Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder

INTPSY-10642; No of Pages 8 International Journal of Psychophysiology xxx (2013) xxx–xxx

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Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder Danielle Mathersul ⁎, Skye McDonald, Jacqueline A. Rushby School of Psychology, University of New South Wales, Sydney, NSW 2052, Australia

a r t i c l e

i n f o

Article history: Received 28 January 2013 Received in revised form 17 April 2013 Accepted 20 April 2013 Available online xxxx Keywords: Autism Asperger's Skin conductance Arousal Empathy Emotion

a b s t r a c t Empirical research into behavioural profiles and autonomic responsivity in individuals with autism spectrum disorders (ASDs) is highly variable and inconsistent. Two preliminary studies of children with ASDs suggest that there may be subgroups of ASDs depending on their resting arousal levels, and that these subgroups show different profiles of autonomic responsivity. The aim of the present study was to determine whether (i) adults with high-functioning ASDs may be separated into subgroups according to variation in resting arousal; and (ii) these ASD arousal subgroups differ in their behavioural profiles for basic emotion recognition, judgements of trustworthiness, and cognitive and affective empathy. Thirty high-functioning adults with ASDs and 34 non-clinical controls participated. Resting arousal was determined as the average skin conductance (SCL) across a 2 min resting period. There was a subgroup of ASD adults with significantly lower resting SCL. These individuals demonstrated poorer emotion recognition, tended to judge faces more negatively, and had atypical relationships between SCL and affective empathy. In contrast, low cognitive empathy was a feature of all ASD adults. These findings have important implications for clinical interventions and future studies investigating autonomic functioning in ASDs. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Individuals with ASDs (including autism and Asperger's Syndrome) 1 display marked impairments in social interaction such as poor social–emotional reciprocity, deficits in the use of non-verbal communication such as eye-gaze and facial expression and also demonstrate repetitive and stereotyped behaviours (APA, 2000). One potential method of objectively investigating social–emotional reciprocity in these individuals is through physiological markers of the orienting response (OR), such as electrodermal activity (skin conductance). ORs are typically elicited by salient environmental stimuli, particularly socially-relevant information such as faces and affective scenes, and assist in the generation of action and approach within an organism (Barry, 1990). They involve a combination of behavioural and physiological changes, and are affected by the novelty, intensity and significance of the evoking stimulus (Barry, 1990; Rushby et al., 2005). Skin conductance responses (SCRs) may reflect the arousal or intensity of motivationally significant stimuli (Lang, 1995; Lang et al., 1990), as well as the allocation of attention to stimuli over time (e.g., Barry, 1990; Barry and Sokolov, 1993; Maltzman, 1977; ⁎ Corresponding author. Tel.: +61 2 9385 3041; fax: +61 2 9385 3641. E-mail address: [email protected] (D. Mathersul). 1 Proposed changes to diagnostic criteria in the upcoming DSM-5 recommend the removal of the distinction between autism and Asperger's (APA, 2011). In line with these proposed changes to nomenclature, individuals with no clinically significant delay in language and an IQ within the normal range will be referred to as high-functioning individuals with ASDs for the purposes of this study.

Maltzman and Boyd, 1984; Rushby and Barry, 2007, 2009; Sokolov, 1990). Past research into phasic, task-dependent ORs (SCRs) in ASDs is inconsistent and appears inconclusive. One study found that ASDs have higher SCRs to socially-relevant stimuli (Kylliäinen and Hietanen, 2006) whilst another demonstrated lower SCRs (Hubert et al., 2009). Still other studies have failed to find any differences in SCRs between individuals with ASDs and controls (Ben Shalom et al., 2006; Joseph et al., 2008). In contrast, a series of studies from our own lab have consistently demonstrated that individuals with ASDs have disruptions in SCRs (Mathersul et al., 2013a, 2013b, submitted for publication-a). Differences in experimental design may partly explain these discrepancies in the direction of the effects. For example, SCRs across face viewing time for neutral faces failed to habituate for individuals with ASDs (Mathersul et al., 2013b), whereas SCRs across tasks to briefly presented emotional faces showed rapid habituation followed by a gradual increase in responses (Mathersul et al., submitted for publication-a). In terms of responses to highly arousing scenes, SCRs were reduced only to affective but not neutral scenes (Mathersul et al., 2013a). Given that the elicitation of an OR (SCRs) to salient information in the environment is directly influenced by baseline arousal levels (both resting and pre-stimulus skin conductance levels (SCLs); Barry and Sokolov, 1993; Sokolov, 1963), it is important to investigate potential differences in baseline arousal. Interestingly, results from our own lab suggest that pre-stimulus SCLs (i.e., slower, more longer lasting changes in arousal related to novel and/or salient stimuli) in individuals with ASDs may

