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Visual Event-Related Potentials to Biological Motion Stimuli in Autism Spectrum Disorders

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Visual Event-Related Potentials to Biological Motion Stimuli in Autism Spectrum Disorders doi:10.1093/scan/nst103 SC AN ( 2014 ) 9, 1214 ^12 2 2 Visual event-related potentials to biological motion stimuli in autism spectrum disorders Anne Kro¨ger,1 Anke Bletsch,1 Christoph Krick,2 Michael Siniatchkin,1 Tomasz A. Jarczok,1 Christine M. Freitag,1 and Stephan Bender1,3 1Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, JW Goethe University Frankfurt, Deutschordenstrasse 50, Frankfurt 60528, Germany, 2Department of Neuroradiology, Saarland University Hospital, Kirrbergerstraße, Homburg/Saar 66424, Germany, and 3Department of Child and Adolescent Psychiatry and Psychotherapy, University of Technology Dresden, Fetscherstraße 74, Dresden 01307, Germany Downloaded from https://academic.oup.com/scan/article/9/8/1214/2375397 by guest on 28 September 2021 Atypical visual processing of biological motion contributes to social impairments in autism spectrum disorders (ASD). However, the exact temporal sequence of deficits of cortical biological motion processing in ASD has not been studied to date. We used 64-channel electroencephalography to study event-related potentials associated with human motion perception in 17 children and adolescents with ASD and 21 typical controls. A spatio-temporal source analysis was performed to assess the brain structures involved in these processes. We expected altered activity already during early stimulus processing and reduced activity during subsequent biological motion specific processes in ASD. In response to both, random and biological motion, the P100 amplitude was decreased suggesting unspecific deficits in visual processing, and the occipito-temporal N200 showed atypical lateralization in ASD suggesting altered hemispheric specialization. A slow positive deflection after 400 ms, reflecting top-down processes, and human motion-specific dipole activation differed slightly between groups, with reduced and more diffuse activation in the ASD-group. The latter could be an indicator of a disrupted neuronal network for biological motion processing in ADS. Furthermore, early visual processing (P100) seems to be correlated to biological motion- specific activation. This emphasizes the relevance of early sensory processing for higher order processing deficits in ASD. Keywords: event-related-potentials; motion perception; P100; N200; hemisphere-asymmetry INTRODUCTION (Price et al., 2012). In other studies, especially with adult samples, Autism spectrum disorder (ASD) is a neurodevelopmental disorder impairments were less prominent (Murphy et al., 2009; Saygin et al., characterized by impairments in social interaction, communication, 2010; Jones et al., 2011; Rutherford and Troje, 2012; Nackaerts et al., and repetitive and stereotyped behaviours and interests (American 2012). Still, adults with ASD were less sensitive to human motion when Psychiatric Association, 2000). Impaired visual processing of biological presented by masked displays (Kaiser et al., 2010a). motion has been the focus of recent neuropsychological and brain The neural mechanisms underlying biological motion perception imaging studies in ASD (Kaiser and Pelphrey, 2012). Recognition of also differ between ASD and typically developing controls (TCs). biological motion, including eye movements, facial expressions and Neuroimaging studies showed reduced or atypical activation of tem- body gestures, is crucial for the development of adequate social inter- poral regions, including the superior temporal sulcus (STS) and gyrus, action and adaptive responses, and usually emerges early in develop- and the fusiform gyrus in ASD (Herrington et al., 2007; Freitag et al., ment (Grossmann and Johnson, 2007; Simion et al., 2008). 2008; Kaiser et al., 2010b; Koldewyn et al., 2011). Other studies ques- Furthermore, biological motion perception deficits might be a tioned the specificity of biological motion perception difficulties. marker of disorders characterized by difficulties in social interaction Atypical neural activation also to arbitrarily moving point-light dis- and social cognition (Pavlova, 2012). plays (Freitag et al., 2008) and reduced activity in the middle temporal Classical human motion stimuli are the so-called point-light displays area (MTþ/V5) to motion stimuli (Herrington et al., 2007) were also introduced by Johansson (1973). Children with autism showed im- reported in ASD. Another study found abnormal brain activation al- paired recognition of human motion from these point-light displays ready in the primary visual cortex (Brieber et al., 2010). (Blake et al., 2003), failed to orient to such motions patterns (Klin In contrast to functional magnetic resonance imaging, electroen- et