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Research Article                                                                                                                                        Open Access

## How do Girls with Low Functioning Autism Compare to Boys with Autism and Typically Developing Girls with regard to Behavior, Cognition, and Psychopathology?

Camilla Nguyen, M.Sc 1 , Angelica Ronald, PhD 2

1 University of Hertfordshire, Hatfield, UK 2 Centre for Brain and Cognitive Development, Department of Psychological Sciences, University of London, UK

- *Corresponding author:

a.ronald@bbk.ac.uk

## Abstract

Background :  The female autism spectrum disorder (ASD) phenotype is currently underresearched. Girls with ASD may differ from boys with ASD, yet few studies have tested this hypothesis, particularly among low functioning individuals. This study compared girls and boys with predominantly low functioning ASD and typically developing girls during middle and late childhood across autism symptoms, cognition, sensory overresponsivity, and co-occurring psychopathology.

Methods :  Three  mental-age-matched  groups  were  compared:  girls  with  ASD  (N  =  27),  boys  with  ASD  (N  =  27),  and typically developing girls (N = 17). Their ages ranged from 7 to 19 years old. The majority of individuals in the ASD sample had an intelligence quotient of less than 70. Participants were assessed on standard social cognition and attention to detail tasks. Parents completed behavior questionnaires.

Results :  Mean  levels  of  autism  symptoms  were  not  significantly  different  for  boys  and  girls  with  ASD,  and  they  were significantly higher than those of typically developing girls. There were some weak trends for boys with ASD to show more compulsive behavior, inattention/hyperactivity and taste sensory overresponsivity than girls with ASD, but differences were not significant after controlling for multiple comparisons. The Block Design task, assessing attention to detail, showed a significant sex difference, with boys with ASD outperforming both girls with ASD and typically developing girls.

Conclusions: Predominantly low functioning girls with ASD differed from typically developing girls but did not differ from boys with ASD with regard to their levels of autism symptoms, sensory overresponsivity, or co-occurring psychopathology. These data feed into debates about whether ASD assessment tools require sex-specific criteria and to what degree treatment should be tailored to the sex of the individual.

Keywords: autism spectrum disorders, sex differences, low functioning, behavior, cognition.

## Introduction

Females with autism spectrum disorders

Both males and females can develop autism spectrum  disorders  (ASD).  However,  ASD  are  up to five  times  more  common  among  males  as compared with females (1). This relationship between sex and ASD has consistently been reported. As a result, in research, females are often underrepresented as compared with males, and they are  rarely  studied  separately  from  males.  A  recent report revealed that only 14.2% of all participants in autism intervention research published in four prominent autism journals between 2009 and 2012

were  female  (2).  For  these  reasons,  our  current understanding of ASD is heavily based on the male rather than the female ASD phenotype. Symptoms in  females  appear  to  be  associated  with  greater etiologic risk (3,4).

Sex differences in core autistic symptoms

Symptoms  of  ASD  include  repetitive  stereotyped behaviors (RSBs) and social-communicative impairments  (5,6).  Over  the  past  three  decades, researchers have examined differences and similarities between males and females related to the core impairments associated with ASD. Twenty-two research studies of this topic were recently included in  a  systematic  review;  meta-analysis  revealed  sex differences for RSBs but not for socialcommunicative  impairments  (7).  Overall,  females with  ASD  displayed  fewer  RSBs  than  males  with ASD starting at the age of 6 years. An independent study  with  the  largest  sample  size  to  date  (N  = 2418) also replicated the finding of fewer restricted interests  among  females  with  ASD  as  compared with males with ASD (8). These differences in the manifestations of RSBs between males and females with ASD may have implications for the diagnosis of  ASD  (9).  Current  evidence  suggests  that,  as compared  with  male,  the  diagnosis  of  ASD  in females  tends  to  be  delayed  (10)  or  missed  by clinicians (11).

These  findings  are  mainly  based  on  studies  of higher  functioning  samples  with  ASD.  Only  two studies  (12,13)  in  the  systematic  review  by  Van Wijngaarden-Cremers and colleagues (7) specifically focused on children with low functioning ASD (i.e., those  with  an  intelligence  quotient  [IQ]  of  <70). Neither  of  these  studies  compared  girls  and  boys with ASD with regard to their levels of RSBs. Given the heterogeneity of ASD, it is important to investigate whether ASD and RSBs in particular are manifested differently in lower functioning samples. Consistent with the findings from the meta-analysis, Lord and colleagues (14) also reported a sex difference  in  RSBs  among  a  lower  functioning sample (mean non-verbal IQ = 40.43; aged 3 to 8 years),  with  girls  with  ASD  (N  =  91)  engaging  in fewer  RSBs  than  boys  with  ASD  (N  =  382). However,  this  sex  difference  finding  is  limited  to lower functioning preschoolers and young children with  ASD  only.  Currently,  there  are  no  studies addressing  whether  males  and  females  with  low functioning  ASD  differ  with  regard  to  RSBs  after they are 8 years old.

## Sex differences in sensory sensitivities and psychopathology in autism samples

Associated autistic features such as sensory sensitivities and psychopathology are also not uncommon among individuals with ASD. Given the high figures of individuals with ASD who experience problems with either sensory sensitivities (95%; 15) or psychopathology (54-70%; 16), there is a  growing  interest  in  understanding  whether  males and  females  with  ASD  differ  in  these  areas.  As compared with males with ASD, females with ASD demonstrate more problems with internalizing symptoms, including emotional problems and depression  (9,17);  however,  they  have  equivalent levels of sensory sensitivities (9). These findings are based on children and adolescents between the ages of 3 and 18 years with high functioning ASD. Thus, these findings may not be generalizable to individuals with low functioning ASD.