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Please cite this article as: Mathersul, D., et al., Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder, International Journal of Psychophysiology (2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.04.014

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D. Mathersul et al. / International Journal of Psychophysiology xxx (2013) xxx–xxx

be either typical (Mathersul et al., 2013b) or atypical (at least initially; Mathersul et al., submitted for publication-a). However, what remains unclear is whether or not resting levels of arousal are typical or atypical in these individuals. This was the first aim of this study. There is generally a paucity of research into resting arousal levels in ASDs, particularly in recent years. Two studies in the 1980s reported no difference from controls in resting SCL (James and Barry, 1980; Zahn et al., 1987), however, other work suggests that individuals with ASDs may not be homogenous in this regard. One study demonstrated that low-functioning children with ASDs could be separated into subgroups depending on their resting arousal levels (spontaneous fluctuations in SCLs), and these subgroups showed significantly different task-dependent ORs (SCRs) to auditory stimuli (van Engeland, 1984). Similarly, a more recent study of highfunctioning children with ASDs again demonstrated separation into subgroups depending on resting arousal levels (SCLs) which showed significantly different SCRs to non-social environmental stimuli (Schoen et al., 2008), although they did not compare to a control group. This issue prompted enquiry into the resting arousal levels of the high-functioning adults who have participated in previous studies from our lab, particularly whether or not the ASD group may be separated into subgroups according to variation in SCLs. This was the second aim of this study. These two findings in children with ASDs that suggest that variability in resting SCL may contribute to variation in SCRs to salient stimuli are intriguing. They may help explain the extensive inconsistencies in behavioural responses to socially-relevant stimuli in the literature. For example, with regard to basic emotion recognition, some studies have demonstrated deficits (e.g., Ashwin et al., 2006a, 2006b, 2006c; Bal et al., 2010; Corden et al., 2008; Teunisse and de Gelder, 2001; Wallace et al., 2008) whilst others have found no differences between ASDs and controls (Adolphs et al., 2001; Boucher et al., 2000; Capps et al., 1992; Grossman et al., 2000; Loveland et al., 1997). Similarly, some studies suggest that individuals with ASDs rate faces as more trustworthy than controls (Adolphs et al., 2001; Couture et al., 2010), whereas other studies have found no differences (Mathersul et al., 2013b; Pinkham et al., 2008). Finally, whilst impaired empathy is clinically considered a central characteristic of ASDs (Baron-Cohen and Wheelwright, 2004; Baron-Cohen et al., 2001a), empirical research is inconsistent, with some studies demonstrating deficits in both cognitive and affective empathy (Mathersul et al., in press; Shamay-Tsoory et al., 2002), whilst others have shown deficits only in cognitive but not affective empathy (Dziobek et al., 2008; Rogers et al., 2007). A potential explanation for these inconsistencies may be variability in resting arousal levels, given the high degree of variability and heterogeneity across the spectrum of ASDs. Therefore, the third and final aim of this study was to explore the behavioural profile(s) of the different ASD subgroups (as determined by resting SCL). In summary, the aim of the present study was to investigate (i) whether adults with high-functioning ASDs differ from controls in their resting arousal levels (SCLs); (ii) whether or not the ASD group may be separated into subgroups according to variation in these resting arousal levels; and (iii) whether or not the ASD arousal subgroups differ in their behavioural profiles for basic emotion recognition, judgements of trustworthiness, and cognitive and affective empathy.

