Introduction
Attention deficit hyperactivity disorder (ADHD) is not only associated with symptoms of inattention, impulsivity, impaired inhibition and hyperactivity (American Psychiatric Association, APA
2013) but also associated with a range of (psycho-)social problems across the lifespan (Asherson et al.
2007; Kooij et al.
2010; Canu and Carlson
2007). Children with ADHD often demonstrate problematic peer functioning, including peer rejection and social isolation (De Boo and Prins
2007; Hinshaw
2002; Hoza et al.
2005), that may be a result of inappropriate social behavior such as frequently interrupting and not listening to others carefully (Guevremont and Dumas
1994). Several studies have, however, related the difficulties in social and interpersonal functioning in ADHD to traits of autism spectrum disorders (ASD) (Nijmeijer et al.
2008), a disorder that is characterized by specific impairments in empathy (Baron-Cohen and Wheelwright
2004; Wheelwright et al.
2006). Part of the childhood population of patients with ADHD have been shown to present problems in social cognition similar to those in ASD and have been described as ‘autistic-like’ (Matson et al.
2013; Luteijn et al.
2000; Mulligan et al.
2009; Santosh and Mijovic
2004; Buitelaar et al.
1999; Greene et al.
1996). Another explanation for social difficulties is the co-occurrence of callous unemotional traits in childhood ADHD. Behavior of children with ADHD may overlap considerably with oppositional defiant disorder or conduct disorder, which in turn aggravates social and emotional impairment (Fowler et al.
2009; Kahn et al.
2012; Nijmeijer et al.
2008).
Social problems of children with ADHD might be related to deficits in social cognition that are often reported in children with ADHD (Uekermann et al.
2010), which may directly or indirectly stem from executive functions deficits (Bora and Pantelis
2016; Hughes
1998; Geurts et al.
2010). Social cognition deficits encompass problems in perceiving emotions in others, for instance affective prosody, facial expression and body posture, which can be regarded as affective social cognition deficits (Uekermann et al.
2010; Maoz et al.
2014). Complex social cognition deficits have been reported in children with ADHD as well, such as problems in the ability to reason about the mental state of others (theory of mind, ToM). A recently published meta-analysis on social cognition in lifespan ADHD reported that adults with ADHD show diminished and less pronounced problems with social cognition than children with ADHD (Bora and Pantelis
2016). Especially ToM (an aspect of complex social cognition) appeared to improve significantly with age, with no evident ToM deficits in adulthood compared to childhood. Deficits in facial emotion recognition (an aspect of affective social cognition) on the other hand did not diminish over time (Bora and Pantelis
2016).
Although ADHD research generally focuses on the childhood period, it has become clear that ADHD can be a lifelong condition, with clinical as well as psychosocial impairments continuing into adulthood (Asherson et al.
2007; Kooij et al.
2010; Canu and Carlson
2007). Studies on adults with ADHD reported friendship problems and poorer social interactions (Young et al.
2003; Kooij et al.
2010), loneliness (Philipsen et al.
2009) as well as poorer intimate relationships and marital adjustment (Eakin et al.
2004). Furthermore, social deficits in adulthood were associated with mood instability and a lack of job and relationship continuity (Kooij et al.
2010). Adults with ADHD also reported experiencing social isolation and a lifetime burden of the disorder (e.g., due to lower educational achievement), and these accumulative problems in social, emotional and occupational areas were linked to a lower reported quality of life (Brod et al.
2012). Very few studies, however, explored performance on objective neuropsychological tests of social cognition in adults with ADHD. Some studies reported problems of adults with ADHD in facial emotion/affect processing and recognition (Ibanez et al.
2011; Marsh and Williams
2006; Miller et al.
2011), whereas others did not find deficits in measures for empathy and social cognition (Bora and Pantelis
2016; Gonzalez-Gadea et al.
2013). If adults with ADHD present with social cognitive deficits, this can have substantial consequences for their quality of social functioning and quality of life. The present study therefore focuses on the relation between social cognitive style, quality of friendships and ADHD symptoms in adults.
