Evidence for Diminished Multisensory Integration in Autism Spectrum Disorders

Individuals with autism spectrum disorders (ASD) exhibit alterations in sensory processing, including changes in the integration of information across the different sensory modalities. In the current study, we used the sound-induced flash illusion to assess multisensory integration in children with ASD and typically-developing (TD) controls. Thirty-one children with ASD and 31 age and IQ matched TD children (average age = 12 years) were presented with simple visual (i.e., flash) and auditory (i.e., beep) stimuli of varying number. In illusory conditions, a single flash was presented with 2–4 beeps. In TD children, these conditions generally result in the perception of multiple flashes, implying a perceptual fusion across vision and audition. In the present study, children with ASD were significantly less likely to perceive the illusion relative to TD controls, suggesting that multisensory integration and cross-modal binding may be weaker in some children with ASD. These results are discussed in the context of previous findings for multisensory integration in ASD and future directions for research.     

Neural correlates of interindividual differences in children's audiovisual speech perception

Children use information from both the auditory and visual modalities to aid in understanding speech. A dramatic illustration of this multisensory integration is the McGurk effect, an illusion in which an auditory syllable is perceived differently when it is paired with an incongruent mouth movement. However, there are significant interindividual differences in McGurk perception: some children never perceive the illusion, while others always do. Because converging evidence suggests that the posterior superior temporal sulcus (STS) is a critical site for multisensory integration, we hypothesized that activity within the STS would predict susceptibility to the McGurk effect. To test this idea, we used BOLD fMRI in 17 children aged 6-12 years to measure brain responses to the following three audiovisual stimulus categories: McGurk incongruent, non-McGurk incongruent, and congruent syllables. Two separate analysis approaches, one using independent functional localizers and another using whole-brain voxel-based regression, showed differences in the left STS between perceivers and nonperceivers. The STS of McGurk perceivers responded significantly more than that of nonperceivers to McGurk syllables, but not to other stimuli, and perceivers' hemodynamic responses in the STS were significantly prolonged. In addition to the STS, weaker differences between perceivers and nonperceivers were observed in the fusiform face area and extrastriate visual cortex. These results suggest that the STS is an important source of interindividual variability in children's audiovisual speech perception.     

Multisensory integration of speech sounds with letters vs. visual speech: only visual speech induces the mismatch negativity

Numerous studies have demonstrated that the vision of lip movements can alter the perception of auditory speech syllables (McGurk effect). While there is ample evidence for integration of text and auditory speech, there are only a few studies on the orthographic equivalent of the McGurk effect. Here, we examined whether written text, like visual speech, can induce an illusory change in the perception of speech sounds on both the behavioural and neural levels. In a sound categorization task, we found that both text and visual speech changed the identity of speech sounds from an /aba/‐/ada/ continuum, but the size of this audiovisual effect was considerably smaller for text than visual speech. To examine at which level in the information processing hierarchy these multisensory interactions occur, we recorded electroencephalography in an audiovisual mismatch negativity (MMN, a component of the event‐related potential reflecting preattentive auditory change detection) paradigm in which deviant text or visual speech was used to induce an illusory change in a sequence of ambiguous sounds halfway between /aba/ and /ada/. We found that only deviant visual speech induced an MMN, but not deviant text, which induced a late P3‐like positive potential. These results demonstrate that text has much weaker effects on sound processing than visual speech does, possibly because text has different biological roots than visual speech.     

Neural processes underlying perceptual enhancement by visual speech gestures

This fMRI study explores brain regions involved with perceptual enhancement afforded by observation of visual speech gesture information. Subjects passively identified words presented in the following conditions: audio-only, audiovisual, audio-only with noise, audiovisual with noise, and visual only. The brain may use concordant audio and visual information to enhance perception by integrating the information in a converging multisensory site. Consistent with response properties of multisensory integration sites, enhanced activity in middle and superior temporal gyrus/sulcus was greatest when concordant audiovisual stimuli were presented with acoustic noise. Activity found in brain regions involved with planning and execution of speech production in response to visual speech presented with degraded or absent auditory stimulation, is consistent with the use of an additional pathway through which speech perception is facilitated by a process of internally simulating the intended speech act of the observed speaker.     

