Cognitive flexibility, central coherence and social ...

The World Journal of Biological Psychiatry, 2013; Early Online: 1–10

ORIGINAL INVESTIGATION

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Cognitive flexibility, central coherence and social emotional processing in males with an eating disorder

ELIZABETH GODDARD1, LAURA CARRAL-FERNÁNDEZ2, EMMA DENNENY3, IAIN C. CAMPBELL1 & JANET TREASURE1 1Section

of Eating Disorders, Department of Psychological Medicine, King’s College London, Institute of Psychiatry, London, UK, Disorders Unit, University Hospital Marqués de Valdecilla, Santander, Spain, and 3Guy’s, King’s and St. Thomas’ School of Medicine, London, UK

2Eating

Abstract Objectives. Females are more likely to develop an eating disorder (ED) than males. Studies of affected men may therefore inform models of risk and resilience to EDs. The aim of this study was to examine putative neurocognitive intermediate phenotypes of EDs in affected males. Methods. Cognitive flexibility, central coherence (global/detail processing), complex emotion recognition and social-threat sensitivity were investigated in men with EDs and healthy men. Measures of distress, perfectionism, and obsessive compulsivity were collected. Results. Men with EDs were more cognitively inflexible across tasks and had more difficulty integrating global information than healthy men. Unexpectedly, there were no group differences on a visuospatial task of detail processing or on social-emotional processing tasks. Men with EDs had higher scores on measures of distress, perfectionism and obsessive compulsivity than healthy men. Conclusions. Men with EDs share some of the intermediate cognitive phenotype present in women with EDs. Like their female counterparts, males with EDs show an inflexible, fragmented cognitive style. However, relative to healthy men, men with EDs do not have superior detail processing abilities, poor emotion recognition or increased sensitivity to social-threat. It is possible that gender differences in social-threat processing contribute to the female preponderance of EDs. Key words: Anorexia nervosa; Eating disorders; Gender; Neuropsychology; Cognitive flexibility

Introduction Females are 10 times more likely to develop an eating disorder (ED) than males (Jacobi et al. 2004). Therefore, studies of males with an ED may inform models of risk and resilience. Studies have shown that there are similarities in the clinical presentation of males and females with an ED (e.g., Carlat et al. 1997; BramonBosch et al. 2000; Crisp 2006; Strober et al. 2006; Button et al. 2008) but some differences have been reported, such as a focus on muscle building rather than thinness (Fernández-Aranda et al. 2004; Woodside et al. 2004; Darcy et al. 2011), higher rates of exercise (Anderson and Bulik 2004), less weight concerns (Fernández-Aranda et al. 2004; Halmi et al. 2005; Strober et al. 2006) and higher rates of homosexuality (Carlat et al. 1997). Men with EDs are reported to share elevated perfectionism and persistence with their

female counterparts but show less harm avoidance and cooperativeness (Fassino et al. 2001; Strober et al. 2006; Núñez-Navarro et al. 2011). The reported differences may be due to aetiological variations or may result from current nosology, measurement bias and gender roles (Anderson and Bulik 2004). Intermediate phenotypes are variables on the path of pathogenesis between genetic vulnerability and the overt symptoms of an illness (Gottesman and Gould 2003). They are not constrained by culture or nosological framework and so offer an opportunity to examine and define commonalities and differences in terms of underlying vulnerability to an illness. Candidate intermediate phenotypes for EDs are cognitive inflexibility (poor set shifting), weak central coherence, and social-emotional processing difficulties (e.g., Tchanturia et al. 2004a, 2010, 2011a; Harrison et al.

Correspondence: Elizabeth Goddard, Section of Eating Disorders, P059, The Basement, 103 Denmark Hill, London SE5 8AF, UK. Tel: 44 207 8485963. Fax: 44 207 8485967. E-mail: [email protected] (Received 8 March 2012 ; accepted 12 November 2012 ) ISSN 1562-2975 print/ISSN 1814-1412 online © 2013 Informa Healthcare DOI: 10.3109/15622975.2012.750014


