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Associations among autistic traits, cognitive and affective empathy, and personality traits in adults with autism spectrum disorder and no intellectual disability Yukihiko Shirayama1*, Kazuki Matsumoto1, Sayo Hamatani1, Katsumasa Muneoka1, Akihiro Okada2 & Koichi Sato1

Reported empathy deficits in autism spectrum disorder (ASD) could be attributable to other ASD- related features. We evaluated 28 ASD adults with no intellectual disability and 24 age-matched non-ASD control subjects using the Autism-Spectrum Quotient (AQ), Questionnaire of Cognitive and Affective Empathy (QCAE), Interpersonal Reactivity Index (IRI), and NEO Personality Inventory- Revised (NEO). Compared to the controls, ASD participants showed lower scores for perspective taking, online simulation, cognitive empathy, and peripheral responsivity on the QCAE, and lower scores for perspective taking and empathic concern on the IRI. Within the ASD group, the AQ scores showed significant relationships with perspective taking, online simulation and cognitive empathy on the QCAE, and perspective taking on the IRI. The ASD group also showed higher scores for neuroticism and lower scores for extraversion on the NEO compared to the controls. However, there were no relationships between AQ scores and NEO factors within the ASD group. Multiple regression analysis with stepwise linear regression demonstrated that perspective taking score on the QCAE and extraversion score on the NEO were good predictor variables to autistic traits on the AQ. These findings help us to understand empathy and personality traits in ASD adults with no intellectual disability.

Abbreviations ADOS-2 The Autism Diagnostic Observation Schedule, 2nd edition ANCOVA Analysis of covariance ASD Autism Spectrum Disorder AQ Autism-Spectrum Quotient BDI Beck Depression Inventory IQ Intelligence Quatient IRI Interpersonal Reactivity Index MANOVA Multiple analysis of variance NEO NEO Personality Inventory-Revised QCAE Questionnaire of Cognitive and Affective Empathy WAIS-III Wechsler Adult Intelligence Scale, 3rd edition

People with autism spectrum disorder (ASD) typically have problems with reciprocal social interaction and communication and show restricted interests. As a result, they can experience challenges that interfere with their activities of daily living. It seems that individuals with ASD often have troubles with social perception and competence due to difficulties in reading nonverbal interactive cues and responding typically in conversations.

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1Department of Psychiatry, Teikyo University Chiba Medical Center, 3426-3 Anesaki, Ichihara 299-0111, Japan. 2Department of Psychology, Sapporo International University, Sapporo, Japan. *email: [email protected] rapid.ocn.ne.jp

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In the Diagnostic and Statistical Manual of Mental Disorders, 5th Edition (DSM-5)1, Asperger syndrome and high-functioning ASD have been rolled into the single category “ASD”, with a note to specify language or intellectual impairment or associated conditions (e.g., genetic or medical diagnosis). Asperger syndrome was once distinguished from other ASD conditions by an association with typical early language development, and individuals with intelligence quotient (IQ) scores within or above the normal average range have been described as “high-functioning”.

Some researchers have suggested that autism is linked to an innate impairment in the ability to perceive and respond to the affective expressions, leading to profound difficulties in social interaction. Impairments in empa- thy were reported in ASD individuals with normal IQ2,3. Empathy involves cognitive and affective components. Cognitive empathy is defined as the capacity to understand other people’s feelings, intentions, and beliefs on an intellectual level, while affective empathy is the emotional response to other people’s affective state or feelings4,5. Some researchers have reported atypical theory of mind in adolescents and adults with ASD6–8. Empathy assess- ment using the Interpersonal Reactivity Index (IRI)4 demonstrated that ASD adults with no intellectual disability showed impairments in perspective taking scale3,8–11, suggesting potential difficulties in representing another person’s psychological perspective. A previous study highlighted that autism is related to cognitive empathy deficits but not for affective empathy12.