Audiovisual Processing in Children with and without Autism Spectrum Disorders

Fifteen children with autism spectrum disorders (ASD) and twenty-one children without ASD completed six perceptual tasks designed to characterize the nature of the audiovisual processing difficulties experienced by children with ASD. Children with ASD scored significantly lower than children without ASD on audiovisual tasks involving human faces and voices, but scored similarly to children without ASD on audiovisual tasks involving nonhuman stimuli (bouncing balls). Results suggest that children with ASD may use visual information for speech differently from children without ASD. Exploratory results support an inverse association between audiovisual speech processing capacities and social impairment in children with ASD.     

Development of an audiovisual speech perception app for children with autism spectrum disorders

Perception of spoken language requires attention to acoustic as well as visible phonetic information. This article reviews the known differences in audiovisual speech perception in children with autism spectrum disorders (ASD) and specifies the need for interventions that address this construct. Elements of an audiovisual training program are described. This researcher-developed program delivered via an iPad app presents natural speech in the context of increasing noise, but supported with a speaking face. Children are cued to attend to visible articulatory information to assist in perception of the spoken words. Data from four children with ASD ages 8–10 are presented showing that the children improved their performance on an untrained auditory speech-in-noise task.     

Neural correlates of multisensory integration of ecologically valid audiovisual events

A question that has emerged over recent years is whether audiovisual (AV) speech perception is a special case of multi-sensory perception. Electrophysiological (ERP) studies have found that auditory neural activity (N1 component of the ERP) induced by speech is suppressed and speeded up when a speech sound is accompanied by concordant lip movements. In Experiment 1, we show that this AV interaction is not speech-specific. Ecologically valid nonspeech AV events (actions performed by an actor such as handclapping) were associated with a similar speeding-up and suppression of auditory N1 amplitude as AV speech (syllables). Experiment 2 demonstrated that these AV interactions were not influenced by whether A and V were congruent or incongruent. In Experiment 3 we show that the AV interaction on N1 was absent when there was no anticipatory visual motion, indicating that the AV interaction only occurred when visual anticipatory motion preceded the sound. These results demonstrate that the visually induced speeding-up and suppression of auditory N1 amplitude reflect multisensory integrative mechanisms of AV events that crucially depend on whether vision predicts when the sound occurs.     

A Comparison of the Development of Audiovisual Integration in Children with Autism Spectrum Disorders and Typically Developing Children

This study aimed to investigate the development of audiovisual integration in children with Autism Spectrum Disorder (ASD). Audiovisual integration was measured using the McGurk effect in children with ASD aged 7–16 years and typically developing children (control group) matched approximately for age, sex, nonverbal ability and verbal ability. Results showed that the children with ASD were delayed in visual accuracy and audiovisual integration compared to the control group. However, in the audiovisual integration measure, children with ASD appeared to ‘catch-up’ with their typically developing peers at the older age ranges. The suggestion that children with ASD show a deficit in audiovisual integration which diminishes with age has clinical implications for those assessing and treating these children.     

The development of multisensory speech perception continues into the late childhood years

Observing a speaker's articulations substantially improves the intelligibility of spoken speech, especially under noisy listening conditions. This multisensory integration of speech inputs is crucial to effective communication. Appropriate development of this ability has major implications for children in classroom and social settings, and deficits in it have been linked to a number of neurodevelopmental disorders, especially autism. It is clear from structural imaging studies that there is a prolonged maturational course within regions of the perisylvian cortex that persists into late childhood, and these regions have been firmly established as being crucial to speech and language functions. Given this protracted maturational timeframe, we reasoned that multisensory speech processing might well show a similarly protracted developmental course. Previous work in adults has shown that audiovisual enhancement in word recognition is most apparent within a restricted range of signal-to-noise ratios (SNRs). Here, we investigated when these properties emerge during childhood by testing multisensory speech recognition abilities in typically developing children aged between 5 and 14 years, and comparing them with those of adults. By parametrically varying SNRs, we found that children benefited significantly less from observing visual articulations, displaying considerably less audiovisual enhancement. The findings suggest that improvement in the ability to recognize speech-in-noise and in audiovisual integration during speech perception continues quite late into the childhood years. The implication is that a considerable amount of multisensory learning remains to be achieved during the later schooling years, and that explicit efforts to accommodate this learning may well be warranted.     