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2011; Oldershaw et al. 2011; Roberts et al. 2012). Cognitive flexibility refers to the ability to switch between different cognitive response sets (Miyake et al. 2000). Cognitive inflexibility is marked in anorexia nervosa (AN) (Roberts et al. 2007; Tchanturia et al. 2011a) and is associated with childhood perfectionism, severity of ED rituals, and with a longer duration of illness (Tchanturia et al. 2004b). Weak central coherence is conceptualised as a perceptual bias with two core components: poor global integration and superior detail/local information processing (Happé and Frith 2006). Women with EDs exhibit both poor global integration and enhanced detail perception (Lopez et al. 2008a,b, 2009; Harrison et al. 2011; Roberts et al. 2012) and these are associated with lower BMI, greater eating concern (Harrison et al. 2011), and obsessive compulsive traits (Lopez et al. 2008a; Roberts et al. 2012). Lastly, a recent systematic review of socio-emotional processing in EDs found evidence of difficulties in recognising complex emotions and an attentional bias in the automatic processing of threatening social stimuli in females with AN (Oldershaw et al. 2011). In a large sample, Harrison et al. (2012) found that social emotional difficulties and cognitive style are independent areas of risk for women with EDs. Neurocognitive data from males with EDs are limited (but see Tchanturia et al. 2011b) and, to our knowledge, no studies investigating neurocognitive characteristics present in women with EDs have examined a male group. In terms of gender differences in the general population, most studies report no differences on common measures of cognitive flexibility (e.g., Wisconsin Card Sorting Test, Brixton Spatial Anticipation Test (Heaton et al. 1993; Burgess and Shallice 1997; Schuepbach et al. 2009) but for central coherence men show an advantage on visuospatial tasks of detail processing (e.g., Group Embedded Figures Test (Witkin 1950; Jolliffe and Baron-Cohen 1997) and a similar bias towards detail on the Rey Osterreith Complex Figure Task (Booth 2006) compared to women. Men also tend to be less accurate on a complex emotion recognition task than women (Baron-Cohen et al. 1997). Therefore, to test the presence of neuropsychological characteristics in males with an ED, this study compared their performance to that of healthy men. This study examined whether neuropsychological characteristics present in women with EDs can be extended to males with the illness, and to inform models of risk. It was hypothesised that, compared to healthy men, those with EDs would (1) be less cognitively flexible; (2) show weaker central coherence; (3) show poorer emotion recognition; (4) have increased sensitivity to social and social-threat stimuli; and (5) have greater obsessive and perfectionistic symptoms.

Method Participants Participants with an ED were recruited from King’s College London volunteer database and ED clinics in South London and Maudsley NHS Trust. The healthy comparison sample was recruited using fliers and a college email circular distributed to students at King’s College London. The study was approved by a National Health Service Research Ethics committee and King’s College London, Institute of Psychiatry, and was conducted in accordance with the Declaration of Helsinki 1964. All participants gave informed consent prior to study participation. Healthy participants were excluded if they had current or previous history of eating problems, were outside the normal Body Mass Index (BMI) range (19.6–26 kg/ m²) or had a history of or current psychiatric diagnosis. All participants were screened for serious head injury or neurological problems, severe comorbidity (e.g., psychosis) and severe learning disability. Men with EDs were diagnosed using the Eating Disorders Examination (Fairburn et al. 2008) or by a clinician according to DSM-IV criteria. Fourteen of the males with an ED had a diagnosis of AN, 2 bulimia nervosa (BN), and 13 eating disorder not otherwise specified (EDNOS). In this last group, 10 presented with anorexic symptoms (e.g., restrictive eating, low body weight above AN threshold, fear of weight gain, rule bound eating patterns) and two presented with bulimic symptoms (binge-purging behaviours below the frequency required for BN). One male diagnosed with EDNOS presented with excessive exercise and muscle building behaviours. All men were currently ill although three reported being in the recovery process but symptoms were not yet remitted. Measures Demographic data, BMI, duration of illness and level of clinical impairment (Clinical Impairment Assessment; CIA (Bohn and Fairburn 2008)) were measured. The National Adult Reading Test (NART) (Nelson 1982) was used to measure premorbid IQ. Self report measures. The Depression, Anxiety and Stress Scale (DASS; Lovibond and Lovibond 1995) is a 21-item scale measuring mood over the past week.The Obsessive Compulsive Inventory – Revised (OCI-R; Foa et al. 2002) was used to measure obsessive compulsive symptoms. Four subscales of the Frost Multidimensional Perfectionism Scale (FMPS; Frost et al. 1990) were selected to measure perfectionism (Concern Over Mistakes, Doubts Over Actions, Organisation, Personal Standards). The