Adults with ASD might well have acquired personality bias. Investigators found that adults with what was once called Asperger syndrome showed elevated harm avoidance and low self-directedness and cooperativeness on the Temperament and Character Inventory (TCI)13–16. Self-directedness and cooperativeness are addressing maturity of personality from the perspective of self and others. The subscales of cooperativeness include social acceptance, empathy, helpfulness and pure-heartedness. Another personality inventory, the NEO Personality Inventory-Revised (NEO)17 is a five-factor model of personality structures in terms of five traits: neuroticism, extraversion, openness, agreeableness, and conscientiousness. Adults with ASD showed high neuroticism and low extraversion, openness, agreeableness and conscientiousness on the NEO18,19. Although the personality traits of neuroticism and extraversion are associated with negative and positive emotional experiences, respectively20, the relationships between the personality traits and autistic traits in ASD are not well documented.

In clinical situations, adults with ASD have personality traits. However, it is unknown whether the autistic behaviors in ASD are related with empathy deficits and personality traits. Here, we hypothesized that empathy deficits and personality traits are constituent parts of autistic behaviors in ASD. To test this hypothesis, we exam- ine what types of components exist in empathy deficits and personality traits and modulate autistic behaviors in ASD adults with no intellectual disability. First, we extracted important components in empathy deficits and personality traits in ASD. Second, we examined the relationships among autistic traits, empathy and personality in each group and compared them. Finally, we quantitatively conducted multiple regression analysis to examine the contribution of empathy and personality traits to the autistic traits.

Methods Participants. This study included 24 ASD adults with no intellectual disability and 28 non-ASD control adults. Inclusion criteria required all participants to be drug-naïve. Participating adults with ASD were recruited from the outpatient clinic of Teikyo University Chiba Medical Center, and all met the DSM-5 criteria for ASD, requiring consensus based on more than 4 months of longitudinal follow-up examination by trained psychia- trists and psychologists. Exclusion criteria were a history of head trauma, seizures or other neurological disor- ders, intellectual disability, or alcohol and substance use disorders. The adults with ASD had no other psychiatric disorders including depression at enrollment. Non-ASD control subjects with no past history of psychiatric disorders or drug dependence were recruited within the social environment of the authors.

Participant characteristics are shown in Table 1. Adults with ASD scored significantly higher for autistic traits (Autism-Spectrum Quotient, AQ)21 compared with healthy controls (p < 0.001) (Table 1). Also, adults with ASD showed statistical significance on the Autism Diagnostic Observation Schedule, second edition (ADOS-2) for clinical use22. The depressive level on the Beck Depression Inventory score (BDI)23 was significantly higher for the adults with ASD compared with unaffected controls (p = 0.012) (Table 1). Full IQ was significantly different between the two groups (p = 0.016) (Table 1), but the IQ of all the subjects were within normal range (IQ > 80).

Table 1. The participant demographics. Data are mean ± SD. AQ autism spectrum quotient, ADOS-2 autism diagnostic observation schedule, 2nd edition, BDI Beck depression inventory, IQ intelligence quotient. *p < 0.05,**p < 0.01,***p < 0.001 compared to the non-ASD controls (Student’s t-test).

Non-ASD control (n = 28) ASD (n = 24) p-values

Age, years (range) 30.4 ± 6.2 (23–44) 27.5 ± 7.5 (18–44) 0.144

Gender (male/female) 12/16 14/10 0.163

AQ 17.3 ± 6.4 32.7 ± 6.5 < 0.001***

ADOS-2 for clinical use 0.5 ± 1.7 7.13 ± 2.7 < 0.001***

BDI 5.3 ± 6.4 10.0 ± 6.5 0.012*

Full IQ 106.2 ± 13.7 97.2 ± 11.7 0.016*

Verbal IQ 106.4 ± 13.1 98.4 ± 13.4 0.033*

Performance IQ 104.9 ± 14.1 96.5 ± 13.8 0.036*

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Instruments. The Autism-Spectrum Quotient (AQ), measuring autistic traits21, is a 50-item self-adminis- tered screening questionnaire to identify the degree to which adults of average intelligence might have autism- related features. This test covers five areas: social skills, attention switching, attention to detail, communication, and imagination. The cutoff for ASD is set at > 32, which captures 80% of adult ASD individuals with no intel- lectual disability; only 2% of unaffected adults surpass this cutoff. Another study reported that the AQ has good discriminative validity and screening properties with a threshold score of 2624. Internal consistency reliability by Cronbach’ alpha was 0.808.