## Sex differences in cognition in autism samples

Studies investigating differences in cognition between males and females with  ASD  remain scarce, and, again, they have only focused on higher functioning individuals. Individuals with ASD often show  excellent  attention  to  detail  (ATTD;  18,19). More recently, using the Block Design (BD) task to test  for  ATTD,  two  independent  studies  reported male superiority for ATTD. Koyama and colleagues (20)  reported  that  females  with  high  functioning ASD  (N  =  26;  mean  age  =  8.2  years)  performed worse on the BD  task than males with high functioning ASD (N = 116; mean age = 9.0 years). This finding was also replicated by Bölte and colleagues  (21)  for  a  group  of  high  functioning adolescent males (N = 35; mean age = 14.0 years) and females (N = 21; mean age = 14.3 years) with ASD.  However,  no  sex  difference  in  ATTD  was found in an adult group of high functioning males (N = 32) and females (N = 32) with ASD on the Embedded  Figures  Test  (22).  In  terms  of  social cognition, the research literature suggests that male and  female  adults  with  high  functioning  ASD  do not show significant differences with regard to their ability  to  understand  other  people's  mental  states (16,22,23). In sum, these findings suggest that there are  sex  differences  in  ATTD  but  not  in  social cognition  that  are  observable  among  adolescents and adults with high functioning ASD.

Although 70% of children with ASD have IQs of less  than  70  (24),  few  studies  have  attempted  to address sex differences among  low  functioning individuals  with  ASD.  Sex  differences  found  for high  functioning  individuals  with  ASD  cannot  be assumed to be the same as those of lower functioning individuals with ASD as a result of the substantial  heterogeneity  among  individuals  with this condition. Furthermore, the existing (yet limited) research literature involving lower functioning children with ASD was conducted more than three decades ago (12-14). Those findings may also  not  be  generalizable  to  today's  children  and adolescents with lower functioning ASD as a result of  methodologic differences in terms of diagnostic criteria and choice of assessment tools. Lastly, there is a lack of research directly comparing females with and without ASD to understand the unique experience  of  being  a  female  with  ASD.  From  a developmental  perspective,  females  with  ASD  go through  similar social and  behavioral stages as typically developing (TD) females due to the nature of being female (25). As compared with  TD females,  females  with  high  functioning  ASD  have equivalent  levels  of  ATTD  (21)  but  significantly greater RSB impairment (11), internalizing problems (17), and social skills deficits (26). To fully capture the  uniqueness  and  implications  of  being  a  female with ASD, it is necessary to compare females with ASD directly to TD females and not only to boys with ASD (17,27).

To  the  best  of  our  knowledge,  this  is  the  first study to predominantly focus on lower functioning children  and  adolescents  with  ASD  and  to  make comparisons between girls and boys with ASD and TD  girls  across  autism  symptoms,  cognition,  and co-occurring psychopathology, including sensory overresponsivity  (SOR). In line  with  past  research, we predicted that girls with ASD would differ from TD girls but not from boys with ASD with regard to social-communicative impairments, sensory problems,  and  social  cognition.  Consistent  with previous  research  findings,  we  hypothesized  that girls  with  ASD  would  have  lower  levels  of  RSB impairment than  boys  with  ASD  but  higher  levels of RSB impairment than TD girls. Furthermore, we also predicted that girls with ASD would have more internalizing problems than boys with ASD and TD girls. Lastly, we predicted that girls with ASD would perform equivalent to TD girls but worse than boys with ASD in the area of ATTD.

## Methods

## Participants

Seventy-one children between 7 and 19 years old ( M = 13.67 years; SD = 2.90 years; 27 boys with ASD, 27 girls with ASD, and 17 TD girls) took part in this study. Children with ASD were recruited from five registered  special  educational  needs  (SEN)  schools in London, United Kingdom. Three of the schools catered  to  children  with  ASD  only,  whereas  the other two schools catered to children with ASD as well  as  to  those  with  intellectual  disabilities  and emotional, behavioral, and physical difficulties. Children attending  SEN  schools  in  the  United Kingdom each have personalized documented statutory  statements  specifying  their  diagnoses  and specific educational needs as set out by each child's Local Education Agency  (28). Confirmation of participants' ASD diagnoses were sought from SEN schools  and  parent  reports.  Schools  had  to  first verify  that  the  child  was  on  the  SEN  register  and then confirm that the child's SEN  statement specified a diagnosis of ASD. In addition, parents of children with ASD had to provide full information about the diagnoses of their children, the place and age of diagnosis, and the name of the clinician who made  the  diagnosis.  The  TD  girls  were  recruited from a local primary school in London and had no diagnosis of ASD or learning difficulties as confirmed  by  school  and  parent  reports.  Schools were asked to send out a questionnaire package to parents  of  the  71  participating  children.  A  total  of 63  parent  questionnaire  packages  from  parents  of 20 girls with ASD, 26 boys with ASD, and 17 TD girls  were  returned  (88.7%).  An  independent t -test showed  that  differences  in  chronological  age  were not  present  for  children  with  ASD  whose  parents completed the questionnaire as compared  with those whose did not complete the questionnaire ( t = 1.47; df = 52; p = .15). The University of Birkbeck's Department of Psychological Science and the National Autistic Society's Research Ethics Committee  both  granted  ethical  approval  for  this study.  Each  family  received  an  incentive  of  £5  to complete this study.  Written  consent  from  parents was obtained for all participants in this study.

## Measures

The  administration  of  assessments  was  conducted by  one  researcher  (CN)  who  had  been  trained  in Applied  Behavior  Analysis  (ABA)  and  who  had  3 years  of  experience  working  with  children  with ASD.

IQ  assessment. Depending  on  their  age,  participants were  administered  either  the  Wechsler  Intelligence Scale  for  Children-Revised  (WISC-R;  29)  or  the Wechsler Abbreviated Scale of Intelligence (WASI; 30).

Core and associated autistic features . The Social Communication Questionnaire (SCQ; 31), the Repetitive Behavior Scale-Revised (RBS-R; 32), the Sensory Over-Responsivity Inventory (SensOR Inventory;  33)  and  the  Strengths  and  Difficulties Questionnaire  (SDQ;  34)  were  employed.  These instruments were selected because they have excellent  psychometric  properties  for  quantifying core  and  associated  autistic  features  and  because they  had  been  previously  employed  for similar  age and participant groups.