Males with eating disorders


Childhood Retrospective Perfectionism Questionnaire (CHIRP; Southgate et al. 2008) is a 20-item self report measure which asks participants about the existence of perfectionistic and obsessive compulsive personality characteristics during childhood. All measures have sound psychometric properties. Cognitive flexibility. The Wisconsin Card Sorting Test (WCST; Heaton et al. 1993). This is a computerised test which asks participants to match a series of stimulus cards with one of four categories according to defined rules. Visual and auditory feedback is given after a card is placed. The sorting rule changes after 10 correct sorts, requiring people to switch strategy. Cognitive flexibility/inflexibility is assessed from the number of raw perseverative errors (PE). The number of categories completed (CC) is also recorded as an indication of general performance. The Trail Making Task (TMT; Reitan 1955). Using an alternative response paradigm, participants are asked to follow an 18-item alphabetical sequence with the computer mouse (Trail A; A-B-C, etc.) followed by an 18-item alphanumeric sequence (Trail B; 1-A-2-B-3-C, etc.). The cognitive flexibility outcomes are based on total time for Trail B and Trail B minus Trail A (B-A), to control for motor speed and attention. The Brixton Task (Burgess and Shallice 1997). This task requires participants to predict the position of a blue ball across 10 circles that move around a 5 2 grid according to a pattern. Participants are told that the pattern may change throughout the task. The number of incorrect predictions, excluding the first change in each sequence, is used as the measure of cognitive flexibility. Central coherence tasks. The Group Embedded Figures Test (GEFT; Witkin et al. 2002). Participants are presented with a booklet containing a series of 18 complex shapes and are asked to locate one of eight simple shapes. The simple shapes remain in view (Booth 2006). The timer starts when the participant begins their search and is stopped when they indicate they have found the simple shape. The participant then traces the lines of the shape on the complex shape. If they are incorrect they are allowed to continue searching and the timer is restarted; a false claim is recorded. Participants have a maximum of 60 s to identify the simple shape, after which a timed out error is recorded. The median response time is the outcome measure. This task has been validated as a measure of local/ global processing (Witkin et al. 2002). The Rey Osterreith Complex Figure (ROCF (Osterrieth 1944). Participants are given paper and coloured pencils and asked to copy the figure that is

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placed in their view as accurately as possible while being videoed. Pencils are proffered according to a set order as each element of the figure is completed. The degree of coherence in drawing strategy is scored according to Booth (2006) (also see Lopez et al. 2008a)): (a) Order Construction Index: the first six elements drawn by the participant are scored 0–4 per element according to their position in the figure; (b) Style Index: six specific elements are scored according to their continuity; (c) A Central Coherence Index (CCI 0–2) is obtained by the proportion of the order (score/3.3) and style indices (score/2). A lower score is indicative of weak central coherence. The intraclass coefficient for the CCI in this study was 0.98. The Fragmented Pictures Task (FPT; Snodgrass et al. 1987). This measures global integration abilities using a series of images that are presented on a computer, over eight screens from their most fragmented through to their most complete form. Each screen is presented for 5 s and begins with a practice trial followed by six test trials. Participants are asked say what they think the image is as soon as they can. The screen/level of fragmentation at which the participant correctly identifies the image is recorded. If participants identify the image incorrectly they are asked to try again and an incorrect response is recorded. Images include a cat (practice item), pig, kite, apple, chair, book, and an elephant and are always presented in that order. The sooner a participant is able to detect the image (i.e. lower scores) the more “global” their approach. Emotion recognition. The Reading the Mind in the Eyes (revised) (RME; Baron-Cohen et al. 2001). This task measures complex emotion recognition. Thirty-six photos are shown. Each depicts only the eye area of the face conveying an emotion. Participants are asked to choose from four words (all of similar emotional valence) the one that most closely matches what the person in the picture is thinking or feeling. Participants are able to use a definition hand-out if they are unsure of a word’s meaning. The task is not timed but the participant is asked to do it as quickly as possible. Seventeen of the photos are females and 19 are males. Social-threat attentional bias. The Pictorial Emotional Stroop Task (E-Stroop; Ashwin et al. 2006). This computerised task records response times using DMDX computer software. Three blocks of 48 stimuli (144 in total) are presented on the screen. Stimuli consist of male and female neutral and angry emotion faces (social stimuli) and chairs (non-social stimuli): one image is displayed per screen. Stimuli


