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Sensory Perception and Temporal Processing in Autism

Abnormalities in sensory behavior is not currently included in the DSM-V criteria for Autism Spectrum Disorders (ASD), though there is building evidence that sensory abnormalities are significantly present in ASD (Rogers and Ozonoff, 2005; reviewed by Kwakye et al., 2011). Research into abnormalities in sensory integration across all sensory modalities has become a topic of interest. Conclusions from numerous studies indicate that the temporal realm of sensory processing may be affected in ASD (Kwakye et al., 2011). Impaired detection of violations temporal synchrony of audiovisual linguistic stimuli were present in children with ASD compared to TD children and those with developmental delays not specific to ASD (Bebko et al., 2006; reviewed by Kwakye et al., 2011). Language and social stimuli are multisensory in nature and a widening in the temporal window of multisensory binding may have severe impacts on children with ASD (Kwakye et al., 2011).

Individuals with Autism characteristically tend to have inhibited social cognition and in most cases a delayed development is observed (Baron-Cohen, Leslie & Frith, 1985; reviewed by Robertson & Baron-Cohen, 2017). Additionally, approximately 90 percent of individuals diagnosed with Autism show atypical sensory experiences of reality in all modalities (Tomchek & Dunn, 2007; reviewed by Robertson & Baron-Cohen, 2017). There have been significant research inquiries about a potential link between sensory experience and inhibited or delayed social cognition. It has been suggested that these sensory traits are phenotypic markers of inhibited social cognition and could even be predictive of future challenges with social interaction (Donaldson, Stauder, & Donkers, 2017; reviewed by Robertson & Baron-Cohen, 2017).

When shown cluttered visual displays, individuals with Autism tend to show quicker detection of targets amongst distracting imagery while showing insensitivity to distracting stimuli (Plaisted, O’Riordan, & Baron-Cohen, 1998; reviewed by Robertson & Baron-Cohen, 2017). This implies that individuals with Autism show a bias toward local over global features of a sensory experience (Baron-Cohen, Ashwin, Ashwin, Tavassoli, & Chakrabarti, 2009; reviewed by Robertson & Baron-Cohen, 2017).  It is very likely that individuals with Autism have superior detection or discrimination thresholds when presented with static stimuli (Mottron L, Dawson M, Soulières I, Hubert B, & Burack J, 2006; reviewed by Robertson & Baron-Cohen, 2017). It is puzzling, however, that basic measures of visual sensitivity in individuals with Autism are the same as typically developed individuals (Tavassoli, Latham, Bach, Dakin, & Baron-Cohen, 2011; reviewed by Robertson & Baron-Cohen, 2017). One explanation for this occurrence is a shift in the temporal pattern of local-global processing towards slower global processing. Supporting evidence posits that temporal processing of local sensory signals is both slower and noisier in individuals with Autism compared to typically developed individuals (Van der Hallen, Evers, Brewaeys, Van den Noortgate, & Wagemans, 2015; reviewed by Robertson & Baron-Cohen, 2017).

Similar impacts on sensory processing have been observed in the realm of auditory processing for individuals with Autism – children with Autism often show difficulty isolating the order of presentation of two closely occurring tones, they also show delayed neural response to tones compared to typically developed children (Kwakye, Foss-Feig, Cascio, Stone, & Wallace, 2011; reviewed by Robertson & Baron-Cohen, 2017). There are significant deficits in multisensory processing in individuals with Autism – they exhibit longer windows of audio-visual temporal binding and are less able to order the presentation of a tone and flash with close temporal offsets compared to controls. They also tend to perceive asynchronous events as synchronous (Stevenson et al., 2018; reviewed by Robertson & Baron-Cohen, 2017). For individuals with Autism, in auditory processing, local stimuli triggers delayed evoked responses and integrating multiple local stimuli into global perception requires a wider window of temporal binding.

These deficits in sensory processing may have impacts on higher order social-cognitive functioning in Autism (Robertson & Baron-Cohen, 2017). There are also implications of limited sensory processing impacting language development and perception. Language perception requires the ability to integrate sensory signals across auditory and visual sensory experiences (Kuhl & Meltzoff, 1982; reviewed by Robertson & Baron-Cohen). This occurrence may likely affect the individual’s ability to accurately understand speech in noisy settings (Stevenson et al., 2018; reviewed by Robertson & Baron-Cohen, 2017)

Kwakye, Foss-Feig, Cascio, Stone, & Wallace (2011) conducted an experiment on auditory and multisensory temporal processing in Autism spectrum disorders (ASD), using typically developed (TD) children as controls. There were thirty-five children with ASD and twenty-seven TD children. All participants were between the ages of 8-17, had an IQ score of above 70, had normal or corrected hearing and/or vision and did not have a diagnosed reading disorder. Participants were asked to perform three separate temporal order judgement (TOJ) tasks – visual, multisensory and auditory.