2. Methods 2.1. Participants Thirty high-functioning adults with ASDs and thirty-four nonclinical control individuals were recruited from Sydney and surrounding regions in New South Wales, Australia, via advertisements,

support groups, clinicians, Aspect (Autism Spectrum Australia) 2 and undergraduate university populations. Individuals were reimbursed for their time or received course credit for participation. Participants gave written informed consent in accordance with the University of New South Wales Human Research Ethics Committee (UNSW HREC). All individuals in the clinical group met DSM-IV-TR (APA, 2000) diagnostic criteria for an ASD, as assessed by experienced clinicians independent of the present study. These clinicians (e.g., clinical psychologists, neuropsychologists, psychiatrists) administered standardised clinical interviews such as the ADI-R (Autism Diagnostic Interview—Revised; Lord et al., 1994) and ADOS-G (Autism Diagnostic Observation Schedule—Generic; Lord et al., 1999), however, the information from these reports was not typically made available to the researchers. As such, the Autism Quotient (AQ; ≥32; Baron-Cohen et al., 2001b) and/or Ritvo Autism Asperger's Diagnostic Scale (RAADS; ≥77; Ritvo et al., 2008) were used to support diagnosis. The AQ has been shown to produce good test–retest reliability (r = .70) and good internal consistency (Cronbach's α = .63–.77; Baron-Cohen et al., 2001b). The RAADS has been shown to produce reliable clinical discrimination (97–100% sensitivity, 100% specificity), high test– retest reliability (r = .99), and good internal consistency (Cronbach's α = .65–.92; Ritvo et al., 2011, 2008). Exclusion criteria were a self-reported personal history of physical brain injury, neurological or developmental disorder (other than an ASD in the clinical group), psychiatric illness, or any other serious medical condition. In addition, control participants were excluded if they had a score above the recommended clinical cut-off on the AQ and/or RAADS. Three control participants were subsequently excluded. One ASD participant was excluded due to smoking immediately prior to arriving, and the data from an additional ASD participant was lost due to equipment problems. The final sample consisted of 28 high-functioning adults with ASDs (aged 18–73 years; 22 males) and 31 non-clinical control individuals (aged 18–72 years; 24 males) (see Table 1). 2.2. Materials and measures 2.2.1. Wechsler Abbreviated Scale of Intelligence The Wechsler Abbreviated Scale of Intelligence (WASI) is a brief, standardised measure of general intellectual functioning that demonstrates good reliability and validity (Wechsler, 1999). All participants were administered the two-subtest format, allowing for a measure of full scale IQ (FSIQ). 2.2.2. The Awareness of Social Inference Test (TASIT) The Awareness of Social Inference Test (TASIT; McDonald et al., 2002) uses video vignettes depicting conversational exchanges to assess basic emotion recognition, as well as the ability to understand more subtle emotions and conversational inferences. Part 1 (The Emotion Evaluation Test) of TASIT assesses the ability to recognise and discriminate six basic emotions (happiness, sadness, anger, fear, surprise, disgust) as well as neutral expressions (overall total score maximum = 28). TASIT has a total playing time of approximately 35 min and an administration viewing time of 60–75 min. Practice items are provided for all parts. The vignettes are presented in a fixed order, randomised between emotion types. TASIT has been shown to have good test–retest reliability (r = .74–.88) (McDonald et al., 2006). It is sensitive to clinical conditions and also predictive of real-world function (McDonald et al., 2004). 2.2.3. Interpersonal Reactivity Index (IRI) The Interpersonal Reactivity Index (IRI; Davis, 1980, 1983) is a 28-item self-report questionnaire designed to assess both cognitive 2 Australia's largest not-for-profit provider of services related to ASDs, including access to information, support groups, blogs, research participation and relevant media releases.