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are presented randomly and are coloured red, yellow, blue or green. Participants are asked to say the colour of each picture and their response time is recorded by the computer programme. Participants have 4 s to respond to each picture but are told to respond as quickly and as accurately as possible. There are two breaks throughout the task and participants are asked to re-start the programme when ready. The primary variables of interest are response latencies (milliseconds) to (i) Male Angry Faces; (ii) Female Angry Faces; (iii) Male Neutral Faces; (iv) Female Neutral Faces; and (v) Non-Social stimuli (Chairs). Two attentional bias variables were also derived to indicate interference of salient stimuli: “social” attentional bias and “social-threat” attentional bias. The social attentional bias was computed by obtaining the mean of all four social conditions (i.e. male neutral, male angry, female neutral, female angry) and subtracting the mean of the non-social stimuli. Therefore positive response latencies represent an interference effect (longer response latencies for social stimuli relative to non-social stimuli). The “social-threat” attentional bias score was calculated by subtracting the mean of the neutral social stimuli (male and female) from the mean of the angry social stimuli (male and female). Therefore a positive attentional bias score indicates longer response latencies to the social-threat stimuli relative to the neutral social stimuli (interference). Statistical analyses Analyses were carried out using SPSS 15.0 for Windows. All variables were normally distributed across groups except outcomes from the WCST and the GEFT. To examine group differences between groups for all tasks (except E-Stroop), t-Tests were used for normally distributed data and Mann– Whitney U-tests for data that were not. Hochberg’s (1988) improved Bonferroni correction for multiple testing was used on main outcome measures. For the E-Stroop, a repeated measures ANOVA was employed to enable comparison between stimuli type. Stimuli Type was entered as the within-subjects factor (Female Angry, Female Neutral, Male Angry, Male Neutral, Non-Social) and Group (ED vs. HC) as the between-subjects factor. A MANOVA analysis was used to compare groups on the attentional bias scores. Cohen’s d effect sizes were calculated for normally distributed data (mean1 mean2/pooled standard deviation) and Rosenthal’s r was calculated for data that were not normally distributed and then converted to Cohen’s d score to enable comparisons across tasks (see Rosenthal 1991). Cohen’s d effect sizes are defined as small (d 0.2), medium (d 0.5) and large (d 0.8) (Cohen 1992). Partial eta-squared effect sizes are reported for ANOVA models.

Statistical power Men with EDs are a relatively rare population and therefore difficult to recruit. As a consequence, obtained power was calculated on completion of recruitment using G∗Power Version 3.0.8 (Faul 1992– 2006). Obtained power for the cognitive flexibility tasks was 0.82, 0.05, 0.90, 0.69 for the TMT Trail B, TMT B-A, the WCST PE and the Brixton respectively (Tchanturia et al. 2004a, 2011a, 2012; Roberts et al. 2010). For central coherence, obtained power was 0.83, 0.80, 0.92 for the ROCF CCI, the GEFT, and the FPT respectively based on a mixed ED sample (Harrison et al. 2011). Obtained power was 0.13 for RME and 0.49 for the E-Stroop social-threat bias for a mixed ED sample (Harrison et al. 2010).

Results Demographic data are presented in Table I and data from self report questionnaires in Table II. Men with EDs and healthy men were similar in age and IQ. The healthy males had more years of education than men with an ED (t(1,67) 2.6, P 0.05). The average duration of illness was 7.5 years (SD 7.0). Participants with an ED had a lower mean BMI than healthy men (t(65) 9.3, P 0.001). Males with an ED had a mean global clinical impairment score of 30.0 (SD 9.8) (a score of 30.2 is the norm for females with an ED; Welch et al. 2011). Thirty-five percent of males with an ED were on medication at the time of testing (mostly antidepressants). Men with EDs had higher levels of distress, obsessive compulsive symptoms, childhood obsessive compulsive personality traits, and perfectionism (most subscales) than healthy men. Group differences remained significant after applying Hochberg’s correction for multiple testing. Self report data were comparable to data reported for females with EDs for DASS (Harrison et al. 2011), CHIRP (Southgate et al. 2008; Roberts 2009) and OCI (Davies et al. 2009; Roberts 2009; Castro et al. 2010) (but note that higher scores for women with AN have been reported in other studies for OCI; Lopez et al. 2008a; Harrison et al. 2011). Scores for subscales of the FMPS were slightly lower in males with EDs than those reported for women with AN (Davies et al. 2009; Halmi et al. 2000). Neuropsychological tasks See Table III for descriptive and statistical data on neurocognitive and social-emotional task performance. Cognitive flexibility. Males with an ED were significantly more cognitively inflexible based on data

