eye-region fixation
1.3.5 Age, why adolescents?
1.4 Relevant theoretical frameworks
1.4.1 Behavioural self-regulation accounts
1.4.2 Social motivation accounts
Chapter 2: Processing of social threats in adolescents with autism spectrum disorders
2.1 Contextual effects on emotion processing in neurotypical populations
2.2 Contextual effects on emotion processing in autism spectrum disorders
2.3 Shared mechanism for emotion processing in adolescents with and without autism (Experiment 1)
Chapter 3: Adaptive responses to social threats in autism spectrum disorders
3.1 Adolescents with autism can use implicit social threat to adapt their behaviour (Experiment 2)
Chapter 4: General Discussion
4.1 Summary of goals
4.2 Preserved processing of social threats in adolescents with autism spectrum disorders
4.3 Preserved responses to social threats in adolescents with autism spectrum disorders
4.4 Impaired social motivation and/or impaired mechanisms?
4.5 Social threats: anger and fear
4.6 Limitations


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