Questionnaire of Cognitive and Affective Empathy (QCAE), which consist of 31 items, comprising five sub- scales: perspective taking, online simulation, emotion contagion, proximal responsivity, and peripheral respon- sivity, was used to assess level of cognitive and affective empathy25. The cognitive empathy subcomponents are perspective taking and online simulation, and the affective empathy subcomponents are emotion contagion, proximal responsivity, and peripheral responsivity. The perspective taking scale reflects placing oneself intui- tively in another person’s shoes. The online simulation component is a more effortful process of attempting to understand the emotional states of others, whereas the emotion contagion reflects the automaticity of mirroring the emotional states of others. Proximal responsivity is the responsiveness of affective situations in a close social context, and peripheral responsivity is the responsiveness to affective situations that occur in a more detached context.

The Interpersonal Reactivity Index (IRI) was used to assess empathy. The IRI consists of 28 items comprising four subscales: perspective taking, fantasy, empathic concern, and personal distress4. The perspective taking scale assesses ability to arrive at a cognitive understanding of what another person thinks or feels. The empathic con- cern scale reflects the tendency to feel emotional compassion and concern for unfortunate others. The personal distress scale measures self-oriented feelings of anxiety and discomfort in response to other people’s suffering. The fantasy scale assesses a person’s ability to self-project into fictional situations.

Personality was assessed using the NEO Personality Inventory-Revised (NEO), which relies on the five-factor model of personality: neuroticism, extraversion, openness, agreeableness, and conscientiousness17. It consists of 240 items answered on a five-point Likert scale. The mean and SD for each dimension are 50 and 10, respectively. The neuroticism scale identifies individuals who are prone to psychological distress. The extraversion scale refers to individuals who are sociable, communicative and prone to adventure and simulation. The openness scale identifies individuals who are open to new ideas and are unconventional in the set of values. The agreeableness scale assesses the type of interaction individuals prefer from compassionate to tough mindedness. The conscien- tiousness scale assesses the degree of organization, persistence, control, and motivation in goal-directed behavior.

Autism Diagnostic Observation Schedule, second edition (ADOS-2) for clinical use was done to check the ASD character22. Beck Depression Inventory score (BDI) was used for assessing depression features23. IQ scores were estimated using the Wechsler Adult Intelligence Scale, 3rd edition (WAIS-III)26.

Statistical analysis. We began using multiple analysis of variance (MANOVA) to analyze data from five domains of QCAE and four domains of IRI to check for the simultaneous significant differences between the two groups. Additional covariate analysis was performed using analysis of covariance (ANCOVA), treating BDI and full-scale IQ scores as covariates. Homogeneity of variance was checked by Box’s M test and Levene’s test. Mul- ticollinearity was checked by multiple regression analysis with stepwise linear method. Multivariate normality and a linear relationship between dependent variables for the independent variable were checked by histogram of residual differences and a scatter P-P plot. Model fit was checked by lack of fit tests.

Coefficients of AQ scores with QCAE or IRI scores, and NEO factors were estimated within each group by Pearson coefficients. Effects size was calculated using G-power (3.1). Bonferroni correction for multiple com- parisons was used when appropriate (QCAE seven scores and IRI four scores, p < 0.05/28 = 0.0018) (QCAE + IRI eleven scores and NEO five scores, p < 0.05/55 = 0.0009).

Multiple regression analysis with stepwise linear regression was conducted, treating AQ scores as the depend- ent variable, and, QCAE five subscales (perspective taking, online simulation, emotion contagion, proximal responsivity, peripheral responsivity), IRI four subscales (perspective taking, empathic concern, personal distress, fantasy), and NEO five subscales (neuroticism, extraversion, openness, agreeableness, conscientiousness) as inde- pendent variables. A better good-fit model was determined by standardized β, adjusted R Square (R2) and F value.

Multiple group structural equation modeling was conducted to examine comparison of patterns of contrib- uting two factors (perspective taking on the QCAE and extraversion on the NEO) to AQ between non-ASD control and ASD groups.

