Background
Social competence is a multidimensional construct in which social, emotional, cognitive and behavioural skills are involved in a dynamic interplay with the environment. This, in turn, facilitates successful social adaptation, including the ability to initiate and maintain satisfactory relationships, with, for example, peers (Iarocci et al.
2007). One way to explore the complex genetic and environmental interactions modulating social competence is to study individuals with a known genetic disorder who also have differences in social behaviour. The 22q11.2 deletion syndrome (22q11DS) also known as velo-cardio-facial syndrome is the most common known microdeletion disorder and occurs in one in every 2,000 to 4,000 live births (Shprintzen
2005; Vorstman et al.
2006). The syndrome has a large phenotypic spectrum but is most commonly associated with developmental anomalies such as cardiac and palatal abnormalities, a syndrome specific typical face, intellectual disabilities and specific social and cognitive impairments. Children with 22q11DS are frequently described as being shy and withdrawn, socially immature and as having difficulties with initiating and maintaining positive peer relationships (Golding-Kushner et al.
1985; Heineman-de Boer et al.
1999; Swillen et al.
1997,
1999; Shprintzen
2000). Children with the syndrome also present with a high rate of psychiatric disorders including autism spectrum disorder, attention-deficit disorder, separation anxiety and affective disorders (Vorstman et al.
2006; Fine et al.
2005; Gothelf et al.
2004; Swillen et al.
2000). The syndrome is further believed to be the third highest known risk factor for developing schizophrenia-like psychotic disorders in late adolescence or early adulthood (Murphy
2002). Many of the psychiatric disorders experienced by people with 22q11DS are associated with a lack of appropriate social competence, and it has been suggested that individual differences in social competence among people with 22q11DS may be associated with the subsequent development of psychiatric disorders such as anxiety and depression (Murphy
2005). Research over the last decade has shown that social functioning in psychiatric disorders such as depression and psychosis (Wang et al.
2008) are linked with deficits in theory of mind, for instance, the ability to judge one’s own and other people’s mental states (Premack and Woodruff
1978).
The ability to accurately understand, reason and predict other people’s behaviour requires the integration of complex skills. It has been argued that theory of mind skills are dependent on two dissociable components, namely a social-perceptual and a social-cognitive component (Tager-Flusberg and Sullivan
2000). The social-perceptual component includes the ability to recognise people and to interpret people’s mental state from facial emotions or body expressions. In healthy individuals, the processing of human faces and, in particular, the ability to accurately recognise facial emotions is vital for social competence and is thought to depend on specialised neural systems including the occipito-temporal cortex (for a review, see (Posamentier and Abdi
2003)). More specifically, it has been suggested that while invariant aspects of faces are dependent on the lateral fusiform gyrus, more changeable aspects such as expression, eye gaze and lip movement are processed in the superior temporal sulcus and associated networks (Haxby et al.
2000). Few studies have specifically examined face processing in people with 22q11DS; however, recently, two functional magnetic resonance imaging (fMRI) studies identified atypical neural activations among children and adults with 22q11DS compared with healthy (Andersson et al.
2008) and learning-disabled comparison subjects (van Amelsvoort et al.
2006) when processing facial expressions. The differences in neural activations were argued to be face-specific and not due to a general visual perceptive deficit since the neural activation pattern in people with 22q11DS were similar to controls when presented with non-face stimuli such as houses (Andersson et al.
2008). Likewise, it appears as if young adults with 22q11DS use atypical strategies while viewing photographs of faces displaying emotions (as measured using visual scanpath technology), and this is associated with poorer accuracy when labelling the displayed emotions (Campbell et al.
2010a). In particular, it was reported that people with 22q11DS spent more time looking at peripheral (off-the-face) rather than internal (eye, nose, mouth) features of the face. The young people with 22q11DS also spent less time looking at the eye region of the face and significantly more time looking at the mouth compared with controls. These studies indicate that people with 22q11DS do not process faces in a typical manner; it also appears as if these atypical processes are associated with poorer skills of encoding and interpreting facial information. Indeed, it has been suggested that short-term memory of unknown faces may be impaired in 22q11DS. In particular, when children with 22q11DS were asked to recognise faces that had been learned immediately before, they performed poorer not only compared with controls but also compared with their performance on other memory tasks (e.g., visual-spatial; Campbell
2006; Lajiness-O’Neill et al.
2005). Furthermore, we recently reported that children with 22q11DS (a subgroup of those reported in the current paper) had a significantly reduced performance on face processing tests of gaze direction, identity and emotion recognition compared with intellectually, age- and gender-matched children with Williams syndrome (WS; Campbell et al.
2009). However, no significant group differences were identified on a facial speech-recognition task (Campbell et al.
2009). These findings have led to the assumption that face processing is atypical in people with 22q11DS. However, since people with WS usually perform in the normal range and significantly better than mental-age-matched controls on such tasks (Tager-Flusberg et al.
2003), we still need to evaluate the face processing skills of people with 22q11DS compared with typically developing controls in order to determine how people with 22q11DS process faces.
