Plasticity of temporal binding in children with autism spectrum disorder: A single case experimental design perceptual training study
Introduction
Autism spectrum disorder (ASD) has historically been defined by deficits in social communication and by the presence of restricted and repetitive patterns of behavior, interests, and activities (American Psychological Association [APA], 2000). Recent changes to diagnostic criteria, however, now recognize sensory differences as a core characteristic of ASD (i.e., one of the four restricted/repetitive behavior features; APA, 2013). Children with ASD may show differences in their patterns of responding to information within the individual sensory modalities (e.g., within vision and audition; Baranek, David, Poe, Stone, & Watson, 2006; see Ben-Sasson et al., 2009 for a review). In addition, children on the autism spectrum display differences in how they combine information across multiple sensory modalities (i.e., in their multisensory integration; Murray, Lewkowicz, Amedi, & Wallace, 2016). Of particular note are differences in the ability to combine audiovisual input during natural speech.
A recent meta-analysis by Feldman et al. (2018) synthesized the large extant literature on audiovisual multisensory integration in individuals with ASD, and reinforced the presence of differences in integrating auditory and visual input in individuals on the autism spectrum. One of the most consistent findings was reduced temporal acuity for audiovisual speech (Noel, De Niear, Stevenson, Alais, & Wallace, 2017; Stevenson et al., 2014; Woynaroski et al., 2013), as indexed by larger temporal binding windows (TBWs; i.e., the period of time over which individuals tend to combine what they see and hear into a unitary percept; Wallace & Stevenson, 2014). Abnormally large TBWs can lead to integration of information that may be unrelated, causing confusion and/or requiring increased processing effort (Bahrick & Todd, 2012), and could ultimately result in weaknesses in the ability to accurately comprehend and represent speech cues (Wallace & Stevenson, 2014). It has been proposed that difficulties in integrating audiovisual speech may contribute to the broader range of “higher-level” core- and related-symptoms, such as language impairments, that are seen in ASD (e.g., Cascio, Woynaroski, Baranek, & Wallace, 2016). Concurrent correlations in the extant literature (e.g., Megnin et al., 2012; Mongillo et al., 2008; Patten, Watson, & Baranek, 2014; Righi et al., 2018; Smith, Zhang, & Bennetto, 2017) lend some empirical support to this theory.
If difficulties integrating audiovisual speech contribute to the other deficits seen in children with ASD, then intervening upon differences in multisensory integration, in particular for audiovisual speech, may translate to improved outcomes for children affected by autism (e.g., Baum, Stevenson, & Wallace, 2015; Cascio et al., 2016; Damiano-Goodwin et al., 2018; Feldman et al., 2018). To our knowledge, though, only two attempts at targeting audiovisual speech perception have been described in children with ASD (Irwin, Preston, Brancazio, D’angelo, & Turcios, 2015; Williams, Massaro, Peel, Bosseler, & Suddendorf, 2004); neither of these studies focused on the temporal domain. Thus, there is a pressing need to determine the extent to which temporal acuity (i.e., TBW) for audiovisual speech is malleable or plastic in children with ASD.
A number of perceptual training programs targeting the audiovisual TBW have been assessed in typically developed (TD) adults. These training programs have provided feedback after each trial of either a simultaneity judgment (SJ) task (i.e., wherein participants indicate whether they perceived auditory and visual stimuli to have occured at the same time; Powers, Hillock, & Wallace, 2009) or a temporal order judgment task (i.e., wherein participants indicate whether they perceived an auditory stimulus or a visual stimulus to have been presented first; Setti et al., 2014). These training programs have been shown to narrow the TBW in TD adults using simple stimuli (i.e., auditory beeps and visual flashes; Powers et al., 2009; Setti et al., 2014; Sürig, Bottari, & Röder, 2018) as well as audiovisual speech stimuli (De Niear, Gupta, Baum, & Wallace, 2018), and to do so in a relatively short period of time (i.e., 4–5 training sessions), particularly when task difficulty is high (De Niear, Koo, & Wallace, 2016). To our knowledge, however, the effects of perceptual training, specifically focused on audiovisual temporal acuity, have not been assessed in children with ASD.
This study represents a preliminary effort to examine the extent to which TBWs for audiovisual speech are malleable with perceptual training in children with ASD. The following specific research questions were posed:
- 1
Does our perceptual training narrow (i.e., decrease) TBW size for audiovisual speech in school-aged children with ASD compared to baseline conditions?
- 2
Do changes in TBW size persist after the training has been withdrawn?
- 3
Can the perceptual training be implemented with a high degree of procedural fidelity?
- 4
Do participants report that the perceptual training was (a) helpful or (b) enjoyable?
Section snippets
Methods
Our Institutional Review Board approved the recruitment and study procedures. Parents provided written informed consent, and participants provided written assent prior to participation in the study. All children were compensated for participating.