Effects size was calculated using G-power (3.1). Internal consistency reliabilities were expressed by Cronbach’ alpha (Supplementary Table S1). Collinearities of variables were checked by variance inflation factor (Sup- plementary Table S2). Comparison of correlations between two groups was conducted using cocor R package (alpha = 0.05, confidence level = 0.95, null value = 0). Chi-square test was used for categorical variables. Differ- ences were set as significant at p < 0.05. Analyses were conducted with SPSS version 20 (IBM) and SPSS AMOS version 28 (IBM).

Ethics declarations. This research was approved by the ethics committee of Teikyo University School of Medicine  (ethical committee approval No.17-105) and performed in accordance with the Declaration of Hel- sinki. Written informed consent was obtained after the procedures had been fully explained to each participant.

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Results Empathy measures. For the QCAE, MANOVA for the five domains indicated a significant group effect (F = 7.425, p < 0.001), demonstrating that participants with ASD had significantly lower scores for perspective taking, online simulation and peripheral responsivity, but not for emotion contagion or proximal responsivity (Table 2). After controlling for the full-scale IQ and BDI values by ANCOVA, significant differences remained for perspective taking, online simulation and peripheral responsivity (Table 2). When we combined the subcat- egory data into the two categories on the QCAE, t-tests showed that adults with ASD had significantly lower scores for cognitive empathy, but not for affective empathy (Table  2). After adjustment for full-scale IQ and BDI values by ANCOVA, the difference in cognitive empathy remained significant, but not in affective empa- thy (Table 2). When Bonferroni corrections were done for these results, the results were statistically significant (p < 0.05/7 = 0.007).

For the IRI, MANOVA of data for the four domains indicated a significant group effect (F = 7.829, p < 0.001), showing that the adults with ASD had significantly lower scores for perspective taking and empathic concern, but not for personal distress or fantasy (Table 2). After controlling for full-scale IQ and BDI scores by ANCOVA, significant differences remained only for perspective taking and empathic concern (Table 2). When Bonferroni corrections were done for these results, the results were statistically significant (p < 0.05/4 = 0.012). The correlations of ASD traits with empathy scores on the QCAE and IRI. Total AQ scores corre- lated significantly with the perspective taking and cognitive empathy scores on the QCAE, within control group and ASD group, respectively (Table  3). Additionally, total AQ scores correlated significantly with the online simulation scores on the QCAE and the perspective taking scores on the IRI only among ASD group (Table 3). However, total AQ scores failed to show significant relationships with the peripheral responsivity on the QCAE and the empathic concern on the IRI among each group in spite of significance of group comparison (Tables 2, 3). When Bonferroni corrections were done for these results, the correlation between AQ scores and cognitive empathy on the QCAE within ASD group was statistically significant (p < 0.05/7 = 0.007). The correlation plots for key results (perspective taking, online simulation, and cognitive empathy on the QCAE and perspective tak- ing on the IRI) were shown in Fig. 1.

The relationships among empathy scores on the QCAE and IRI. The purpose of the correlation analyses between subscales in the QCAE and subscales in the IRI was to examine the difference and relations between the items for empathic traits on the two questionnaires within non-ASD control and ASD groups.

As for empathy scores, we found strong correlations of the perspective taking scores on the IRI with the perspective taking, online simulation and cognitive empathy scores on the QCAE for controls and ASD group, respectively (Table 3). This replicated a previous report in control subjects27. Also we found significant correla- tions between peripheral responsivity on the QCAE and fantasy scores on the IRI for control group and for

Table 2. Empathy data on the QCAE and IRI. Data are mean ± SD. The number in the bracket is 95% confidence intervals (CI). η2 semi-partial eta-squared. Effect size represents a sample-based estimate of the quality, QCAE Questionnaire of Cognitive and Affective Empathy, IRI Interpersonal Reactivity Index. *p < 0.05,**p < 0.01,***p < 0.001. Uncorrected p-values are determined by MANOVA followed by t-tests. Corrected p-values were obtained by a subsequent ANCOVA treating the BDI ad full-scale IQ scores as covariates.