Theory  of  mind. Participants  who  demonstrated  a mental  age  of  4  years  or  more  were  asked  to perform  the  Sally-Ann  false  belief  task  (35).  Participants  with  mental  ages  of  less  than  4  years  were given  spontaneous  play  (36,37)  and  joint  attention tasks (38), because these are more suitable for lower functioning  children  and  adolescents  with  ASD. Specific  instructions  and  scoring  information  for these tasks are described in Appendix A.

Attention to detail .  Each  participant  was  given  a version  of  either  the  WISC-R  (29)  or  the  WASI's (30) BD task.

## Procedures

Each  participant  was  tested  individually  in  a  quiet room  at  the  participant's  school  and  accompanied by  a  school  staff  member.  Testing  was  done  over one to two sessions and was limited to a maximum of  40  minutes  per  session.  The  total  testing  time varied  between  20  minutes  and  1  hour  and  20 minutes,  depending  on  the  participant's  abilities. The testing was performed in this order: IQ assessment,  including  the  BD,  followed  by  either spontaneous  play  and  joint  attention  or  the  SallyAnn false belief task, depending on the participant's mental age. Parents completed the questionnaires in their own time.

## Statistical analysis

If data were missing for more than half of the items on a scale, then the total score was coded as missing and excluded from the analysis.

The Kolmogorov-Smirnov tests revealed that the SCQ,  RBS-R,  SensOR  Inventory,  and  SDQ  scales were  not  normally  distributed  (all p values  were <.05).  As  such,  univariate  nonparametric  KruskalWallis  tests  (rather  than  multivariate  analyses  of variance) were conducted to compare  the raw scores  of  the  three  groups  (girls  with  ASD,  boys with  ASD,  and  TD  girls)  for  the  SCQ,  RBS-R, SensOR Inventory, and SDQ scales. As a result of the  increased  risk  of  family-wise  error  in  multiple comparisons, adjusted p-values using the Bonferroni  correction  were  applied  to  the  number of  tests  within  a  scale.  Significant  findings  were followed  up  with  Mann-Whitney  post  hoc  tests  to examine two specific planned contrasts on the SCQ, RBS-R, SensOR Inventory and SDQ scales: 1) girls with ASD versus boys with ASD; and 2) girls with ASD versus TD girls. A second Bonferroni correction was applied to the two planned contrasts to  control  for  type  1  errors  across  all  tests  within each scale.

A one-way analysis of variance was conducted to examine  children's  performance  on  the  BD  test. Significant findings were  followed up with the Tukey  honest  significant  difference  post-hoc  test. The  Sally-Ann  false  belief  task  was  recorded  as either  'Passing'  or  'Not  passing' for  the  children in  the  three  groups.  A  2*3  Pearson's  chi-squared test  with  an  exact  significance  test  was  employed, because  three  cells  had  an  expected  count  of  less than 5.  Independent t -tests were  conducted  to compare  girls  and  boys  with  ASD  with  regard  to joint  attention  and  spontaneous  play  measures.  A Bonferroni  correction  was  employed  within  each measure.

## Results

Table  1  lists  participant  descriptives.  We  obtained full IQ scores from 17 girls and 17 boys with ASD, and their results did not demonstrate any significant differences  ( t [32]  =  -1.69; p =  .10; r =  0.08).  We found that 71% of the children with ASD were low functioning (IQ of <70) and that the high functioning individuals (IQ of ≥70) had IQ scores between  70  and  100.  There  was  no  significant difference  in  IQ  distribution  (i.e.,  low  vs.  high) between girls and boys with ASD ( χ 2 [1, N = 34] = 2.27; p = .13). The 17 girls and 17 boys with ASD from  whom  we  obtained  full IQ  scores were matched  for  mean  mental  age  with  17  TD  girls. Mental  age  was  cal-culated  by  using  the  formula method (IQ = Mental age/Chronological age) (39), because  participants'  IQs  and  chronological  ages were  already  known  to  the  researchers.  Although the TD girls had lower chronological ages than the participants with ASD, no significant difference was found for mean mental age across the three groups ( H [2] = 0.47; p = .80).

As  a result of their  noncompliance,  minimal verbal, or nonverbal communication, 10 girls and 10 boys  with  ASD  were  classified  as  untested  on  the WISC-R or WASI. These participants were suspected of having IQs of less than 45. They were still  included  in  the  study  because  the  aim  was  to examine differences and similarities across the three groups  with  regard  to  core  and  associated  autistic features and thinking styles in children and adolescents  with  and  without  ASD,  irrespective  of IQ  performance  and  language  level.  An  independent t -test showed that the chronological ages of the children for which IQ could not be measured was significantly  higher  than  those  of  other  children from whom IQ could be obtained ( t =  3.39;  df  = 69; p = .001).

TABLE 1. Participant characteristics

|                          | Girls with ASD (N = 17)   | Boys with ASD (N = 17)   | TD girls (N = 17)   |
|--------------------------|---------------------------|--------------------------|---------------------|
| Chronological Age*       |                           |                          |                     |
| Mean (SD)                | 15.07 (2.70)              | 14.21 (2.25)             | 10.30 (.64)         |
| Range                    | 7.20-18.90                | 7.70-19.10               | 9.10-11.70          |
| Full IQ                  |                           |                          |                     |
| Mean (SD)                | 63.00 (8.10)              | 68.88 (11.85)            | 91.88 (11.60)       |
| Proportion low IQ (<70)  | 82.40%                    | 58.80%                   | 0%                  |
| Proportion high IQ (≥70) | 17.60%                    | 41.20%                   | 100%                |
| Mental Age               |                           |                          |                     |
| Median                   | 9.44                      | 9.83                     | 9.39                |
| Range                    | 4.26-13.05                | 5.27-12.98               | 8.43-11.52          |

ASD, Autism spectrum disorder; TD, typically developing.

*Chronological age data available for N = 71 (27 girls with ASD, 27 boys with ASD, 17 TD girls).