Please cite this article as: Mathersul, D., et al., Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder, International Journal of Psychophysiology (2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.04.014

D. Mathersul et al. / International Journal of Psychophysiology xxx (2013) xxx–xxx Table 1 Group demographics. Measure; mean (SD)

Control

ASD

Age Years of education FSIQ-2 AQ RAADS

41.7 15.9 113.5 16.0 39.0

38.9 15.0 114.3 31.3 119.1

(17.5) (2.1) (22.1) (5.6) (27.4)

(17.2) (2.5) (15.0) (7.7) (42.8)

Note. FSIQ-2 = Full Scale Intelligence Quotient, 2-subtest version; AQ = Autism Quotient; RAADS = Ritvo Autism Asperger's Diagnostic Scale.

and affective empathy. Responses are made on a 5-point Likert scale ranging from 0 (does not describe me well) to 4 (describes me very well). The IRI consists of four, 7-item subscales: Perspective Taking (PT; the ability to imagine the cognitive viewpoint of others), Fantasy (FS; the tendency to emotionally identify with fictional characters in novels and movies), Empathic Concern (EC; the capacity to form an emotional response (e.g., warmth, compassion, concern) to the emotional state of another person), and Personal Distress (PD; the extent to which one forms a self-centred emotional response (fear, discomfort, distress) to another's misfortunes). All four subscales demonstrate good internal (.71–.77) and good test–retest (.62–.71) reliabilities (Davis, 1980). The PT and EC subscales are considered the strongest representations of cognitive and affective empathy, respectively (Davis, 1983), and as such, were the measures employed in the present study. 2.2.4. Empathy Quotient (EQ) The Empathy Quotient (EQ; Baron-Cohen and Wheelwright, 2004) is a 60-item self-report questionnaire consisting of 40 empathy items and 20 “filler” items, to distract participants from the focus on empathy. Responses are made on a 4-point Likert scale ranging from strongly agree to strongly disagree. The EQ allows for a measure of overall empathy, as well as the separation of affective empathy (“emotional reactivity”; EQ-ER) and cognitive empathy (EQ-CE; 11 items each; Lawrence et al., 2004; Muncer and Ling, 2006). Both the total EQ (Cronbach's α = .85) and the two subscales (Cronbach's α = .76–.84) have been shown to demonstrate good internal consistency (Muncer and Ling, 2006). The total EQ also has high test–retest reliability (r = .97) (Baron-Cohen and Wheelwright, 2004). Both the total EQ and the EQ-ER subscale have strong correlations with IRI-PT (.44–.49) and IRI-EC (.42–.58), however the EQ-CE does not correlate significantly with any of the IRI subscales (Lawrence et al., 2004). 2.3. Procedure On the day of psychophysiology acquisition, participants were asked to refrain from consuming nicotine or caffeine within 2 h of testing (as recommended by Barry et al., 2008). On arrival, an overview of the recording procedure was provided, and informed consent and diagnostic information were obtained. Participants subsequently completed the EQ and IRI. The WASI and TASIT were either conducted following the psychophysiological procedure or during a separate session. Once relaxed and comfortable, participants were seated and recording devices were attached. Participants were instructed to close their eyes and rest quietly for 2 min. Following this rest period, a series of studies were conducted, as reported elsewhere (see Mathersul et al., 2013a, 2013b, submitted for publication-a, in press).3 (Due to

3 Please note that each of these studies was discrete and independent, with specific aims and a priori hypotheses. Furthermore, none of these studies reported on the resting arousal (SCL) data that are presented in the present study. Overall group differences (ASD vs. controls) for some of the behavioural data are previously presented in some of these studies (and referenced accordingly where appropriate), however, the behavioural differences by ASD (SCL) subgroups are unique to this study. Data were collected in this mass format due to difficulty in recruitment of the clinical population, and the concurrent studies were designed for a Doctoral thesis.