Males with eating disorders Table I. Demographic information of men with and without eating disorders. Mean (SD)


Age BMI Years Education IQ estimate

Ethnicity White British/other White Asian/Chinese Level of education No qualifications O-level/GSCE A level/NVQ/Diploma/BTEC University/postgraduate degree Employment status Full time/part time Student Unemployed/house-/retired/ sick leave Marital status Married/living together Single Divorced Living arrangements Alone With parents/other family With friends/partner

Male ED (N 29)

Male HC (N 42)

26.2 (8.2) 17.7 (2.2) 14.3 (2.4) 106.9 (9.4)

26.4 (7.2) 23.2 (2.5) 16.0 (2.8) 108.4 (8.2)

%

%

93 7

90 7

4 14 50 29

0 7 34 54

36 39 25

58 42 0

11 86 4

34 66 0

29 47 14

20 15 61

Central coherence. Men with EDs had weaker central coherence as measured by the ROCF (medium-large effects) and more difficulty with global integration measured by the FPT task (medium effect size). Unexpectedly, men with an ED were slower than healthy males on the GEFT (medium effect size). They had more timed out errors, consistent with more difficulties locating the simple shape, but did not differ on the number of false claims. Significant group differences on central coherence outcomes remained significant after applying Hochberg’s correction for multiple testing. On inspection of outliers using z scores, there were three outliers in the ED group on the GEFT (none in the HC group). The GEFT response time analysis was re-run excluding these three cases and the group difference reduced to trend level (P 0.096, d 0.1). Social emotional functioning Emotion recognition. Men with EDs did not differ significantly from healthy men on the RME task.

from the WCST, Brixton and Trail B of TMT (all medium effect sizes). Group differences did not reach statistical significance forTMTTrail B-A. Performance differences on the WCST and TMT Trail B remained significant after applying Hochberg’s correction for multiple testing.

Sensitivity to social-threat. On the E-Stroop task, there was no main effect for group (F1, 61 2.6, P 0.112, ηp² 0.04), stimuli type (F1, 61 0.5, P 725, ηp² 0.01) nor was the interaction for Group Stimuli Type significant (F1, 61 0.7, P 0.587, ηp² 0.01). There was no Stroop interference effect for social (F1, 61 1.3, P 0.258, ηp² 0.02) or social-threat stimuli (F1, 61 0.2 0.683, ηp² 0.003) in men with an ED. Effect of medication Within the ED group, there were no differences between groups with or without medication indicating that this did not have a confounding effect.

Table II. Personality and clinical characteristics (mood, obsessionality, perfectionism). Mean (SD) Male ED totala

DASS Depressiona Anxietya Stressa OCI FMPS – Organisation FMPS – Personal Standards FMPS – Concern Over Mistakes FMPS – Doubts Over Actions CHIRPa

5

52.1 (30.2) 18.5 (12.2) 12.3 (9.7) 21.4 (10.1) 21.4 (14.2) 15.8 (4.4) 20.1 (5.1) 20.2 (8.8) 9.8 (4.1) 8.0 (6.8)

Male HC 9.6 3.8 1.9 4.9 7.3 15.1 16.8 14.2 6.2 3.0

(9.7) (2.7) (2.7) (5.0) (5.7) (4.8) (4.9) (8.2) (2.8) (3.0)

t

U

P

d

81.5 108.5 129.5 68.5

0.001c

1.9 1.7 1.5 2.0 1.8 0.2 0.7 0.7 1.1 1.1

4.6b 0.60 2.5 2.8 4.1 177.5

0.001 0.001 0.001 0.001 0.554 0.014 0.007 0.001 0.001

SD, standard deviation; ED, eating disorders; HC, healthy control; DASS, Depression, Anxiety, and Stress Scale; OCI, Obsessive Compulsive Inventory; FMPS, Frost Multi Perfectionism Scale; CHIRP, Childhood Retrospective Perfectionism Questionnaire. aMedian and Interquartile range reported for non-parametric data. bEqual variances not assumed. cBold values indicate a statistically significant result.

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Table III. Neuropsychological task scores presented by group.