Non-ASD control (n = 28) [95% CI]

ASD (n = 24) [95% CI] p-values (uncorrected) p-values with cofactors η2 Effect size

QCAE Perspective taking

35.0 ± 6.4 [32.5–38.2]

24.3 ± 7.7 [20.8–27.0] < 0.001*** < 0.001*** 0.364 1.511

QCAE Online simulation

34.1 ± 5.1 [31.5–36.6]

26.5 ± 7.6 [23.7–29.3] < 0.001*** < 0.001*** 0.232 1.174

QCAE Emotion contagion

13.1 ± 2.8 [11.7–14.6]

13.2 ± 4.3 [11.6–14.7] 0.919 0.950 0.000 0.027

QCAE Proximal responsivity

12.0 ± 2.6 [10.7–13.1]

10.7 ± 3.3 [9.4–12.0] 0.111 0.185 0.036 0.437

QCAE Peripheral responsivity

14.2 ± 2.4 [13.3–15.6]

11.9 ± 3.2 [10.3–12.7] 0.005** 0.001** 0.194 0.813

QCAE Cognitive empathy

69.0 ± 10.8 [64.5 – 74.3]

50.6 ± 13.4 [44.9 – 55.6] < 0.001*** < 0.001*** 0.346 1.512

QCAE Affective empathy

39.3 ± 6.2 [36.7 – 42.3]

35.7 ± 8.0 [32.4 – 38.5] 0.079 0.067 0.068 0.503

IRI Perspective taking

21.2 ± 2.8 [19.8–22.5]

16.6 ± 3.6 [15.3–18.1] < 0.001*** < 0.001*** 0.292 1.426

IRI Empathic concern

20.7 ± 3.2 [19.7–21.9]

18.7 ± 2.4 [17.3–19.7] 0.010* 0.010* 0.130 0.707

IRI Personal distress

17.5 ± 4.0 [15.9–19.4]

19.3 ± 4.6 [17.3–21.1] 0.147 0.247 0.028 0.417

IRI Fantasy

19.8 ± 3.7 [18.3–21.5]

17.7 ± 4.4 [15.7–19.2] 0.067 0.059 0.072 0.516

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ASD group (Table 3). When Bonferroni corrections were done for these results, the correlations between online simulation and cognitive empathy on the QCAE and perspective taking on the IRI were statistically significant (p < 0.05/28 = 0.0014).

On the contrary, we found different patterns between the two groups. Among control group there existed correlations between the empathic concern scores on the IRI and the proximal responsivity, peripheral respon- sivity and affective empathy on the QCAE in addition to between fantasy scores on the IRI and affective scores on the QCAE (Table 3), whereas among ASD group there existed correlations between the empathic concern scores on the IRI and emotional contagion scores on the QCAE in addition to between the personal distress scores on the IRI and emotional contagion, proximal responsivity and affective empathy scores on the QCAE (Table 3). Comparison of correlations by cocor demonstrated significant differences in the correlations between the online simulation on the QCAE and perspective taking on the IRI, the emotional contagion on the QCAE and personal distress on the IRI, and the peripheral responsivity on the QCAE and empathic concern on the IRI between the two groups. However, when Bonferroni corrections were done for these results, correlations were not statistically significant (p < 0.05/20 = 0.0025).

Personality scores. For the NEO, MANOVA indicated a significant group effect (F = 8.951, p < 0.001), demonstrating that compared with control subjects, the adults with ASD had significantly higher scores for neu- roticism and lower scores for extraversion, agreeableness and conscientiousness, but no differences in openness, on the NEO, (Table 4). After controlling for the full scale IQ and BDI scales by ANCOVA, significant differences remained in neuroticism and extraversion, but not in agreeableness or conscientiousness (Table 4). When Bon- ferroni corrections were done for these results, the results were statistically significant (p < 0.05/5 = 0.01).

Correlations of AQ scores with NEO personality scores. We found significant correlations between AQ scores and NEO personality scores: for neuroticism among non-ASD controls and total participants, but not among ASD group; for extraversion among healthy controls and total participants, but not among ASD group; for conscientiousness among healthy controls and total participants, but not among ASD group (Table 5).