While the use of objective neuropsychological measures is valuable for estimating different aspects of social cognitive functions, they are time-consuming and many relevant aspects of our social life are not accessible via objective testing. This is particularly due to the low ecological validity of neuropsychological measures. Therefore, self-report questionnaires represent a valuable approach for the assessment of social cognitive functioning in everyday life. For instance, the quality of friendships can be measured by means of the Friendship Questionnaire (FQ), measuring the social engagement and the enjoyment and importance of friendships (Baron-Cohen and Wheelwright
2004). From the literature on ASD, particularly the Empathy Questionnaire (EQ) (Baron-Cohen and Wheelwright
2004) and the Systemizing Questionnaire (SQ) (Baron-Cohen and Wheelwright
2003) have been described as reliable and valid tools for assessing a person’s social cognitive style (see for a review: Groen et al.
2015). Based on the empathizing–systemizing theory (Baron-Cohen
2009), the EQ and SQ assess two complementary cognitive styles that allow people to efficiently process and react to complex social or non-social information. A person’s cognitive style can on the one hand be relatively empathizing and on the other hand relatively more systemizing, which is characterized by a drive to construct systems, to analyze its variables and to derive its underlying rules (Baron-Cohen
2002). Based on numerous studies, it can be stated that on average, females adopt a more empathizing cognitive style, whereas males adopt a more systemizing cognitive style (see for a review: Groen et al.
2015). A short version of the EQ has also become available, which additionally allows examination of different aspects of empathy by means of the subscale Emotional Empathy (EE) and subjectively experienced complex social cognitive functioning by means of the subscales Cognitive Empathy (CE) and Social Skills (SS) (Groen et al.
2015; Lawrence et al.
2004). Large sex differences have been demonstrated for EE, but only small sex differences for the CE and SS subscales (Groen et al.
2015). The EQ and SQ have been well validated in patients with ASD, who on average present with a strong systemizing and a weak or deficient empathizing cognitive style (Baron-Cohen and Wheelwright
2003; Baron-Cohen and Wheelwright
2004; Berthoz et al.
2008; Wakabayashi et al.
2007; Wheelwright et al.
2006). The extreme male brain (EMB) theory of autism consequently states that ASD can be considered as an extreme male cognitive style (Baron-Cohen
2002,
2009). Since ASD and ADHD show overlap with regard to social dysfunctions, the relation between symptoms of ADHD and the empathizing–systemizing cognitive style is addressed in the present study.
The present study
The present study was undertaken in the light of the sparse literature on social cognitive functioning in adult ADHD and the easy implementation and high informative value of the EQ-SQ. The aim was to explore the relationship between subjectively reported social cognitive style, quality of friendships and symptoms of ADHD in a typically developing population. Therefore, it was examined whether adults with no formal diagnosis of ADHD but who scored above thresholds in screening instruments indicating clinical levels of ADHD symptomatology (i.e., ‘subclincial ADHD’) differed from matched controls in their reports of social cognitive style. It was hypothesized that people with subclinical ADHD would present with a more ‘autistic-like’ cognitive profile, with lower scores on EQ and FQ and higher scores on SQ and brain type (i.e., a male profile). The subscale scores (EE, CE and SS) were explored in order to get more refined insight into the different aspects of social cognitive style. In order to draw conclusions on the impact of the cognitive profile on the quality of friendships, it was furthermore explored how reports of social cognitive functioning (in interaction with ADHD symptoms) in a community sample relate to self-reports of the quality of friendships.
Discussion
This exploratory study on the relation between subclinical ADHD symptoms and self-reported social cognitive functioning is one of the first studies examining self-reported social cognitive style in adult ADHD. We demonstrated that adults with a subclinical DSM-5 ADHD diagnosis reported reduced emotional empathy and a more systemizing cognitive style compared to the control group and that this pattern appeared to be independent of sex and ADHD subtype. The reduced emotional empathy score of the subclinical ADHD group was, however, still within the normal range compared to normative data (above the 10th percentile), which might be explained by the fact that not all of the participants of the subclinical ADHD group would meet the criteria of a formal diagnosis of ADHD. Therefore, this study ought to be replicated in a clinical sample of adult patients with a formal ADHD diagnosis. Moreover, additional measures assessing various domains of social cognition should be included. We do, however, speculate that reduced emotional empathy in people with subclinical ADHD is in accordance with studies showing problems with affective social cognition in patients with ADHD (Kooij et al.
