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Abstract

The new DSM-5 diagnostic criteria for autism spectrum disorders (ASDs) include sensory disturbances in addition to the well-established language, communication, and social deficits. One sensory disturbance seen in ASD is an impaired ability to integrate multisensory information into a unified percept. This may arise from an underlying impairment in which individuals with ASD have difficulty perceiving the temporal relationship between cross-modal inputs, an important cue for multisensory integration. Such impairments in multisensory processing may cascade into higher-level deficits, impairing day-to-day functioning on tasks, such as speech perception. To investigate multisensory temporal processing deficits in ASD and their links to speech processing, the current study mapped performance on a number of multisensory temporal tasks (with both simple and complex stimuli) onto the ability of individuals with ASD to perceptually bind audiovisual speech signals. High-functioning children with ASD were compared with a group of typically developing children. Performance on the multisensory temporal tasks varied with stimulus complexity for both groups; less precise temporal processing was observed with increasing stimulus complexity. Notably, individuals with ASD showed a speech-specific deficit in multisensory temporal processing. Most importantly, the strength of perceptual binding of audiovisual speech observed in individuals with ASD was strongly related to their low-level multisensory temporal processing abilities. Collectively, the results represent the first to illustrate links between multisensory temporal function and speech processing in ASD, strongly suggesting that deficits in low-level sensory processing may cascade into higher-order domains, such as language and communication.

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... Autism spectrum disorder (ASD) refers to a type of neurodevelopmental disorder, characterized by behavioral dysfunctions in specific developmental areas, such as social interaction, communication, and a restricted range of interests and stereotyped behaviors (American Psychiatric Association, 2013). In addition to social and behavioral symptoms, people with ASD are reported to have difficulties in sensory processing, including over-or under-sensitivity to sensory stimuli, and deficits in multisensory integration (Iarocci and McDonald, 2006;Bennetto et al., 2007;Oberman and Ramachandran, 2008;Foss-Feig et al., 2010;Cascio et al., 2012a;Tavassoli and Baron-Cohen, 2012;Occelli et al., 2013;Stevenson et al., 2014a;Wallace and Stevenson, 2014;DuBois et al., 2017). The impaired ability to integrate multisensory information in individuals with ASD may arise from an underlying impairment in perceiving the relationships between cross-modal inputs (Stevenson et al., 2014a). ...
... In addition to social and behavioral symptoms, people with ASD are reported to have difficulties in sensory processing, including over-or under-sensitivity to sensory stimuli, and deficits in multisensory integration (Iarocci and McDonald, 2006;Bennetto et al., 2007;Oberman and Ramachandran, 2008;Foss-Feig et al., 2010;Cascio et al., 2012a;Tavassoli and Baron-Cohen, 2012;Occelli et al., 2013;Stevenson et al., 2014a;Wallace and Stevenson, 2014;DuBois et al., 2017). The impaired ability to integrate multisensory information in individuals with ASD may arise from an underlying impairment in perceiving the relationships between cross-modal inputs (Stevenson et al., 2014a). For example, the most studied "bouba-kiki" effect (i.e., people associate rounded shapes with words like "bouba" or "maluma, " and spiky shapes with words like "kiki" or "takete"; Köhler, 1947) was reported to be less pronounced in individuals with autism compared to controls (Oberman and Ramachandran, 2008;Occelli et al., 2013;Gold and Segal, 2017;Król and Ferenc, 2020). ...
... According to the Bayesian priors ("hypo-priors") hypothesis, the sensoryperceptual representations of the world are built based on a Bayesian statistic; based on prior knowledge, a weighted, generated model is constructed from sensory inputs and an internal probability map. Individuals with autism tend to have a decreased ability to perform statistical learning with co-occurrences and regularities in the environment, leading to difficulties in associating and integrating sensory information across modalities (Pellicano and Burr, 2012;Stevenson et al., 2014aStevenson et al., , 2017. The autistic effect was observed on color-taste/ shape-color associations, which might be mainly constructed through statistical learning with regularities in the environment (Koch and Koch, 2003;Spence et al., 2015;Saluja and Stevenson, 2018;Hanada, 2019;Higgins and Hayes, 2019;Spence, 2019), while no significant autistic effect was observed on shape-taste associations, which might be mainly explained by semantic meaning correspondences (e.g., hedonic dimensions; Salgado-Montejo et al., 2015;Velasco et al., 2015Velasco et al., , 2016bBlazhenkova and Kumar, 2018;Turoman et al., 2018;De Sousa et al., 2020;Hamamoto et al., 2020;Motoki and Velasco, 2021). ...
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Crossmodal correspondences between visual features (e.g., color/shape) and tastes have been extensively documented in recent years. Visual colors and shapes have been shown to consensually match to specific tastes. Meanwhile, individuals with autism spectrum disorder are reported to have atypical sensory processing and deficits in multisensory integration. However, the influence of autistic traits on the formation of such correspondences is relatively unknown. Here, we examined whether autistic traits could influence visual–taste associations using an online questionnaire survey among Japanese participants. The results showed that the participants exhibited strong color–taste, shape–taste, and shape–color associations, and the proportions of choosing the consensual color–taste/shape–color associations were significantly associated with autistic traits. The participants with higher autistic quotient scores chose fewer of the consensual color–taste/shape–color associations while there was no difference in choosing shape–taste associations. We interpreted the results as statistical learning with a reduced prior knowledge effect in participants with higher autistic quotient scores.
... In the course of audiovisual speech perception development, children with ASD lagged behind typically developing (TD) children (Foxe et al., 2015;Taylor et al., 2010). This delayed audiovisual speech perception in children with ASD was proposed to be correlated with their weaker temporal processing (Stevenson et al., 2014), poorer lipreading ability (Iarocci et al., 2010), atypical face viewing patterns (Bebko et al., 2014;Irwin et al., 2011), and weaker tendency to combine the elementary stimulus parts into a coherent one (Baum et al., 2015;Happé & Frith, 2006). Previous studies found that, for TD infants, performance of audiovisual speech perception at 6 months predicted the levels of receptive vocabulary (i.e., the collection of words understood by an individual) at 12 months (Altvater-Mackensen & Grossmann, 2015;Imafuku et al., 2019). ...
... The rate of the fused perception is usually taken as the strength of the McGurk effect (MacDonald, 2017;McGurk & MacDonald, 1976). Most of studies using the McGurk effect to investigate the audiovisual speech integration in children with ASD showed that children with ASD had weaker audiovisual speech perception than TD children did, as shown by their weaker McGurk effect (e.g., Bebko et al., 2014;de Gelder et al., 1991;Irwin et al., 2011;Mongillo et al., 2008;Stevenson et al., 2014). Meanwhile, some other studies demonstrated that children with ASD and TD children showed similar audiovisual speech perception (i.e., similar McGurk effect Iarocci et al., 2010;Woynaroski et al., 2013). ...
... In the TOJ task, participants were required to judge which component-the auditory part or the visual part-comes first. Compared with the TD counterparts, children with ASD viewed the synchronized-audiovisual speech less in the preferential looking task (Bebko et al., 2006;Grossman et al., 2015), made more simultaneity judgements in the SJ task (Stevenson et al., 2014), and demonstrated diminished temporal order sensitivities in the TOJ task (de Boer-Schellekens et al., 2013). These findings suggested that children with ASD showed less acute temporal processing for speech stimuli than TD children did. ...
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Children with autism spectrum disorder (ASD) have deficits in audiovisual speech perception and temporal processing. The current study has examined the relationship between the audiovisual speech perception deficits and temporal processing deficits in children with and without ASD. To this end, using the McGurk paradigm, we implemented two experiments to explore audiovisual speech perception (Experiment 1) and temporal processing (Experiment 2), as well as the correlation between them, in children with ASD and typically developing (TD) children. We recruited 4- to 8-year-old children, some with ASD and some TD, to perform a McGurk task in Experiment 1 (24 children with ASD, 26 TD children) and to complete a simultaneity judgement task in Experiment 2 (31 children with ASD, 29 TD children). On the basis of the data from participants who participated in both Experiment 1 and Experiment 2 (20 children with ASD, 21 TD children), we analyzed the correlation between audiovisual speech perception and temporal processing in children with ASD and TD children separately. We found that children with ASD showed weaker audiovisual speech perception (based on the population) and less acute temporal processing compared with TD children. The correlation analysis revealed that audiovisual speech perception and temporal processing were correlated in TD children when the visual led the audio but not when the audio led the visual. No such correlation was found in children with ASD either when the visual led the audio or when the audio led the visual. The present study implicated that the correlation between audiovisual speech perception and temporal processing might be contingent on the range of individual temporal processing abilities.
... Abnormal theta tracking of speech syllable modulations might be associated or even follow from a stronger theta synchronization with the visual input. The posterior-occipital thetatracking topography in children with ASD ( Figure 2) could suggest that they track more 1 1 visual motion than auditory modulations, a functional anomaly that could possibly underpin atypical audio-visual integration [98][99][100][101][102][103][104][105][106][107]. This conjecture was partly confirmed by the direct comparison of visual and speech tracking ( Figure S4), showing an imbalance in the visual vs. auditory tracking in the ASD group, with a predominant tracking od visual motion. ...
... In addition, the PAC frequency was higher than expected for speech processing, indicating that it is most likely local visual information, rather than auditory, that is modulated at theta rhythm. Overall, these results demonstrate a weak engagement of the auditory system in speech processing in very young children with ASD, and show that visual motion processing dominates when they watch a natural audio-visual scene involving moving and talking characters, as previously reported in adults/children [99][100][101][102]. ...
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Communication difficulties in autism spectrum disorder (ASD) involve a speech reception deficit, whose biological causes are not yet identified. This deficit could denote atypical neuronal ensemble activity, as reflected by neural oscillations. Atypical cross-frequency oscillation coupling in particular could disrupt the possibility to jointly track and predict dynamic acoustic stimuli, a dual process that is essential for speech comprehension. Whether such oscillation anomalies can already be found in very young children with ASD, and with what specificity they relate to individual language reception capacity is unknown. In this study, neural activity was collected using EEG in 64 very young children with and without ASD (mean age 3) while they were exposed to naturalistic-continuous speech via an age-appropriate cartoon. EEG power typically associated with phrase-level chunking (delta, 1-3Hz), phonemic encoding (low-gamma, 25-35Hz) and top-down control (beta, 12-20Hz) was markedly reduced in ASD relative to typically developing (TD) children. Speech neural-tracking by delta and theta oscillations was also weaker in ASD than TD children. Critically, children with ASD exhibited slightly atypical theta/gamma coupling (PAC) involving a higher-than-normal gamma frequency, and markedly atypical beta/gamma PAC. Even though many oscillation features were atypical in our sample of 31 very young children with ASD, the beta/gamma coupling anomaly was the single best predictor of individual speech reception difficulties. These findings suggest that early interventions targeting the normalization of low-gamma and low-beta activity, might help young children with ASD to engage more in oral interactions. Highlights Very young children diagnosed with autism spectrum disorder already present marked alterations of neural oscillatory activity in response to natural speech. The hierarchical processing of phonemic- and syllabic-range information (theta/gamma coupling) is atypical in young ASD children. Speech reception deficit in children with ASD is indexed by abnormal bottom-up (low-gamma) and top-down (low-beta) coordination.
... For more than five decades Multisensory processing abnormalities have been described in individuals with ASD (Camarata et al., 2020) and proposed as the abnormality responsible for the syndrome (Stevenson et al., 2014;Camarata et al., 2020;Kawakami et al., 2020;Siemann et al., 2020). More recently, a Bayesian model of ASD was proposed based on new computational frameworks suggesting that multisensory integration follows Bayesian rules of causal inference (French and DeAngelis, 2020). ...
... A variety of ASD theories are based on abnormal multisensory functions is instead selective and might be related with autistic symptoms dependent on specific SC functions. (Stevenson et al., 2014;Camarata et al., 2020;Kawakami et al., 2020;Siemann et al., 2020). Motor, autonomic, emotional, and several other variables are included in the micro-movement perspective theory (Torres et al., 2013) and the abnormal interpersonal synchrony theory (McNaughton and Redcay, 2020). ...