The visual TOJ task, multisensory TOJ task and auditory TOJ tasks were used to measure the acuity of the visual, audio-visual and auditory systems. During the visual TOJ task, the participants had to determine which of two circles – located above and below a fixation cross – appeared on the computer screen first. The circles were presented in close temporal proximity with stimulus onset asynchronies (SOAs) ranging between 7 and 252 milliseconds. Participants got to complete ten practice trials and received feedback regarding their accuracy. After the practice trials, researchers used a staircase procedure to determine each individual participant’s threshold SOA required to perform the TOJ task with 70-75% accuracy.

Task irrelevant auditory stimuli were added to the visual TOJ task during the multisensory TOJ task. The multisensory TOJ task was the same as the visual TOJ task except the SOAs between the two circles was fixed according to each individual’s threshold value. Two identical sounds were presented, always synchronously with the first visual stimulus onset. The second sound was delayed from anywhere between 0-500 milliseconds relative to the onset of the second circle. During the auditory TOJ task, participants had two identical clicks presented to each ear in close temporal proximity. A white fixation cross appeared on a black computer screen for 1000 milliseconds. Immediately after the fixation cross, the first of two clicks were presented through headphones to either the right or left ear. Subsequently, the second identical click was presented to the opposite ear based on a variable SOA. The fixation cross then turned red which signaled the participant to respond with an answer for which circle appeared first (Fig. 1).

Researchers then asked whether visual and auditory temporal processing differed in children with ASD compared to TD children. The temporal binding window for both ASD and TD participants was defined by the span of consecutive multisensory delay conditions within which there were statistically significant gains in accuracy or response times. To determine this, researchers conducted one-sample t-tests for each multi-sensory delay condition and then compared accuracy increases or response time decreases to an alternative value of 0. The alternative value of 0 represented no gain in accuracy or response time relative to baseline conditions. Threshold values for children with ASD on the visual TOJ task were at 52.7 milliseconds compared to TD children who had a threshold of 60.7 milliseconds (Fig. 2a). Threshold values for children with ASD on the auditory TOJ task were at 107.8 milliseconds compared to TD children who had a threshold of 73 milliseconds (Fig. 2b). The threshold SOA values at which participants could report which of the two circles appeared first was at approximately 75% accuracy. There was no significant difference between groups on visual TOJ task performance, however, performance on the auditory TOJ task did differ significantly. Children with ASD required 48% more time between auditory stimuli to accurately determine which circle appeared first.

Then researchers explored what effect task-irrelevant auditory stimuli had on performance during the visual TOJ as well as what the temporal aspects of performance enhancements on the representation of the hallmark of multisensory integration in the task. Between-group comparisons were conducted for both accuracy and response times for trials with no delay between onset of a second presentation of visual and auditory stimuli and trials during which only visual stimuli were presented. Children with ASD performed with approximately 79% accuracy on trials with no multisensory delay and 72% accuracy on visual only trials compared to TD children who performed at a rate of 74% accuracy on trials with no multisensory delay and 75% accuracy on visual only trials (Fig. 3a). Children with ASD had a response time of 850 milliseconds compared to TD children at 1100 milliseconds on trials with no multisensory delay. On visual only trials, children with ASD had a response time of 900 milliseconds compared to TD children with a response time of 1100 milliseconds visual only trials (Fig. 3b). Both groups performed nearly equally on the baseline visual TOJ task in context of the multisensory TOJ task which was confirmed by the fact that accuracy percentages and response times for visual-only trials had no significant difference between ASD children and TD children.

Researchers asked for the percentage of improvement in accuracy relative to visual-only performance as a function of multi-sensory delay. For each group, the temporal binding window was defined by the contiguous span of multi-sensory delays within which there were statistically significant improvements over the visual TOJ task baseline. The windows were defined for each group using accuracy and response time data. Performance improvements differed significantly between TD children and children with ASD based on the range of delays in the multisensory temporal window. Significant improvements in accuracy were observed in children with ASD from the 0 – 300 millisecond delay condition while significant improvements in accuracy were observed from the 50-150 millisecond delay condition in TD children. Children with ASD had shown improvements in response time 100 milliseconds longer than TD children even though TD children showed statistically significant improvements in response time over a greater range of delays relative to accuracy (Fig. 4).