3

time constraints, some participants did not complete all tasks, so only the data from those who completed all tasks is presented for this study.) SCLs were recorded simultaneously from an 8/30 Powerlab Data Acquisition System (ADInstruments, Castle Hill, Australia), connected to a PC and controlled by DMDX. Sampling occurred continuously across the task. SCL was recorded from two dry, bright-plated bipolar electrodes placed on the distal phalanges of digits II and IV of the non-dominant hand. The signal was calibrated before each session to detect activity in the range of 0–40 μS (microSiemens) and recorded using an ADInstruments Model ML116 GSRAmp. 2.4. Data reduction and analyses Resting arousal levels were determined for each participant as the average SCL across the 2 min resting period. K-means (or “Quick”) cluster analysis was conducted on the ASD group with resting SCL as the defining variable, using the default setting of two clusters. Factor analyses were first conducted to produce summary scores of “cognitive empathy” (IRI-PT and EQ-CE) and “affective empathy” (IRI-EC and EQ-ER). Resting arousal (SCL) was analysed using one-way ANOVAs with Group ((i) ASD vs. control; (ii) ASD subgroup 1 vs. ASD subgroup 2 vs. control) as the between-subjects factor. Behavioural data (emotion recognition, judgements of trustworthiness, cognitive and affective empathy factor scores) were analysed using one-way ANOVAs with Group (ASD subgroup 1 vs. ASD subgroup 2 vs. control) as the between-subjects factor. Planned a priori contrasts compared each of the groups on all behavioural measures. 3. Results 3.1. Demographic and clinical group characteristics There were no significant differences between groups on age (F(1,58) = 0.4, p = .531), gender ratio (χ 2 = .01, p = .915), years of education (F(1,58) = 2.0, p = .164), or full scale IQ (F(1,58) = 0.02, p = .881). Confirming diagnostic group, the ASD group was significantly higher on the AQ (F(1,58) = 72.4, p b 0.001) and RAADS (F(1,58) = 69.8, p b 0.001; Table 1). 3.2. Resting arousal There were no significant differences between the overall ASD group and the control group on SCL (F(1,58) = 2.1, p = .155). However, the ASD group was more variable than the control group (ASD SD = 2.70, control SD = 2.48; ASD SEM = .51, control SEM = .46). Boxplots revealed that resting SCL for the control group had a skewed distribution with more individuals demonstrating higher SCL, whereas resting SCL for the ASD group demonstrated a wider, normal distribution and lower SCL in the bottom quartile compared to the controls (see Fig. 1a). These features suggest the presence of different subgroups within the ASD group. Hence, performance of cluster analysis on the ASD group was justified. The cluster analyses revealed distinct ASD subgroups according to resting SCL (F(1,26) = 47.5, p b .001; Fig. 1b). The “low SCL ASD” subgroup had significantly lower SCL than the “high SCL ASD” subgroup (t(56) = 6.6, p b .001) and the control group (t(56) = 4.8, p b .001), whilst there were no differences in SCL between the “high SCL ASD” and control groups (p = .360; Fig. 1b). Henceforth, the “high SCL ASD” subgroup will be referred to as the “typical SCL ASD” subgroup. The cluster analysis allocated 11 ASD individuals to the “low SCL ASD” subgroup and 17 ASD individuals to the “typical SCL ASD” subgroup (F(1,26) = 47.5, p b .001). There were no significant differences between the “low SCL ASD” and “typical SCL ASD” subgroups on age (F(1,27) = 1.2, p = .274), gender ratio (χ 2 = 2.4, p = .121),

Please cite this article as: Mathersul, D., et al., Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder, International Journal of Psychophysiology (2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.04.014

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Fig. 1. Group distribution of resting SCL for (a) high-functioning ASD vs. control participants and (b) the two ASD subgroups (as determined by cluster analysis; “low SCL ASD” vs. “typical SCL ASD”) vs. control participants. SCL = skin conductance level.