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A better understanding of the pathogenesis of autism will help clarify our conception of the complexity of normal brain development. The crucial deficit may lie in the postnatal changes that vision produces in the brainstem nuclei during early life. The superior colliculus is the primary brainstem visual center. Although difficult to examine in humans with present techniques, it is known to support behaviors essential for every vertebrate to survive, such as the ability to pay attention to relevant stimuli and to produce automatic motor responses based on sensory input. From birth to death, it acts as a brain sentinel that influences basic aspects of our behavior. It is the main brainstem hub that lies between the environment and the rest of the higher neural system, making continuous, implicit decisions about where to direct our attention. The conserved cortex-like organization of the superior colliculus in all vertebrates allows the early appearance of primitive emotionally-related behaviors essential for survival. It contains first-line specialized neurons enabling the detection and tracking of faces and movements from birth. During development, it also sends the appropriate impulses to help shape brain areas necessary for social-communicative abilities. These abilities require the analysis of numerous variables, such as the simultaneous evaluation of incoming information sustained by separate brain networks (visual, auditory and sensory-motor, social, emotional, etc.), and predictive capabilities which compare present events to previous experiences and possible responses. These critical aspects of decision-making allow us to evaluate the impact that our response or behavior may provoke in others. The purpose of this review is to show that several enigmas about the complexity of autism might be explained by disruptions of collicular and brainstem functions. The results of two separate lines of investigation: 1. the cognitive, etiologic, and pathogenic aspects of autism on one hand, and two. the functional anatomy of the colliculus on the other, are considered in order to bridge the gap between basic brain science and clinical studies and to promote future research in this unexplored area.
... Indeed, only within an optimal TBW the combination of information from different modalities can promote significant neural, behavioral and perceptual gains (Stein et al. 1993). For instance, as shown in some neuropsychiatric diseases such as dyslexia , autism spectrum disorders (Bebko et al. 2006;de Boer-Schellekens et al. 2013;Foss-Feig et al. 2010;Kwakye et al. 2011;Stevenson et al. 2014;Wallace and Stevenson 2014) and schizophrenia (Hahn et al. 2014;Stekelenburg et al. 2013;Wallace and Stevenson 2014), deficits of multisensory integration, by affecting perception and recognition of complex stimuli due to increased ambiguity about stimulus identity, negatively impact on high-level cognitive functions, among which language (Bebko et al. 2006;de Boer-Schellekens et al. 2013;Foss-Feig et al. 2010;Kwakye et al. 2011;Stevenson et al. 2014), frontal-executive functioning and visuo-spatial processing (Karussis 2014), the last shown to be impaired in MS too (Karussis 2014). Moreover, the 'perceptual incoherence' resulting from defective multisensory integration may give rise to incoherent self-experiences including depersonalization, ambivalence, diminished sense of agency and 'loosening of associations' between thoughts (Postmes et al. 2014). ...
... Indeed, only within an optimal TBW the combination of information from different modalities can promote significant neural, behavioral and perceptual gains (Stein et al. 1993). For instance, as shown in some neuropsychiatric diseases such as dyslexia , autism spectrum disorders (Bebko et al. 2006;de Boer-Schellekens et al. 2013;Foss-Feig et al. 2010;Kwakye et al. 2011;Stevenson et al. 2014;Wallace and Stevenson 2014) and schizophrenia (Hahn et al. 2014;Stekelenburg et al. 2013;Wallace and Stevenson 2014), deficits of multisensory integration, by affecting perception and recognition of complex stimuli due to increased ambiguity about stimulus identity, negatively impact on high-level cognitive functions, among which language (Bebko et al. 2006;de Boer-Schellekens et al. 2013;Foss-Feig et al. 2010;Kwakye et al. 2011;Stevenson et al. 2014), frontal-executive functioning and visuo-spatial processing (Karussis 2014), the last shown to be impaired in MS too (Karussis 2014). Moreover, the 'perceptual incoherence' resulting from defective multisensory integration may give rise to incoherent self-experiences including depersonalization, ambivalence, diminished sense of agency and 'loosening of associations' between thoughts (Postmes et al. 2014). ...
Article
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Temporal Binding Window (TBW) represents a reliable index of efficient multisensory integration process, which allows individuals to infer which sensory inputs from different modalities pertain to the same event. TBW alterations have been reported in some neurological and neuropsychiatric disorders and seem to negatively affects cognition and behavior. So far, it is still unknown whether deficits of multisensory integration, as indexed by an abnormal TBW, are present even in Multiple Sclerosis. We addressed this issue by testing 25 participants affected by relapsing-remitting Multiple Sclerosis (RRMS) and 30 age-matched healthy controls. Participants completed a simultaneity judgment task (SJ2) to assess the audiovisual TBW; two unimodal SJ2 versions were used as control tasks. Individuals with RRMS showed an enlarged audiovisual TBW (width range = from − 166 ms to + 198 ms), as compared to healthy controls (width range = − 177/ + 66 ms), thus showing an increased tendency to integrate temporally asynchronous visual and auditory stimuli. Instead, simultaneity perception of unimodal (visual or auditory) events overall did not differ from that of controls. These results provide first evidence of a selective deficit of multisensory integration in individuals affected by RRMS, besides the well-known motor and cognitive impairments. The reduced multisensory temporal acuity is likely caused by a disruption of the neural interplay between different sensory systems caused by multiple sclerosis.
... Specifically, several past studies have suggested that youth with autism with altered tactile responsiveness might not benefit from (or even tolerate wearing) RM systems (Rance 2014;Schafer et al. 2016Schafer et al. , 2019. Furthermore, it is possible that the effects of RM system use could vary according to one's ability to integrate auditory information provided via an RM system with the corresponding visual speech cues (Feldman et al. 2018;Stevenson et al. 2014Stevenson et al. , 2018. ...
Article
Objectives: This study examined whether remote microphone (RM) systems improved listening-in-noise performance in youth with autism. We explored effects of RM system use on both listening-in-noise accuracy and listening effort in a well-characterized sample of participants with autism. We hypothesized that listening-in-noise accuracy would be enhanced and listening effort reduced, on average, when participants used the RM system. Furthermore, we predicted that effects of RM system use on listening-in-noise accuracy and listening effort would vary according to participant characteristics. Specifically, we hypothesized that participants who were chronologically older, had greater nonverbal cognitive and language ability, displayed fewer features of autism, and presented with more typical sensory and multisensory profiles might exhibit greater benefits of RM system use than participants who were younger, had less nonverbal cognitive or language ability, displayed more features of autism, and presented with greater sensory and multisensory disruptions. Design: We implemented a within-subjects design to investigate our hypotheses, wherein 32 youth with autism completed listening-in-noise testing with and without an RM system. Listening-in-noise accuracy and listening effort were evaluated simultaneously using a dual-task paradigm for stimuli varying in complexity (i.e., syllable-, word-, sentence-, and passage-level). In addition, several putative moderators of RM system effects (i.e., sensory and multisensory function, language, nonverbal cognition, and broader features of autism) on outcomes of interest were evaluated. Results: Overall, RM system use resulted in higher listening-in-noise accuracy in youth with autism compared with no RM system use. The observed benefits were all large in magnitude, although the benefits on average were greater for more complex stimuli (e.g., key words embedded in sentences) and relatively smaller for less complex stimuli (e.g., syllables). Notably, none of the putative moderators significantly influenced the effects of the RM system on listening-in-noise accuracy, indicating that RM system benefits did not vary according to any of the participant characteristics assessed. On average, RM system use did not have an effect on listening effort across all youth with autism compared with no RM system use but instead yielded effects that varied according to participant profile. Specifically, moderated effects indicated that RM system use was associated with increased listening effort for youth who had (a) average to below-average nonverbal cognitive ability, (b) below-average language ability, and (c) reduced audiovisual integration. RM system use was also associated with decreased listening effort for youth with very high nonverbal cognitive ability. Conclusions: This study extends prior work by showing that RM systems have the potential to boost listening-in-noise accuracy for youth with autism. However, this boost in accuracy was coupled with increased listening effort, as indexed by longer reaction times while using an RM system, for some youth with autism, perhaps suggesting greater engagement in the listening-in-noise tasks when using the RM system for youth who had lower cognitive abilities, were less linguistically able, and/or have difficulty integrating seen and heard speech. These findings have important implications for clinical practice, suggesting RM system use in classrooms could potentially improve listening-in-noise performance for some youth with autism.
... This might cause weakened RTI responses (Wada et al., 2019). In individuals with ASD, atypical occurrence of the RHI (Cascio et al., 2012;Paton et al., 2012) and atypical multisensory integrations (Stevenson et al., 2014) have been reported. Moreover, previous human imaging studies suggest that multisensory integration in PPC is important for the occurrence of RHI (Ehrsson et al., 2004(Ehrsson et al., , 2005Ehrsson, 2012). ...
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Rubber hand illusion (RHI), a kind of body ownership illusion, is sometimes atypical in individuals with autism spectrum disorder; however, the brain regions associated with the illusion are still unclear. We previously reported that mice responded as if their own tails were being touched when rubber tails were grasped following synchronous stroking to rubber tails and their tails (a “rubber tail illusion”, RTI), which is a task based on the human RHI; furthermore, we reported that the RTI response was diminished in Ca2+-dependent activator protein for secretion 2-knockout (Caps2-KO) mice that exhibit autistic-like phenotypes. Importance of the posterior parietal cortex in the formation of illusory perception has previously been reported in human imaging studies. However, the local neural circuits and cell properties associated with this process are not clear. Therefore, we aimed to elucidate the neural basis of the RTI response and its impairment by investigating the c-Fos expression in both wild-type (WT) and Caps2-KO mice during the task since the c-Fos expression occurred soon after the neural activation. Immediately following the delivery of the synchronous stroking to both rubber tails and actual tails, the mice were perfused. Subsequently, whole brains were cryo-sectioned, and each section was immunostained with anti-c-Fos antibody; finally, c-Fos positive cell densities among the groups were compared. The c-Fos expression in the posterior parietal cortex was significantly lower in the Caps2-KO mice than in the WT mice. Additionally, we compared the c-Fos expression in the WT mice between synchronous and asynchronous conditions and found that the c-Fos-positive cell densities were significantly higher in the claustrum and primary somatosensory cortex of the WT mice exposed to the synchronous condition than those exposed to the asynchronous condition. Hence, the results suggest that decreased c-Fos expression in the posterior parietal cortex may be related to impaired multisensory integrations in Caps2-KO mice.
... Indeed, understanding these mechanisms is not only important from a comparative perspective with our own species, but may represent a fundamental contribution to issues concerning mental health. In particular, autistic individuals are often challenged by understanding social scenes, including the integration of auditory and visual information (Feldman et al., 2018;Stevenson, Siemann, Schneider, et al., 2014;Stevenson, Siemann, Woynaroski, et al., 2014a, b). Such de cits may result from not only de cits in face and voice processing on their own, but the ability to integrate each modality in the service of predicting and understanding social interactions. ...
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Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. In primates, both audition and vision serve the interpretation of communicative signals. Autistic individuals present deficits in both social communication and audio-visual integration. At present, the neural mechanisms subserving the interpretation of complex audio-visual social events are unknown. Based on heart rate estimates and functional neuroimaging, we show that macaque monkeys associate affiliative facial expressions or social scenes with corresponding affiliative vocalizations, aggressive expressions or scenes with corresponding aggressive vocalizations and escape visual scenes with scream vocalizations, while suppressing vocalizations that are incongruent with the visual context. This process is subserved by two distinct functional networks, homologous to the human emotional and attentional networks activated during the processing of visual social information. These networks are thus critical for the construction of social meaning representation, and provide grounds for the audio-visual deficits observed in autism. One-sentence summary Macaques extract social meaning from visual and auditory input recruiting face and voice patches and a broader emotional and attentional network.
... Moreover, additional factors may hinder the organization of adaptive and reflective mental processing with respect to attachment representations and interpersonal schemas. Specifically, child unusual brain structure and functional connectivity (Crittenden, 2017;Cole et al., 2019), atypical neuroendocrine processes and dysregulation (Naber et al., 2007;Sivaratnam et al., 2015) hypo or hyper-sensitivity to sensory stimulation (Marco et al., 2011) difficulties in multisensory integration (Stevenson et al., 2014) can pose multiple challenges for children with ASD. Moreover, an additional source of risk is the frequent exposure to potential traumatic events. ...
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The study of Autism Spectrum Disorder (ASD) represents one of the most challenging areas for attachment research in view of the complex interrelation between socio-communication impairments and attachment processes (Vivanti and Nuske, 2017, Mckenzie and Dallos, 2017). The fascinating debate, which focuses on whether ASD hampers the development of secure attachment, has not received sufficient attention so far. Prior studies often focused on attachment behaviors in preschoolers with ASD, whereas the study of attachment representations in older children remains mainly unexplored. The most recent systematic review (Teague et al., 2017) highlighted crucial unresolved questions in the study of attachment and ASD with reference to the paucity of data about predictors, correlates and outcomes of attachment in children with ASD. For instance, there is mixed evidence on the association between parental …
... Possible explanations for this divergence include variation in the age of participants, with some researchers suggesting that maturation of multisensory integration is delayed in autism (Beker et al., 2018;Feldman et al., 2018). Additionally, there is more consistent evidence of differential multisensory processing when complex, speech-based stimuli are used, relative to simplified, non-social stimuli such as flashes and tones (Stevenson et al., 2014;Meilleur et al., 2020). ...