Table 3. Relationships between empathy’s components on the QCAE and IRI and autistic traits on the AQ. Values are Pearson’s r correlations. AQ autism-spectrum quotient, IRI Interpersonal Reactivity Index, QCAE Questionnaire of Cognitive and Affective Empathy, C only within non-ASD control subjects, A only within ASD subjects. *p < 0.05,**p < 0.01,***p < 0.001 in each group.

AQ IRI Perspective taking

IRI Empathic concern

IRI Personal distress

IRI Fantasy

Non-ASD control (n = 28)

AQ −0.315 0.056 0.301 −0.054

QCAE Perspective taking −0.387* 0.597** 0.136 −0.186 0.113

QCAE Online simulation −0.299 0.669*** 0.214 −0.227 0.163

QCAE Emotional contagion −0.002 0.011 0.281 0.158 0.335

QCAE Proximal responsivity −0.068 −0.064 0.395* C 0.166 0.279

QCAE Peripheral responsivity −0.361 0.010 0.443* C 0.069 0.561**

QCAE Cognitive empathy −0.375* 0.670*** 0.182 -0.215 0.148

QCAE Affective empathy −0.172 0.007 0.468* C 0.168 0.490** C

ASD subjects (n = 24)

AQ −0.430* A −0.078 0.308 −0.064

QCAE Perspective taking −0.510* 0.581** 0.079 −0.327 −0.066

QCAE Online simulation −0.499* A 0.821*** -0.115 −0.292 −0.030

QCAE Emotional contagion 0.098 0.095 0.528** A 0.576** A 0.223

QCAE Proximal responsivity 0.010 0.290 0.294 0.555** A 0.074

QCAE Peripheral responsivity −0.085 0.007 −0.028 −0.170 0.541**

QCAE Cognitive empathy −0.579** 0.791*** −0.019 −0.355 −0.057

QCAE Affective empathy 0.022 0.174 0.394 0.471* A 0.370

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When Bonferroni corrections were done for these results, the correlations between AQ scores and the neu- roticism, extraversion and conscientiousness on the NEO within total subjects were statistically significant (p < 0.05/5 = 0.01). The correlation plots for key results (neuroticism, extraversion and conscientiousness on the NEO) were shown in Fig. 2.

Relationships of personality factors on the NEO with empathy scales on the QCAE and IRI. Within each control group and ASD group, we found significant correlations of neuroticism on the NEO with emotion contagion and affective empathy on the QCAE, and with fantasy on the IRI (Table 6). Further, we found significant correlations of extraversion on the NEO with peripheral responsivity on the QCAE, and of openness on the NEO with peripheral responsivity on the QCAE within each group (Table 6).

Within only control group, there existed significant correlations between neuroticism on the NEO and prox- ismal responsivity on the QCAE, openness on the NEO and proxismal responsivity and affective empathy on the QCAE, and conscientiousness on the NEO and personal distress on the IRI (Table 6).

Within only ASD group, we found significant correlations between neuroticism on the NEO and personal distress on the IRI, extraversion on the NEO and online simulation on the QCAE, extraversion on the NEO and affective empathy on the QCAE, openness on the NEO and online simulation on the QCAE, and conscientious- ness on the NEO and perspective taking on the IRI (Table 6).

Figure 1. The correlation plots for the association between autistic traits and empathy. (A,B) The correlations between autistic traits on the AQ and perspective taking on the QCAE in the control and ASD subjects. (C,D) The correlations between autistic traits on the AQ and online simulation on the QCAE in the control and ASD subjects. (E,F) The correlations between autistic traits on the AQ and cognitive empathy on the QCAE in the control and ASD subjects. (G,H) The correlations between autistic traits on the AQ and perspective taking on the IRI in the control and ASD subjects.

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When Bonferroni corrections were done for these results, correlations were not statistically significant (p < 0.05/55 = 0.0009).

Comparison of correlations by cocor failed to demonstrate significant differences in the correlations between personality factors and empathy scales between the two groups.

Contributory factors of empathy and personality to autistic traits by multiple regression analysis. Multiple regression analysis with stepwise linear regression showed goodness-of-fit statistics (R = 0.872, adjusted R2 = 0.750, F = 77.55, p < 0.001). Results indicated that two factors, extraversion on the NEO (standardized coefficient beta = −0.556, p < 0.001) and perspective

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