al., 2009; Annaz et al., 2012), and showed an abnormal development cephalography (EEG) has a higher temporal resolution. Thus, EEG of human motion recognition abilities during development (Annaz represents an excellent tool to assess the temporal sequence of different et al., 2010). Similarly, in adolescents with ASD higher detection neuronal sub-processes. EEG studies on biological motion perception thresholds for human motion (Koldewyn et al., 2010) and a reduced in healthy populations have described several event-related potentials sensitivity towards irregularities in human motion were reported (ERPs). Two studies found increased activation peaks 100 ms after stimulus-onset especially in right occipital regions to human compared Received 21 December 2012; Revised 24 May 2013; Accepted 16 July 2013 to non-biological motion (Hirai et al., 2009; Krakowski et al., 2011). Advance Access publication 24 July 2013 This P100 can be interpreted as a marker of elementary stimulus fea- C. Freitag and S. Bender contributed equally to this work. ture processing (Allison et al., 1999) and early motion detection First, we thank all families, who supported our work by participating in our study. We also thank Jennifer Bçhm and Katharina Hof for assistance with the data collection, Benjamin Teufert for data calculations and our clinical (Krakowski et al., 2011). After this first component, a stronger negative colleagues for helping us with recruiting participants. This work was supported by the foundation of Marie Christine deflection to human compared to non-biological motion stimuli peak- Held and Erika Hecker to A.K., the German Research foundation ‘Deutsche Forschungsgemeinschaft’ to C.M.F. ing around 200 ms is frequently described (Hirai et al., 2003, 2009; (FR2069/2-1), and by the LOEWE-Program ‘Neuronal Coordination Research Focus Frankfurt’ (NeFF) to C.M.F. Jokisch et al., 2005; Hirai and Kakigi, 2008). It seems to reflect more and S.B. Correspondence should be addressed to Anne Krçger, Department of Child and Adolescent Psychiatry, specific motion processing (Hirai and Kakigi, 2008) including detec- Psychosomatics, and Psychotherapy, JW-Goethe University Frankfurt, Deutschordenstraße 50, 60528 Frankfurt, tion of motion direction (Niedeggen and Wist, 1999) in MTþ/V5. Germany. E-mail: [email protected] Using high-density electrical mapping and source analysis on ß The Author (2013). Published by Oxford University Press. For Permissions, please email: [email protected] BiologicalmotionprocessinginASD SCAN(2014) 1215 difference waves (biological–random motion), Krakowski et al. Table 1 Descriptive data and behavioural data (mean Æ s.d.) described a dipolar activity starting after approximately 300 ms. Its source was located in posterior middle temporal regions bilateral Mean Æ s.d. ASD-patients TCs (N ¼ 21) Statistics near the posterior STS (Krakowski et al., 2011), a neuronal region (N ¼ 17) important for social information processing (Hein and Knight, Age 11.9 Æ 2.2 11.63 Æ 2.4 t ¼0.34, P ¼ 0.73 2008). Finally, a positive deflection at centro-parietal electrodes start- IQ (Raven) percent rank 77.6 Æ 30.2 59.1 Æ 38.2 Z ¼1.5, P ¼ 0.14 ing approximately after 400 ms was described (P400þ), with greater Correct responses to ‘walker’ (%) 85.7 Æ 4.8 (95.2%) 84.8 Æ 6.8 (94.2%) Z ¼0.4, P ¼ 0.73 Correct responses to ‘scramble’ (%) 85.2 Æ 4.2 (94.7%) 83.8 Æ 9.5 (93.1%) Z ¼0.5, P ¼ 0.62 amplitudes during human motion processing when the human motion Reaction time to ‘walker’ (s) 1.41 Æ 0.27 1.35 Æ 0.29 t ¼0.63, P ¼ 0.53 aspect of the stimuli was actively attended (Krakowski et al., 2011). Reaction time to ‘scramble’ (s) 1.45 Æ 0.28 1.43 Æ 0.28 t ¼0.26, P ¼ 0.80 This component was interpreted as a marker of top-down cognitive processes involved in active decoding of stimulus content and might be a sub-component of the so-called late positive complex (LPC). A not- ably later and more broadly distributed LPC around 500–600 ms has TCs were recruited from local schools and screened with the Downloaded from https://academic.oup.com/scan/article/9/8/1214/2375397 by guest on 28 September 2021 also been observed, for example when object parts were difficult to German version of the Child Behavior Checklist (Arbeitsgruppe recover (Schendan and Kutas, 2007). Kinder-, Jugend- und Familiendiagnostik, 1998) for any clinically rele- To date, no study has been performed assessing different stages of vant symptoms. Participants with T-scores >60 on the second order biological motion compared to non-biological motion processing in scales or >70 on any first order subscales, respectively, were excluded. ASD using ERPs. Because of the contradictory findings of specifically IQ was assessed using the standard (above 11.5 years) or coloured impaired biological motion processing vs generally impaired motion (below 11.5 years) progressive matrices
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