A second key component of theory of mind is described by Tager-Flusberg and Sullivan (
2000) as social-cognitive. The social-cognitive component underlies the ability to understand that other people have mental states that are independent from one's own including independent thoughts, beliefs and intentions and to make attributions about these (Castelli et al.
2002). Social-cognitive skills are crucial to understand and correctly predict peoples’ actions and are often measured using classical false-belief tasks such as the Sally-Ann scenario (Baron-Cohen et al.
1985) and mentalising tasks such as the Strange Stories (Happé
1994; Jolliffe and Baron-Cohen
1999). The neurobiological substrate most strongly linked with the social-cognitive component is the medial frontal region of the brain (Siegal and Varley
2002). Recently, it was reported that a sample of children (Niklasson et al.
2002) and adults (Bassett et al.
2007; Chow et al.
2006) with 22q11DS had theory of mind deficits. These studies were valuable first steps. However, one study (Niklasson et al.
2002) did not include a control group, and the other study focussed solely on adults with 22q11DS and schizophrenia (Bassett et al.
2007; Chow et al.
2006). In contrast, we recently reported that children with 22q11DS, compared with matched children with WS, did not perform poorer on false-belief tasks (Campbell et al.
2009). There were some group differences (with the 22q11DS group performing poorer) on the Strange Stories task, although the result may have been confounded by low comprehension or on stories requiring mentalising skills (Campbell et al.
2009). However, the study was limited by a small sample size and did not examine how children with 22q11DS performed compared with typically developing children.
The objectives of the current study were to examine the two proposed components of theory of mind, social-perception (face processing) and social-cognitive (false beliefs) in a cohort of children with 22q11DS compared with typically developing sibling controls. Furthermore, we aimed to investigate if performance on these tasks was related to everyday social competence and emotional problems, as rated by the parent(s). We tested the hypotheses that: compared with age- and gender-matched sibling controls (1) children with 22q11DS participants have specific deficits in face processing tasks most related to social competence, i.e., emotion recognition and gaze direction; (2) children with 22q11DS show a deficit on the false-belief and mentalising tasks; and (3) that parent-rated social competence is correlated with performance on these theory of mind tests (face processing tasks, false-belief and mentalising tasks)
Discussion
The current investigation is the first to investigate social-cognitive and social-perceptual mechanisms and their relationship to social competence and emotional problems among children with 22q11DS and typically developing sibling controls.
We predicted that the 22q11DS participants would have specific deficits in the social-perceptual tasks of face processing. In particular, we predicted that children with 22q11DS would have problems with tasks of a high salience to social functioning, such as emotion and gaze identification. We did indeed identify deficits in these aspects of face processing compared with sibling controls, although we also identified deficits in identity recognition and facial speech indicating a general deficit in facial processing. The greatest deficit, however, was identified in the Gaze direction task, and while this may have been at least partly due to an increased level of difficulty, we do not believe that this fully explains this finding. An independent study of visual scan path strategies in young people with 22q11DS indicate that people with the syndrome spend less time looking at the eyes compared with the mouth when judging facial emotions (Campbell et al.
2010a). This may be indicative of inefficient facial perceptual strategies which might have influenced the performance on the gaze identification tasks carried out in the current study. Our findings are in agreement with current neurobiological knowledge of specific brain anomalies among people with 22q11DS. In particular, it has been reported that social-perceptual ability is dependent on the occipito-temporal cortex including the lateral fusiform gyrus and also the superior temporal sulcus and associated networks (Haxby et al.
2000). It has been well established that the occipital and temporal regions of the brain are affected by a deletion at chromosome 22q11.2 (Campbell
2006; Henry et al.
2002). Findings from magnetic resonance imaging (MRI) studies support the idea that social-perceptual impairments in the 22q11DS group may be due to atypical neural structures and brain functioning and have identified less insular and frontal cortical activation and relatively more activation in bilateral occipital cortex when viewing emotional faces (Andersson et al.
2008; van Amelsvoort et al.
2006). In addition, atypical scanning patterns of photographs of emotional human faces have been revealed (Campbell et al.
2010a). However, it is still unknown what strategies children with 2211DS use to judge the identity of a person or when determining eye gaze direction or facial speech.
It is also unknown whether the observed problems in facial perception are due to a general visual perceptual impairment or a face-specific social-perceptual impairment. Although not directly comparable, we have revealed impairments in some aspects of object perception such as identifying objects from unusual viewpoints in children (Campbell
2006) and adults (Henry et al.
2002) with 22q11DS, indicating that there may be generalised problems with visual perception present in this population. However, the fMRI data reported by Andersson and colleagues did not find any group differences in neural activation when the groups were presented with objects such as houses which the authors interpreted as evidence for a face-specific neural anomaly (Andersson et al.