years of education (F(1,27) = 0.7, p = .412), full scale IQ (F(1,27) = 0.05, p = .819), AQ (F(1,27) = 0.01, p = .912) or RAADS (F(1,27) b 0.001, p = .996). 3.3. Arousal and emotion recognition There were no significant differences between the overall ASD group and the control group for emotion recognition on TASIT Part 1. However, the “low SCL ASD” subgroup had a trend towards lower overall emotion recognition than the control group on TASIT (t(56) = 2.1, p = .052; Fig. 2). There were no significant differences in emotion recognition between the “typical SCL ASD” subgroup and either the control group or the “low SCL” subgroup. 3.4. Arousal and judgement ratings As was reported in our previous study (see Mathersul et al., 2013b), the overall ASD group had a trend towards rating faces more negatively than the controls, although this effect was not significant. In the present study, the “low SCL ASD” subgroup also had a trend towards rating the faces more negatively than controls (t(56) = 1.9, p = .067; Fig. 3). There were no significant differences in judgement ratings between the “typical SCL ASD” subgroup and either the control group or the “low SCL ASD” subgroup.

3.5. Arousal and empathy Factor analyses of EQ-CE and IRI-PT resulted in a single “cognitive empathy” factor (eigenvalue 1.601), which explained 80.1% of the variance. Factor analyses of EQ-ER and IRI-EC resulted in a single “affective empathy” factor (eigenvalue 1.664), which explained 83.2% of the variance. As was reported in our previous study (see Mathersul et al., in press), the overall ASD group had significantly lower cognitive and affective empathy than controls. Similarly, in the present study, both the “typical SCL ASD” (t(56) = 4.7, p b .001) and “low SCL ASD” (t(56) = 4.5, p b .001) subgroups had significantly lower cognitive empathy than the control group (Fig. 4). In contrast, the “typical SCL ASD” subgroup had significantly lower affective empathy than the controls (t(56) = 2.3, p = .023), whereas the “low SCL” subgroup did not differ significantly from either the “typical SCL ASD” subgroup or the control group on affective empathy (Fig. 4). Given the unexpected finding that the “typical SCL ASD” but not the “low SCL ASD” subgroup demonstrated atypical levels of affective empathy, exploratory bivariate correlations were also conducted between resting arousal levels (SCLs) and cognitive and affective empathy, separately by group. An adjusted probability level of .05/2 = .025 was used to control for repeated comparisons. Overall, the control group had significant negative correlations between SCL and both cognitive and affective empathy (Table 2). Similarly, the “typical

25

Mean Judgement Ratings

Mean Accuracy

0.5 24

23

22

21 ASD Low SCL

ASD 'Typical' SCL

Control

0.0

-0.5

-1.0

-1.5 ASD Low SCL

Fig. 2. Mean accuracy for basic emotion recognition on TASIT for high-functioning ASD and control participants. The ASD group is separated into subgroups by resting SCL (as determined by cluster analysis). Error bars represent standard errors. SCL = skin conductance level.

ASD 'Typical' SCL

Control

Fig. 3. Mean judgement ratings for high-functioning ASD and control participants. The ASD group is separated into subgroups by resting SCL (as determined by cluster analysis). Error bars represent standard errors. SCL = skin conductance level.

Please cite this article as: Mathersul, D., et al., Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder, International Journal of Psychophysiology (2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.04.014

D. Mathersul et al. / International Journal of Psychophysiology xxx (2013) xxx–xxx

1.0

Mean Affective Empathy

1.0

Mean Cognitive Empathy

5

0.5

0.0

-0.5

0.5

0.0

-0.5

-1.0

-1.0 ASD Low SCL ASD 'Typical' SCL

Control

ASD Low SCL

ASD 'Typical' SCL

Control

Fig. 4. Mean cognitive empathy (left graph) and affective empathy (right graph) for high-functioning ASD and control participants. The ASD group is separated into subgroups by resting SCL (as determined by cluster analysis). Error bars represent standard errors. SCL = skin conductance level. Note. **p b .001; *p b .05.

SCL ASD” subgroup had significant negative correlations between SCL and cognitive and affective empathy, whereas for the “low SCL ASD” subgroup, there was a trend towards a negative correlation for cognitive empathy only (Table 2).