Table  2  presents  the  mean  differences  between groups on the SCQ, RBS-R, SensOR Inventory, and SDQ scales. Separate Kruskal Wallis tests showed a significant  main  effect  of  group  on  all  four  SCQ subscales  ( H (2)  =  32.78-37.30,  all p s  <  .001,  after employing Bonferroni adjusted p -level  of  .012),  on all  six  subscales  of  RBS-R  ( H (2)  =  12.54-31.60,  all p s  <  .001,  after  employing  Bonferroni  adjusted p -level  of  .008),  on  total,  tactile,  visual,  taste  and auditory  SOR ( H (2)  =  10.39-19.21,  all ps <  0.006)

but  not  for  smell  SOR  ( H (2)  =  1.27, p =  .53)  or movement  SOR  ( H (2) =  7.81, p =  .02), after Bonferroni  correction  (.0071),  and  on  all  six  SDQ

scales  ( H (2)  =  11.07-32.42,  all p s  <  .001,  after Bonferroni correction (.008).

TABLE 2. Descriptive statistics and Mann-Whitney tests of parent-reported Social Communication Questionnaire, Repetitive Behavior Scale-Revised, Strengths and Difficulties Questionnaire, and the Sensory Over-Responsivity Inventory scales by group

| Scale                                | ASD Girls (N=20) ----------    | ASD Boys (N=26) ----------     | TD Girls (N=17) ----------   | Statistics a ----------------------------   | Statistics a ----------------------------   | ES b ----------   | Statistics c   | ----------------------------   | ES d      |
|--------------------------------------|--------------------------------|--------------------------------|------------------------------|---------------------------------------------|---------------------------------------------|-------------------|----------------|--------------------------------|-----------|
|                                      | Median (range)                 | Median                         | Median (range)               | U                                           | p                                           | r                 | U              | p                              | ------- r |
| Social Communication Questionnaire   |                                | (range)                        |                              |                                             |                                             |                   |                |                                |           |
| Total                                | 29.00                          | 29.00                          | 4.00 (0-7.00)                | 259.50                                      | .99                                         | -.001             | 0              | <.001*                         | -.85      |
| Social interaction                   | (16.00-34.00) 12.00            | (16-36.00) 12.00               | 0                            | 323.50                                      | .54                                         | -.09              | 0              | <.001*                         | -.86      |
| Communication                        | (4.00-15.00) 8.50 (4.00-12.00) | (6.00-15.00) 8.50 (5.00-13.00) | (0-3.00) 1.00 (0-3.00)       | 240.50                                      | .66                                         | -.06              | 0              | <.001*                         | -.86      |
| Repetitive stereotyped behaviors     | 5.50 (1.00-8.00)               | 6.00 (3.00-6.00)               | 0 (0-4.00)                   | 241.50                                      | .68                                         | -.06              | 17.00          | <.001*                         | -.78      |
| Repetitive Behavior Scale-Revised    |                                |                                |                              |                                             |                                             |                   |                |                                |           |
| Total                                | 22.50                          | 31.50                          | 1.00                         | 207.50                                      | .24                                         | -.17              | 11.50          | <.001**                        | -.80      |
| Stereotypic                          | (7.00-67.009 4.00              | (2.00-87.00) 7.50              | (0-16.00) 0                  | 187.00                                      | .10                                         | -.24              | 48.50          | <.001**                        | -.64      |
| Self-injurious                       | (0-18.00) 5.00 (0-18.00)       | (0-24.00) 1.50 (0-11.00)       | (0-6.00) 0 (0-2.00)          | 216.40                                      | .33                                         | -.14              | 59.00          | <.001**                        | -.58      |
| Compulsive behavior                  | 2.50 (0-15.00)                 | 4.00 (0-14.00)                 | 0 (0-5.00)                   | 161.50                                      | .03                                         | -.32              | 112.00         | <.001**                        | -.31      |
| Ritualistic/sameness                 | 7.50 (0-30.00)                 | 12.50 (0-32.00)                | 0 (0-8.00)                   | 228.00                                      | .48                                         | -.10              | 26.50          | <.001**                        | -.73      |
| Restricted interests                 | 2.00 (0-7.00)                  | 3.00 (0-9.00)                  | 0 (0-1.00)                   | 207.50                                      | .24                                         | -.17              | 29.50          | <.001**                        | -.76      |
| Strengths and Difficulties           |                                |                                |                              |                                             |                                             |                   |                |                                |           |
| Questionnaire Total problem          | 17.00 (9.00-29.00)             | 21 (6.00-32.00)                | 6.00 (1.00-13.00)            | 194.50                                      | .15                                         | -.21              | 6.00           | <.001**                        | -.82      |
| Emotional symptoms                   | 4.00 (2.00-9.00)               | 5.00 (0-10.00)                 | 2.00 (0-5.00)                | 231.00                                      | .52                                         | -.10              | 72.00          | .002**                         | -.50      |
| Conduct problems                     | 1.50 (0-7.00)                  | 2.00 (0-8.00)                  | 0 (0-2.00)                   | 212.50                                      | .29                                         | -.16              | 79.00          | .004**                         | -.47      |
| Hyperactivity/inattenti on           | 5.00 (1.00-10.00)              | 7.50 (2.00-10.00)              | 2.00 (0-7.00)                | 159.00                                      | .02                                         | -.33              | 54.50          | <.001**                        | -.59      |
| Peer problems                        | 6.00 (2.00-10.00)              | 6.00 (2.00-8.00)               | 1.00 (0-5.00)                | 234.50                                      | .57                                         | -.08              | 11.00          | <.001**                        | -.80      |
| Prosocial behavior                   | 3.50 (0-10.00)                 | 4.50 (2.00-10.00)              | 9.00 (2.00-10.00)            | 222.50                                      | .40                                         | -.12              | 44.00          | <.001**                        | -.64      |
| Sensory Over- Responsivity Inventory |                                |                                |                              |                                             |                                             |                   |                |                                |           |
| Total                                | 9.50                           | 15.00 (0-55.00)                | 3.00 (0-10.00)               | 221.00                                      | .39                                         | -.13              | 47.50          | .001***                        | -.62      |
| Tactile                              | (1.00-42.00) 4.50 (0-18.00)    | 6.00 (0-27.00)                 | 2.00 (0-6.00)                | 226.50                                      | .46                                         | -.11              | 63.00          | .001***                        | -.54      |
| Visual                               | 0 (0-3.00)                     | 1.50 (0-4.00)                  | 0 (0-1.00)                   | 188.00                                      | .09                                         | -.25              | 132.00         | .16                            | -.23      |
| Smell                                | 0                              | 0                              | 0                            | -                                           | -                                           | -                 | -              | -                              | -         |
| Taste                                | (0-3.00) 1.00                  | (0-5.00) 3.00                  | (0-2.00) 0                   | 146.00                                      | .01                                         | -.38              | 103.50         | 0.27                           | -.36      |
|                                      | (0-4.00) 3.00                  | (0-9.00) 3.00                  | (0-1.00) 0                   | 238.50                                      | .63                                         | -.07              | 60.00          | <.001**                        | -.57      |
| Auditory                             | (0-18.00)                      | (0-18.00)                      | (0-2.00)                     |                                             |                                             |                   |                | *                              |           |
| Movement                             | .50 (0-5.00)                   | .50 (0-6.00)                   | 0 (0-2.00)                   | -                                           | -                                           | -                 | -              | -                              | -         |