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Interpersonal synchrony – the tendency for social partners to temporally co-ordinate their behaviour when interacting – is a ubiquitous feature of social interactions. Synchronous interactions play a key role in development, and promote social bonding and a range of pro-social behavioural outcomes across the lifespan. The process of achieving and maintaining interpersonal synchrony is highly complex, with inputs required from across perceptual, temporal, motor, and socio-cognitive domains. In this conceptual analysis, we synthesise evidence from across these domains to establish the key components underpinning successful non-verbal interpersonal synchrony, how such processes interact, and factors that may moderate their operation. We also consider emerging evidence that interpersonal synchrony is reduced in autistic populations. We use our account of the components contributing to interpersonal synchrony in the typical population to identify potential points of divergence in interpersonal synchrony in autism. The relationship between interpersonal synchrony and broader aspects of social communication in autism are also considered, together with implications for future research.
... Another potentially important consideration is our use of an intersensory design, whereby the auditory target is preceded by visual cues. Since there are well-documented deficits in multisensory integration in children with autism (71,91,93,(107)(108)(109)(110)(111)(112), it is possible that impaired ITPC is due to poor cross-sensory communication and that what we are observing reflects a multisensory deficit rather than a general entrainment issue. Arguing against a pure multisensory deficit account, the ASD group showed faster RTs in the cued compared with the uncued condition, demonstrating intact use of a cross-sensory cue. ...
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Anticipating near-future events is fundamental to adaptive behavior, whereby neural processing of predictable stimuli is significantly facilitated relative to non-predictable events. Neural oscillations appear to be a key anticipatory mechanism by which processing of upcoming stimuli is modified, and they often entrain to rhythmic environmental sequences. Clinical and anecdotal observations have led to the hypothesis that people with Autism Spectrum Disorder (ASD) may have deficits in generating predictions, and as such, a candidate neural mechanism may be failure to adequately entrain neural activity to repetitive environmental patterns to facilitate temporal predictions. We tested this hypothesis by interrogating temporal predictions and rhythmic entrainment using behavioral and electrophysiological approaches. We recorded high-density electroencephalography in children with ASD and Typically Developing (TD) age- and IQ-matched controls, while they reacted to an auditory target as quickly as possible. This auditory event was either preceded by predictive rhythmic visual cues, or not. Both ASD and control groups presented comparable behavioral facilitation in response to the Cue vs. No-Cue condition, challenging the hypothesis that children with ASD have deficits in generating temporal predictions. Analyses of the electrophysiological data, in contrast, revealed significantly reduced neural entrainment to the visual cues, and altered anticipatory processes in the ASD group. This was the case despite intact stimulus evoked visual responses. These results support intact temporal prediction in response to a cue in ASD, in the face of altered entrainment and anticipatory processes.
... integration of sensory stimuli is thought to underlie the altered perception of such cues [4]. This highlights the importance of neural circuits in the processing of sensory information to coordinate a behavioural output in the social domain [5]. ...
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Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterised by a triad of behavioural impairments and includes disruption in social behaviour. ASD has a clear genetic underpinning and hundreds of genes are implicated in its aetiology. However, how single penetrant genes disrupt activity of neural circuits which lead to affected behaviours is only beginning to be understood and less is known about how low penetrant genes interact to disrupt emergent behaviours. Investigations are well served by experimental approaches that allow tractable investigation of the underpinning genetic basis of circuits that control behaviours that operate in the biological domains that are neuro-atypical in autism. The model organism C . elegans provides an experimental platform to investigate the effect of genetic mutations on behavioural outputs including those that impact social biology. Here we use progeny-derived social cues that modulate C . elegans food leaving to assay genetic determinants of social behaviour. We used the SAFRI Gene database to identify C . elegans orthologues of human ASD associated genes. We identified a number of mutants that displayed selective deficits in response to progeny. The genetic determinants of this complex social behaviour highlight the important contribution of synaptopathy and implicates genes within cell signalling, epigenetics and phospholipid metabolism functional domains. The approach overlaps with a growing number of studies that investigate potential molecular determinants of autism in C . elegans . However, our use of a complex, sensory integrative, emergent behaviour provides routes to enrich new or underexplored biology with the identification of novel candidate genes with a definable role in social behaviour.
... Similarly, individuals with autism spectrum disorder(ASD) exhibit an impaired ability to integrate cross-modal inputs into a coherent percept due to functional hyperconnectivity among brain modalities, with greater hyperconnectivity resulting in more severe social deficits [93]. For example, children with ASD have difficulty processing temporally correlated percepts, causing them an inability to perceive speech [91]. In some cases, hyperconnectivity between sensory modalities can lead to unique experiences such as synaesthesia, a neurodevelopmental condition (not catalogued as a disease) wherein perception of one stimulus produces the consistent, involuntary experience of another. ...
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Our survival is dependent on the brain's ability to maximize use of available information at any given instant. To improve sensitivity and reduce ambiguity, sensory inputs are integrated across and within modalities via a process known as multisensory integration. Understanding the precise neural circuit architecture for multisensory interactions is key in determining the computations underlying this synergy and therefore the ability of an animal to best respond to challenges from its environment. On the basis of the fully mapped brain connectome of Drosophila larva, we investigated how mechanosensory and visual inputs interact to produce locomotion in this animal. In particular, we focused on the interaction between mechanosensory chordotonal(MeCh) neurons and Rh5 Photoreceptors (Rh5-PRs), exploring how their synergy directs activity of Mooncrawler descending neurons (MDNs), a pair of command-like neurons known to trigger escape behaviour via backward locomotion in the fruit fly larva. The neural wiring diagram revealed a complex multimodal architecture with a central neuron promoting the interactions between MeCh and Rh5-PRs, and onto which information from both senses converge. This neuron, known as Convergence Neuron 29 - or CN29 for short - was found to mediate the synergy between visual and mechanosensory inputs and direct the processed signal via polysynaptic pathways to MDNs. Further investigation into CN29 complemented by Immunohistochemistry revealed that this neuron is most likely cholinergic, sending excitatory input to downstream activatory neurons that synapse onto MDNs. Optogenetic activation of the GAL4 driver line labelling CN29 combined with behavioural assays revealed that this neuron is involved in escape behaviour, as its activation inhibits forward crawling while promoting head casts and backwards crawling, suggesting it acts as a switch that brings attention of the animal to a newly detected threat. Simulating activity of the multisensory integration circuit via a computational rate-model constrained by EM data and neurotransmitter identity provided us with a mechanistic understanding of the network, and allowed for predictions that can be used for future studies exploring this synergy.
... Neuroatypical individuals have been shown to produce altered behavioural outputs in response to a range of sensory cues (Balasco, Provenzano and Bozzi, 2020), including chemosensory cues that drive social behaviours (Endevelt-Shapira et al., 2018). Impairment within the integration of sensory stimuli is thought to underlie the altered perception of such cues (Stevenson et al., 2014a). This highlights the importance of neural circuits in the processing of sensory information to coordinate a behavioural output in the social domain (Marco et al., 2011). ...
Thesis
Autism spectrum disorder (ASD) is a neurodevelopmental disorder which is clinically characterised by core behavioural deficits including disruption to social behaviour. ASD has a clear genetic underpinning and hundreds of genes, with varying penetrance, have been implicated in its aetiology. Here I use the model organism C. elegans as an experimental platform to investigate the effect of genetic mutation on social behaviour. To do this I utilised a social paradigm in C. elegans that is based on observing a complex, sensory-integrative, food leaving behaviour. Adult worms increasingly leave an otherwise replete food source as the number of progeny populating the environment increases. This behaviour is mediated by a progeny-derived social cue and hence represent an inter-organismal social interaction. In this thesis I first designed a bioinformatic pipeline to filter high risk ASD-associated genes to select those that could be investigated using the progeny-induced food leaving assay. I identified several candidate human genes by defining C. elegans orthologues which when mutated result in selective deficits in social behaviour. This work highlights that genetic determinants within synaptic, cell signalling, epigenetic modification and phospholipid metabolism functional domains have a role in the co-ordination of C. elegans social behaviour. Using a null mutant, I show that C. elegans social behaviour is dependent on the nlg-1 gene. I refine this approach by generating a mutation in C. elegans which is synonymous to a highly penetrant ASD-associated variant identified in humans. In doing this I used and optimised a CRISPR/Cas9 technique to precisely edit C. elegans genes. Overall, the combined use of social behaviour analysis and genetic intervention in C. elegans provides a useful model to investigate the genetic determinants of autism. ASD is a complex disorder in which disruption within the biological system can influence different levels of biological organisation. Therefore, this thesis provides an avenue for future research to probe the effect of genetic disruption at different levels of the biological system to further understand the emergence of disrupted social behaviour.
... Remarkably, just like other conditions that are reviewed in the present article, autism has repeatedly been considered a time processing disorder (for a review, see: [187]), with impairment in different dimensions of time processing such as: time perception (experiencing and assessing the length and passage of time, including interval timing), time orientation (awareness of the day, date, month and year, as well as the ability to situate events on a timeline), and time management (the ability to prioritize one task among others, to order a set of tasks, and to allocate the optimum amount of time to each task [188]). It is noteworthy that, just as in the case of dyslexia, ASD has been associated with decreased susceptibility to the McGurk effect [189], or poorer judgement of simultaneity in an audiovisual task, suggesting a specific deficit in crossmodal sensory integration. This deficit would be potentially causal to social cognition impairment, due to a cascading effect from multisensory processing to speech perception [190]. ...
Article
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In a now-classic article published a couple of decades ago (Brain, 2000; 123: 2373–2399), I proposed an “extended temporal processing deficit hypothesis of dyslexia”, suggesting that a deficit in temporal processing could explain not only language-related peculiarities usually noticed in dyslexic children, but also a wider range of symptoms related to impaired processing of time in general. In the present review paper, I will revisit this “historical” hypothesis both in the light of a new clinical perspective, including the central yet poorly explained notion of comorbidity, and also taking a new look at the most recent experimental work, mainly focusing on brain imaging data. First, consistent with daily clinical practice, I propose to distinguish three groups of children who fail to learn to read, of fairly equal occurrence, who share the same initial presentation (difficulty in mastering the rules of grapheme–phoneme correspondence) but with differing associated signs and/or comorbid conditions (language disorders in the first group, attentional deficits in the second one, and motor coordination problems in the last one), thus suggesting, at least in part, potentially different triggering mechanisms. It is then suggested, in the light of brain imaging information available to date, that the three main clinical presentations/associations of cognitive impairments that compromise reading skills acquisition correspond to three distinct patterns of miswiring or “disconnectivity” in specific brain networks which have in common their involvement in the process of learning and their heavy reliance on temporal features of information processing. With reference to the classic temporal processing deficit of dyslexia and to recent evidence of an inability of the dyslexic brain to achieve adequate coupling of oscillatory brain activity to the temporal features of external events, a general model is proposed according to which a common mechanism of temporal uncoupling between various disconnected—and/or mis-wired—processors may account for distinct forms of specific learning disorders, with reading impairment being a more or less constant feature. Finally, the potential therapeutic implications of such a view are considered, with special emphasis on methods seeking to enhance cross-modal connectivity between separate brain systems, including those using rhythmic and musical training in dyslexic patients.
... For instance, in tasks assessing time based prospective memory which is the capacity to remember to complete a given action after a specified time (Altgassen, Koban, & Kliegel, 2012;Henry et al., 2014;Kretschmer, Altgassen, Rendell, & Bölte, 2014), or in diachronic thinking which is an aspect of temporal cognition involving the ability to conceive of changes over time (Boucher, Pons, Lind, & Williams, 2007). While studies investigating basic duration and relative timing judgements observed that performance in the autistic group was reduced (Kargas & Lo, 2015;Stevenson et al., 2014), superior (Falter, Braeutigam, Nathan, Carrington, & Bailey, 2013 and comparable Puts, Wodka, Tommerdahl, Mostofsky, & Edden, 2014). Similarly, studies using experimental tasks to investigate duration perception within an SET framework have reported mixed findings (Allman, DeLeon, & Wearden, 2011;Falter, Noreika, Wearden, & Bailey, 2012;Gil, Chambres, Hyvert, Fanget, & Droit-Volet, 2012). ...