4. Discussion The present study found that whilst adults with high-functioning ASDs did not differ overall from controls in their resting arousal levels (SCLs), there were different subgroups within the ASD group based on differences in resting SCL. Furthermore, these ASD subgroups differed in their behavioural profiles. Specifically, the ASD group with significantly lower resting SCL demonstrated poorer recognition of basic emotions and tended to rate faces more negatively than controls. In contrast, the ASD group with “typical” resting SCL did not differ from controls on emotion recognition or judgement ratings. Interestingly, whilst both ASD subgroups had significantly lower cognitive empathy than controls, only the “typical SCL ASD” subgroup had significantly lower affective empathy. Exploratory correlations revealed that relationships between SCL and empathy were atypical only for the “low SCL ASD” subgroup and affective empathy. The results from the present study suggest that there is an optimal level for resting, baseline arousal in ASDs. Arousal levels that are too low may result in poor recognition of basic emotions and failure to appropriately judge the trustworthiness of faces. A potential explanation is that (some) individuals with ASDs fail to orient to novel or salient environmental stimuli (i.e., socially-relevant stimuli). Baseline arousal levels (including resting SCL) directly influence elicitation of an OR to salient information in the environment (Barry and Sokolov, 1993; Sokolov, 1963) and assist in the generation of action and approach within an organism (Barry, 1990). Therefore, variability in resting arousal levels provides a potential explanation for inconsistencies in the literature with regard to behavioural profiles in ASDs, including emotion recognition and judgement ratings. Although pre-stimulus arousal levels (SCLs) are typically controlled for when investigating task-dependent ORs (e.g., SCRs), these present findings, in conjunction with two earlier studies (Schoen et al., 2008; van Engeland, 1984), suggest that pervasive differences in resting arousal levels may also need to be taken into account when investigating

Table 2 Correlations. Factor

Control group

ASD subgroup (typical SCL)

ASD subgroup (low SCL)

Cognitive empathy Affective empathy

−.459⁎ −.480⁎

−.583⁎ −.592⁎

−.491ˆ −.269

⁎ Significant (p b .025). ˆ Trend (p b .05).

autonomic responses to socially relevant stimuli. This is a potential area for future research. Results from the self-reported empathy questionnaires tapped a different level of socially-relevant responding. Specifically, the questionnaires asked for self-evaluations regarding general patterns of empathic behaviour. We found that low cognitive empathy was core to both subgroups of individuals with ASDs. This accords with past research that consistently demonstrates deficits in cognitive empathy in ASDs (Dziobek et al., 2008; Mathersul et al., in press; Rogers et al., 2007; Shamay-Tsoory et al., 2002). Given that cognitive empathy is closely linked to traditional theory of mind abilities such as perspective taking and cognitive flexibility (Blair, 2008; Davis, 1980, 1983; Rankin et al., 2005; Shamay-Tsoory and Aharon-Peretz, 2007; Shamay-Tsoory et al., 2003), these findings provide further support for a theory of mind deficit in ASDs (see Baron-Cohen et al., 1999; Castelli et al., 2002; Craig et al., 2004; Happé, 1994; Hubert et al., 2007; Mathersul et al., in press). Furthermore, the finding that cognitive empathy was negatively associated with arousal in both ASD subgroups and controls, suggests a linear relationship whereby higher resting arousal (such as might occur with anxiety) interferes with the ability to consider another person's perspective. Indeed, the increased arousal seen in anxiety disorders results in hypervigilance to personally-relevant (that is, feared) stimuli, and consequently interferes with processing of other potentially salient information (see Pole, 2007 for meta-analysis). That higher resting arousal levels in ASDs are associated with poorer cognitive empathy suggests that this social cognitive ability is not naturally salient to these individuals, and provides further support for their marked preference (hypervigilance) for inanimate objects over people (Adrien et al., 1993; Kuhl et al., 2005; Pierce et al., 2011). Findings for affective empathy were more complex than those for cognitive empathy. Notably, performance on affective empathy differed across the two subgroups of ASDs, which is also consistent with prior research demonstrating that affective empathy (unlike cognitive empathy) is highly variable within the ASD population (see Dziobek et al., 2008; Mathersul et al., in press; Rogers et al., 2007; Shamay-Tsoory et al., 2002). Similarly to cognitive empathy, the “typical SCL ASD” subgroup had lower affective empathy than controls, but at the same time, demonstrated a negative trend between heightened arousal and lower empathy (similar to controls). That is, higher resting arousal (associated with anxiety) impairs affective empathic processes such as emotion recognition and responsivity in both healthy controls and a subgroup of ASDs. In contrast, the ASD subgroup with significantly lower resting SCL failed to show a relationship between arousal and affective empathy, despite reporting similar levels of affective empathy to controls. One potential explanation for this dissociation is the inverted-U hypothesis of optimal state (Anshel, 2012; Yerkes and Dodson, 1908), which is commonly applied in sport psychology. This theory argues that optimum performance (in this case, affective empathy) relies on an optimal level of arousal, such that arousal levels that

