Blain et al (2017) Schiz Res

SCHRES-07032; No of Pages 4 Schizophrenia Research xxx (2016) xxx–xxx

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Subtle cues missed: Impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits Scott D. Blain ⁎, Joel S. Peterman, Sohee Park Department of Psychology, Vanderbilt University, 111, 21st Avenue South, Nashville, TN 37240, United States

a r t i c l e

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Article history: Received 10 June 2016 Received in revised form 4 October 2016 Accepted 4 November 2016 Available online xxxx Keywords: Biological motion Embodiment Emotion perception Schizophrenia Autism

a b s t r a c t Background: Deficits in emotion perception are central features of schizophrenia and autism spectrum disorders.

These conditions are also associated with disrupted embodiment and impaired processing of biological motion.

However, medication and the impact of illness over time complicate the study of socioemotional processing in such neuropsychiatric populations. Thus, the current study investigated the perception of emotional cues from gait, in relation to autistic and schizotypal traits in the general population.

Methods: Self-report measures of schizotypy and autism-spectrum were obtained from 107 healthy participants.

An affective biological motion task that required participants to discriminate emotions from the gait patterns of polygonal avatars at varying levels of emotional intensity was used to assess accuracy of emotion perception.

Results: Emotion perception accuracy depended on the stimulus intensity. Those with elevated autism spectrum quotient and those with elevated positive syndrome (cognitive-perceptual) schizotypy showed deficits in emotion perception from gait.

Conclusions: Perception of emotion from low-intensity gait cues is compromised in those who may carry liability for autism or psychosis. Emotion perception deficits may be a core feature of autism and schizophrenia, rather than simply being a downstream consequence of illness duration or medication. © 2016 Published by Elsevier B.V.

1. Introduction Accurate emotion perception serves adaptive functions in the “real world” and predicts social outcome (Elfenbein et al., 2007; Hooker and Park, 2002). Typically, emotion perception has been investigated using faces (e.g., Ekman, 1993) but in daily life, we utilize multiple channels including voices, postures, and movements to perceive and express emotions. Bodily cues such as gait patterns are especially useful when stimuli are at a distance or faces are obscured (Atkinson et al., 2007; de Gelder, 2006). Deciphering the emotion of an approaching person can influence social decision-making in real time (e.g., decision to approach or withdraw).

Social impairments including deficits of facial emotion perception are well documented in schizophrenia (Couture et al., 2010; Pinkham et al., 2008) and autism (Lozier et al., 2014; Pinkham et al., 2008).

Schizophrenia and autism are also associated with impaired decoding of emotions from gait and posture (Atkinson, 2009; Hubert et al., 2007; Peterman et al., 2014). Both autism- and schizophrenia-spectrum show social cognitive impairments, including deficits of face processing, emotion recognition, and theory of mind at the behavioral and neural ⁎ Corresponding author.

E-mail addresses: scottblain7@icloud.com (S.D. Blain), joel.peterman@vanderbilt.edu (J.S. Peterman), sohee.park@vanderbilt.edu (S. Park).

levels (see Sasson et al., 2011; Pinkham et al., 2008). Nonetheless, given the impact of the illness and medication over time, it is difficult to conclude whether emotion processing impairment is a fundamental feature of these conditions, or an outcome of the illness itself. Studying elevated autistic or schizotypal traits in healthy participants can address these concerns. Facial emotion perception impairments are associated with schizotypy (e.g., Brown and Cohen, 2010; Germine and Hooker, 2011), and elevated autism-spectrum traits (e.g., Harms et al., 2010; Poljac et al., 2013). Less is known about emotion perception from gait or body posture. Biological motion perception deficits have been shown in autism (Blake et al., 2003; Miller and Saygin, 2013) and schizophrenia (Kim et al., 2005; Kim et al., 2011), but emotion perception from gait has not been elucidated in relation to autistic/schizotypal traits. Thus, we sought to elucidate emotional gait perception in relation to schizotypal and autism traits.

We hypothesized that schizotypal and autistic traits would correlate inversely with gait perception accuracy. Current psychometric models of schizotypy consist of three factors (cognitive-perceptual, interpersonal and disorganized) that correspond to positive, negative and disorganized syndromes of schizophrenia (Raine, 1991; Raine et al., 1994).

Depending on the nature of the deficits in emotion perception in schizophrenia (e.g., perceptual abnormalities or socio-emotional processing), performance on the affective gait task may be differentially associated with the sub-factors of schizotpy. If emotion perception deficits in

http://dx.doi.org/10.1016/j.schres.2016.11.003 0920-9964/© 2016 Published by Elsevier B.V.

Please cite this article as: Blain, S.D., et al., Subtle cues missed: Impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits, Schizophr. Res. (2016), http://dx.doi.org/10.1016/j.schres.2016.11.003

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schizotypal individuals stem from perceptual difficulties, gait task accuracy would be inversely correlated with the perceptual-cognitive factor.