2010; Canu and Carlson
2007). This refers to the basic perception of the emotions of others by adequately interpreting for instance prosody, body language and facial expression. The present study adds to the existing scarce knowledge by showing that even a non-clinical adult population with subclinical ADHD present with lower emotional empathy based on self-report questionnaires.
Analysis of the social cognitive predictors of the quality of friendships (as measured by the FQ) in our community sample revealed that the higher quality of friendships is best predicted by the female gender and by a stronger experience of emotional empathy. Female respondents with higher emotional empathy scores reported higher levels of social engagement, enjoyment and importance of friendships. The self-reported quality of friendships was not related to either ADHD symptoms or the combination of more ADHD symptoms and reduced self-reported social cognitive functioning. Even though our findings did not support a lower quality of friendships in subclinical ADHD, people with ADHD might be at higher risk of having a lower quality of friendships since the literature states that adults with clinical ADHD suffer from friendship problems, poorer social interactions and intimate relationships and loneliness (Young et al.
2003; Kooij et al.
2010; Philipsen et al.
2009; Eakin et al.
2004). Since emotional empathy is correlated with the quality of friendships, we speculate that problems in emotional empathy may (indirectly) affect the quality of friendships in groups with clinical levels of ADHD, despite not finding a direct link between the quality of friendships and subclinical ADHD symptoms in the present study. We suggest that future studies should further investigate this potential relation. When our finding that emotional empathy is an important predictor of self-reported quality of friendships in a community sample would hold true for patients with an ADHD diagnosis, it could be of high value for our knowledge of and treatment of adult ADHD, e.g., to assess and target emotional empathy for improving social outcomes of these patients.
The second finding at first glance appeared to confirm our expectation that people with subclinical ADHD report to have a more systemizing cognitive style compared to the control group. However, people with subclinical ADHD obtained similar scores on the SQ as matched controls. Therefore, the more systemizing cognitive style in this sample is primarily due to the reduced (emotional) empathy and does not represent a typical ASD-like profile, which typically shows overall reduced empathy scores and increased systemizing scores (Baron-Cohen and Wheelwright
2003; Baron-Cohen and Wheelwright
2004; Berthoz et al.
2008; Wakabayashi et al.
2007; Wheelwright et al.
2006). The present study points to a quite specific relation between ADHD symptoms and reduced emotional empathy. This profile therefore appears not to resemble ASD profiles, but rather shows overlap with psychopathic traits. Oliver et al. (
2016), for example, described that emotional empathy is not related to autistic traits but is associated with ‘cold-hearted,’ psychopathic traits. Unfortunately, we did not control for comorbidities and thus psychopathic traits in the present study, but these speculations point to the need of examining psychopathological comorbidities as well when examining social cognitive styles in patients with ADHD.
The social cognitive profile that we observed in our study in adults with subclinical ADHD (i.e., diminished emotional empathy but no differences in cognitive empathy) appears to be in line with previous studies on social cognitive functioning in adults with ADHD. Bora and Pantelis (
2016) stressed that adults with ADHD persistently show difficulties in affect recognition, but that ToM functioning normalizes into adulthood. Our finding that specifically emotional empathy was reduced in our adult sample is in line with these outcomes. It has been proposed that social cognition deficits are related to other neurocognitive deficits such as inattention, impulsivity and problems with executive functioning, rather than a separate developmental abnormality (Bora and Pantelis
2016). It could be the case that a broader range of neurocognitive functions improve with age and that higher-order functional neural organization is delayed, but that it is (partly) caught up in adulthood (Sripada et al.
2014). Furthermore, an improvement in social cognitive abilities into adulthood is in line with the ‘prefrontal recovery hypothesis’ as described by Halperin and Schulz (
2006), proposing that the remission of several higher-order cognitive functions in adult ADHD is related to the neural development of the prefrontal cortex.