Please cite this article as: Mathersul, D., et al., Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder, International Journal of Psychophysiology (2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.04.014

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are too high or low negatively affect performance. Regarding the ASD individuals with low arousal, they may be relying on compensatory mechanisms (that is, other than arousal levels) in order to demonstrate intact affective empathy. This is particularly interesting given that psychopathy is associated with both impaired affective empathy (see Blair, 2008 for review) and hypoarousal (Raine et al., 1990, 1995). Furthermore, it has been argued that hypoarousal is a marker of psychopathy, given that arousal levels (resting SCLs) during development are predictive of criminality later in life (Raine et al., 1990, 1995). However, the results from the present study suggest that hypoarousal may be more indicative of disruptions in the mechanisms underlying affective empathy (e.g., relying on compensatory mechanisms for performance) rather than a marker of psychopathy per se. This accords with studies demonstrating that hypoarousal and impaired empathy are also features of other clinical disorders, such as attention deficit/hyperactivity disorder (AD/HD; Lawrence et al., 2005; Marton et al., 2009; Satterfield and Cantwell, 1974) and schizophrenia (Gruzelier and Venables, 1973; Shamay-Tsoory et al., 2007; Sparks et al., 2010).

4.1. Clinical implications Studies have shown that children with AD/HD have atypical resting arousal levels that may be corrected with stimulant medication (Lawrence et al., 2005; Satterfield and Cantwell, 1974). Furthermore, amelioration of these arousal differences also results in significant improvements in their clinical symptoms. This has potential implications for clinical interventions for ASDs. Interestingly, there are numerous studies that have administered stimulants such as methylphenidate or dexamphetamine (typical treatments for AD/HD) to individuals with ASDs. Overwhelmingly, improvements appear to be most common in hyperactivity (Posey et al., 2005; Quintana et al., 1995), whereas the impact on clinical symptoms of ASDs is mixed with some studies demonstrating improvements (Handen et al., 2000; Jahromi et al., 2009) whilst others show no effects (Di Martino et al., 2004; Posey et al., 2007). Furthermore, negative side-effects are common, including depression and social withdrawal. Given that the present study found differences in resting arousal profiles of ASDs, this may account for the variability in the findings. Furthermore, it suggests that treatments may need to be individually tailored according to resting arousal levels.

4.2. Conclusion In conclusion, this study demonstrated that high-functioning individuals with ASDs will show different behavioural profiles depending on their resting arousal levels (SCLs). This provides a potential explanation for the high degree of variability in the literature with respect to social cognitive abilities in ASDs, including basic emotion recognition, judgements of trustworthiness, and cognitive and affective empathy. Therefore, future studies should account for differences in resting arousal levels when investigating behavioural responses in this population. These findings also have important implications for clinical interventions.

Acknowledgements DM is supported by an Australian Postgraduate Award (APA). JAR is supported by an Australian National Health and Medical Research Council (NHMRC) Postdoctoral Fellowship (Clinical Training; APP1013796). This research was funded by the Australian NHMRC. We would like to thank the individuals who gave their time to participate in this study and the clinicians who assisted with participant recruitment.

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