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It has previously been proposed that autistic people have problems with timing which underlie the behavioural and cognitive differences in the condition. However, the nature of this postulated timing issue has not been well specified and the existing experimental literature has generated mixed findings. In the current study, we attempted a systematic investigation of timing processes in autistic adults using Scalar Expectancy Theory as a theoretical framework. Autistic (n = 58) and non-autistic (neurotypical; n = 91) adults matched for age, sex and full-scale IQ completed a battery of auditory and visual timing tasks measuring basic sub-second duration perception (temporal difference thresholds), clock processes (verbal estimation), clock and memory processes (temporal generalisation), and relative timing (temporal order judgements). Participants also completed supra-second retrospective duration estimates where the participant was not warned in advanced that they would be required to make a timing judgement, and questionnaires measuring self-reported timing behaviours in daily life. The groups reported differences on questionnaires, but measures of timing performance were comparable overall. In an exploratory analysis, we performed principal components analysis to investigate the relationship between timing judgements and participants' self-reported social-communicative, sensory and motor traits. Measures of timing performance were not well correlated with these questionnaire scores. The current study is not supportive of reduced timing performance in autistic adults, nor of a relationship between sub-second timing perception and social-communicative, sensory or motor traits.
... MATLAB code for the task, pre-generated object stimuli, and anonymized data are available at https://osf.io/976ta/. Wallace, 2016;Stevenson et al., 2014;Stevenson et al., 2019). Though there has been much progress made in understanding feature integration, there remains no strong consensus among researchers regarding how objects are represented in the mind based on their constituent features. ...
Article
Though much progress has been made to understand feature integration, debate remains regarding how objects are represented in mind based on their constituent features. Here, we advance this debate by introducing a novel shape-color “conjunction task” to reconstruct memory resolution for multiple object features simultaneously. In a first experiment, we replicate and extend a classic paradigm originally tested using a change detection task. Replicating previous work, memory resolution for individual features was reduced when the number of objects increased, regardless of the number of to-be-remembered features. Extending previous work, we found that high resolution memory near perfect in resemblance to the target was selectively impacted by the number of to-be-remembered features. Applying a data-driven statistical model of stochastic dependence, we found robust evidence of integration for lower-resolution feature memories, but less evidence for integration of high-resolution feature memories. These results suggest that memory resolution for individual features can be higher than memory resolution for their integration. In a second experiment which manipulated the nature of distracting information, we examined whether object features were directly bound to each other or by virtue of shared spatial location. Feature integration was disrupted by distractors sharing visual features of target objects but not when distractors shared spatial location – suggesting that feature integration can be driven by direct binding between shape and color features in memory. Our results constrain theoretical models of object representation, providing empirical support for hierarchical representations of both integrated and independent features.
... To date, several studies have employed the McGurk illusion to assess AV speech perception in ASD (Stevenson et al., 2014;Stevenson & Wallace, 2013). Although a number of these investigations have found that autistic children show reduced levels of integration in response to incongruent McGurk stimuli (de Gelder et al., 1991;Irwin et al., 2011;Mongillo et al., 2008;Williams et al., 2004), other studies have reported inconsistent findings. ...
Article
Atypical sensory responses are included in the diagnostic criteria of autism spectrum disorder (ASD). Autistic individuals perform poorly during conditions that require integration across multiple sensory modalities such as audiovisual (AV) integration. Previous research investigated neural processing of AV integration in infancy. Yet, this has never been studied in infants at higher likelihood of later ASD (HR) using neurophysiological (EEG/ERP) techniques. In this study, we investigated whether ERP measures of AV integration differentiate HR infants from low-risk (LR) infants and whether early AV integration abilities are associated with clinical measures of sensory responsiveness. At age 12 months, AV integration in HR (n = 21) and LR infants (n = 19) was characterized in a novel ERP paradigm measuring the McGurk effect, and clinical measures of sensory responsiveness were evaluated. Different brain responses over the left temporal area emerge between HR and LR infants, specifically when AV stimuli cannot be integrated into a fusible percept. Furthermore, ERP responses related to integration of AV incongruent stimuli were found to be associated with sensory responsiveness, with reduced effects of AV incongruency being associated with reduced sensory reactivity. These data suggest that early identification of AV deficits may pave the way to innovative therapeutic strategies for the autistic symptomatology. Further replications in independent cohorts are needed for generalizability of findings.
... integration of sensory stimuli is thought to underlie the altered perception of such cues [4]. This highlights the importance of neural circuits in the processing of sensory information to coordinate a behavioural output in the social domain [5]. ...
Article
Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterised by a triad of behavioural impairments and includes disruption in social behaviour. ASD has a clear genetic underpinning and hundreds of genes are implicated in its aetiology. However, how single penetrant genes disrupt activity of neural circuits which lead to affected behaviours is only beginning to be understood and less is known about how low penetrant genes interact to disrupt emergent behaviours. Investigations are well served by experimental approaches that allow tractable investigation of the underpinning genetic basis of circuits that control behaviours that operate in the biological domains that are neuro-atypical in autism. The model organism C. elegans provides an experimental platform to investigate the effect of genetic mutations on behavioural outputs including those that impact social biology. Here we use progeny-derived social cues that modulate C. elegans food leaving to assay genetic determinants of social behaviour. We used the SAFRI Gene database to identify C. elegans orthologues of human ASD associated genes. We identified a number of mutants that displayed selective deficits in response to progeny. The genetic determinants of this complex social behaviour highlight the important contribution of synaptopathy and implicates genes within cell signalling, epigenetics and phospholipid metabolism functional domains. The approach overlaps with a growing number of studies that investigate potential molecular determinants of autism in C. elegans. However, our use of a complex, sensory integrative, emergent behaviour provides routes to enrich new or underexplored biology with the identification of novel candidate genes with a definable role in social behaviour.
... Several studies found the differential width of the TBW based on different groups. For instance, as compared with controls, people with schizophrenia (Stevenson et al., 2017) and autism spectrum disorders (Stevenson et al., 2014) have wider TBWs. Musicians relative to non-musicians showed significantly narrower TBWs for music and sine-wave speech (Lee and Noppeney, 2014). ...
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Our research aimed to investigate the effectiveness of auditory, visual, and audiovisual warning signals for capturing the attention of the pilot, and how stimulus onset asynchronies (SOA) in audiovisual stimuli affect pilots perceiving the bimodal warning signals under different perceptual load conditions. In experiment 1 of the low perceptual load condition, participants discriminated the location (right vs. left) of visual targets preceded by five different types of warning signals. In experiment 2 of high perceptual load, participants completed the location task identical to a low load condition and a digit detection task in a rapid serial visual presentation (RSVP) stream. The main effect of warning signals in two experiments showed that visual and auditory cues presented simultaneously (AV) could effectively and efficiently arouse the attention of the pilots in high and low load conditions. Specifically, auditory (A), AV, and visual preceding auditory stimulus by 100 ms (VA100) increased the spatial orientation to a valid position in low load conditions. With the increase in visual perceptual load, auditory preceding the visual stimulus by 100 ms (AV100) and A warning signals had stronger spatial orientation. The results are expected to theoretically support the optimization design of the cockpit display interface, contributing to immediate flight crew awareness.
... 45 Although the literature is not consistent, several studies in different sensory domains suggest that individuals with ASD may experience hypersensitivity to sensations, 46-49 may process lowlevel stimulus features with higher sensory precision, [15][16][17]46,50,51 and may have difficulties in processing more complex sensory stimuli 50,52 and integrating multiple sensory domains. 53,54 Sensory processing can be investigated in many different ways. We chose a well-established experimental paradigm (moving dots task with different motion coherence levels 55 ) that allowed us to quantify sensory processing using a drift diffusion model (DDM). ...
Preprint
Background Bayesian theories of perception have provided a variety of alternative mechanistic explanations for autistic symptoms, including (1) overprecise sensations, (2) imprecise priors, (3) inflexible priors, and (4) altered hierarchical learning. Here, we designed a set of experiments to systematically test predictions from each of the four hypotheses in individuals with autism spectrum disorder (ASD). Methods Two versions of a two-alternative forced-choice (2AFC) random dot motion task were developed to disentangle the influence of sensory inputs and prior expectations and test implications of the four Bayesian hypotheses. Using a cross-sectional observational study design, behavioural data were obtained from participants with autism spectrum disorder ( N =47) and a control group ( N =50). Analyses used mixed effects models and a drift diffusion model. Results Contrary to the sensory overprecision hypothesis, individuals with ASD did not differ from controls in performance or parameter estimates during the perceptual 2AFC task. When adding cues to the task, individuals with ASD profited less from this prior information than controls, as predicted by the imprecise prior hypothesis. However, individuals with ASD were still able to update their initial priors, contradicting the inflexible prior hypothesis. Finally, in line with the hierarchical learning hypothesis, volatility differentially modulated expectation effects, exerting a significantly smaller effect in the ASD group compared to the control group. Conclusion Our findings support two mutually compatible alterations of perception in ASD (imprecise priors and, to a lesser degree, altered hierarchical learning). By contrast, they are not compatible with the notions of sensory overprecision and inflexible priors.
... Different SOAs can be set according to the needs of different studies. The SOA of nonverbal stimuli is 0-300 ms in general, and that of verbal stimuli is 0-400 ms (Stevenson et al. 2014). Then, a Gaussian curve can be drawn based on the percentage of "synchronous" responses under different SOAs to obtain the point of subjective simultaneity (PSS) and temporal binding window (TBW) (Keetels and Vroomen 2012), where the PSS is the highest point of the Gaussian function curve, and the width of the TBW depends on the value of the abscissa corresponding to 75% y max of the curve. ...
Article
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Motion perception in real situations is often stimulated by multisensory information. Speed is an essential characteristic of moving objects; however, at present, it is not clear whether speed affects the process of audiovisual temporal integration in motion perception. Therefore, this study used a streaming-bouncing task (a bistable motion perception; SB task) combined with a simultaneous judgment task (SJ task) to explore the effect of speed on audiovisual temporal integration from implicit and explicit perspectives. The experiment had a within-subjects design, two speed conditions (fast/slow), eleven audiovisual conditions [stimulus onset asynchrony (SOA): 0 ms/ ± 60 ms/ ± 120 ms/ ± 180 ms/ ± 240 ms/ ± 300 ms], and a visual-only condition. A total of 30 subjects were recruited for the study. These participants completed the SB task and the SJ task successively. The results showed the following outcomes: (1) the optimal times needed to induce the “bouncing” illusion and maximum audiovisual bounce-inducing effect (ABE) magnitude were much earlier than that for the optimal time of audiovisual synchrony, (2) speed as a bottom-up factor could affect the proportion of “bouncing” perception in SB illusions but did not affect the ABE magnitude, (3) speed could also affect the ability of audiovisual temporal integration in motion perception, and the main manifestation was that the point of subjective simultaneity (PSS) in fast speed conditions was earlier than that of slow speed conditions in the SJ task and (4) the SB task and SJ task were not related. In conclusion, the time to complete the maximum audiovisual integration was different from the optimal time for synchrony perception; moreover, speed could affect audiovisual temporal integration in motion perception but only in explicit temporal tasks.
... For both visual and auditory processing, temporal coherence across assemblies of neurons that code for different stimulus features is thought to promote binding of those features into coherent perceptual objects [3,4]. A leading hypothesis about sensory processing abnormalities in autism spectrum disorder (ASD) is that this kind of temporal "synthesis" of sensory information is atypical [5][6][7][8]. This hypothesis stems from behavioral data indicating that individuals with ASD often show impaired processing of dynamic stimuli, such as the coherent motion of visual dots [9]. ...
Article
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Organizing sensory information into coherent perceptual objects is fundamental to everyday perception and communication. In the visual domain, indirect evidence from cortical responses suggests that children with autism spectrum disorder (ASD) have anomalous figure–ground segregation. While auditory processing abnormalities are common in ASD, especially in environments with multiple sound sources, to date, the question of scene segregation in ASD has not been directly investigated in audition. Using magnetoencephalography, we measured cortical responses to unattended (passively experienced) auditory stimuli while parametrically manipulating the degree of temporal coherence that facilitates auditory figure–ground segregation. Results from 21 children with ASD (aged 7–17 years) and 26 age- and IQ-matched typically developing children provide evidence that children with ASD show anomalous growth of cortical neural responses with increasing temporal coherence of the auditory figure. The documented neurophysiological abnormalities did not depend on age, and were reflected both in the response evoked by changes in temporal coherence of the auditory scene and in the associated induced gamma rhythms. Furthermore, the individual neural measures were predictive of diagnosis (83% accuracy) and also correlated with behavioral measures of ASD severity and auditory processing abnormalities. These findings offer new insight into the neural mechanisms underlying auditory perceptual deficits and sensory overload in ASD, and suggest that temporal-coherence-based auditory scene analysis and suprathreshold processing of coherent auditory objects may be atypical in ASD.
