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Biological Motion Perception in Autism Spectrum Disorder: a Meta-Analysis Greta Krasimirova Todorova1* , Rosalind Elizabeth Mcbean Hatton2 and Frank Earl Pollick1

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Biological Motion Perception in Autism Spectrum Disorder: a Meta-Analysis Greta Krasimirova Todorova1* , Rosalind Elizabeth Mcbean Hatton2 and Frank Earl Pollick1 Todorova et al. Molecular Autism (2019) 10:49 https://doi.org/10.1186/s13229-019-0299-8 RESEARCH Open Access Biological motion perception in autism spectrum disorder: a meta-analysis Greta Krasimirova Todorova1* , Rosalind Elizabeth Mcbean Hatton2 and Frank Earl Pollick1 Abstract Background: Biological motion, namely the movement of others, conveys information that allows the identification of affective states and intentions. This makes it an important avenue of research in autism spectrum disorder where social functioning is one of the main areas of difficulty. We aimed to create a quantitative summary of previous findings and investigate potential factors, which could explain the variable results found in the literature investigating biological motion perception in autism. Methods: A search from five electronic databases yielded 52 papers eligible for a quantitative summarisation, including behavioural, eye-tracking, electroencephalography and functional magnetic resonance imaging studies. Results: Using a three-level random effects meta-analytic approach, we found that individuals with autism generally showed decreased performance in perception and interpretation of biological motion. Results additionally suggest decreased performance when higher order information, such as emotion, is required. Moreover, with the increase of age, the difference between autistic and neurotypical individuals decreases, with children showing the largest effect size overall. Conclusion: We highlight the need for methodological standards and clear distinctions between the age groups and paradigms utilised when trying to interpret differences between the two populations. Keywords: Autism spectrum disorders, Biological motion, Meta-analysis, Age, Emotion recognition Background intellectual disability have been shown to have no prob- Biological motion (BM), namely the movement of other lem in identifying different types of motion [5, 6], humans, conveys information that allows the identifica- whereas individuals with social functioning difficulties tion of affective states and intentions [1–3]. BM process- such as autism spectrum disorder (ASD) have shown re- ing specifically is the ability of individuals to detect, label duced ability in extracting social information from BM and interpret human movement and to allocate certain [7]. Indeed, ASD’s main diagnostic characteristics in- emotional states to it. Thus, BM is an important compo- clude problems with social interaction and communica- nent of social perception. Moreover, neurotypically de- tion as well as repetitive and/or restrictive behaviours veloping (NT) individuals have been shown to be able to [8]. Thus, the social impairment in ASD can, to some readily extract socially relevant information from sparse extent, be readily related to a reduced ability to extract visual displays [1, 2]. Specifically, point-light displays information from BM. (PLDs), which portray BM with points located only on However, findings on BM in ASD tend to be mixed the major joints, are readily recognised as depicting dif- [7]. For example, some studies, which investigated the fering actions by NT [4]. identification or recognition of actions from BM [9–12], Pavlova [2] argues that an inability to extract socially did not find significant differences between NT and relevant information from BM could have damaging ef- ASD individuals, whereas others have found differences fects on social functioning. In fact, individuals with an between the two groups [13–15]. Simmons et al. [7] and McKay et al. [14] argue that this is because there is vari- ability between ASD individuals. Several factors have * Correspondence: [email protected] 1University of Glasgow, 62 Hillhead Street, Glasgow G12 8AD, UK been suggested to introduce this variability. Full list of author information is available at the end of the article © The Author(s). 2019, corrected publication 2021 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Todorova et al. Molecular Autism (2019) 10:49 Page 2 of 28 One of these potential factors is age. Specifically, on reduced visual orientation to biological motion [5, 26, 27]. the one hand, it appears that research in children tends This difference between NT and ASD has not been found to consistently show an impairment in BM interpret- in adults [28]. In contrast, Fujisawa et al. [29]showthat ation [5, 13, 16]. Whilst, on the other hand, research in pre-school children tend to have a greater preference for adults does not find differences in performance in action upright than inverted BM, which was additionally greater perception and BM recognition [9–11]. than that in NT children. Hence, it is apparent that incon- Person characteristics such as sex and IQ have also sistencies in eye-tracking studies also exist but cannot be been suggested to contribute to the variability of re- simply explained by age as a driving factor. sults. Specifically, IQ has been identified as a predictor One study argued that the mixed findings in the BM of performance in some studies [17, 18]butnotin literature within ASD are due to ASD utilising different others [9, 19, 20]. Furthermore, a recent meta-analysis brain networks which develop later in life. Hence, by Van der Hallen et al. [21] looked at local vs. global McKay et al. [14] investigated BM perception between paradigms, where individuals have to ignore the global ASD and NT and found that the brain areas that com- context to be able to focus and perform a task on the municate with each other in ASD are not the same as specific parts or vice-a-versa. They observed greater dif- the ones found in NT. Specifically, functional magnetic ferences when the proportion of females was higher. resonance imaging (fMRI) studies tend to find reduced Hence, these demographic characteristics of the sam- activation in ASD for areas such as the superior tem- ples should be investigated as potential contributors to poral sulcus, middle temporal gyrus and inferior parietal the variability in the findings. lobule. These are all areas that have been found to be re- The task at hand has also been considered as a con- lated to the perception and interpretation of human mo- tributing factor. Koldewyn et al. [22] argue that individ- tion and actions [30–32]. NT individuals, however, show uals with ASD are able to identify BM presented connectivity within areas involved with action and hu- through simple PLDs from noise and classify them; how- man motion observation—such as the inferior and su- ever, it is the extraction of higher order information, perior parietal lobules. On the other hand, individuals such as emotional content, that shows the largest per- with autism have been found to have brain networks formance difference. In fact, although Hubert et al. [9] that involve connectivity with the fusiform, middle tem- and Parron et al. [12] did not find differences between poral and occipital gyri, which are all areas considered to NT and ASD in action recognition, they found differ- be involved in more basic level motion perception rather ences in emotion recognition from biological motion for than action recognition [14, 31]. adults and children. Additionally, Fridenson-Hayo et al. Similarly, the mirror neuron network (MNN) has been [23] found that in children, this difference in emotion implied to be related to social functioning as it is associ- recognition from BM is evident for both basic (e.g. ated with observing and understanding the actions of happy, sad) and complex emotions (e.g. disappointed, others. Thus, Kaiser and Shiffrar [33] argue that the proud) as well as being evident cross culturally (Britain, MNN could contribute to the impairments seen in ASD. Sweden, Israel). Thus, both children and adults with Moreover, Villalobos et al. [34] have shown reduced ASD tend to be less sensitive to emotional content. functional connectivity in the prefrontal mirror neuron It has been suggested that eye-tracking research can in- area in individuals with ASD. The MNN has mainly form our understanding of the social difficulties in ASD. been investigated in imitation paradigms [35, 36] and in- A review and meta-analysis of eye-tracking studies showed deed, dysfunctional activation has been identified in in- that in ASD, attention to social versus non-social stimuli dividuals with ASD. However, since the MNN is also may be reduced [24]. The analysis also found that de- involved in understanding others’ actions, its activation creased attention might be given to the eyes and increased during simple action observation has also been investi- attention to the mouth and body compared to NT individ- gated in ASD because understanding others’ actions is uals. However, Chita-Tegmark [24] noted that the results an integral part of social functioning. Most commonly, were very mixed. This may have been because the authors mu-suppression has been used to assess human mirror tried to include a large number of studies and thus inevit- activity [37] and reduced mu-suppression
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