Cognition & Emotion

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Sex differences in theory of mind: A male advantage on Happé's “cartoon” task Tamara A. Russell ab; Kate Tchanturia a; Qazi Rahman c; Ulrike Schmidt a a Institute of Psychiatry, Kings College London, London, UK b Macquarie Centre for Cognitive Science, Sydney, New South Wales, Australia c University of East London, London, UK First Published on: 13 June 2007 To cite this Article: Russell, Tamara A., Tchanturia, Kate, Rahman, Qazi and Schmidt, Ulrike (2007) 'Sex differences in theory of mind: A male advantage on Happé's “cartoon” task', Cognition & Emotion, 21:7, 1554 — 1564 To link to this article: DOI: 10.1080/02699930601117096 URL: http://dx.doi.org/10.1080/02699930601117096

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COGNITION AND EMOTION 2007, 21 (7), 1554 1564

BRIEF REPORT

Sex differences in theory of mind: A male advantage on Happe´’s ‘‘cartoon’’ task Tamara A. Russell Institute of Psychiatry, Kings College London, London, UK, and Macquarie Centre for Cognitive Science, Sydney, New South Wales, Australia

Kate Tchanturia Institute of Psychiatry, Kings College London, London, UK

Qazi Rahman University of East London, London, UK

Ulrike Schmidt Institute of Psychiatry, Kings College London, London, UK

It is a commonly held stereotype that women show superior performance on tests of social cognition such as face processing and theory of mind (ToM) compared to men. However, such purported differences have not been empirically tested. In this study 40 healthy men and 40 women matched for age and years of education completed a well-known experimental ToM test requiring the attribution of either physical or mental states (Happe´’s cartoon task). Men showed superior performance compared to women, with a medium effect size, on both the mental state and physical state cartoons. It is suggested that men may use a cognitive systemising strategy during these tasks. The results emphasise the task-specific nature of sex differences in social cognition and necessitate future work to elucidate individual differences at the interface of cognitive and affective processes.

Correspondence should be addressed to: Dr Tamara Russell, Section of Neuroscience and Emotion, PO Box 69, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, UK. E-mail: [email protected] # 2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business www.psypress.com/cogemotion DOI: 10.1080/02699930601117096

SEX AND THEORY OF MIND

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INTRODUCTION Sex differences in human cognitive abilities are well established. Males are typically found to excel on certain tests of mathematical reasoning and visuo-spatial processing, in particular on tests of mental rotation, while females excel on tests of verbal fluency, perceptual speed and spatial memory for object locations (Kimura, 1999; Voyer, Voyer, & Bryden, 1995). However, these differences are also task specific. For example, although males achieve higher scores on tests of mathematical aptitude, females do better on tests involving computation (Kimura, 1999). Additionally, females excel at one type of spatial memory task *the encoding and retrieval of object locations, while the oft-cited female superiority in ‘‘verbal abilities’’ is limited to tests of verbal fluency*the generation of words or categories to phonetic or semantic exemplars (Eals & Silverman, 1994; Kimura, 1999; Rahman, Wilson, & Abrahams, 2003). However, while these ‘‘cold cognitive’’ abilities have been dealt with at some length, the less-defined interaction between cognitive processes on the one hand, and emotional processes on the other, has received almost no attention in this and other individual differences literature. These unique processes, which we refer to as ‘‘hot cognitive’’ or ‘‘social-cognitive’’ abilities, are the focus of the current work. The presence of sex differences in ‘‘social-cognitive’’ functions (or ‘‘hot’’/affective cognition) is less well established. Nonetheless, several reviews and empirical studies suggest a female advantage in the recognition of facial affect (Campbell et al., 2002; Erwin et al., 1992; Hall, 1978; McClure, 2000; Thayer & Johnsen, 2000). A popular assumption regarding sex differences in social cognition is the notion that females are better than males at the attribution of mental states to others, and in appropriate affective responses to another’s affective state. The ability to make inferences about others’ mental states and the use of these inferences to predict and explain behaviours has been termed ‘‘theory of mind’’ (ToM). It underlies humans’ ability to engage in complex social interaction, and may be the product of an evolved, innately predisposed, and domain-specific cognitive mechanism (Leslie, 1995). Although environmental effects on the rate of ToM development have been reported, it is striking that children across different cultures and backgrounds develop insight into others’ mental states at approximately age four (Wellman & Lagattuta, 2000). Little is known about how ToM develops beyond childhood, although one study suggests that performance on ToM tasks may improve over the later adult years (Happe´, Winner, & Brownell, 1998). ToM is selectively impaired in the developmental disorder autism, while other aspects of cognition are relatively spared (Happe´, 1994). ToM is compromised in healthy adults following acquired damage to frontal regions or areas of the non-dominant hemisphere (Brownell, Griffin, Winner,