... Integration of information processing between this network and others that play a role in embodied somatosensory and social cognitive processing 34,35 , such as the somatomotor network (IC12), could be important for explaining the more pronounced difficulties these individuals have within SC compared to RRB. Somatomotor hypoconnectivity with perisylvian auditory and visual association circuitry could also be important for pointing towards atypical multisensory integration that has been documented in autism 36,37 , particularly with regards to auditory-somatosensory 38 and visualsomatomotor integration [39][40][41][42][43] . ...
Article
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Social-communication (SC) and restricted repetitive behaviors (RRB) are autism diagnostic symptom domains. SC and RRB severity can markedly differ within and between individuals and may be underpinned by different neural circuitry and genetic mechanisms. Modeling SC-RRB balance could help identify how neural circuitry and genetic mechanisms map onto such phenotypic heterogeneity. Here, we developed a phenotypic stratification model that makes highly accurate (97–99%) out-of-sample SC = RRB, SC > RRB, and RRB > SC subtype predictions. Applying this model to resting state fMRI data from the EU-AIMS LEAP dataset ( n = 509), we find that while the phenotypic subtypes share many commonalities in terms of intrinsic functional connectivity, they also show replicable differences within some networks compared to a typically-developing group (TD). Specifically, the somatomotor network is hypoconnected with perisylvian circuitry in SC > RRB and visual association circuitry in SC = RRB. The SC = RRB subtype show hyperconnectivity between medial motor and anterior salience circuitry. Genes that are highly expressed within these networks show a differential enrichment pattern with known autism-associated genes, indicating that such circuits are affected by differing autism-associated genomic mechanisms. These results suggest that SC-RRB imbalance subtypes share many commonalities, but also express subtle differences in functional neural circuitry and the genomic underpinnings behind such circuitry.
... Research using temporal psychophysics has revealed some evidence that autistic children are less precise in the perception and reproduction of duration Brenner et al., 2016;Isaksson et al., 2018;Lepistö et al., 2005Lepistö et al., , 2006; although see Gil et al., 2012;Jones et al., 2017;Wallace & Happé, 2008 for contradictory findings) and the perception of relative timing of stimuli (Kwakye et al., 2011;Stevenson et al., 2014; although see Puts et al., 2014) compared with neurotypical controls. Time-based prospective memory, the ability to remember to complete one's previous intentions after some duration, is reduced in autistic children (Altgassen et al., 2019;Henry et al., 2014;Williams et al., 2013Williams et al., , 2014. ...
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Lay abstract: Many everyday activities require us to organise our behaviours with respect to time. There is some evidence that autistic children have problems with how they perceive and understand time. However, little is currently known about this, or the ways in which behaviours related to time are impacted in daily life. In this study, 113 parents of autistic children and 201 parents of neurotypical children completed a questionnaire and open-ended questions about their child's behaviour relating to time. Questionnaire scores were lower in the autistic group compared with neurotypicals, which suggests that behaviours relating to time are affected in autistic children. The open-ended responses further confirmed that the autistic children struggled with time and that this impacted on them and their family. Three key themes were identified. Theme 1: autistic children have problems with learning about concepts relating to time such as telling the time from a clock and using words to describe time (hours, minutes, etc.) appropriately. Theme 2: autistic children think about the future differently. Planning and working under time pressure were described as a problem. Theme 3: autistic children have strong interests which take up a lot of their attention and worrying about having sufficient time to pursue these interests causes anxiety. This research indicates that behaviours related to time can have a considerable impact on the lives of autistic children and that targeted support may be required.
... Recently, it has been assumed to appear also in multisensory processing (e.g., Happé and Frith, 2006), that is, detail-focused processing leads to difficulty in the 'grouping of stimuli', which may cause a weaker reliance on visual input during multisensory processing. Indeed, by demonstrating a close link between poor acuity of audiovisual temporal binding and a weaker McGurk effect in autistic individuals, Stevenson et al. (2014) suggested that common deficits emerge in the integration processes at both lower and higher levels. ...
Article
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While visual information from facial speech modulates auditory speech perception, it is less influential on audiovisual speech perception among autistic individuals than among typically developed individuals. In this study, we investigated the relationship between autistic traits (Autism-Spectrum Quotient; AQ) and the influence of visual speech on the recognition of Rubin’s vase-type speech stimuli with degraded facial speech information. Participants were 31 university students (13 males and 18 females; mean age: 19.2, SD: 1.13 years) who reported normal (or corrected-to-normal) hearing and vision. All participants completed three speech recognition tasks (visual, auditory, and audiovisual stimuli) and the AQ–Japanese version. The results showed that accuracies of speech recognition for visual (i.e., lip-reading) and auditory stimuli were not significantly related to participants’ AQ. In contrast, audiovisual speech perception was less susceptible to facial speech perception among individuals with high rather than low autistic traits. The weaker influence of visual information on audiovisual speech perception in autism spectrum disorder (ASD) was robust regardless of the clarity of the visual information, suggesting a difficulty in the process of audiovisual integration rather than in the visual processing of facial speech.
... This protracted development of audiovisual skills makes a lot of sense given that the temporal lobe-the seat of the key components of the audiovisual integration network-is among the last cortical areas to mature [5,6]. Impairments in the development of audiovisual function have now been documented in several neurodevelopmental disorders, such as autism (e.g., [7][8][9][10]), dyslexia [11,12], and developmental language disorder (DLD, also known as specific language impairment or SLI, e.g., [13,14]). The nature of the impairments in each group and their relationship to other aspects of these disorders require a great deal more research; however, at least in some cases, audiovisual deficits appear to contribute critically to key aspects of these disorders (e.g., [15,16]). ...
Article
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We examined whether children with developmental language disorder (DLD) differed from their peers with typical development (TD) in the degree to which they encode information about a talker’s mouth shape into long-term phonemic representations. Children watched a talker’s face and listened to rare changes from [i] to [u] or the reverse. In the neutral condition, the talker’s face had a closed mouth throughout. In the audiovisual violation condition, the mouth shape always matched the frequent vowel, even when the rare vowel was played. We hypothesized that in the neutral condition no long-term audiovisual memory traces for speech sounds would be activated. Therefore, the neural response elicited by deviants would reflect only a violation of the observed audiovisual sequence. In contrast, we expected that in the audiovisual violation condition, a long-term memory trace for the speech sound/lip configuration typical for the frequent vowel would be activated. In this condition then, the neural response elicited by rare sound changes would reflect a violation of not only observed audiovisual patterns but also of a long-term memory representation for how a given vowel looks when articulated. Children pressed a response button whenever they saw a talker’s face assume a silly expression. We found that in children with TD, rare auditory changes produced a significant mismatch negativity (MMN) event-related potential (ERP) component over the posterior scalp in the audiovisual violation condition but not in the neutral condition. In children with DLD, no MMN was present in either condition. Rare vowel changes elicited a significant P3 in both groups and conditions, indicating that all children noticed auditory changes. Our results suggest that children with TD, but not children with DLD, incorporate visual information into long-term phonemic representations and detect violations in audiovisual phonemic congruency even when they perform a task that is unrelated to phonemic processing.
... Recently, there has been a growing interest concerning how these seemingly independent sensory symptoms may relate to one another. Very few studies measure sensory responses to different types of sensory stimuli in the same individuals making it difficult to examine how different aspects of autism behavior can manifest simultaneously [as recommended by (2); for example, when measuring the effects of stimulus complexity on the temporal binding window, (3,4); speech, (5); or word complexity, (6)]. Therefore, in the current study, we examined sensory processing to simple auditory stimuli (that differ in their pitch) that are processed early in the auditory system and processing to stimuli (that differ in their emotion) that are processed later in the auditory system in the same individuals with autism to examine the co-occurrence of different sensory profiles. ...
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Individuals with autism typically experience a range of symptoms, including abnormal sensory sensitivities. However, there are conflicting reports on the sensory profiles that characterize the sensory experience in autism that often depend on the type of stimulus. Here, we examine early auditory processing to simple changes in pitch and later auditory processing of more complex emotional utterances. We measured electroencephalography in 24 adults with autism and 28 controls. First, tones (1046.5Hz/C6, 1108.7Hz/C#6, or 1244.5Hz/D#6) were repeated three times or nine times before the pitch changed. Second, utterances of delight or frustration were repeated three or six times before the emotion changed. In response to the simple pitched tones, the autism group exhibited larger mismatch negativity (MMN) after nine standards compared to controls and produced greater trial-to-trial variability (TTV). In response to the prosodic utterances, the autism group showed smaller P3 responses when delight changed to frustration compared to controls. There was no significant correlation between ERPs to pitch and ERPs to prosody. Together, this suggests that early auditory processing is hyper-sensitive in autism whereas later processing of prosodic information is hypo-sensitive. The impact the different sensory profiles have on perceptual experience in autism may be key to identifying behavioral treatments to reduce symptoms.
... Left MTG and left IFG both exhibit morphometric alterations in adults with ASD (Libero et al., 2014). Right MTG has shown metabolic activation related to multimodal integration of communication cues (i.e., gaze, speech and gesture) (Holler et al., 2015) in TD, processes known to be challenging for individuals with ASD (Stevenson et al., 2014). The right precuneus is a key component of the default mode network (DMN), which is implicated in mentalizing (i.e., building inferences about others' mental states). ...
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Background Recent neuroimaging studies have highlighted differences in cerebral maturation in individuals with autism spectrum disorder (ASD) in comparison to typical development. For instance, the contrast of the gray-white matter boundary is decreased in adults with ASD. To determine how gray-white matter boundary integrity relates to early ASD phenotypes, we used a regional structural MRI index of gray-white matter contrast (GWC) on a sample of toddlers with a hereditary high risk for ASD. Materials and Methods We used a surface-based approach to compute vertex-wise GWC in a longitudinal cohort of toddlers at high-risk for ASD imaged twice between 12 and 24 months ( n = 20). A full clinical assessment of ASD-related symptoms was performed in conjunction with imaging and again at 3 years of age for diagnostic outcome. Three outcome groups were defined (ASD, n = 9; typical development, n = 8; non-typical development, n = 3). Results ASD diagnostic outcome at age 3 was associated with widespread increases in GWC between age 12 and 24 months. Many cortical regions were affected, including regions implicated in social processing and language acquisition. In parallel, we found that early onset of ASD symptoms (i.e., prior to 18-months) was specifically associated with slower GWC rates of change during the second year of life. These alterations were found in areas mainly belonging to the central executive network. Limitations Our study is the first to measure maturational changes in GWC in toddlers who developed autism, but given the limited size of our sample results should be considered exploratory and warrant further replication in independent and larger samples. Conclusion These preliminary results suggest that ASD is linked to early alterations of the gray-white matter boundary in widespread brain regions. Early onset of ASD diagnosis constitutes an independent clinical parameter associated with a specific corresponding neurobiological developmental trajectory. Altered neural migration and/or altered myelination processes potentially explain these findings.
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Background: Recent neuroimaging studies have highlighted differences in cerebral maturation in individuals with autism spectrum disorder (ASD) in comparison to typical development. For instance, the contrast of the gray-white matter boundary is decreased in adults with ASD. To determine how gray-white matter boundary integrity relates to early ASD phenotypes, we used a regional structural MRI index of gray-white matter contrast (GWC) on a sample of toddlers with a hereditary high risk for ASD. Methods: We used a surface-based approach to compute vertex-wise GWC in a longitudinal cohort of toddlers at high-risk for ASD imaged twice between 12 and 24 months (n=20). A full clinical assessment of ASD-related symptoms was performed in conjunction with imaging and again at three years of age for diagnostic outcome. Three outcome groups were defined (ASD, n=9; typical development, n=8; non-typical development, n=3). Results: ASD diagnostic outcome at age 3 was associated with widespread increases in GWC between age 12 and 24 months. Many cortical regions were affected, including regions implicated in social processing and language acquisition. In parallel, we found that early onset of ASD symptoms (i.e. prior to 18-months) was specifically associated with slower GWC rates of change during the second year of life. These alterations were found in areas mainly belonging to the central executive network. Limitations: Our study is the first to measure maturational changes in GWC in toddlers who developed autism, but given the limited size of our sample results should be considered exploratory and warrant further replication in independent and larger samples. Conclusion: These preliminary results suggest that ASD is linked to early alterations of the gray-white matter boundary in widespread brain regions. Early onset of ASD diagnosis constitutes an independent clinical parameter associated with a specific corresponding neurobiological developmental trajectory. Altered neural migration and/or altered myelination processes potentially explain these findings.