Follow-up Mann-Whitney tests on the SCQ results using an adjusted p value of <.006 showed that girls with ASD were not significantly different from boys with ASD (all p values were >.006). Girls with ASD also had significantly greater autistic impairment as compared with TD girls (all p values were <.001) on all subscales.

Follow-up  Mann-Whitney  tests  on  the  RBS-R results  showed  no  significant  differences  between boys  and  girls  with  ASD  on  any  of  the  subscales, although  there  was  a  trend  for  boys  with  ASD  to show more compulsive behavior ( p = .03) than girls with  ASD,  but  the  difference  was  not  significant after a second Bonferroni-adjusted p value  of  .004. As expected, girls with ASD had significantly more repetitive, restricted, and stereotyped behaviors than TD girls (all p values were <.001).

Follow-up  Mann-Whitney  tests  on  the  SensOR Inventory  results  showed  that  boys  and  girls  with ASD did not differ on any subscales when using a second  adjusted p value  of  .0036.  However,  there was  a  trend  for  boys  having  greater  symptoms  of SOR on  the  taste  scale  than  girls  with  ASD  ( p = .01).  Girls  with  ASD  showed greater symptoms of SOR than TD girls on the total, tactile, and auditory scales  ( p = .001) but not on other SOR subscales. Table 3 shows that more than three fourths of both girls and boys with ASD reached the clinical criteria for  SOR  as  compared  with  only  1  of  the  17  TD girls.  The  relationship  between  the  type  of  group and  the  tendency  toward  SOR  was  significant  (χ2 [2, N = 63] = 26.87; p < .001).

Follow-up Mann-Whitney tests on the  SDQ results  showed  a  trend  toward  boys  with  ASD having greater levels of hyperactivity and inattention than girls with ASD ( p = .02). However, this trend, along  with  other  adaption  and  psychopathology problems,  did  not  reach  significance  with  the  new adjusted p value  of  .004.  Girls  with  ASD  showed fewer  prosocial  behaviors  ( p <  .001)  and  greater adaption and psychopathology problems (all p values  were  <.004)  as  compared  with  TD  girls. Table  3  shows  that  none  of  the  TD  girls  scored within the abnormal range for psychopathology. On the contrary, nearly three quarters of the boys with ASD (73.1%) and more than half of the girls with ASD (53.0%) scored within the clinical criteria  for abnormal psychopathology. The relationship between the type of group and adaption and psychopathology was significant (χ2 [2, N = 63] = 37.84; p < .001).

The majority of TD girls passed the Sally-Ann test (94.10%), followed by boys with ASD (82.40%) and girls  with  ASD  (64.70%).  However,  no  significant differences  were  found  between  the  groups  with regard to passing the Sally-Ann false belief test (χ2 [2, N = 51] = 4.73; exact p = .12).

TABLE  3. Proportion  of  sample  falling  above  cutoffs  on  the  sensory  overresponsivity and adaption and psychopathology scales*

|                  | ASD Girls (N = 20) ----- N (%)   | ASD Boys (N = 26) ----- N (%)   | TD Girls (N = 17) ----- N (%)   |
|------------------|----------------------------------|---------------------------------|---------------------------------|
| SensOR Inventory |                                  |                                 |                                 |
| Present SOR      | 16 (80.0)                        | 20 (76.9)                       | 1 (5.9)                         |
| Absent SOR       | 4 (20.0)                         | 6 (23.1)                        | 16 (94.1)                       |
| SDQ              |                                  |                                 |                                 |
| Normal           | 4 (20.0)                         | 4 (15.4)                        | 17 (100.0)                      |
| Borderline       | 5 (25.0)                         | 3 (11.5)                        | -                               |
| Abnormal         | 11 (55.0)                        | 19 (73.1)                       | -                               |

ASD, Autism  spectrum  disorder; SDQ, Strengths  and  Difficulties  Questionnaire; SensOR Inventory, Sensory Over-Responsivity Inventory; SOR, sensory overresponsivity; TD, typically developing.

*The cutoff point for SOR was the presence of four or more tactile or auditory items on the SensOR Inventory (see ref. 33). Scores on the SDQ were used to divide the participants  into  normal  (0  to  13),  borderline  (14  to  16),  and  abnormal  (17  to  40) categories (see ref. 34).

Joint attention and spontaneous play were assessed in 20 children with ASD (10 boys and 10 girls)  who had mental ages of less than four years. Joint  attention  data  for  one  participant  (one  girl) and spontaneous play data for two participants (one boy  and  one  girl) were  excluded  from  further analyses in response to noncompliance during testing. As shown in Table 4, separate independent t -tests involving an adjusted pvalue of .017 demonstrated no differences between girls and boys with ASD in terms of engagement in eye contact in the blocking, teasing, and joint attention categories. Further separate independent t -tests for spontaneous play also indicated that girls and boys with  ASD  did  not  differ  from  each  other  in  the production  of  functional,  ordering,  sensorimotor, pretend,  ambiguous  play,  and  no  play  categories after Bonferroni correction (.008).