If, on the other hand, emotion perception deficits arise from abnormal socio-emotional processing rather than perceptual problems, accuracy should be inversely associated with interpersonal schizotypy.

Table 2 Gait perception accuracy.

Task performance at three intensities

Mean raw score (s.d.)

Mean % correct (s.d.)

Total

50.0 (6.2) 59.6 (4.5) 61.7 (3.6)

78.2 (9.6) 93.1 (7.1) 96.4 (5.6)

2. Methods

50% 100% 150%

2.1. Participants 107 students (75 women) were recruited from Vanderbilt University. Exclusion criteria were diagnosed psychiatric and neurological disorders, substance use within 6 months, history of head injury and current psychotropic medication. See Table 1 for demographic information. The study protocol was approved by the Vanderbilt University Institutional Review Board. Participants gave written informed consent and received course credit.

2.2. Procedure All participants completed self-report measures before the gait perception task.

2.3. Self-report questionnaires The Schizotypal Personality Questionnaire (SPQ; Raine, 1991) is a 74item, true/false, questionnaire consisting of cognitive-perceptual, interpersonal, and disorganized factors.

The Autism-spectrum Quotient 10 (AQ-10; Allison et al., 2012) is designed to assess autism traits in adults. Participants respond using a four-point scale (1 = strongly disagree; 4 = strongly agree). Responses are coded as zero or one, with one point awarded if a participant endorses the “autistic trait.”

2.4. Emotion perception from gait The stimuli were polygonal ‘walking’ avatars created with motion morphing, which allowed for parametric adjustment of the emotional ‘signal’ in the stimulus (see Roether et al., 2009 for the details of standardization of the emotional gait stimuli). There were both angry and happy stimuli, each with three intensity levels: 50% (attenuated), 100% (prototypical) and 150% (exaggerated). Aspects of the movement that defined the emotional content were flexion of the head and arms (head tilted forward for anger and tilted backward for happy), and postural positioning of the torso (pitched forward for anger and leaned back for happy).

For each trial, participants were asked to view a walking avatar on a computer screen for 1 s and determine whether the avatar's gait resembled happy or angry emotion. Participants indicated their choice by pressing the “H” key for happy or “A” key for angry. There was no time limit. Accuracy and reaction time were recorded. Happy and

Angry stimuli were interspersed randomly. There were 96 happy stimuli (32 per intensity level), 96 angry stimuli (32 per intensity). There were 10 practice trials before testing. See Fig. 1 for the stimuli and procedure.

3. Results Repeated-measures ANOVA showed a significant effect of intensity on accuracy (F (2, 216) = 414.07, p b 0.001). A repeated-measures ANCOVA revealed a significant interaction effect of intensity and AQ on accuracy (F (2, 214) = 4.27, p b 0.05). Although there was no effect of intensity on accuracy for SPQ-total (F (2, 214) = 1.49, p N 0.23), there was a significant interaction of stimulus intensity and cognitive-perceptual factor of SPQ (F (2, 214) = 5.47, p b 0.01). There were no interactions of intensity and interpersonal or disorganized factors of schizotypy (p N 0.05).

Overall accuracy for 100% and 150% intensity was at ceiling (Table 2).

Thus, correlations between 50% (low-intensity) gait perception accuracy and self-report measures were calculated. There was a significant correlation between AQ and gait perception accuracy at 50% (r = −0.26, p b 0.01). Although total SPQ score was not significantly associated with gait perception, since the cognitive-perceptual factor had a significant interaction effect with intensity on accuracy, we examined correlations between gait perception and SPQ factors. Gait perception accuracy at 50% intensity correlated negatively with cognitive-perceptual (ρ = −0.22, p = 0.023), but not with interpersonal (p N 0.86) or disorganization (p N 0.51) factors. Correlations of gait perception with AQ and SPQ could not be explained by selection bias for happy stimuli, as bias was not directly correlated with AQ or SPQ (p b 0.05). Furthermore, there were no significant correlations with reaction time at any intensity (p b 0.05).

Multiple regression analysis was conducted to assess the independent effects of AQ and SPQ sub-factors on gait perception accuracy at 50%. The overall model had significant fit (F (4, 104) = 4.57, R2 = 0.15, p = 0.002). AQ (β = −0.32, p = 0.002) and cognitive-perceptual schizotypy (β = −0.30, p = 0.007) had independent negative effects on accuracy, while affective schizotypy and disorganization had no significant effects (p b 0.05).

Lastly, AQ was positively correlated with SPQ (ρ = 0.40, p b 0.001) as well as cognitive-perceptual (ρ = 0.28, p b 0.01), affective (ρ = 0.36, p b 0.001), and disorganization (ρ = 0.36, p b 0.001) sub-factors.

4. Discussion

Table 1 Demographic information and self-report data.