N

Cognitive flexibility Brixton WCST-PEa WCST-CCa TMT B TMT B-A Central coherence/detail processing REY Order REY Style Rey CCI GEFT Mediana GEFT TOa GEFT FCa FRAG Mean FRAG IRa Complex emotion recognition RME – total Social-threat attentional bias Non-Social (Chairs) Male Angry Male Neutral Female Angry Female Neutral Social attentional bias Social-threat attentional bias

M (SD)

ED

HC

Male ED

29 29 29 22 22

42 42 42 35 35

13.0 9.0 6.0 34.4 12.9

(7.9) (17.0) (2.8) (10.2) (9.8)

10.1 7.5 6.0 27.6 9.8

(4.4) (6.3) (0.0) (7.2) (6.4)

2.0 (69)

29 29 29 28 28 28 29 29

41 41 41 41 41 41 42 42

1.8 1.2 1.2 8.4 2.0 3.0 5.0 1.0

(0.6) (0.5) (0.4) (10.6) (1.8) (3.0) (0.6) (1.5)

2.1 1.5 1.4 6.4 1.0 2.0 4.7 1.0

(0.6) (0.4) (0.4) (3.7) (2.0) (2.0) (0.6) (3.3)

2.0 (68) 3.1 (68) 2.7 (68)

28

41

28 28 28 28 28 28 28

35 35 35 35 35 35 35

73.0 (12.0) 600.8 607.5 606.1 599.8 604.2 3.6 1.4

(130.8) (129.8) (146.3) (133.4) (142.6) (26.3) (33.1)

Male HC

74.5 (11.0) 661.2 658.9 645.6 654.8 662.5 5.8 2.8

(126.8) (130.4) (132.9) (129.1) (142.4) (36.3) (45.5)

t(df)

U

366.5 412.5 2.7 (34) 1.3 (32)

386.5 378.0 491.5 2.4 (69) 558.2 0.51 (67) – – – – – – –

– – – – – – –

P

d

0.046 0.004b 0.002b 0.010b 0.197

0.5 0.7 0.8 0.8 0.4

0.053 0.003b 0.009b 0.022b 0.019b 0.386 0.022b 0.541

0.5 ⴚ0.7 ⴚ0.5 0.6 0.6 0.2 0.5 0.1

0.610

0.1

– – – – – – –

0.5 0.4 0.3 0.4 0.4 0.3 0.1

N, sample size; M, mean; SD, standard deviation; ED, eating disorders; HC, healthy control; t, t-test statistic; U, Mann–Whitney U-test statistic; d, Cohen’s effect size; WCST, Wisconsin Card Sorting Test; PE, perseverative errors; CC, categories completed; CCI, Central Coherence Index; GEFT, Group Embedded Figures Test; TO, time out errors; FC, false claims incorrect response; FRAG, fragmented pictures; IR, incorrect responses. aMedian and interquartile range reported. bSignificant after Hochberg’s correction.

Effect of diagnosis

Discussion

Main analyses were re-run including only those who had a diagnosis of AN or EDNOS AN and were underweight (BMI 19.6 kg/m²; Hebebrand et al. 1996). Nineteen of the 29 men with an ED (66%) were included in the analyses. Results were similar to those previously reported where men were more cognitive inflexible across all tasks (d 0.5–1.4) and had a detailed, fragmented cognitive style measured by the ROCF CCI (d 0.7) and FPT (d 0.6). Groups did not differ significantly on the GEFT, RME nor E-Stroop.

This study examined cognitive flexibility, central coherence and emotional processing in males with an ED. Men with EDs were less cognitively flexible than healthy men (consistent with hypothesis 1). Men with EDs had difficulty integrating global information and tended to have a fragmented, detailed cognitive style; however, they did not perform better on a visuospatial task of detail processing (partial support for hypothesis 2). Men with EDs did not differ from healthy men in complex emotion recognition (i.e. hypothesis 3 was not supported). Men with EDs did not differ from healthy men in response to social or social-threat cues (i.e. hypothesis 4 was not supported). Lastly, men with EDs had more negative mood symptoms, higher perfectionism and higher childhood obsessive compulsive personality traits than healthy males (consistent with hypothesis 5).

Correlations between tasks Where multiple tasks were used to measure a cognitive domain, correlations were conducted between tasks (whole sample). For cognitive inflexibility, WCST PE was positively correlated with TMT Trail B (ρ 0.31, P 0.02) and Brixton errors (ρ 0.38, P 0.001) but not TMT B-A. Brixton was not correlated with either TMT variable. None of the central coherence tasks correlated with each other.