TABLE 4. Mean scores, standard deviations, and inferential statistics for joint attention and spontaneous play by group*

| Measure           | ASD Girls (N = 9) --------------   | ASD Boys (N = 10) ---------------   | Statistics ---------------------   | Statistics ---------------------   | Effect Size ----------   |
|-------------------|------------------------------------|-------------------------------------|------------------------------------|------------------------------------|--------------------------|
|                   | M(SD)                              | M(SD)                               | t                                  | p                                  | r                        |
| Joint Attention   |                                    |                                     |                                    |                                    |                          |
| Blocking          | 1.88 (1.36)                        | 2.20 (1.14)                         | -.54                               | .60                                | .15                      |
| Teasing           | 2.33 (1.00)                        | 2.40 (1.17)                         | -.13                               | .90                                | .03                      |
| Active toy        | 2.67 (1.00)                        | 3.00 (.94)                          | -.75                               | .47                                | .18                      |
| Spontaneous Play† |                                    |                                     |                                    |                                    |                          |
| Functional        | 2.67 (3.16)                        | 2.00 (2.24)                         | -.52                               | .61                                | .13                      |
| Ordering          | 0.61 (.60)                         | 1.00 (.79)                          | -1.18                              | .26                                | .28                      |
| Sensorimotor      | 11.33 (5.31)                       | 13.44 (5.17)                        | -.83                               | .42                                | .20                      |
| Pretend           | 0.89 (1.00)                        | 1.00 (1.25)                         | -.16                               | .88                                | .04                      |
| Ambiguous         | 1.39 (.50)                         | 1.24 (.56)                          | 1.96                               | .07                                | .44                      |
| No play           | 3.11 (4.34)                        | 1.94 (4.44)                         | .56                                | .58                                | .14                      |

ASD, Autism  spectrum  disorder; M, mean, r =  Pearson's r coefficient; SD, standard deviation.

*Maximum score for blocking, teasing, and active toy was four respectively. On spontaneous play, maximum score for each category of play was 20 with high scores indicating better social cognition performance.

†Spontaneous play data were available for 9 girls with ASD and 9 boys with ASD.

Figure  1  shows  the  mean  scores  by  group  for  the BD task. A one-way independent ANOVA showed Mean Block Design Scaled Score

12.00~

10.00-

4.00-

0.00- that there was a significant main effect of group on the  BD  task  ( F [2,  48]  =  5.52; p =  .007; Further  analysis  involving  the  Tukey  honest  signi ficant  difference  post-hoc  test  showed  that  boys with ASD performed significantly better on the BD task  than  girls  with  ASD  ( p <  .05),  whereas  girls with ASD and TD girls did not differ with regard to the performance of this task ( p > .05). effect of group on =  .007; r =  .43). Further  analysis  involving  the  Tukey  honest  signihoc  test  showed  that  boys with ASD performed significantly better on the BD .05),  whereas  girls with ASD and TD girls did not differ with regard to > .05).

Group

FIGURE 1. Error  bar  chart  of  the  mean  scaled  scores  on  the  Block Design by group. Equal sample size in each of the three groups (N =17). Error  bar  chart  of  the  mean  scaled  scores  on  the  Block Design by group. Equal sample size in each of the three groups (N

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## Discussion

The existing research on sex differences in ASD has reported subtle differences across behavioral symptoms  and  cognitive  domains.  In  the  present study, we examined the female ASD phenotype by comparing  girls  and  boys  with  predominantly  low functioning ASD during childhood and adolescence to  TD girls.  In  addition  to  noting  a  sex  difference with regard to ATTD among individuals with ASD, our findings indicated that girls with predominantly low  functioning  ASD  were  similar  to  boys  with predominantly low functioning ASD and that they were,  as  expected,  significantly  different  from  TD girls. The existing research on sex differences in ASD has reported subtle differences across behavioral symptoms  and  cognitive  domains.  In  the  present study, we examined the female ASD phenotype by comparing  girls  and  boys  with  predominantly  low during childhood and adolescence to  TD girls.  In  addition  to  noting  a  sex  difference with regard to ATTD among individuals with ASD, our findings indicated that girls with predominantly low  functioning  ASD  were  similar  to  boys  with oning ASD and that they were,  as  expected,  significantly  different  from  TD

The similarities between girls and boys with ASD with regard to RSBs are surprising considering that a body of research suggests that females with ASD show fewer impairments in RSBs than do boys with ASD  (7-9,14).  Although  a  similar  sex  difference trend in compulsive behavior emerged in the present  study  ( p =  .03),  the  difference  did  not become significant after multiple testing comparisons.  Although  the  current  study  focused predominantly  on  a  lower  functioning  sample,  the research evidence from a prior meta-analysis (7) was based on studies of higher functioning samples with ASD only. Taking into account of the heterogeneity of individuals with ASD, different patterns of RSB The similarities between girls and boys with ASD with regard to RSBs are surprising considering that a body of research suggests that females with ASD in RSBs than do boys with Although  a  similar  sex  difference trend in compulsive behavior emerged in the =  .03),  the  difference  did  not become significant after multiple testing comparisons.  Although  the  current  study  focused predominantly  on  a  lower  functioning  sample,  the analysis (7) was based on studies of higher functioning samples with ASD only. Taking into account of the heterogeneity of individuals with ASD, different patterns of RSBs between males and females with ASD may be more observable in the high functioning ASD population. It might be the case that higher functioning females with ASD  have  managed  to  develop  skills to camouflage their behavioral impairments (40). Lower functioning females with ASD, on the other hand, may lack the capacity to develop such skills. Among  younger  children with low functioning ASD, Lord and colleagues (14) reported more RSBs among boys than girls. Unlike in the present study, those researchers recruited a larger sample size with a  very  narrow  age  range;  they  used  direct  obser vation rather than parent reports, and they did not control for multiple  testing  comparisons.  Thus, sampling  and  methodologic  differences  between current study and that of Lord a be responsible for the inconsistent findings involving  lower  functioning  individuals  with  ASD. Overall, our findings support the notion that lower functioning  boys  and  girls  with  ASD  have  similar presentations of the core symptoms of  ASD (12,13,17,41,42). between males and females with ASD may be more observable in the high functioning ASD population. It might be the case that higher functioning females with ASD  have  managed  to  develop  skills to camouflage their behavioral impairments (40). ing females with ASD, on the other hand, may lack the capacity to develop such skills. Among  younger  children with low functioning ASD, Lord and colleagues (14) reported more RSBs among boys than girls. Unlike in the present study, ted a larger sample size with a  very  narrow  age  range;  they  used  direct  observation rather than parent reports, and they did not control for multiple  testing  comparisons.  Thus, sampling  and  methodologic  differences  between current study and that of Lord and colleagues may be responsible for the inconsistent findings involving  lower  functioning  individuals  with  ASD. Overall, our findings support the notion that lower functioning  boys  and  girls  with  ASD  have  similar presentations of the core symptoms of  ASD