Strengths and limitations
This study presented with several limitations. First, social cognitive style was merely measured by self-report questionnaires which rely on a realistic self-perception. It is possible that people with a subclinical diagnosis of ADHD over- or underestimate their empathic and social skills. For example, several studies have shown that children, adolescents and adults with ADHD show a ‘positive illusory bias,’ as defined by ‘a self-enhancing discrepancy between self-reports of competence and external indices of competence, such as ratings by other informants (e.g. teachers, parents, peers) or objective measures of performance’ (Emeh et al.
2015; Hoza et al.
2010; Prevatt et al.
2012; Volz-Sidiropoulou et al.
2016). However, more realistic and lower levels of self-reflections have also been found in adults with ADHD (Fuermaier et al.
2015). A great limitation of the use of self-report questionnaires in general is that the outcomes might be influenced by these types of biases. Future studies should therefore control for such a bias and/or confirm these findings by the use of objective neuropsychological tests and/or other-report questionnaires. A second limitation is that our study sample included participants with a subclinical diagnosis of ADHD and that the results therefore cannot be directly generalized to clinical samples of patients with ADHD. It is possible that the social cognitive profile of people with clinical ADHD diagnoses differs from the one found in this study. Based on previous studies on social cognition in ADHD, it is expected that in adults diagnosed with ADHD, the effects might be stronger and/or not limited to emotional empathy (Ibanez et al.
2011; Marsh and Williams
2006; Miller et al.
2011). A final limitation is that, based on the measures included in the present study, it remains unclear to what extent the reduced social empathy in the subclinical ADHD group might have been caused by other factors that have been related to reduced empathy, such as traits of autism or callousness.
A major strength of this study is that it is one of the very few studies examining social cognitive functioning in adults with (subclinical) ADHD. As social cognitive functions of adults with ADHD remains a relatively underexposed research field, our study contributes to the scarce existing knowledge on this topic. Furthermore, all participants were assessed with well-validated self-report questionnaires. The fact that we found lower emotional empathy scores in a subclinical ADHD group points to the relevance of replication and extension of this study in clinical ADHD groups.
Overall conclusion and future directions
Based on self-reported questionnaires in a subclinical, adult ADHD group, we found lower self-perceived emotional empathy scores, independent of sex and ADHD subtype. Self-perceived cognitive empathy and social skills were not diminished compared to the control group, which is in line with a recently published meta-analysis on social cognition in adult ADHD (Bora and Pantelis
2016). Since the emotional empathy score of the subclinical ADHD group was within the normal range and our sample consisted mainly of adults without a formal ADHD diagnosis, this study should be replicated and extended in adults with a clinical ADHD diagnosis. We furthermore suggest that future studies should apply neuropsychological tests rather than only self-report questionnaires as well as tests assessing not only various social cognitive domains but also other neuropsychological domains (e.g., attention, impulsivity, executive functions). The potential relation between emotional empathy and friendship quality in adults with ADHD should be assessed as well. Moreover, comorbidities to ADHD, such as ASD, should be taken into account, in order to find out whether reduced emotional empathy is specific for ADHD or whether it relates more strongly to other traits. Lastly, future studies should explore the relation between emotional empathy and emotion regulation in adults with ADHD. We cautiously suggest that reduced emotional empathy might be related to a broader phenomenon reported in ADHD, namely a reduced emotion regulation/emotional lability in patients with ADHD (Kooij et al.
2010). Emotional lability is reflected by irritable moods with changeable and volatile emotions and has been suggested to be a core dimension of ADHD (American Psychiatric Association
2000; Asherson
2005; Barkley and Fischer
2010; Reimherr et al.
2010; Skirrow et al.
2009; Skirrow and Asherson
2013; Skirrow et al.
2014). Emotional lability is thought to be related to problems in many areas of life (e.g., community activities, school/work, home, Barkley and Fischer
2010; Barkley and Murphy
2010; Skirrow and Asherson
2013) and may be related to reduced (emotional) empathy as well. Future studies should therefore extend our findings by thoroughly assessing a broader range of social cognitive and neurocognitive functions in adults with clinical ADHD.