Mismatch negativity evoked by the McGurk-MacDonald effect: a phonetic representation within short-term memory.

OBJECTIVES: The McGurk-MacDonald illusory percept is obtained by dubbing an incongruent articulatory movement on an auditory phoneme. This type of audiovisual speech perception contributes to the assessment of theories of speech perception. The mismatch negativity (MMN) reflects the detection of a deviant stimulus within the auditory short-term memory and besides an acoustic component, possesses, under certain conditions, a phonetic one. The present study assessed the existence of an MMN evoked by McGurk-MacDonald percepts elicited by audiovisual stimuli with constant auditory components. METHODS: Cortical evoked potentials were recorded using the oddball paradigm on 8 adults in 3 experimental conditions: auditory alone, visual alone and audiovisual stimulation. Obtaining illusory percepts was confirmed in an additional psychophysical condition. RESULTS: The auditory deviant syllables and the audiovisual incongruent syllables elicited a significant MMN at Fz. In the visual condition, no negativity was observed either at Fz, or at O(z). CONCLUSIONS: An MMN can be evoked by visual articulatory deviants, provided they are presented in a suitable auditory context leading to a phonetically significant interaction. The recording of an MMN elicited by illusory McGurk percepts suggests that audiovisual integration mechanisms in speech take place rather early during the perceptual processes.     

Electrocorticography reveals continuous auditory and visual speech tracking in temporal and occipital cortex

During natural speech perception, humans must parse temporally continuous auditory and visual speech signals into sequences of words. However, most studies of speech perception present only single words or syllables. We used electrocorticography (subdural electrodes implanted on the brains of epileptic patients) to investigate the neural mechanisms for processing continuous audiovisual speech signals consisting of individual sentences. Using partial correlation analysis, we found that posterior superior temporal gyrus (pSTG) and medial occipital cortex tracked both the auditory and the visual speech envelopes. These same regions, as well as inferior temporal cortex, responded more strongly to a dynamic video of a talking face compared to auditory speech paired with a static face. Occipital cortex and pSTG carry temporal information about both auditory and visual speech dynamics. Visual speech tracking in pSTG may be a mechanism for enhancing perception of degraded auditory speech.     

Audiovisual Speech Perception and Eye Gaze Behavior of Adults with Asperger Syndrome

Audiovisual speech perception was studied in adults with Asperger syndrome (AS), by utilizing the McGurk effect, in which conflicting visual articulation alters the perception of heard speech. The AS group perceived the audiovisual stimuli differently from age, sex and IQ matched controls. When a voice saying /p/ was presented with a face articulating /k/, the controls predominantly heard /k/. Instead, the AS group heard /k/ and /t/ with almost equal frequency, but with large differences between individuals. There were no differences in gaze direction or unisensory perception between the AS and control participants that could have contributed to the audiovisual differences. We suggest an explanation in terms of weak support from the motor system for audiovisual speech perception in AS.     

Neurophysiological Indices of Audiovisual Speech Processing Reveal a Hierarchy of Multisensory Integration Effects

Seeing a speaker''s face benefits speech comprehension, especially in challenging listening conditions. This perceptual benefit is thought to stem from the neural integration of visual and auditory speech at multiple stages of processing, whereby movement of a speaker''s face provides temporal cues to auditory cortex, and articulatory information from the speaker''s mouth can aid recognizing specific linguistic units (e.g., phonemes, syllables). However, it remains unclear how the integration of these cues varies as a function of listening conditions. Here, we sought to provide insight on these questions by examining EEG responses in humans (males and females) to natural audiovisual (AV), audio, and visual speech in quiet and in noise. We represented our speech stimuli in terms of their spectrograms and their phonetic features and then quantified the strength of the encoding of those features in the EEG using canonical correlation analysis (CCA). The encoding of both spectrotemporal and phonetic features was shown to be more robust in AV speech responses than what would have been expected from the summation of the audio and visual speech responses, suggesting that multisensory integration occurs at both spectrotemporal and phonetic stages of speech processing. We also found evidence to suggest that the integration effects may change with listening conditions; however, this was an exploratory analysis and future work will be required to examine this effect using a within-subject design. These findings demonstrate that integration of audio and visual speech occurs at multiple stages along the speech processing hierarchy.SIGNIFICANCE STATEMENT During conversation, visual cues impact our perception of speech. Integration of auditory and visual speech is thought to occur at multiple stages of speech processing and vary flexibly depending on the listening conditions. Here, we examine audiovisual (AV) integration at two stages of speech processing using the speech spectrogram and a phonetic representation, and test how AV integration adapts to degraded listening conditions. We find significant integration at both of these stages regardless of listening conditions. These findings reveal neural indices of multisensory interactions at different stages of processing and provide support for the multistage integration framework.     