Cognitive flexibility Men with EDs were less cognitively flexible (medium sized effect) than healthy men across all tasks


Males with eating disorders examined. Similar sized group differences were found in males to those reported for females on the Brixton and Wisconsin Card Sorting Test (WCST; medium effect; Tchanturia et al. 2004a, 2011a, 2012; Roberts et al. 2010; Tenconi et al. 2010). Group differences on Trail Making Test (TMT) were comparable to results reported for women with AN and BN (e.g., Tchanturia et al. 2004a; Holliday et al. 2005; Roberts et al. 2010). In the general population, men and women are reported to perform similarly on tasks of cognitive flexibility (Heaton et al. 1993; Burgess and Shallice 1997). Therefore, cognitive inflexibility is present in both males and females with an ED and is unlikely to provide an explanation for the higher incidence of EDs in females. Central coherence Central coherence is not a single construct and is comprised of detail and global information processing. It has been reported that these two dimensions may be independent aspects of the central coherence construct (Happé and Booth 2008). This is supported in the present study by the lack of correlations between tasks used to measure central coherence. Similar findings have been reported in a female sample (Harrison et al. 2012). On the basis of data from the Rey Osterreith Complex Figure task (ROCF) and the Fragmented Pictures task (FPT), men with EDs have a more fragmented cognitive style and more difficulties with global integration than healthy men. The data are therefore consistent with previous observations in females, where medium to large effect sizes for the central coherence index (CCI) of the ROCF have been reported in women with AN and small to medium effects in those with BN (Lopez et al. 2008a,b; Tenconi et al. 2010; Harrison et al. 2011). Men with EDs had more difficulty integrating global information on the FPT than healthy men, although the effect was slightly smaller than reported for females with AN (Harrison et al. 2011). Therefore in ED, a fragmented style with difficulties integrating global information is consistent across genders and is unlikely to contribute to the gender difference in EDs. Data from the Group Embedded Figures Test (GEFT) were not consistent with the results from the other two tasks of central coherence. The men with EDs did not perform better on the GEFT (detail processing) than healthy men. This is surprising given that females with EDs are better at this task than healthy women (Lopez et al. 2008a; Harrison et al. 2011; Roberts et al. 2012). There is a gender difference on this task where men perform better than women (e.g., Jolliffe and Baron-Cohen 1997) and scores of females with EDs (Lopez et al. 2008a,b; Harrison et al. 2011;

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Roberts et al. 2012) are comparable to those of both healthy men and men with EDs included in this study. Our results indicate that men with EDs (unlike their female counterparts) do not have superior visuospatial detail processing (measured by the GEFT) compared to healthy men but, when outliers were removed, there was little evidence of impaired performance on this task. On the basis of these data, superior detail processing is associated with EDs in females but may not be associated with the illness in males. Emotion recognition Men with EDs did not differ from healthy men in their ability to recognise complex emotions (measured using the Reading the Mind in the Eyes task) (RME; BaronCohen et al. 2001). Scores were similar to those reported for healthy men (Baron-Cohen et al. 2001). This is in contrast to data showing that females with EDs, particularly AN, have difficulties on this task compared to healthy women (Kucharska-Pietura et al. 2004; Harrison et al. 2009, 2010; Russell et al. 2009; Oldershaw et al. 2010). Healthy women tend to be better at this task than healthy males (Baron-Cohen et al. 1997) and women with AN perform at a similar level to men (Russell et al. 2009; Harrison et al. 2010). In this context, it is of note that oestrogen has been reported to facilitate better emotion recognition (Pearson and Lewis 2005) and may contribute to the superior performance of healthy females on this task. Social-threat attentional bias No attentional biases for social or social-threat stimuli were seen in males with an ED relative to healthy males (pictorial E-Stroop task). In contrast, women with EDs have been reported to have a greater sensitivity to threat than healthy females (Stroop interference) (Harrison et al. 2010). Similar to the pattern observed in people with high trait anxiety (Mogg et al. 2007), women with EDs also have an attentional bias towards negative or critical faces and also have difficulty disengaging from these stimuli (Cardi et al. 2012). Our data are consistent with patterns observed in the general population where females have a greater sensitivity to threat and stress than males, particularly around puberty (Pigott 1999; Parker and Brotchie 2004). Theoretical models of the pathogenesis of EDs suggest that gender differences in stress response at puberty may contribute to the female preponderance of EDs (e.g., Connan et al. 2003; Kaye 2008). In addition, a gender difference in harm avoidance has been reported in EDs (men have lower levels than females) (Fassino et al. 2001; Fernández-Aranda et al. 2004; Núñez-Navarro et al. 2011), although the data on