Researchers asked for the rate of improvement in response times relative to visual-only performances as a function of multi-sensory delay. For each group, the temporal binding window was defined by the contiguous span of multi-sensory delays within which there were statistically significant improvements over the visual TOJ task baseline. The windows were defined for each group using accuracy and response time data. Children with ASD showed faster responses from the 0-300 millisecond delay condition compared to TD children from 0-200 millisecond delay condition. The temporal binding window for multi-sensory stimuli had a doubled rate of accuracy in children with ASD compared to TD children (Fig. 5).

One primary concern in terms of abnormalities in multisensory integration in ASD children is that it can have a significant impact on language development and language perception which plays a huge part in social interaction. Kwakye et al. (2011) validated in their study on audiovisual temporal integration in ASD that children with ASD have wider temporal processing windows for multisensory stimuli than TD children. This wider temporal binding window can impact language acquisition, thus impairing the child’s ability to make associations between visual and auditory aspects of speech – this would delay or prevent language acquisition (Kwakye et al., 2011). As previously mentioned, abnormal sensory processing is not included in the diagnostic criteria for ASD in the DSM-V although it was proposed. Based on the findings on Kwakye et al. (2011) and other studies with similar conclusions, it would be beneficial to consider sensory processing issues as significant markers of ASD – as primary rather than secondary symptoms. Identifying sensory processing issues early in child development may be crucial for intervention.

References

Baron-Cohen, S., Ashwin, E., Ashwin, C., Tavassoli, T., & Chakrabarti, B. (2009). Talent in autism: hyper-systemizing, hyper-attention to detail and sensory hypersensitivity. Philosophical Transactions of the Royal Society B: Biological Sciences364(1522), 1377–1383. https://doi.org/10.1098/rstb.2008.0337

Bebko, J. M., Weiss, J. A., Demark, J. L., & Gomez, P. (2006). Discrimination of temporal synchrony in intermodal events by children with autism and children with developmental disabilities without autism. Journal of Child Psychology and Psychiatry47(1), 88–98. https://doi.org/10.1111/j.1469-7610.2005.01443.x

Donaldson, C., Stauder, J., & Donkers, F. (2017). Increased Sensory Processing Atypicalities in Parents of Multiplex ASD Families Versus Typically Developing and Simplex ASD Families. Journal of Autism & Developmental Disorders47(3), 535–548. https://doi.org/10.1007/s10803-016-2888-0

Kuhl, P. K., & Meltzoff, A. N. (1982). The Bimodal Perception of Speech in Infancy. Science218(4577), 1138–1141.

Kwakye, L. D., Foss-Feig, J. H., Cascio, C. J., Stone, W. L., & Wallace, M. T. (2011). Altered Auditory and Multisensory Temporal Processing in Autism Spectrum Disorders. Frontiers in Integrative Neuroscience4. https://doi.org/10.3389/fnint.2010.00129

Mottron L, Dawson M, Soulières I, Hubert B, & Burack J. (2006). Enhanced perceptual functioning in autism: an update, and eight principles of autistic perception. Journal of Autism & Developmental Disorders36(1), 27–43.

Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998). Enhanced visual search for a conjunctive target in autism: A research note. Journal of Child Psychology & Psychiatry & Allied Disciplines39(5), 777.

Robertson, C. E., & Baron-Cohen, S. (2017). Sensory perception in autism. Nature Reviews Neuroscience18(11), 671–684. https://doi.org/10.1038/nrn.2017.112

Rogers, S. J., & Ozonoff, S. (2005). Annotation: What do we know about sensory dysfunction in autism? A critical review of the empirical evidence. Journal of Child Psychology & Psychiatry46(12), 1255–1268. https://doi.org/10.1111/j.1469-7610.2005.01431.x

Stevenson, R. A., Segers, M., Ncube, B. L., Black, K. R., Bebko, J. M., Ferber, S., & Barense, M. D. (2018). The cascading influence of multisensory processing on speech perception in autism. Autism22(5), 609–624. https://doi.org/10.1177/1362361317704413

Tavassoli, T., Latham, K., Bach, M., Dakin, S. C., & Baron-Cohen, S. (2011). Psychophysical measures of visual acuity in autism spectrum conditions. Vision Research51(15), 1778–1780. https://doi.org/10.1016/j.visres.2011.06.004

Tomchek, S. D., & Dunn, W. (2007). Sensory processing in children with and without autism: a comparative study using the short sensory profile. AJOT: American Journal of Occupational Therapy61(2), 190-.

Van der Hallen, R. Evers, K., Brewaeys, K., Van den Noortgate, W. & Wagemans, J.

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