Furthermore,  there  were  no  differences  between girls  and  boys  with  ASD  in  terms  of  SOR  aside from  boys  with  ASD  showing  slightly  more  taste SOR as compared with  girls  with  ASD.  Thus,  the present  study  did  not  replicate  the  findings  of  Lai and  colleagues  (16),  who  reported  fewer  sensory issues among  high functioning male adults as compared with female adults. One possible reason could  be  that  those  researchers  used  the  Autism Diagnostic  Interview-Revised  (43),  which  is  not specifically designed to detect sensory issues. Alternatively,  sex  differences  in  SOR  may  exist  in higher functioning adults but not in predominantly lower functioning children with ASD. Our findings indicated  that  up  to  80%  of  girls  and  boys  with ASD  have sensory issues. frequency  of  both  boys  and  girls  with  ASD  being affected  by  SOR;  this  was  reported  both  in  the present study and previous studies (15,44). Furthermore,  there  were  no  differences  between girls  and  boys  with  ASD  in  terms  of  SOR  aside from  boys  with  ASD  showing  slightly  more  taste as  compared  with  girls  with  ASD.  Thus,  the present  study  did  not  replicate  the  findings  of  Lai and  colleagues  (16),  who  reported  fewer  sensory issues among  high functioning male adults as compared with female adults. One possible reason could  be  that  those  researchers  used  the  Autism Revised  (43),  which  is  not gned to detect sensory issues. Alternatively,  sex  differences  in  SOR  may  exist  in higher functioning adults but not in predominantly lower functioning children with ASD. Our findings indicated  that  up  to  80%  of  girls  and  boys  with ASD  have sensory issues. There was a high frequency  of  both  boys  and  girls  with  ASD  being affected  by  SOR;  this  was  reported  both  in  the present study and previous studies (15,44).

Like SOR, psychopathology was also common. In the  present  study,  a  high  percentage  of  both  boys (73.1%) and girls (55.0%) with ASD met the criteria for  abnormal  psychopathology.  Nonetheless,  our findings suggested that psychopathology was equally represented in girls and boys with ASD, except for a trend  ( p =  .02)  towards  boys  with  ASD  displaying higher  levels  of  hyperactivity  and  inattention  as compared  with  girls  with  ASD.  Our  sex  trend mirrors  previous  teacher-reported  (9)  and  parent reported (45) findings for higher functioning children and adolescents with ASD, which indicated that  hyperactivity  and  inattention  were  more  often present  in  the  male  phenotype  rather  than  the female phenotype.  It is also notable that twin studies  have  reported  a  higher  degree  of  genetic Like SOR, psychopathology was also common. In the  present  study,  a  high  percentage  of  both  boys 1%) and girls (55.0%) with ASD met the criteria for  abnormal  psychopathology.  Nonetheless,  our findings suggested that psychopathology was equally represented in girls and boys with ASD, except for a = .02)  towards  boys  with  ASD  displaying levels  of  hyperactivity  and  inattention  as compared  with  girls  with  ASD.  Our  sex  trend reported  (9)  and  parentreported (45) findings for higher functioning children and adolescents with ASD, which indicated inattention  were  more  often present  in  the  male  phenotype  rather  than  the female phenotype.  It is also notable that twin studies  have  reported  a  higher  degree  of  genetic overlap between traits of ASD  and  attentiondeficit/hyperactivity disorder  among  males  than females  (46),  which  suggests  that  these  conditions are  more  likely  to  co-occur  in  males  than  females for genetic reasons.

Individuals  with  ASD  were  compared  for  social cognition  and  ATTD; sex differences  were  detectable for the latter but not the former. The present study  replicated  the  findings  of  previous  studies, which found that males and females with ASD had equivalent levels of impairments in social cognition (16,22,23).  Not  being  able  to  understand  other people's mental states (36), as suggested by impaired social cognition, may also explain the social communication  difficulties  underlying  ASD  at  the behavioral level (47).

Our  findings  from  the  BD  task  are  consistent with those of previous studies. In general, girls with ASD perform equivalent to TD girls (21) but worse than  boys  with  ASD  (20,21).  Our  findings  suggest that  girls  with  ASD  are  more  similar  to  TD  girls than  boys  with  ASD  with  regard  to  ATTD.  This suggests  that  superior  ATTD  is  not  a  universal feature of the autistic brain but rather a feature of the  male  ASD phenotype. Therefore, it is  possible to speculate that interventions such as visual guidance may be suitable for boys but not girls with ASD (21). This intervention has been shown to help with the reduction of both executive malfunctioning and RSBs in ASD (48). However, a limitation of the current study is the exclusion of a TD male group. It may be that the observed sex difference in ATTD was  not  ASD  specific;  however,  without  a  control group of TD boys, our study could not make such conclusion.  Thus,  it  may  be  necessary  for  future studies to include both TD male and female groups to  investigate  ASD-specific  and  non-ASD-specific sex differences.