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anxiety are inconclusive (Bramon-Bosch et al. 2000; Woodside et al. 2004; Strober et al. 2006). The findings from the present study are consistent with a fractionable model of non-social cognitive and social emotional risk to EDs (Steinglass et al. 2011; Harrison et al. 2012). It can be hypothesised that males and females with EDs share non-social cognitive risk factors (e.g., cognitive inflexibility and weak central coherence) but women have greater social emotional risk (specifically increased sensitivity to social threat). An increased sensitivity to negative social cues (e.g., anger, criticism) in women compared to men may contribute to the gender difference in EDs. Limitations and future research For some tasks, findings may be affected by reduced power to detect group differences. The diagnostic heterogeneity of the sample may have affected results, particularly in areas where differences between women with AN and BN are observed, for example, local processing and emotion recognition (e.g., Kenyon et al. 2012; Roberts et al. 2012). We chose tasks that had previously been used in studies of women with EDs: future work could use more sensitive tasks, particularly for social-emotional processing. It is also possible that other cognitive factors influenced performance on the GEFT, e.g., attention. This study requires further replication before more comprehensive interpretation, but future research could examine the interaction between neurocognitive and social-emotional features of EDs. This may provide new insights into the pathways by which these factors influence the pathogenesis and presentation of ED symptoms in both males and females. Future work should clarify the relationship between clinical features and neurocognitive style in EDs and assess whether gender differences in socialemotional characteristics affect the maintenance of the illness (Schmidt and Treasure 2006). Future studies could include men who have recovered from the illness and a direct comparison of men and women with EDs.

Conclusion Men with EDs share some, but not all, of the neuropsychological characteristics seen in women with EDs. Like women with AN, they show a rigid, fragmented cognitive style (associated with a longer duration of illness) and report high levels of distress and obsessive compulsive personality traits. However, relative to healthy men, males with the illness do not show superior visuospatial detail processing,

difficulties in emotion recognition or greater sensitivity to social-threat cues. In sum, men and women with EDs share aspects of a cognitive phenotype but differences in social-threat processing may contribute to the increased prevalence of EDs in females. Acknowledgments None. Statement of interest This article discusses independent research funded by the National Institute for Health Research (NIHR) under its Programme Grants for Applied Research scheme (RP-PG-0606-1043). EG was supported by research funded by NIHR under its Research for Patient Benefit programme (PBPG-0609-19025). The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. Laura Carral-Fernández was supported by a jointly funded research training fellowship from the Marqués de Valdecilla Public Foundation-Research Institute (FMV-IFIMAV, Santander, Spain) and the Institute of Health Carlos III (Spain). References Anderson CB, Bulik CM. 2004. Gender differences in compensatory behaviors, weight and shape salience, and drive for thinness. Eat Behav 5:1–11. Ashwin C, Wheelwright S, Baron-Cohen S. 2006. Attention bias to faces in Asperger Syndrome: A pictorial emotion Stroop study. Psychol Med 36:835–843. Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M. 1997. Another advanced test of theory of mind: Evidence from very high functioning adults with autism or Asperger Syndrome. J Child Psychol Psychiatry 38:813–822. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. 2001. The “reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger Syndrome or high-functioning autism. J Child Psychol Psychiatry 42: 241–251. Bohn K, Fairburn CG. 2008. Clinical impairment assessment questionnaire (CIA 3.0). In: Fairburn CG, ed. Cognitive behavior therapy for eating disorders. New York: Guildford Press. p. 315–317. Booth RDL. 2006. Local-global processing and cognitive style in autism spectrum disorder and typical development. [PhD thesis]. London: King’s College London, Institute of Psychiatry. 411 pp. Bramon-Bosch E, Troop NA, Treasure JL. 2000. Eating disorders in males: a comparison with female patients. Eur Eat Disord Rev 8:321–328. Burgess PW, Shallice T. 1997. The Hayling and Brixton tests. UK: Thames Valley Test Company Ltd. Button E, Aldridge S, Palmer R. 2008. Males assessed by a specialized adult eating disorders service: Patterns over time and comparisons with females. Int J Eat Disord 41:758–761.


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