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Friedman, & Happe´, 2000; Happe´, Brownell, & Winner, 1999; Rowe, Bullock, Polkey, & Morris, 2001; Stuss, Gallup, & Alexander, 2001; Winner, Brownell, Happe´, Blum, & Pincus, 1998;) and impairments are also seen in the course of dementia (Gregory et al., 2002; Lough, Gregory, & Hodges, 2001). These findings concur with neuroimaging data implicating frontal and temporal regions in healthy adults attempting to ‘‘read’’ a character’s mind (Brunet, Sarfati, Hardy-Bayle, & Decety, 2000; Castelli, Frith, Happe´, & Frith, 2002; Fletcher et al., 1995; Gallagher et al., 2000). It should be noted, however, that the majority of these imaging studies have been conducted using exclusively male subjects and as such can really only provide information about the neural basis of ToM in the male brain. If we plan to make inferences about mental function and neural organisation relating to ToM on the basis of these results, it is important to ascertain if sex differences are present on these types of tasks. In his recent conceptualisation of the ‘‘extreme male brain theory of autism’’, Baron-Cohen (2002) has cited several lines of evidence for a female advantage on social cognitive tests, including the Reading the Mind in the Eyes test in adults (Baron-Cohen, Jolliffe, Mortimore, & Robertson, 1997), and the Faux Pas test (Baron-Cohen, O’Riordan, Stone, Jones, & Plaisted, 1999), false belief tasks (Happe´, 1995), perspective-taking and affective labelling (Dunn, Brown, Slomkowski, Tesla, & Youngblade, 1991) in children. Women also score higher on a psychometric construct called ‘‘empathising’’ (which involves identifying another’s thoughts and emotions and responding appropriately) compared to men who score higher on ‘‘systemising’’ (the analysis of rule-driven behaviour in systems; BaronCohen, Richler, Bisarya, Gurunathan, & Wheelwright, 2003). However, few of these studies explicitly explored male and female ability profiles outside of the context of experimental comparison with the performance of individuals with autism or Asperger’s syndrome on these tests. Moreover, there are almost no experimental studies on adults. It is uncertain whether sex differences in either ‘‘cold’’ or ‘‘hot’’ cognition stem from biological or psychosocial determinants, although recent interest has focused on the role of organisational and activational effects of gonadal hormones and variation in neural substrates underlying performance on these tasks (Baron-Cohen, 2002; Collaer & Hines, 1995; Frederiske, Lu, Aylward, Barta, & Pearlson,1999; Grimshaw, Sitarenios, & Finegan, 1995; Gur et al., 2000; Hines, 2000). Lutchmaya, Baron-Cohen, and Raggatt (2002) reported sex differences in social and non-social orienting responses as early as 12 months in human infants, suggesting that maturational factors on social cognition operate early in development. The question of sex differences in ToM is particularly pertinent with the increased attention in the psychiatric literature to social cognition. Several psychiatric disorders show sexually dimorphic clinical and developmental



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characteristics and ToM impairments. In schizophrenia attention has begun to turn to the profile of the social cognitive deficits seen in this group, given that it is these types of difficulties that are a good predictor of outcome (Penn, Combs, & Mohamed, 2001; Rocone et al., 2002). Although the prevalence of schizophrenia is equivalent across the sexes, there are differences in the age of onset, with male onset peaking between 20 to 24 years, while in females a smaller peak is seen at approximately 35 years of age (World Health Organization, 1979; Hafner, Maurer, Loffler, & ReicherRosslet, 1993). One effect of this sex dimorphic onset is that the majority of studies reported in the literature are based on predominantly male samples. Psychopathic personality disorder, attention deficit hyperactivity disorder and conduct disorder are also far more common in males and there are several reports of social cognitive deficits in these conditions (Blair, Jones, Clark, & Smith, 1997; Hughes, Dunn, & White, 1998; Biederman et al., 2002; cf. Richell et al., 2003; Widom, 1976). Also, and by far the clearest example, is autism, characterised by a high male prevalence and pervasive deficits in social cognition. As has already been alluded, Baron-Cohen (2002) has suggested that autism is evidenced by a very male-typical cognitive ability profile, including impaired ToM, communication and language processing, and facial affect processing, yet superior ‘‘systemising’’ abilities such as attention to detail, preference for constructional and vehicle toys, and islets of ability in factual and rule-based systems or academic subjects. Lastly, a recent study has suggested that females with anorexia nervosa (AN) have persevered ToM abilities, despite suggested similarities between AN and autism-spectrum disorders (Fisman, Steele, Short, Byrne, & Lavalee, 1996; Tchanturia et al., 2005). Clearly, further empirical data on normative sex differences (as well as other individual differences) in ToM is essential to furthering our understanding of impairments in social cognition in these clinical disorders. The aim of the present investigation was to utilise a well-established ToM task (Happe´’s cartoon task; Happe´ et al., 1999) in a sample of healthy adult males and females matched for age and years of education. The cartoon task comprises twelve cartoons, taken from newspapers; half of which require the understanding of a character’s mental state in order to get the joke and the other half requiring the understanding of physical states. It has been used previously to assess ToM in brain-damaged individuals (Happe´ et al., 1999), and with patients with schizophrenia; Russell, 2002). This represents the first study of its kind. The dearth of prior literature precludes directional hypothesising. However, on the basis of the extant literature for a female advantage in other domains of social cognition and the theoretical proposal that females should be adept at inference of mental states specifically (Baron-Cohen, 2002), it was predicted that