One limitation of this study is that the number of participants  was  small.  Nonetheless,  the  present study had a similar number of female participants as past  studies  that  reported  sex  differences  for  ASD (49,50). The  weak  sex  difference trends across RSBs,  SOR,  and  psychopathology  may  become significant with a larger sample (8). This study also lacked  perfect  mental  age  matching.  We  could  not compose full IQ scores for children with IQ scores of less than 45, who were predominantly nonverbal. Therefore, it is possible that lower functioning girls and boys with ASD may differ with regard to their IQs and mental ages, respectively. Furthermore, the correction needed for multiple testing comparisons may  have  increased  type  2  errors.  The  Sally-Ann task  might have been too easy for our participants with mental ages of 4 years or older, because more than 60% of the children with ASD passed the test. Hence, our findings may not be a true reflection of the social cognition difficulties associated with ASD.  The  authors  of  this  study  did  not  assess diagnoses  of  ASD  in  the  sample  themselves  but rather relied on information from specialist schools, SEN  statements, and parents. This may have introduced some error into the study. One possible source of error may be that some individuals do not have ASD but rather have severe learning disabilities or attention-deficit/hyperactivity disorder; it  is  known  that  a  considerable  degree  of 'diagnostic  substitution'  can  occur  for  individuals who require clinical attention and specialist schooling.  It  is  notable  that  individuals  considered to  have  ASD  according  to  the  parent,  school,  and SEN  sources  all  scored  above  the  cutoff  on  the SCQ,  which  is  a  well-respected  screen  for  ASD. Given  the  heterogeneity  of  individuals  with  ASD, our findings may be representative of lower functioning  but  not  higher  functioning  individuals with ASD.

At present, impairment requirements and symptom criteria for the diagnosis of ASD are not sex specific (6). Most screening and diagnostic tools do  not  employ  different  thresholds  or  items  for assessing  ASD  in  males  and  females.  One  study found that some specific items improved an instrument's  ability  to  capture  the  female  ASD phenotype  (41);  example  items  include  'Avoids demands'  and  'Very  determined.'  Our  findings suggest  that  existing  measures  employed  here  do not detect mean sex differences in levels of autism symptoms, social cognition, SOR, and psychopathology in lower functioning children with ASD during childhood and adolescence. The possibility remains that sex differences in symptoms are present but that currently available measures are not  sensitive  to  these  phenotypic  sex  differences. These  data  can  inform  debates  regarding  whether ASD-related  assessment  tools  require  sex-specific criteria or thresholds and to what degree treatment should be tailored to the sex of the individual.

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## Acknowledgements

We  would  like  to  thank  the  children  and  their families  for  the  invaluable  time  that  they  took  to take part in this study. We are also indebted to those school staff that recruited the participants and supported our visits. Finally, we would like to thank the National Autistic Society for their collaboration and  support.  We  thank  Dr  Geoff  Bird  for  his comments on an earlier version of this manuscript. The authors have no conflicts of interests to declare with respect to this manuscript.

## Appendix A. Complete instructions and scoring for social cognition tasks

Sally-Ann  false  belief  task. In  the  Sally-Ann  task  (35), participants  were  told  a  story  accompanied  by  toy props. 'This is Sally. Sally has a basket. This is Ann. Ann has a box. Sally has a marble and she puts it in her basket and  leaves  the  room.  Ann  takes  the  marble  from  Sally's basket  and  puts  it  in  her  box.  Ann  leaves  the  room.  Sally comes  back  to  the  room.' The  researcher  then  asks  the participant, 'Where will Sally look for her marble?' Evidence of intact theory of mind was scored 1 point if the participant could take into account the representation  of  Sally's  belief  and  0  points  if  the participant failed to represent Sally's belief. The SallyAnn task took approximately one minute to administer.

Spontaneous  play. On  the  basis  of  previous  studies (36,37),  two  5-minute  spontaneous  play  trials  were administered to the participants with different sets of toys: 1) a kitchen toy set; and 2) a toy medical kit. In both trials,  soft  animals  were  included,  and  sponges were used for object substitution. When the participant  arrived  in  the  room,  the  first  set  of  toys was spread on a table. The researcher gave the same instructions  to  each  participant: 'You can play and do anything  you  want  with  the  toys.' The  5-minute  trial began  when  the  child  reached  for  the  toys.  If  the participant did not initiate play after 30 seconds, the researcher verbally prompted the participant by saying, 'Play with toys.' The same verbal prompt was delivered a second time if the participant still had not begun playing after another 30 seconds. The researcher began the 5-minute trial regardless of the participant's response after the second verbal prompt. After the first trial, the toys were substituted with the second set of toys. The same procedure was repeated. The researcher did not model any play for the  participants.  During  each  trial,  play  was  rated  at every  15-second  interval  as  falling  into  one  of  six categories: functional, ordering, sensorimotor, pretend play, ambiguous, or no play. The definitions of these ratings were based on the original assessment (36). In sum, 40 sequences were recorded for the two 5-minute trials.

Joint attention. Three joint attention experiments were used:  blocking,  teasing,  and  active-toy  experiments (38). A series of toys were provided to the participants  to  choose  from  and  play  with.  In  the blocking experiment, the researcher blocked the participant's hands for 5 seconds after he or she was visually  and  manually  engaged  with  a  toy.  In  the teasing  experiment,  the  experimenter  tempted  the participant with the same toy as used in the blocking experiment. When the child reached out for the toy, the  researcher  withdrew  the  toy.  In  the  active-toy experiment, the researcher used two mechanical toys, a  walking/roaring  dinosaur  and  an  electric  car,  to provoke a mixed response of uncertainty and attraction  among  the  participants.  These  toys  were controlled by the researcher; they were turned on for 30  seconds  and  then  stopped.  All  participants  were administered all three joint attention tasks four times each.  One  point  was  scored  for  each  trial  if  the participants engaged in eye contact within 5 seconds after the researcher either blocked participants' hands (blocking  task),  withdrew  the  toy  (teasing  task),  or turned  off  the  toy  (active-toy  task).  After  each  trial, the  participants  were  given  the  toy  to  play  with regardless of their engagement in eye contact. A total of 12 points could be scored overall. This task took approximately 5 minutes to administer.