Sociability is an umbrella term that encompasses a broad range of skills and behaviors that contribute to an individual’s social competence. Most research on the components of sociability within genetic syndromes has focused on autistic traits (Galéra et al.
2009; Mulder et al.
2017; Grados et al.
2017; Moss et al.
2013b; Hogan et al.
2017; Waite et al.
2015; Davenport et al.
2016). Many genetic syndromes have been shown to evidence heightened levels of autistic traits but also show unique profiles of sociability that are not captured fully by diagnostic measures of autism (Moss et al.
2013b,
2016). For example, children with Angelman syndrome often reach clinical cut off scores on assessments of autism (Trillingsgaard and Østergaard
2004; Williams
2010), yet are characterised by high rates of smiling and laugher (Horsler and Oliver
2006), and social approach behaviors (Heald et al.
2013). Identifying autistic characteristics in theses syndromes is essential in ensuring that individual’s receive appropriate services and support (Moss and Howlin
2009). However, other aspects of sociability also warrant investigation in order to tailor this support accordingly (Moss et al.
2013a,
b).
CdLS, FXS and RTS are neurodevelopmental disorders associated with mild to moderate disability (Oliver et al.
2008; Bennetto and Pennington
2002; Hennekam
2006; Kline et al.
2018), distinguishable by their behavioral phenotypes. Individuals with RTS exhibit greater social competence (Galéra et al.
2009; Hennekam
2006; Moss et al.
2016) in comparison to individuals with CdLS and FXS, whose behavior is characterised by social anxiety (Nelson et al.
2017; Richards et al.
2009; Hall and Venema
2017) and autistic traits (Oliver et al.
2011). Individuals with FXS and CdLS show differences in the profile and developmental trajectory of autism characteristics compared to those with non-syndromic autism (McDuffie et al.
2015; Wolff et al.
2012; Basile et al.
2007; Moss et al.
2008). For example, individuals with CdLS show greater communication difficulties (Moss et al.
2008) compared to non-syndromic autistic individuals, whilst children with FXS show greater impairments in pragmatic language (Martin et al.
2017). These groups show different patterns of change with chronological age. Carer reports indicate that older individuals with CdLS show lower levels of sociability (Moss et al.
2016), lower mood and greater insistence in sameness (Moss et al.
2017) but no changes in autistic traits (Basile et al.
2007; Nakanishi et al.
2012; Cochran et al.
2015). The association between autism and chronological age in FXS has been inconsistent within the literature (Cochran et al.
2015; O'Brien and Bevan
2011; Hatton et al.
2006) and changes with age have been anecdotally reported in individuals with RTS.
Discussion
In this study, observable behaviors indicative of social enjoyment, social motivation, social interaction skills and social discomfort were investigated in individuals with CdLS, FXS and RTS. The first aim was to compare the frequency and quality of these components of sociability between individuals with CdLS, FXS and RTS. Contrary to our hypothesis, behaviors indicative of sociability in RTS were not more frequent or of greater quality to those observed in those with CdLS and FXS, despite previous parent and anecdotal reports of social competence in this group. Rather, those with RTS demonstrated similarities in the quality and frequency of eye contact to those with FXS; a syndrome characterised by gaze aversion (Hall et al. 2009; Cohen et al.
1989). However, findings are consistent with studies that have directly observed operationalised social interaction skills and behaviors indicate subtle difficulties in those with RTS, such as understanding other’s gaze cues and social anxiety, despite showing apparently intact motivation to interact (Powis
2014; Crawford et al.
2019). Other syndromes associated with high levels of sociability such as Down syndrome and Williams syndrome (Moss et al.
2016) have also shown overlap of in specific characteristics of autism on the ADOS-2 (Hepburn et al.
2008; Klein-Tasman et al.
2009; Tordjman et al.
2012), emphasising the importance of direct observations of components of sociability in addition to the use of diagnostic autism measures.
Findings indicate that individuals with FXS and RTS may benefit from interventions aiming to improve the quality and frequency of their eye contact. Individuals with FXS may benefit from desensitisation therapy to help modulate anxiety associated with hyperarousal that is observed in this group, due to impaired neural processing and increased sensitivity when looking at other’s faces (Bruno et al.
2014). Similarly, poor eye contact observed in autistic individuals may be due to abnormally high activation in the subcortical face processing areas when looking at another’s face and gaze (Hadjikhani et al.
2017), suggesting that this may be an overlapping cause of poor eye contact across groups who show gaze aversion.
Individuals with CdLS showed more frequent and appropriate eye contact than individuals with FXS and RTS. Previous literature investigating eye contact in individuals with CdLS has revealed mixed findings (Moss et al.
2012; Sarimski
2007). These mixed findings potentially reflect the genetic heterogeneity and subsequently the variability in the quality of social interaction skills and behaviors previously reported in this syndrome (Gillis et al.
2004; Moss et al.
2017; Nakanishi et al.
2012; Sarimski
2007). Eye contact in those with CdLS is also influenced differently across environments. Whereas individuals with CdLS show more eye contact than those with Down syndrome during a social performance task (Nelson et al.
2017), they also show more fleeting eye contact in comparison to individuals with Cri du Chat syndrome during conditions when the examiner maintained high levels of verbal attention and kept within close proximity to the participant (Richards et al.
2009). These findings highlight that eye contact may vary greatly in those with CdLS dependent upon the social context and type of causal mutation and certain individuals with CdLS may also benefit from intervention aiming to improve eye contact within specific environments.