Abnormal cortical responses elicited by audiovisual movies in patients with autism spectrum disorder with atypical sensory behavior: A magnetoencephalographic study

BackgroundAtypical sensory behavior disrupts behavioral adaptation in children with autism spectrum disorder (ASD); however, neural correlates of sensory dysfunction using magnetoencephalography (MEG) remain unclear.MethodWe used MEG to measure the cortical activation elicited by visual (uni)/audiovisual (multisensory) movies in 46 children (7–14 years) were included in final analysis: 13 boys with atypical audiovisual behavior in ASD (AAV+), 10 without this condition, and 23 age-matched typically developing boys.ResultsThe AAV+ group demonstrated an increase in the cortical activation in the bilateral insula in response to unisensory movies and in the left occipital, right superior temporal sulcus (rSTS), and temporal regions to multisensory movies. These increased responses were correlated with severity of the sensory impairment. Increased theta-low gamma oscillations were observed in the rSTS in AAV+.ConclusionThe findings suggest that AAV is attributed to atypical neural networks centered on the rSTS.     

Bimodal speech: early suppressive visual effects in human auditory cortex

While everyone has experienced that seeing lip movements may improve speech perception, little is known about the neural mechanisms by which audiovisual speech information is combined. Event-related potentials (ERPs) were recorded while subjects performed an auditory recognition task among four different natural syllables randomly presented in the auditory (A), visual (V) or congruent bimodal (AV) condition. We found that: (i) bimodal syllables were identified more rapidly than auditory alone stimuli; (ii) this behavioural facilitation was associated with cross-modal [AV-(A+V)] ERP effects around 120-190 ms latency, expressed mainly as a decrease of unimodal N1 generator activities in the auditory cortex. This finding provides evidence for suppressive, speech-specific audiovisual integration mechanisms, which are likely to be related to the dominance of the auditory modality for speech perception. Furthermore, the latency of the effect indicates that integration operates at pre-representational stages of stimulus analysis, probably via feedback projections from visual and/or polymodal areas.     

Brain responses to audiovisual speech mismatch in infants are associated with individual differences in looking behaviour

Research on audiovisual speech integration has reported high levels of individual variability, especially among young infants. In the present study we tested the hypothesis that this variability results from individual differences in the maturation of audiovisual speech processing during infancy. A developmental shift in selective attention to audiovisual speech has been demonstrated between 6 and 9 months with an increase in the time spent looking to articulating mouths as compared to eyes (Lewkowicz & Hansen‐Tift. (2012) Proc. Natl Acad. Sci. USA, 109 , 1431–1436; Tomalski et al. (2012) Eur. J. Dev. Psychol., 1–14). In the present study we tested whether these changes in behavioural maturational level are associated with differences in brain responses to audiovisual speech across this age range. We measured high‐density event‐related potentials (ERPs) in response to videos of audiovisually matching and mismatched syllables /ba/ and /ga/, and subsequently examined visual scanning of the same stimuli with eye‐tracking. There were no clear age‐specific changes in ERPs, but the amplitude of audiovisual mismatch response (AVMMR) to the combination of visual /ba/ and auditory /ga/ was strongly negatively associated with looking time to the mouth in the same condition. These results have significant implications for our understanding of individual differences in neural signatures of audiovisual speech processing in infants, suggesting that they are not strictly related to chronological age but instead associated with the maturation of looking behaviour, and develop at individual rates in the second half of the first year of life.     