2008). It is also unknown if the origins of the observed face social-perceptual impairments are due to early face processing problems which may have resulted in worse social competence and hence less social interactions (and less practice) or if problems in another related area could have resulted in the observed problems. Unfortunately, no study of infant social-perception/cognition has yet been undertaken in 22q11DS, so the developmental trajectory of these skills is not clear. One could also argue that the group differences are simply due to the lower intellectual functioning of the clinical group. However, we have previously compared a subgroup of the current sample with a group of age-, gender- and intellectually matched children with Williams syndrome and subsequently identified a specific impairment in the 22q11DS group when performing the identity, emotion and gaze tasks while no significant group differences were identified in the facial speech task or the object perceptual tasks. Hence, we do not believe that the failure on these tasks are simply due to lower intellectual functioning in these children but rather a combination of lower intellectual functioning and syndrome specific differences.
However, it does seem as if language skills (in particular grammatical skills) and working memory ability are important to take into consideration when evaluating social-perceptual skills in this group of people. In the present context, consideration of semantic memory skills may elucidate the association reported between measures of face processing and grammatical skills (measured by TROG), for one who is proficient at storing and retrieving verbal concepts is liable to be proficient on tasks of verbal ability, as both require efficient access to words/concepts. Whilst the processes involved in identifying an individual are considered distinct from those required to perceive emotion and speech related actions of the mouth (Bruce and Young
1986), these processes have in common a reliance on semantic memory. As such, despite our best efforts to minimise the influence of both language and working memory in the design of the face processing tasks by using simple forced-choice matching tasks without requiring verbal responses, the findings from this study would suggest that face processing, by nature, requires these abilities.
For future studies, it will be important to compare social-perceptual skills of people with 22q11DS with people with other developmental disorders characterised by lower intellectual functioning and also to investigate if the observed facial processing deficits are specific or if similar deficits exist in other visual perceptual tasks. In addition, it would be valuable to use more naturalistic stimuli and tasks in order to determine the exact nature of the face processing deficits in 22q11DS. To conclude, considering the importance of social-perception in communication and social competence, the face processing deficits observed in the 22q11DS group needs further investigation.
We also predicted that the 22q11DS group would perform poorer on the social-cognitive tasks compared with the sibling control group. Our data suggests that social-cognitive deficits only occurred among the younger 22q11DS participants and only for more advanced second-order false-belief tasks and Strange Stories signifying that the acquisition of more complex social-cognitive tasks of false belief is suppressed in 22q11.2, but that this reflects a delay rather than a deficit. The influence of age on social-cognitive skills in children with 22q11DS may be related to a delay in the maturation of the frontal cortex among children with 22q11DS (Jablensky
2000). Van Amelsvoort and colleagues suggested that volumetric differences in the frontal lobes normalises somewhat in adults with 22q11DS Van Amelsvoort et al.
2001. Other factors such as gender and COMT phenotype has also been found to moderate frontal lobe morphology in 22q11DS and could potentially have an effect on our findings (Sands and Harrow
1995). However, our study did not identify any significant gender differences in the 22q11DS group. Future prospective studies will be designed to test this hypothesis further. In particular, it is important to include tasks that are largely independent from language to exclude the possibility that task performance is not simply attributable to language impairments. The tasks included in the current study included detailed narratives and both these, and the test-questions were grammatically complex (with the exception of the Smarties task). Indeed, our data indicate that performance on the false-belief tasks was related to grammatical competence as measured by the TROG. In addition, the pass or fail nature of the first- and second-order false-belief tasks produced ceiling effects amongst the older participants and the sibling controls, limiting our ability to detect the range of false-belief skills present in the two groups and possibly concealing any significant between-group differences. In order to take this into account, the Strange Stories were included in the study; however, due to the complex narratives, the performance of the participants with 22q11DS may not truly reflect their mentalising ability. It will also be important to control for other cognitive processes such as inhibition and working memory.
Finally, our data suggest that social competence in the 22q11DS group is strongly associated with emotional problems, reflecting anxious and depressive traits. It has been reported that poor premorbid social functioning is related to worse outcomes among people with both depression and psychotic disorders (Jablensky
2000; Sands and Harrow
1995) and associated with poor theory of mind skills (Wang et al.
2008). Hence, children with 22q11DS with poor social competence due to underlying problems with, e.g. the social-perceptual components of theory of mind may be at particularly high risk of later psychopathology. This highlights the need to properly assess the mechanisms underlying social competence among children with 22q11DS in order to be able to design evidence-based interventions aimed at increasing resilience in this group of children at high risk of developing mood and psychotic disorders. Taken together, lack of social competence and associated emotional problems are likely to have a very significant negative impact on the quality of life and long-term functioning of young people with 22q11DS (Kiley-Brabeck and Sobin
2006).
To conclude, the current study provides an important first step in identifying the social-perceptual and social-cognitive mechanisms associated with social competence in 22q11DS. We found that theory of mind skills are related to parent-rated social competence and emotional problems among children and adolescents with 22q11DS. Whilst people with 22q11DS may have general impairments in face processing, our data suggests that young children with 22q11DS may have a developmental delay in acquiring false-belief and mentalising skills, although this may be related to lower intellectual functioning and/or language ability. Finally, studies of the mechanisms underlying social dysfunction among children with 22q11DS will be useful in order to produce targeted management and remediation of social skills in 22q11DS.