Results
Fig. 4 shows participants’ TBWs in the baseline, perceptual training, and maintenance conditions.
Discussion
This study represents the first experimental manipulation designed to impact the temporal acuity of multisensory integration, specifically targeting the temporal binding window for audiovisual speech, in children with ASD. The primary results indicate that TBWs may be malleable in at least some children with ASD, as evidenced by narrowing during computer-based perceptual training (and widening during baseline). Although there was some evidence to suggest that perceptual training may induce
Conclusion
This study was the first to empirically assess the impact of perceptual training on audiovisual temporal function in children with ASD. Although we cannot yet conclude that there is a functional relation between the training and changes in the TBWs for audiovisual speech, there was evidence for the plasticity of TBWs at school age in this clinical population. Future research utilizing single case research methods or a well-controlled group design is warranted to further evaluate the potential
Author contributions
TGW, MTW, and JIF posed the research questions and designed the study. DMS designed the probe and training tasks and wrote analysis scripts. TGW, JIF, KD, JGC, AT, NB and DMS collected, scored, and organized the data. YL and MC coded procedural fidelity and interobserver reliability data. TGW and JIF analyzed the data, interpreted the results, and drafted the manuscript. All authors read and approved the final manuscript.
Acknowledgements
This work was supported by NIHU54 HD083211 (PI: Neul), NIH/NCATSKL2TR000446 (PI: Woynaroski), NIH/NIDCD1R21 DC016144 (PI: Woynaroski), NIH T32 MH064913 (PI: Winder), and NIH/NCATS UL1 TR000445 (PI: Bernard). The authors would like to thank the families who participated in our study, as well as the thoughtful comments from our reviewers that led to a vastly improved manuscript.
References (44)
- et al.
Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder
Progress in Neurobiology
(2015) - et al.
Developmental sequelae and neurophysiologic substrates of sensory seeking in infant siblings of children with autism spectrum disorder
Developmental Cognitive Neuroscience
(2018) - et al.
Perceptual training enhances temporal acuity for multisensory speech
Neurobiology of Learning and Memory
(2018) - et al.
Audiovisual multisensory integration in individuals with autism spectrum disorder: A systematic review and meta-analysis
Neuroscience and Biobehavioral Reviews
(2018) - et al.
Research electronic data capture (REDCap) – A metadata-driven methodology and workflow process for providing translational research informatics support
Journal of Biomedical Informatics
(2009) - et al.
Multisensory processes: A balancing act across the lifespan
Trends in Neurosciences
(2016) - et al.
Improving the efficiency of multisensory integration in older adults: Audio-visual temporal discrimination training reduces susceptibility to the sound-induced flash illusion
Neuropsychologia
(2014) - et al.
Temporal synchrony and audiovisual integration of speech and object stimuli in autism
Research in Autism Spectrum Disorders
(2017) - et al.
The construct of the multisensory temporal binding window and its dysregulation in developmental disabilities
Neuropsychologia
(2014) - et al.
Visual–auditory integration during speech imitation in autism
Research in Developmental Disabilities
(2004)
A new social communication intervention for children with autism: Pilot randomised controlled treatment study suggesting effectiveness
Journal of Child Psychology and Psychiatry
Diagnostic and statistical manual of mental disorders-IV-TR
Diagnostic and statistical manual of mental disorders-5
Multisensory processing in autism spectrum disorders: Intersensory processing disturbance as atypical development
Sensory Experiences Questionnaire: Discriminating sensory features in young children with autism, developmental delays, and typical development
Journal of Child Psychology and Psychiatry
A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders
Journal of Autism and Developmental Disorders
Toward an interdisciplinary approach to understanding sensory function in autism spectrum disorder
Autism Research
Multisensory perceptual learning is dependent upon task difficulty
Experimental Brain Research
Brief report: Differences in multisensory integration covary with differences in sensory responsiveness in children with and without autism spectrum disorder
Journal of Autism and Developmental Disabilities
irr: Various coefficients of interrater reliability and agreement (Version 0.84)
Single case research methodology: Applications in special education and behavioral sciences
Measuring changes in social communication behaviors: Preliminary development of the Brief Observation of Social Communication Change (BOSCC)
Journal of Autism and Developmental Disorders
Cited by (11)
A Comparison of Listening Skills of Autistic and Non-Autistic Youth While Using and Not Using Remote Microphone Systems
2023, Journal of Speech, Language, and Hearing ResearchA Randomized Controlled Trial for Audiovisual Multisensory Perception in Autistic Youth
2023, Journal of Autism and Developmental DisordersAudiovisual temporal binding window narrows with age in autistic individuals
2023, Autism ResearchRelations Between the McGurk Effect, Social and Communication Skill, and Autistic Features in Children with and without Autism
2022, Journal of Autism and Developmental Disorders
- 1
Present address.