Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum

Abstract

Background Biological motion imparts rich information related to the movement, actions, intentions and affective state of others, which can provide foundational support for various aspects of social cognition and behavior. Given that atypical social communication and cognition are hallmark symptoms of autism spectrum disorder (ASD), many have theorized that a potential source of this deficit may lie in dysfunctional neural mechanisms of biological motion processing. Synthesis of existing literature provides some support for biological motion processing deficits in autism spectrum disorder, although high study heterogeneity and inconsistent findings complicate interpretation. Here, we attempted to reconcile some of this residual controversy by investigating a possible modulating role for attention in biological motion processing in ASD. Methods We employed high-density electroencephalographic recordings while participants observed point-light displays of upright, inverted and scrambled biological motion under two task conditions to explore spatiotemporal dynamics of intentional and unintentional biological motion processing in children and adolescents with ASD (n = 27), comparing them to a control cohort of neurotypical (NT) participants (n = 35). Results Behaviorally, ASD participants were able to discriminate biological motion with similar accuracy to NT controls. However, electrophysiologic investigation revealed reduced automatic selective processing of upright biologic versus scrambled motion stimuli in ASD relative to NT individuals, which was ameliorated when task demands required explicit attention to biological motion. Additionally, we observed distinctive patterns of covariance between visual potentials evoked by biological motion and functional social ability, such that Vineland Adaptive Behavior Scale-Socialization domain scores were differentially associated with biological motion processing in the N1 period in the ASD but not the NT group. Limitations The cross-sectional design of this study does not allow us to definitively answer the question of whether developmental differences in attention to biological motion cause disruption in social communication, and the sample was limited to children with average or above cognitive ability. Conclusions Together, these data suggest that individuals with ASD are able to discriminate, with explicit attention, biological from non-biological motion but demonstrate diminished automatic neural specificity for biological motion processing, which may have cascading implications for the development of higher-order social cognition.

Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum

“…Therefore, one possible interpretation is that attenuated IC processing in the ASD group may reflect, in part, a tendency to overfocus on the color change task with less allocation of attentional resources toward the IC stimuli. A recent investigation involving other visual tasks has indicated a modulating role of attention in contributing to electrophysiological visual processing deficits observed in ASD, whereby children with ASD may have specific deficits in automatic processing that can be partially to completely ameliorated by explicit attention to processing these stimuli ( Knight et al, 2022a ). Potentially supportive of this possibility are the ASD-associated differences in contour integration that extend beyond the lateral occipital region into the left frontotemporal and parietal regions that were identified here through exploratory analysis, although this finding should be interpreted with much caution given the post hoc design.…”

Neural correlates of audiovisual narrative speech perception in children and adults on the autism spectrum: A functional magnetic resonance imaging study

“…We also compared both groups in regard to their brain responses to the unisensory auditory and visual conditions. We expected altered responses to the visual stimulus on the basis of ample evidence for decreased brain responses in ASD to human faces (Kuno‐Fujita et al, 2020; Nomi & Uddin, 2015; Pierce et al, 2001; Riddiford et al, 2022) and biological motion (Blake et al, 2003; Federici et al, 2020; Foglia et al, 2022; Klin et al, 2009; Knight et al, 2022; Van der Hallen et al, 2019) as well as speechreading (Iarocci et al, 2010; Schelinski et al, 2014; Smith & Bennetto, 2007). We also expected that previous findings of deficits in more general language (Vogindroukas et al, 2022) and social cognitive functions (Castelli et al, 2002; Misra, 2014; Oliver et al, 2021) would manifest in regions associated with auditory and semantic processing and social cognition.…”

“…While we expected to find between group differences in the auditory alone condition, we did not formulate more specific hypotheses in regard to cortical location due to several factors: The complexity of our naturalistic auditory stimulus, the fact that in ASD abnormalities have been reported across the auditory processing hierarchy from early sensory (Chen et al, 2020; Key & D'Ambrose Slaboch, 2021; Schwartz et al, 2018) to higher order language (Vogindroukas et al, 2022) and social‐cognitive functions (Bottema‐Beutel et al, 2019; Goodwill et al, 2023; Lartseva et al, 2014; Velikonja et al, 2019); and there is the possibility of complex interactions between processing stages (Crosse et al, 2022). Similarly, neural processes underlying the analysis and integration of visual articulatory motion span multiple processing stages for most of which deficits have been reported in ASD including eye‐gaze and face processing (Kuno‐Fujita et al, 2020; Nomi & Uddin, 2015; Pierce et al, 2001; Riddiford et al, 2022) global and biological motion perception (Blake et al, 2003; Federici et al, 2020; Foglia et al, 2022; Knight et al, 2022; Van der Hallen et al, 2019) with possible downstream impacts on speechreading (Iarocci et al, 2010; Schelinski et al, 2014; Smith & Bennetto, 2007). We therefore expected to find group differences in this condition as well but could not specify locations other than regions activated by the task.…”

It’s all in the timing: Delayed feedback in autism may weaken predictive mechanisms during contour integration

“…Notably, all paradigms that rely on behavioral identification of illusory contour presence or absence necessarily force explicit attention to contour integration whereas electrophysiologic paradigms allow for examination of automatic contour integration processing while attention is directed elsewhere. It remains a possibility that neural mechanisms of contour integration are augmented when participants are explicitly attending to illusory contour presence/absence, a phenomenon that has been described in other types of global visual perception in autism (Knight EJ et al, 2022). Additional studies to compare across developmental disability populations such as ADHD and to directly assess the role of attention by comparing contour integration in attended vs. passive processing would be highly interesting.…”