Right Temporoparietal Gray Matter Predicts Accuracy of Social Perception in the Autism Spectrum

Individuals with an autism spectrum disorder (ASD) show hallmark deficits in social perception. These difficulties might also reflect fundamental deficits in integrating visual signals. We contrasted predictions of a social perception and a spatial–temporal integration deficit account. Participants with ASD and matched controls performed two tasks: the first required spatiotemporal integration of global motion signals without social meaning, the second required processing of socially relevant local motion. The ASD group only showed differences to controls in social motion evaluation. In addition, gray matter volume in the temporal–parietal junction correlated positively with accuracy in social motion perception in the ASD group. Our findings suggest that social–perceptual difficulties in ASD cannot be reduced to deficits in spatial–temporal integration.     

Behavioural evidence for separate mechanisms of audiovisual temporal binding as a function of leading sensory modality

The ability to integrate auditory and visual information is critical for effective perception and interaction with the environment, and is thought to be abnormal in some clinical populations. Several studies have investigated the time window over which audiovisual events are integrated, also called the temporal binding window, and revealed asymmetries depending on the order of audiovisual input (i.e. the leading sense). When judging audiovisual simultaneity, the binding window appears narrower and non‐malleable for auditory‐leading stimulus pairs and wider and trainable for visual‐leading pairs. Here we specifically examined the level of independence of binding mechanisms when auditory‐before‐visual vs. visual‐before‐auditory input is bound. Three groups of healthy participants practiced audiovisual simultaneity detection with feedback, selectively training on auditory‐leading stimulus pairs (group 1), visual‐leading stimulus pairs (group 2) or both (group 3). Subsequently, we tested for learning transfer (crossover) from trained stimulus pairs to non‐trained pairs with opposite audiovisual input. Our data confirmed the known asymmetry in size and trainability for auditory–visual vs. visual–auditory binding windows. More importantly, practicing one type of audiovisual integration (e.g. auditory–visual) did not affect the other type (e.g. visual–auditory), even if trainable by within‐condition practice. Together, these results provide crucial evidence that audiovisual temporal binding for auditory‐leading vs. visual‐leading stimulus pairs are independent, possibly tapping into different circuits for audiovisual integration due to engagement of different multisensory sampling mechanisms depending on leading sense. Our results have implications for informing the study of multisensory interactions in healthy participants and clinical populations with dysfunctional multisensory integration.     

Spatial attention can modulate audiovisual integration at multiple cortical and subcortical sites

The role of attention in multisensory integration (MI) is presently uncertain, with some studies supporting an automatic, pre-attentive process and others suggesting possible modulation through selective attention. The goal of this functional magnetic resonance imaging study was to investigate the role of spatial attention on the processing of congruent audiovisual speech stimuli (here indexing MI). Subjects were presented with two simultaneous visual streams (speaking lips in the left and right visual hemifields) plus a single central audio stream (spoken words). In the selective attention conditions, the auditory stream was congruent with one of the two visual streams. Subjects attended to either the congruent or the incongruent visual stream, allowing the comparison of brain activity for attended vs. unattended MI while the amount of multisensory information in the environment and the overall attentional requirements were held constant. Meridian mapping and a lateralized 'speaking-lips' localizer were used to identify early visual areas and to localize regions responding to contralateral visual stimulations. Results showed that attention to the congruent audiovisual stimulus resulted in increased activation in the superior temporal sulcus, striate and extrastriate retinotopic visual cortex, and superior colliculus. These findings demonstrate that audiovisual integration and spatial attention jointly interact to influence activity in an extensive network of brain areas, including associative regions, early sensory-specific visual cortex and subcortical structures that together contribute to the perception of a fused audiovisual percept.     

Multisensory Integration of Low-level Information in Autism Spectrum Disorder: Measuring Susceptibility to the Flash-Beep Illusion

Previous studies have suggested audiovisual multisensory integration (MSI) may be atypical in Autism Spectrum Disorder (ASD). However, much of the research having found an alteration in MSI in ASD involved socio-communicative stimuli. The goal of the current study was to investigate MSI abilities in ASD using lower-level stimuli that are not socio-communicative in nature by testing susceptibility to auditory-guided visual illusions. Adolescents and adults with ASD and typically-developing (TD) individuals were shown to have similar susceptibility to a fission illusion. However, the ASD group was significantly more susceptible to the fusion illusion. Results suggest that individuals with ASD demonstrate MSI on the flash-beep illusion task but that their integration of audiovisual sensory information may be less selective than for TD individuals.