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females would perform better than males on the mental states (MS) component of the task. No sex differences were expected on the physical states (PS) component of the task, as these do not involve inferences about mental states.

METHOD Participants These were 40 females and 40 males matched for age and years of education (males mean age 34.3, SD /10.58, range /18 61; education level mean 13.8 years, SD/2.9, range 8 21; females mean age 30.35, SD/9.39, range 19 66; education level mean 14.32 years, SD/2.36, range 920). Participants were screened by a clinical psychologist (KT) and an experienced research psychologist (TR) to ensure no prior history of psychiatric or neurological morbidity, or learning disabilities.

Measures Happe´’s theory of mind cartoon task was used (Happe´ et al., 1999). Half the cartoons (6 stimuli) required the understanding of a physical state in order to ‘‘get’’ the joke (PS cartoons) and half required the understanding of a mental state (MS cartoons) in order to appreciate the joke. The cartoons were scored using guidelines provided by Happe´, with a score of 3 given for a full explanation; 2 for a partial explanation; 1 if the subject mentioned relevant details of the picture or gave a description only; and 0 if the subject mentioned only irrelevant aspects of the picture. A maximum score of 18 was obtainable in each condition (MS and PS). The cartoons were presented to each subject in a different order to minimise ordering and fatigue effects on performance.

Procedure Participants were seen individually in a session lasting approximately 30 minutes. Each participant was remunerated for his or her time. The Ethical (Research) Committee of the Institute of Psychiatry and Maudsley Hospital, London, approved all procedures.

Statistical analysis To determine whether the data were normally distributed, box-plots were computed for each variable. Group differences in age and years in education were analysed by the one-way analyses of variance (ANOVA) using the Statistical Package for the Social Sciences (SPSS) Version 10.0. Group



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differences in ToM performance were examined using General Linear Model (GLM) repeated measures ANOVA with Sex as the between-subjects factor and Cartoon Condition (MS or PS) as the within-subject repeated factor. Effect size was calculated as [mean 1 /mean 2]/[(SD 1/SD 2)/2], where 0.2 is a small effect, 0.5 a medium effect and 0.8 a large effect by standard criteria (Cohen, 1988). Alpha level was set at .05. Interrater reliability for scores on the cartoon task was assessed by two raters for 31 subjects (Kappa /.81).

RESULTS Participant characteristics There were no significant between-group difference in years of education, F(1, 78) /0.78, p/.37, nor age, F(1, 78) /3.11, p /.08.

ToM Performance Males had a mean score of 15.75 (SD /2.45, range 7 18) on the MS cartoons while females had a mean of 13.37 (SD /3.97, range 5 18). On the PS cartoons, the male mean was 15.95 (SD /1.79, range 918) while the female mean was 13.77 (SD /2.92, range 6 18). There was a main effect of sex, F(1, 78) /16.18, p /.001. Irrespective of cartoon type, male subjects were more accurate than female subjects on this task (male mean /15.85, SD/1.80; female mean /13.57, SD /3.08). There was no main effect of cartoon type, Wilks’ Lambda/.988, F(1, 78) /0.91, p /.34, nor any interaction between sex and cartoon type, Wilks’ Lambda / .99, F(1, 78) /0.10, p/.75. Effect sizes were calculated using the average score of MS and PS cartoons and resulted in an effect size (Cohen’s d) of 0.80. Calculating these separately for the MS and the PS cartoons revealed effect sizes of 0.53 and 0.86 respectively.