Article
The study of sensory phenotypes has great potential for increasing research translation between species, a necessity to decipher the neural mechanisms that contribute to higher‐order differences in neurological conditions such as autism spectrum disorder (ASD). Over the past decade, despite separate advances in our understanding of the structural and functional differences within the brain of autistic and non‐autistic individuals and in rodent models for ASD, researchers have had difficulty translating the findings in murine species to humans, mostly due to incompatibility in experimental methodologies used to screen for ASD phenotypes. Focusing on sensory phenotypes offers an avenue to close the species gap because sensory pathways are highly conserved across species and are affected by the same risk‐factors as the higher‐order brain areas mostly responsible for the diagnostic criteria for ASD. By first reviewing how sensory processing has been studied to date, we direct our focus to electrophysiological and behavioral techniques that can be used to study sensory phenotypes consistently across species. Using auditory sensory phenotypes as a template, we seek to improve the accessibility of translational methods by providing a framework for collecting cohesive data in both rodents and humans. Specifically, evoked‐potentials, acoustic startle paradigms, and psychophysical detection/discrimination paradigms can be created and implemented in a coordinated and systematic fashion across species. Through careful protocol design and collaboration, sensory processing phenotypes can be harnessed to bridge the gap that exists between preclinical animal studies and human testing, so that mutually held questions in autism research can be answered. Lay Summary It has always been difficult to relate results from animal research to humans. We try to close this gap by studying changes in sensory processing using careful protocol design and collaboration between clinicians and researchers. Sensory pathways are comparable between animals and humans, and are affected in the same way as the rest of the brain in ASD. Using changes in hearing as a template, we point the field in an innovative direction by providing a framework for collecting cohesive data in rodents and humans.
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This scoping review provides a descriptive synthesis of available evidence on children's audiovisual speech perception. We used eight databases to identify the experimental studies published 2000–2019, and reported the data using the guidelines of PRISMA-ScR designed for scoping reviews. While research conducted prior to 2000 provided a strong foundation in this area, the past two decades have brought technical advances that have allowed for more precise measurement of audiovisual speech perception. Thirty-eight studies were identified: 18 articles that focused on children with typical development, 9 focused on children with autism spectrum disorder, 8 focused on children with speech and language disorders, and 3 focused on children with hearing loss. Most of the studies identified were behavioral studies, while a minority reported on neuroanatomical correlates underlying the audiovisual speech perception. Through this scoping review, key gaps were identified that include few studies in clinical populations, a few studies on languages other than English, and variability in terminology to describe similar or overlapping concepts. Further research is needed to inform the development and mechanisms of audiovisual speech integration in children with different language development paths. In addition, the use of common terminology in future research would improve access to evidence and the communication of this knowledge for researchers and clinicians.
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Objectives: The aim of this study was to assess the relationship between sensory processing and a broad range of eating behaviours across the lifespan. Methods: Five electronic databases of published and unpublished quantitative studies were systematically searched, evaluated for risk of bias and synthesised according to identified eating outcomes. Results: Across 25 studies, there was consistent evidence of a relationship between sensory processing and a range of eating behaviours. There was early evidence for the particular role of taste/smell sensitivities, as well as hypersensitivities, although future research is needed looking at different sensory patterns and modalities. There was also tentative evidence to suggest this relationship extends across development. Discussion: Study findings are discussed in relation to implications for sensory-based eating and feeding interventions and the development of eating disorders. Methodological and conceptual limitations are discussed and suggestions for future research are made to address these limitations. A broader investigation of multi-sensory issues and clearly defined eating behaviours, including disordered eating in clinically diagnosed samples, will allow for a more comprehensive and robust understanding of the relationship between sensory processing and eating behaviours in autism.
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Multisensory integration, the process by which sensory information from different sensory modalities are bound together, is hypothesized to contribute to perceptual symptomatology in schizophrenia, in whom multisensory integration differences have been consistently found. Evidence is emerging that these differences extend across the schizophrenia spectrum, including individuals in the general population with higher levels of schizotypal traits. In the current study, we used the McGurk task as a measure of multisensory integration. We measured schizotypal traits using the Schizotypal Personality Questionnaire (SPQ), hypothesizing that higher levels of schizotypal traits, specifically Unusual Perceptual Experiences and Odd Speech subscales, would be associated with decreased multisensory integration of speech. Surprisingly, Unusual Perceptual Experiences were not associated with multisensory integration. However, Odd Speech was associated with multisensory integration, and this association extended more broadly across the Disorganized factor of the SPQ, including Odd or Eccentric Behaviour. Individuals with higher levels of Odd or Eccentric Behaviour scores also demonstrated poorer lip-reading abilities, which partially explained performance in the McGurk task. This suggests that aberrant perceptual processes affecting individuals across the schizophrenia spectrum may relate to disorganized symptomatology.
Article
Audiovisual (AV) integration plays a crucial role in supporting social functions and communication in autism spectrum disorder (ASD). However, behavioral findings remain mixed and, importantly, little is known about the underlying neurophysiological bases. Studies in neurotypical adults indicate that oscillatory brain activity in different frequencies subserves AV integration, pointing to a central role of (i) individual alpha frequency (IAF), which would determine the width of the cross-modal binding window; (ii) pre-/peri-stimulus theta oscillations, which would ref lect the expectation of AV co-occurrence; (iii) post-stimulus oscillatory phase reset, which would temporally align the different unisensory signals. Here, we investigate the neural correlates of AV integration in children with ASD and typically developing (TD) peers, measuring electroencephalography during resting state and in an AV integration paradigm. As for neurotypical adults, AV integration dynamics in TD children could be predicted by the IAF measured at rest and by a modulation of anticipatory theta oscillations at single-trial level. Conversely, in ASD participants, AV integration/segregation was driven exclusively by the neural processing of the auditory stimulus and the consequent auditory-induced phase reset in visual regions, suggesting that a disproportionate elaboration of the auditory input could be the main factor characterizing atypical AV integration in autism.
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Pre‐stimulus EEG oscillations, especially in the alpha range (8‐13 Hz), can affect the sensitivity to temporal lags between modalities in multisensory perception. The effects of alpha power are often explained in terms of alpha’s inhibitory functions, whereas effects of alpha frequency have bolstered theories of discrete perceptual cycles, where the length of a cycle, or window of integration, is determined by alpha frequency. Such studies typically employ visual detection paradigms with near‐threshold or even illusory stimuli. It is unclear whether such results generalize to above‐threshold stimuli. Here, we recorded electroencephalography, while measuring temporal discrimination sensitivity in a temporal order judgement task using above‐threshold auditory and visual stimuli. We tested whether the power and instantaneous frequency of pre‐stimulus oscillations predict audio‐visual temporal discrimination sensitivity on a trial‐by‐trial basis. By applying a jackknife procedure to link single‐trial pre‐stimulus oscillatory power and instantaneous frequency to psychometric measures, we identified a posterior cluster where lower alpha power was associated with higher temporal sensitivity of audiovisual discrimination. No statistically significant relationship between instantaneous alpha frequency and temporal sensitivity was found. These results suggest that temporal sensitivity for above‐threshold multisensory stimuli fluctuates from moment to moment and is indexed by modulations in alpha power.
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The sound-induced flash illusion (SIFI) occurs when a rapidly presented visual stimulus is accompanied by two auditory stimuli, creating the illusory percept of two visual stimuli. While much research has focused on how the temporal proximity of the audiovisual stimuli impacts susceptibility to the illusion, comparatively less research has focused on the impact of spatial manipulations. Here, we aimed to assess whether manipulating the eccentricity of visual flash stimuli altered the properties of the temporal binding window associated with the SIFI. Twenty participants were required to report whether they perceived one or two flashes that were concurrently presented with one or two beeps. Visual stimuli were presented at one of four different retinal eccentricities (2.5, 5, 7.5, or 10 degrees below fixation) and audiovisual stimuli were separated by one of eight stimulus-onset asynchronies. In keeping with previous findings, increasing stimulus-onset asynchrony between the auditory and visual stimuli led to a marked decrease in susceptibility to the illusion allowing us to estimate the width and amplitude of the temporal binding window. However, varying the eccentricity of the visual stimulus had no effect on either the width or the peak amplitude of the temporal binding window, with a similar pattern of results observed for both the “fission” and “fusion” variants of the illusion. Thus, spatial manipulations of the audiovisual stimuli used to elicit the SIFI appear to have a weaker effect on the integration of sensory signals than temporal manipulations, a finding which has implications for neuroanatomical models of multisensory integration.
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Autism spectrum disorder (ASD) is a heterogeneous syndrome characterized by behavioral features such as impaired social communication, repetitive behavior patterns, and a lack of interest in novel objects. A multimodal neuroimaging using magnetic resonance imaging (MRI) in patients with ASD shows highly heterogeneous abnormalities in function and structure in the brain associated with specific behavioral features. To elucidate the mechanism of ASD, several ASD mouse models have been generated, by focusing on some of the ASD risk genes. A specific behavioral feature of an ASD mouse model is caused by an altered gene expression or a modification of a gene product. Using these mouse models, a high field preclinical MRI enables us to non-invasively investigate the neuronal mechanism of the altered brain function associated with the behavior and ASD risk genes. Thus, MRI is a promising translational approach to bridge the gap between mice and humans. This review presents the evidence for multimodal MRI, including functional MRI (fMRI), diffusion tensor imaging (DTI), and volumetric analysis, in ASD mouse models and in patients with ASD and discusses the future directions for the translational study of ASD.
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Disorders, or more properly, Conditions of Autism Spectrum (ASC), are a pervasive, neurodevelopmental, lifelong condition that develops through complications in socio-emotional reciprocity, communication difficulties, and restrictive and repetitive behaviors. The establishment of ASC in the cognitive dimension of young people can cause comorbidity and therefore, the assessment and treatment of ASC should be applied immediately when symptoms are emerged. However, the difficulties in dealing with, but also in the detection of ASC in combination with the high rates of misdiagnosis, poses the imperative need for effective interventions. Satisfactory therapeutic tools have been developed to help young people with an ASC. The present literature review targeted two of them: Animal Assistant Therapy (AAT) and Virtual Reality Interventions (VR-I). These were investigated by evaluating their effectiveness by scoping Randomized Clinical Trials, derived from the PubMed.gov and Clinicaltrials.gov databases. AAT will be evaluated on its effectiveness in improving the Aspects of Interpersonal and Functional Problems, Theory of Mind and hyperactivity behaviors, while the VR-I will be evaluated on its effectiveness in enhancing the expression and regulation of emotions, socio-emotional reciprocity and the adaptation of motor and cognitive skills. The results of the study highlight deficiencies in the structure of the research methods evaluated, the effect of interventions on the second level symptoms, while a pioneering use of VR-I will be discussed, which can utilize motor learning as a bridge, providing potential for improvements to individuals with an ASC.
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The lateral cortex of the inferior colliculus (LCIC) is a multimodal subdivision of the midbrain inferior colliculus (IC) that plays a key role in sensory integration. The LCIC is compartmentally-organized, exhibiting a series of discontinuous patches or modules surrounded by an extramodular matrix. In adult mice, somatosensory afferents target LCIC modular zones, while auditory afferents terminate throughout the encompassing matrix. Recently, we defined an early LCIC critical period (birth: postnatal day 0 to P12) based upon the concurrent emergence of its neurochemical compartments (modules: glutamic acid decarboxylase, GAD+; matrix: calretinin, CR+), matching Eph-ephrin guidance patterns, and specificity of auditory inputs for its matrix. Currently lacking are analogous experiments that address somatosensory afferent shaping and the construction of discrete LCIC multisensory maps. Combining living slice tract-tracing and immunocytochemical approaches in a developmental series of GAD67-GFP knock-in mice, the present study characterizes: (1) the targeting of somatosensory terminals for emerging LCIC modular fields; and (2) the relative separation of somatosensory and auditory inputs over the course of its established critical period. Results indicate a similar time course and progression of LCIC projection shaping for both somatosensory (corticocollicular) and auditory (intracollicular) inputs. While somewhat sparse and intermingling at birth, modality-specific projection patterns soon emerge (P4–P8), coincident with peak guidance expression and the appearance of LCIC compartments. By P12, an adult-like arrangement is in place, with fully segregated multimodal afferent arrays. Quantitative measures confirm increasingly distinct input maps, exhibiting less projection overlap with age. Potential mechanisms whereby multisensory LCIC afferent systems recognize and interface with its emerging modular-matrix framework are discussed.