Mean age

19.73 (SD = 1.30)

Race/ethnicity

59.6% White 20.2% Asian 10.1% African-American 0.9% Hispanic/Latino 8.3% Multiracial 0.9% Other 3.0 (SD = 1.6), Range = [0, 7] 18.4 (SD = 10.7), Range = [1, 54] 6.8 (SD = 5.2), Range = [0, 24] 8.9 (SD = 6.2), Range = [0, 26] 4.6 (SD = 3.5), Range = [0, 15]

AQ-10 SPQ

Total Cognitive-perceptual Interpersonal Disorganized

Recent research showed impaired perception of emotional cues in gait, in patients with schizophrenia (Peterman et al., 2014), adding to a growing body of work documenting emotion perception deficits in individuals with schizophrenia and autism (Couture et al., 2010; Hubert et al., 2007; Lozier et al., 2014), as well as those with latent liability (Miller and Lenzenweger, 2012; Miller and Saygin, 2013; Platek et al., 2005; Poljac et al., 2013). We sought to extend this research by investigating gait perception in relation to schizotypy and autistic traits.

Cognitive-perceptual schizotypy and autism-spectrum quotient were negatively associated with emotion perception at low stimulus intensity, despite intact ability to categorize emotions at higher intensities. Furthermore, these associations remained after inclusion of AQ

Please cite this article as: Blain, S.D., et al., Subtle cues missed: Impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits, Schizophr. Res. (2016), http://dx.doi.org/10.1016/j.schres.2016.11.003

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Fig. 1. Schematic diagram of the task procedure. Participants viewed a fixation cross for 1000 ms and then each stimulus was presented for 1000 ms. After stimulus presentation, participants indicated their chosen response with one of two keys. There was no response time limit.

and all SPQ sub-factors in a multiple regression model, indicating independent effects. Perception of low-intensity emotions is important for initial social judgments in daily life (Bar et al., 2006; Young et al., 1997).

Impaired emotion perception by individuals with high cognitiveperceptual schizotypy has previously been reported (van't Wout et al., 2004). Findings of impaired gait perception also build on research demonstrating impaired recognition of biological motion in schizophrenia (Kim et al., 2005; Kim et al., 2011). One possible explanation for impaired gait perception is disrupted embodiment and sense of bodily self, associated with the schizophrenia-spectrum (Germine et al., 2013; Stanghellini, 2009; Thakkar et al., 2011; Michael and Park, 2016); anomalous embodiment may contribute to disrupted processing of emotional cues in the bodies of others.

Negative correlations between low-intensity gait perception accuracy and AQ found in our study are concordant with past studies of emotion perception from static stimuli (Miller and Saygin, 2013; Poljac et al., 2013). Our findings suggest that individuals with high AQ may find it difficult to detect emotional cues in gait. This is in line with research demonstrating impaired recognition of emotional-biological motion among individuals with ASD (Hubert et al., 2007).

These results also serve to further validate the AQ-10. The majority of studies showing correlations of AQ with emotion perception utilized the full 50-item version (e.g., Aaron et al., 2015; Miller and Saygin, 2013). Results of a recent study found the AQ-10 is as valid as the original AQ for predicting whether an individual has a diagnosable autism spectrum disorder (Booth et al., 2013). Our replication of correlations of AQ with SPQ, as well as emotion perception, suggest that the AQ-10 may be useful as a less time-intensive measure.

There are limitations to our study. First, while the discrete emotion labels “happy” and “angry” were used, these labels and their connotations could have influenced performance (Barrett et al., 2007). In future studies, it may be best to replace such labels with “positive” and “negative” affect. Second, we only used two types of emotional gait stimuli, which limits the generalizability of our results to the full range of emotions. Finally, the participants in the current study were sampled from a high-functioning group of undergraduate students, and thus the range of SPQ (1 to 54) and AQ (0 to 7) scores is not large. On the other hand, the SPQ was developed using college samples that are demographically very similar to our study participants (see Raine, 1991 for details). The main advantage of using a “clean” sample is that confounding illness or pharmacological medication variables can be minimized, and our results suggest that further investigation of gait perception in autism and schizotypy is warranted.

Despite these limitations, the finding of significant relationships between low-intensity emotion perception and latent liability for conditions like autism and schizophrenia, suggests that such difficulties may be more directly related to the core features of these disorders rather than a downstream consequence of the full manifestation of the condition.

Role of the funding source This work was supported in part by the Gertrude Conaway Vanderbilt Endowment Professorship Fund to Sohee Park.

Contributors Sohee Park, Scott Blain and Joel Peterman designed the study and the protocol. Scott Blain and Sohee Park managed the literature search and analyses. Scott Blain undertook the statistical analysis, wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.

Conflict of interest All authors declare that they have no conflicts of interest.

Acknowledgement We would like to thank Matthew Snodgress, Kamyl Harvey, Zidong Zhao, and Heath Nichols for their help.

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Please cite this article as: Blain, S.D., et al., Subtle cues missed: Impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits, Schizophr. Res. (2016), http://dx.doi.org/10.1016/j.schres.2016.11.003