DISCUSSION The aim of the present study was to explore the notion that adult females would show better performance than adult males on a ToM task requiring mental state inferences in contrast to physical state inferences (for which no sex differences were predicted). Such tasks are a hallmark feature of psychological investigations at the interface of cognitive, affective and social processes. The results clearly show no support for this hypothesis. Rather, we found, for the first time, strong evidence that the opposite is true *that men performed better on our ToM task across both conditions compared to


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women. These findings are inconsistent with the suggestion that females (both girls and adults) should perform better on tasks designed to tap into the ability to make accurate inferences about the mental states of others (Baron-Cohen, 2002; Baron-Cohen et al., 1997, 1999, 2003; Dunn et al., 1991; Happe´, 1995). The effect size for the difference was in the medium to large range (Cohen, 1988). Given the size of the effect it is unlikely that this finding is spurious and makes this sex difference similar to the male advantage on the mental rotation test (Voyer et al., 1995). Moreover, the sample comprised healthy adults screened for any evidence of psychiatric or neurological morbidity, learning disabilities and matched on age and years of education. Thus, the finding appears somewhat robust. Other task details, such as the requirement to ‘‘get the joke’’, are unlikely to explain the findings as there are no clear sex differences in the appreciation of humour. The observation that males in the present study showed better inference of mental and physical states compared to women suggests a generalised male advantage for understanding the rules underlying inferential processes regardless of whether they involve animate (which includes systems that ‘‘mentalise’’, i.e., other humans) or inanimate objects. We propose that the male advantage observed here reflects a task-specific ‘‘systemising’’ strategy employed by men, ‘‘systemising’’ being a construct on which men are known to score particularly highly when evaluated psychometrically (Baron-Cohen et al., 2003). The ‘‘cartoon’’ task and, in fact, many standardised ToM measures require the understanding and prediction of law-governed behaviour. The cartoon task comprises an inductive process from which one formulates a rule about how the system, or in this case the inferential components of the task, works. This is comparable to many standardised decision-making tasks. In support of this explanation Reavis and Overman (2001) reported a robust male advantage on the Iowa Card Sorting task, a reward-related decision-making task. Performance on this task has previously been shown to depend on the integrity of the orbital prefrontal cortex, a region also implicated in ToM processing (Reavis & Overman, 2001). Thus, a common neural substrate underlying systemic decision-making and ToM may explain the male advantage. In monkeys, the orbital prefrontal region matures faster in males than in females and, consequently, infant male monkeys outperform infant females on another decision-making task, the object reversal task (see Reavis & Overman, 2001, for a review). The present findings also add to an increasing body of experimental work in another domain of social or ‘‘affective’’ cognition *facial emotion recognition*where mixed results regarding sex differences have been found (Campbell et al., 2002; Thayer & Johnsen, 2000; cf. Erwin et al., 1992). This brings into question the extent to which sex differences in social cognition can be generalised across measures used to test them. As with sex differences



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in facial emotion recognition, there are more consistent findings for a stable difference favouring female infants, children and adolescents (for facial emotion recognition see McClure, 2000; for ToM see Baron-Cohen et al., 1999; Dunn et al., 1991; Happe´, 1995; Hughes & Dunn, 1998). Thus it is possible that early sex differences do not extend into adulthood. This would make social cognitive ability similar to many aspects of verbal ability (aside from verbal fluency) in which girls mature faster than boys but the female advantage has dissipated by adulthood (Kimura, 1999; Lynn, 1994). Lastly, the male advantage demonstrated in the present study may be a reflection of the type of task used. While this test has been used by a number of studies to probe ToM, it is not clear how performance on this task relates to actual social functioning, which may include a more affective component. While it has yet to be empirically investigated, it may be the case that there are both ‘‘hot’’ and ‘‘cold’’ routes to solve ToM problems with the cartoon task probing a ‘‘cold’’ route. To test the prediction that females might be better on more affective ToM tasks (for example on Baron-Cohen’s Reading the Mind in the Eyes test) different types of ToM tasks should be used in the same sample of participants. In conclusion, we have shown, for the first time, a male advantage on one well-established test of ToM, Happe´’s cartoon task, and have suggested that this is due to a task-specific systemising strategy used by men. These data suggest sexual dimorphism in social abilities that involve both cognitive and affective components to their execution. These findings should alert investigators to the potential pitfalls of using tasks with several unspecified cognitive subcomponents and be wary of models of sex differences based on little more than stereotypical gender schemas. Future studies will have to employ a range of ToM tasks that incorporate the major dimensions of both ‘‘systemising’’ and ‘‘empathising’’ in order to explicate fully normative sex differences. Manuscript received 9 July Revised manuscript received 13 October Manuscript accepted 9 November First published online 13 June

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