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The term ‘timing’ is interchangeably used to convey processing of the order or the duration of events. Yet, whereas temporal order processing means judging when one event happens relative to another (first or second), duration estimation means measuring how long the event lasts. In this Review, we show that the functional distinction between these two temporal features is reflected in their discrete neural substrates. Temporal order processing preferentially engages the left inferior parietal cortex, whereas duration estimation recruits the supplementary motor area, basal ganglia and cerebellum. The functional distinction between temporal order processing and duration estimation also enables better characterization of temporal perturbations present in clinical disorders. For instance, individuals with schizophrenia have trouble individuating and ordering consecutive events in time and show atypical responses to stimuli that do not appear when expected. Therefore, individuals with schizophrenia might have a fundamental impairment in processing when a stimulus occurs relative to another event, rather than in estimating how long it lasts. These neural and clinical dissociations demonstrate that the phenomenological sensation of a unitary and cohesive flow of time (‘time’s arrow’) can be separated into two distinct, though intertwined, components. Subjective time perception involves processing when an event happens relative to another event versus how long an event lasts. In this Review, Coull and Giersch describe the functional and neural differences between temporal order processing and duration estimation by exploring perturbations in individuals with schizophrenia.
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Microglial cells (MGCs) are highly dynamic and have been implicated in shaping discrete neural maps in several unimodal systems. MGCs respond to numerous cues in their microenvironment, including the neuronally expressed chemokine, fractalkine (CX3CL1), via interactions with its corresponding fractalkine receptor (CX3CR1). The present study examines microglial and CX3CL1 patterns with regard to the emerging modular-extramodular matrix organization within the lateral cortex of the inferior colliculus (LCIC). The LCIC is a multisensory shell region of the midbrain inferior colliculus where discrete compartments receive modality-specific connections. Somatosensory inputs terminate within modular confines, while auditory inputs target the surrounding matrix. Glutamic acid decarboxylase (GAD) is an established marker of LCIC modules in developing mouse. During early postnatal development, multimodal LCIC afferents segregate into discrete, neurochemically defined compartments. Here, we analyzed neonatal GAD67-GFP (GFP is defined as green fluorescent protein) and CX3CR1-GFP mice to assess: (1) whether MGCs are recruited to distinct LCIC compartments known to be undergoing active circuit assembly, and (2) if such behaviors are fractalkine signaling-dependent. MGCs colonize the nascent LCIC by birth and increase in density until postnatal day 12 (P12). At the peak critical period (P4-P8), MGCs conspicuously border emerging LCIC modules, prior to their subsequent invasion by P12. CX3CL1 expression becomes distinctly modular at P12, in keeping with the notion of fractalkine-mediated recruitment of microglia to modular centers. In CX3CR1GFP/GFP mice with compromised fractalkine signaling, microglial recruitment into modules is delayed. Taken together, these results suggest a potential role for microglia and fractalkine signaling in sculpting multisensory LCIC maps during an early critical period.
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Temporal synchrony is the alignment of processes in time within or across individuals in social interaction and is observed and studied in various domains using wide-ranging paradigms. Evidence suggesting reduced temporal synchrony in autism (e.g. compared to neurotypicals) has hitherto not been reviewed. To systematically review the magnitude and generalisability of the difference across different tasks and contexts, EBSCO, OVID, Web of Science, and Scopus databases were searched. Thirty-two studies were identified that met our inclusion criteria in audio-visual, audio-motor, visuo-tactile, visuo-motor, social motor, and conversational synchrony domains. Additionally, two intervention studies were included. The findings suggest that autistic participants showed reduced synchrony tendencies in every category of temporal synchrony reviewed. Implications, methodological weaknesses, and evidence gaps are discussed.
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Autism Spectrum Disorder (ASD) is a highly heterogeneous neurodevelopmental disorder characterized by deficits in social communication and by patterns of restricted interests and/or repetitive behaviors. The Simons Foundation Autism Research Initiative’s Human Gene and CNV Modules now list over 1,000 genes implicated in ASD and over 2,000 copy number variant loci reported in individuals with ASD. Given this ever-growing list of genetic changes associated with ASD, it has become evident that there is likely not a single genetic cause of this disorder nor a single neurobiological basis of this disorder. Instead, it is likely that many different neurobiological perturbations (which may represent subtypes of ASD) can result in the set of behavioral symptoms that we called ASD. One such of possible subtype of ASD may be associated with dopamine dysfunction. Precise regulation of synaptic dopamine (DA) is required for reward processing and behavioral learning, behaviors which are disrupted in ASD. Here we review evidence for DA dysfunction in ASD and in animal models of ASD. Further, we propose that these studies provide a scaffold for scientists and clinicians to consider subcategorizing the ASD diagnosis based on the genetic changes, neurobiological difference, and behavioral features identified in individuals with ASD.
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Background: As a kind of neurodevelopmental disorder, the deficiency of social interaction and communication ability is the core symptom of autism spectrum disorder (ASD). However, ASD usually has sensory abnormalities, which may be an important influencing factor of social function. Here, the aim of the current study is to explore the abnormal sensory characteristics of ASD children and the correlation between social behavior. And further clarify the predictive effect of sensory expression on ASD social ability. Methods: A case-control study was conducted, with children aged 3 to 10 years including ASD and typical development (TD) as subjects. We used Short Sensory Profile (SSP) questionnaire to evaluate the sensory characteristics in ASD group and TD group. And Social Responsiveness Scale (SRS) was employed to assess the social function of ASD. The differences of SSP scores between two groups of children were compared, and the correlation between SSP in ASD group and SRS was further analyzed. Furthermore, by constructing random forest classification model and support vector machine classification model, the predictive ability of each perception on social level is discussed. Results: Significant differences were found between ASD children and TD children in the performance of each sensory field. The abnormal sensory rate of children in ASD group is as high as 91.4%, and 74% of them are accompanied by sensory disorders in multiple dimensions.It is worth noting that there is a significant negative correlation between the scores of ASD group children in all dimensions of SSP and the scores of SRS scale. Evaluation and comparison results of full-feature and 7-feature models show that the random forest model and SVM model with all-feature factors have higher sensitivity, while the random forest model with 7-feature factors has the highest specificity. Moreover, the maximum of area value under (AUC) of receiver operating characteristic (ROC) curve between the four models up to 0.859, suggest that the good prediction effect of the models. Conclusion: Our results suggest autism children have obvious abnormalities in many sensory fields, and there is a significant correlation between this atypical sensory performance and social function. The social level of this group can be well predicted by their sensory characteristics.
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Autism is a neurodevelopmental disorder characterized by impaired social skills, motor and perceptual atypicalities. These difficulties were explained within the Bayesian framework as either reflecting oversensitivity to prediction errors or – just the opposite – slow updating of such errors. To test these opposing theories, we administer paced finger-tapping, a synchronization task that requires use of recent sensory information for fast error-correction. We use computational modelling to disentangle the contributions of error-correction from that of noise in keeping temporal intervals, and in executing motor responses. To assess the specificity of tapping characteristics to autism, we compare performance to both neurotypical individuals and individuals with dyslexia. Only the autism group shows poor sensorimotor synchronization. Trial-by-trial modelling reveals typical noise levels in interval representations and motor responses. However, rate of error correction is reduced in autism, impeding synchronization ability. These results provide evidence for slow updating of internal representations in autism.
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Autistic children show audiovisual speech integration deficits, though the underlying mechanisms remain unclear. The present study examined how audiovisual speech integration deficits in autistic children could be affected by their looking patterns. We measured audiovisual speech integration in 26 autistic children and 26 typically developing (TD) children (4- to 7-year-old) employing the McGurk task (a videotaped speaker uttering phonemes with her eyes open or closed) and tracked their eye movements. We found that, compared with TD children, autistic children showed weaker audiovisual speech integration (i.e., the McGurk effect) in the open-eyes condition and similar audiovisual speech integration in the closed-eyes condition. Autistic children viewed the speaker's mouth less in non-McGurk trials than in McGurk trials in both conditions. Importantly, autistic children's weaker audiovisual speech integration could be predicted by their reduced mouth-looking time. The present study indicated that atypical face-viewing patterns could serve as one of the cognitive mechanisms of audiovisual speech integration deficits in autistic children. Lay Summary McGurk effect occurs when the visual part of a phoneme (e.g., “ga”) and the auditory part of another phoneme (e.g., “ba”) uttered by a speaker were integrated into a fused perception (e.g., “da”). The present study examined how McGurk effect in autistic children could be affected by their looking patterns for the speaker's face. We found that less looking time for the speaker's mouth in autistic children could predict weaker McGurk effect. As McGurk effect manifests audiovisual speech integration, our findings imply that we could improve audiovisual speech integration in autistic children by directing them to look at the speaker's mouth in future intervention.
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Impaired audiovisual temporal integration, manifested as an abnormally widened temporal-binding window (TBW) for integrating sensory information, is found in both autism spectrum disorder (ASD) and schizophrenia (SCZ) and contributes to aberrant perceptual experiences and impaired social communication. We conducted two experiments using age-comparable samples of participants with early-onset SCZ and participants with ASD. Sophisticated paradigms, including a unisensory temporal-order-judgment task (TOJ), an audiovisual-simultaneity-judgment task (SJ), and an eye-tracking task were used. Results showed generalized deficits in temporal processing in SCZ ranging from unisensory to multisensory modalities and from nonspeech to speech stimuli. In contrast, the widened TBW in ASD mainly affected speech stimuli processing. Applying the eye-tracking task with ecologically valid linguistic stimuli, we found that both participants with SCZ and participants with ASD exhibited reduced sensitivity of detecting audiovisual speech asynchrony. This impaired audiovisual speech integration correlated with negative symptoms. Although both ASD and SCZ have impaired multisensory temporal integration, ASD impairs speech-related processing, and SCZ is associated with generalized deficits.
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Prosody or “melody in speech” in autism spectrum disorder (ASD) is often perceived as atypical. This study examined perception and production of statements and questions in 84 children, adolescents and adults with and without ASD, as well as participants’ pitch direction discrimination thresholds. The results suggested that the abilities to discriminate (in both speech and music conditions), identify, and imitate statement-question intonation were intact in individuals with ASD across age cohorts. Sensitivity to pitch direction predicted performance on intonation processing in both groups, who also exhibited similar developmental changes. These findings provide evidence for shared mechanisms in pitch processing between speech and music, as well as associations between low- and high-level pitch processing and between perception and production of pitch.
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Background: Autism spectrum disorder (ASD) affects many aspects of life, from social interactions to (multi)sensory processing. Similarly, the condition expresses at the variety of levels of description, from genetics to neural circuits and interpersonal behavior. We attempt to bridge between domains and levels of description by detailing the behavioral, electrophysiological, and putative neural network basis of peri-personal space (PPS) updating in ASD during a social context, given that the encoding of this space relies on appropriate multisensory integration, is malleable by social context, and thought to delineate the boundary between self and other. Methods: Fifty (20 male/30 female) young adults, either diagnosed with ASD or age- and gender-matched individuals took part in a visuo-tactile reaction time task indexing PPS, while high-density electroencephalography (EEG) was continuously recorded. Neural network modeling was performed in silico. Results: Multisensory psychophysics demonstrates that while PPS in neurotypical individuals shrinks in the presence of others - as to "give space" - this does not occur in ASD. Likewise, EEG recordings suggest that multisensory integration is altered by social context in neurotypical but not ASD individuals. Lastly, a biologically plausible neural network model shows, as proof-of-principle, that PPS updating may be inflexible in ASD due to the altered excitatory/inhibitory (E/I) balance that characterizes neural circuits in animal models of ASD. Conclusion: Findings are conceptually in line with recent statistical inference accounts suggesting diminished flexibility in ASD, and further these observations by suggesting within an example relevant for social cognition that such inflexibility may be due to E/I imbalances.