Individuals with CdLS likely showed more person focused attention than individuals with FXS due to (1) more frequent eye contact with the examiner in individuals with CdLS (indicated by higher scores on the
eye contact item) and (2) the extreme gaze aversion demonstrated in those with FXS. However, no differences were found in focus of attention between those with RTS or FXS. Despite individuals with RTS showing poor eye contact, their relatively intact social interest (Moss et al.
2016; Galéra et al.
2009; Verhoeven et al.
2010) may have compensated for the effect of poor eye contact and led to more person focused attention in RTS compared to individuals with FXS.
The second aim of the study was to explore the association between the frequency and quality of components of sociability in CdLS, FXS and RTS and the severity of autism characteristics. Different patterns of association were observed between groups. Individuals with CdLS who showed more motivation for adult engagement scored lower on autism characteristics. In FXS, those who showed more social anxiety scored higher on an autism measure. Lower levels of positive emotional affect and reduced quality of eye contact were associated with higher scores on a measure of autism in individuals with RTS.
Whilst it is unsurprising that some components of sociability are associated with the severity of autistic characteristics, it is interesting that the pattern of associations between groups differ. The nature of these association may be mediated by other variables at the neurobiological or cognitive levels that may or may not be the same as those with non-syndromic autism. Both boys with FXS and boys with non-syndromic autism have a heightened likelihood of reaching cut-off scores for social anxiety disorder compared to the typically developing population (Maddox and White
2015). However, direct comparisons reveal differences in the profile of social anxiety in those with FXS and non-syndromic autism, suggesting that the aetiological mechanism driving social anxiety in these groups differ (Scherr et al.
2017). Overall, findings indicate that future work should investigate the refined differences across individuals with syndrome groups and autism on the underlying mechanisms of components of sociability, even when groups show superficial similarities. Outlining these differences may be essential in guiding whether or not individuals with specific genetic syndromes would benefit from autism specific interventions.
The final aim was to explore the association between components of sociability and chronological age in CdLS, FXS and RTS. Older individuals with CdLS showed more frequent and better-quality social communication skills, more positive emotional affect, less avoidance of social interaction
but more signs of social anxiety. The finding of increased social anxiety in CdLS with chronological age is consistent with other reported areas of change with age including lower levels of sociability (Moss et al.
2016), lower mood and greater insistence in sameness (Moss et al.
2017), and greater impairment in executive function. One suggestion is that the cumulative effects of impaired repair and oxidative stress over time resultant from the syndrome related genetic abnormality (Gimigliano et al.
2012) may account for such changes.
Similarly, older participants with FXS showed more frequent and better social communication skills and social responses and more social anxiety, corresponding to previous reports of higher rates of social phobia (Cordeiro et al.
2011) in older individuals with FXS. This increase in social anxiety with age may be associated with neurobiological changes specific to FXS. Individuals with FXS produce low levels of Fragile X Mental Retardation Protein (FMRP), which regulates expression of proteins involved in synapse formation and function (Tang et al.
2015; Olmos-Serrano et al.
2010) and neural migration (Moro et al.
2006). Subsequently, FMR1 knockout mice show structural deficits in dendritic spines in adulthood but not at 4 weeks old (Kazdoba et al.
2014; Galvez and Greenough
2005) and preliminary evidence has identified Pukinje cell loss or misplacement in the cerebellum in older adults with FXS (Sabaratnam
2000; Greco et al.
2011). Whilst cerebellum damage primarily leads to movement disorders (Choi
2016; Grimaldi
2013), of which older men with FXS are at heightened risk of (Utari et al.
2010), it has also been associated with social anxiety (Caulfield and Servatius
2013; Phillips et al.
2015; Moreno-Rius
2018).
Alternatively, in both CdLS and FXS, the fact that some components of sociability
improve with chronological age while others demonstrate decline is of interest and suggests that the reported increase in social anxiety may not reflect a general downward trend in behaviors and skills and might be more likely to indicate limited resources to cope with increased cognitive and social demands that individuals face as they become older (Cochran et al.
2019). Interventions for social anxiety may be critical as individuals with CdLS and FXS get older.
Individuals with RTS did not show any associations between age and components of sociability, even on items expected to be associated with cognitive ability (i.e.
Social Communication Skills and
Social Responsiveness). The lack of development of these skills in RTS may be due to mutations that act on the cyclic adenosine monophosphate response element binding protein (CREBBP) (Petrij et al.
1995; Park et al.
2014). These mutations have been linked to short- and long-term learning and memory impairments in mice models (Chen et al.
2010) and individuals with RTS show working memory span deficits relative to their overall mental age (Waite et al. 2016). Working memory span is associated with vocabulary acquisition (Newbury et al.
2015; Ellis and Sinclair
1996; Gathercole and Baddeley
1993; Gupta and MacWhinney
1997) and speech and sentence production (Wiseheart and Altmann
2018; Adams
1996; Acheson and MacDonald
2009). These skills are likely to be important for building more complex social communication skills and social responses and may contribute to the lack of development of these components of sociability in those with RTS.
The cross-sectional nature of the study limits the extent to which we can infer causal direction of associations between sociability, autism characteristics and chronological age. Whilst participants took part in both verbal and non-verbal cognitive assessments, non-verbal mental age was the variable that was available for the greatest number of participants. These findings may reflect the uneven profiles of cognitive abilities within these syndromes (Mulder et al.
2017; Grados et al.
2017; Stevens et al.
1990,
2011; Fung et al.
2012; Lorusso et al.
2007). Whilst these data were missing for only a few participants, it is important to take these into account when interpreting the evidence of comparability of level of ability between syndromes included in analyses.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.