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Under noisy listening conditions, visualizing a speaker's articulations substantially improves speech intelligibility. This multisensory speech integration ability is crucial to effective communication, and the appropriate development of this capacity greatly impacts a child's ability to successfully navigate educational and social settings. Research shows that multisensory integration abilities continue developing late into childhood. The primary aim here was to track the development of these abilities in children with autism, since multisensory deficits are increasingly recognized as a component of the autism spectrum disorder (ASD) phenotype. The abilities of high-functioning ASD children (n = 84) to integrate seen and heard speech were assessed cross-sectionally, while environmental noise levels were systematically manipulated, comparing them with age-matched neurotypical children (n = 142). Severe integration deficits were uncovered in ASD, which were increasingly pronounced as background noise increased. These deficits were evident in school-aged ASD children (5-12 year olds), but were fully ameliorated in ASD children entering adolescence (13-15 year olds). The severity of multisensory deficits uncovered has important implications for educators and clinicians working in ASD. We consider the observation that the multisensory speech system recovers substantially in adolescence as an indication that it is likely amenable to intervention during earlier childhood, with potentially profound implications for the development of social communication abilities in ASD children.
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The notion of the temporal window of integration, when applied in a multisensory context, refers to the breadth of the interval across which the brain perceives two stimuli from different sensory modalities as synchronous. It maintains a unitary perception of multisensory events despite physical and biophysical timing differences between the senses. The boundaries of the window can be influenced by attention and past sensory experience. Here we examined whether task demands could also influence the multisensory temporal window of integration. We varied the stimulus onset asynchrony between simple, short-lasting auditory and visual stimuli while participants performed two tasks in separate blocks: a temporal order judgment task that required the discrimination of subtle auditory-visual asynchronies, and a reaction time task to the first incoming stimulus irrespective of its sensory modality. We defined the temporal window of integration as the range of stimulus onset asynchronies where performance was below 75% in the temporal order judgment task, as well as the range of stimulus onset asynchronies where responses showed multisensory facilitation (race model violation) in the reaction time task. In 5 of 11 participants, we observed audio-visual stimulus onset asynchronies where reaction time was significantly accelerated (indicating successful integration in this task) while performance was accurate in the temporal order judgment task (indicating successful segregation in that task). This dissociation suggests that in some participants, the boundaries of the temporal window of integration can adaptively recalibrate in order to optimize performance according to specific task demands.
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We examined sensitivity of audiovisual temporal order in adolescents with autism spectrum disorder (ASD) using an audiovisual temporal order judgment (TOJ) task. In order to assess domain-specific impairments, the stimuli varied in social complexity from simple flash/beeps to videos of a handclap or a speaking face. Compared to typically-developing controls, individuals with ASD were generally less sensitive in judgments of audiovisual temporal order (larger just noticeable differences, JNDs), but there was no specific impairment with social stimuli. This suggests that people with ASD suffer from a more general impairment in audiovisual temporal processing.
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The Autism Diagnostic Observation Schedule—Generic (ADOS-G) is a semistructured, standardized assessment of social interaction, communication, play, and imaginative use of materials for individuals suspected of having autism spectrum disorders. The observational schedule consists of four 30-minute modules, each designed to be administered to different individuals according to their level of expressive language. Psychometric data are presented for 223 children and adults with Autistic Disorder (autism), Pervasive Developmental Disorder Not Otherwise Specified (PDDNOS) or nonspectrum diagnoses. Within each module, diagnostic groups were equivalent on expressive language level. Results indicate substantial interrater and test—retest reliability for individual items, excellent interrater reliability within domains and excellent internal consistency. Comparisons of means indicated consistent differentiation of autism and PDDNOS from nonspectrum individuals, with some, but less consistent, differentiation of autism from PDDNOS. A priori operationalization of DSM-IV/ICD-10 criteria, factor analyses, and ROC curves were used to generate diagnostic algorithms with thresholds set for autism and broader autism spectrum/PDD. Algorithm sensitivities and specificities for autism and PDDNOS relative to nonspectrum disorders were excellent, with moderate differentiation of autism from PDDNOS.
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Successful integration of auditory and visual inputs is crucial for both basic perceptual functions and for higher-order processes related to social cognition. Autism spectrum disorders (ASD) are characterized by impairments in social cognition and are associated with abnormalities in sensory and perceptual processes. Several groups have reported that individuals with ASD are impaired in their ability to integrate socially relevant audiovisual (AV) information, and it has been suggested that this contributes to the higher-order social and cognitive deficits observed in ASD. However, successful integration of auditory and visual inputs also influences detection and perception of nonsocial stimuli, and integration deficits may impair earlier stages of information processing, with cascading downstream effects. To assess the integrity of basic AV integration, we recorded high-density electrophysiology from a cohort of high-functioning children with ASD (7-16 years) while they performed a simple AV reaction time task. Children with ASD showed considerably less behavioral facilitation to multisensory inputs, deficits that were paralleled by less effective neural integration. Evidence for processing differences relative to typically developing children was seen as early as 100 ms poststimulation, and topographic analysis suggested that children with ASD relied on different cortical networks during this early multisensory processing stage.
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The brain's ability to bind incoming auditory and visual stimuli depends critically on the temporal structure of this information. Specifically, there exists a temporal window of audiovisual integration within which stimuli are highly likely to be perceived as part of the same environmental event. Several studies have described the temporal bounds of this window, but few have investigated its malleability. Recently, our laboratory has demonstrated that a perceptual training paradigm is capable of eliciting a 40% narrowing in the width of this window that is stable for at least 1 week after cessation of training. In the current study, we sought to reveal the neural substrates of these changes. Eleven human subjects completed an audiovisual simultaneity judgment training paradigm, immediately before and after which they performed the same task during an event-related 3T fMRI session. The posterior superior temporal sulcus (pSTS) and areas of auditory and visual cortex exhibited robust BOLD decreases following training, and resting state and effective connectivity analyses revealed significant increases in coupling among these cortices after training. These results provide the first evidence of the neural correlates underlying changes in multisensory temporal binding likely representing the substrate for a multisensory temporal binding window.
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Autism spectrum disorders (ASD) are characterized by deficits in social reciprocity and communication, as well as by repetitive behaviors and restricted interests. Unusual responses to sensory input and disruptions in the processing of both unisensory and multisensory stimuli also have been reported frequently. However, the specific aspects of sensory processing that are disrupted in ASD have yet to be fully elucidated. Recent published work has shown that children with ASD can integrate low-level audiovisual stimuli, but do so over an extended range of time when compared with typically developing (TD) children. However, the possible contributions of altered unisensory temporal processes to the demonstrated changes in multisensory function are yet unknown. In the current study, unisensory temporal acuity was measured by determining individual thresholds on visual and auditory temporal order judgment (TOJ) tasks, and multisensory temporal function was assessed through a cross-modal version of the TOJ task. Whereas no differences in thresholds for the visual TOJ task were seen between children with ASD and TD, thresholds were higher in ASD on the auditory TOJ task, providing preliminary evidence for impairment in auditory temporal processing. On the multisensory TOJ task, children with ASD showed performance improvements over a wider range of temporal intervals than TD children, reinforcing prior work showing an extended temporal window of multisensory integration in ASD. These findings contribute to a better understanding of basic sensory processing differences, which may be critical for understanding more complex social and cognitive deficits in ASD, and ultimately may contribute to more effective diagnostic and interventional strategies.
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"Oral speech intelligibility tests were conducted with, and without, supplementary visual observation of the speaker's facial and lip movements. The difference between these two conditions was examined as a function of the speech-to-noise ratio and of the size of the vocabulary under test. The visual contribution to oral speech intelligibility (relative to its possible contribution) is, to a first approximation, independent of the speech-to-noise ratio under test. However, since there is a much greater opportunity for the visual contribution at low speech-to-noise ratios, its absolute contribution can be exploited most profitably under these conditions." (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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The temporal synchrony of auditory and visual signals is known to affect the perception of an external event, yet it is unclear what neural mechanisms underlie the influence of temporal synchrony on perception. Using parametrically varied levels of stimulus asynchrony in combination with BOLD fMRI, we identified two anatomically distinct subregions of multisensory superior temporal cortex (mSTC) that showed qualitatively distinct BOLD activation patterns. A synchrony-defined subregion of mSTC (synchronous > asynchronous) responded only when auditory and visual stimuli were synchronous, whereas a bimodal subregion of mSTC (auditory > baseline and visual > baseline) showed significant activation to all presentations, but showed monotonically increasing activation with increasing levels of asynchrony. The presence of two distinct activation patterns suggests that the two subregions of mSTC may rely on different neural mechanisms to integrate audiovisual sensory signals. An additional whole-brain analysis revealed a network of regions responding more with synchronous than asynchronous speech, including right mSTC, and bilateral superior colliculus, fusiform gyrus, lateral occipital cortex, and extrastriate visual cortex. The spatial location of individual mSTC ROIs was much more variable in the left than right hemisphere, suggesting that individual differences may contribute to the right lateralization of mSTC in a group SPM. These findings suggest that bilateral mSTC is composed of distinct multisensory subregions that integrate audiovisual speech signals through qualitatively different mechanisms, and may be differentially sensitive to stimulus properties including, but not limited to, temporal synchrony.
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Human multisensory systems are known to bind inputs from the different sensory modalities into a unified percept, a process that leads to measurable behavioral benefits. This integrative process can be observed through multisensory illusions, including the McGurk effect and the sound-induced flash illusion, both of which demonstrate the ability of one sensory modality to modulate perception in a second modality. Such multisensory integration is highly dependent upon the temporal relationship of the different sensory inputs, with perceptual binding occurring within a limited range of asynchronies known as the temporal binding window (TBW). Previous studies have shown that this window is highly variable across individuals, but it is unclear how these variations in the TBW relate to an individual's ability to integrate multisensory cues. Here we provide evidence linking individual differences in multisensory temporal processes to differences in the individual's audiovisual integration of illusory stimuli. Our data provide strong evidence that the temporal processing of multiple sensory signals and the merging of multiple signals into a single, unified perception, are highly related. Specifically, the width of right side of an individuals' TBW, where the auditory stimulus follows the visual, is significantly correlated with the strength of illusory percepts, as indexed via both an increase in the strength of binding synchronous sensory signals and in an improvement in correctly dissociating asynchronous signals. These findings are discussed in terms of their possible neurobiological basis, relevance to the development of sensory integration, and possible importance for clinical conditions in which there is growing evidence that multisensory integration is compromised. (PsycINFO Database Record (c) 2012 APA, all rights reserved).
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This study used eye-tracking methodology to assess audiovisual speech perception in 26 children ranging in age from 5 to 15 years, half with autism spectrum disorders (ASD) and half with typical development. Given the characteristic reduction in gaze to the faces of others in children with ASD, it was hypothesized that they would show reduced influence of visual information on heard speech. Responses were compared on a set of auditory, visual, and audiovisual speech perception tasks. Even when fixated on the face of the speaker, children with ASD were less visually influenced than typical development controls. This indicates fundamental differences in the processing of audiovisual speech in children with ASD, which may contribute to their language and communication impairments.
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The McGurk effect is a compelling illusion in which humans perceive mismatched audiovisual speech as a completely different syllable. However, some normal individuals do not experience the illusion, reporting that the stimulus sounds the same with or without visual input. Converging evidence suggests that the left superior temporal sulcus (STS) is critical for audiovisual integration during speech perception. We used blood-oxygen level dependent functional magnetic resonance imaging (BOLD fMRI) to measure brain activity as McGurk perceivers and non-perceivers were presented with congruent audiovisual syllables, McGurk audiovisual syllables, and non-McGurk incongruent syllables. The inferior frontal gyrus showed an effect of stimulus condition (greater responses for incongruent stimuli) but not susceptibility group, while the left auditory cortex showed an effect of susceptibility group (greater response in susceptible individuals) but not stimulus condition. Only one brain region, the left STS, showed a significant effect of both susceptibility and stimulus condition. The amplitude of the response in the left STS was significantly correlated with the likelihood of perceiving the McGurk effect: a weak STS response meant that a subject was less likely to perceive the McGurk effect, while a strong response meant that a subject was more likely to perceive it. These results suggest that the left STS is a key locus for interindividual differences in speech perception.
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Atypical sensory-based behaviors are a ubiquitous feature of autism spectrum disorders (ASDs). In this article, we review the neural underpinnings of sensory processing in autism by reviewing the literature on neurophysiological responses to auditory, tactile, and visual stimuli in autistic individuals. We review studies of unimodal sensory processing and multisensory integration that use a variety of neuroimaging techniques, including electroencephalography (EEG), magnetoencephalography (MEG), and functional MRI. We then explore the impact of covert and overt attention on sensory processing. With additional characterization, neurophysiologic profiles of sensory processing in ASD may serve as valuable biomarkers for diagnosis and monitoring of therapeutic interventions for autism and reveal potential strategies and target brain regions for therapeutic interventions.