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Individual differences in multisensory integration and timing
The senses have traditionally been studied separately, but it is now recognised that the brain is just as richly multisensory as is our natural environment. This creates fresh challenges for understanding how complex multisensory information is organised and coordinated around the brain. Take timing for example: the sight and sound of a person speaking or a ball bouncing may seem simultaneous, but their neural signals from each modality arrive at different multisensory areas in the brain at different times. How do we nevertheless perceive the synchrony of the original events correctly? It is popularly assumed that this is achieved via some mechanism of multisensory temporal recalibration. But recent work from my lab on normal and pathological individual differences show that sight and sound are nevertheless markedly out of synch by different amounts for each individual and even for different tasks performed by the same individual. Indeed, the more an individual perceive the same multisensory event as having an auditory lead and an auditory lag at the same time. This evidence of apparent temporal disunity sheds new light on the deep problem of understanding how neural timing relates to perceptual timing of multisensory events. It also leads to concrete therapeutic applications: for example, we may now be able to improve an individual’s speech comprehension by simply delaying sound or vision to compensate for their individual perceptual asynchrony
Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion
Identifying with a body is central to being a conscious self. The now classic “rubber hand illusion” demonstrates that the experience of body ownership can be modulated by manipulating the timing of exteroceptive(visual and tactile)body-related feedback. Moreover,the strength of this modulation is related to individual differences in sensitivity to internal bodily signals(interoception). However the interaction of exteroceptive and interoceptive signals in determining the experience of body-ownership within an individual remains poorly understood.Here, we demonstrate that this depends on the online integration of exteroceptive and interoceptive signals by implementing an innovative “cardiac rubber hand illusion” that combined computer-generated augmented-reality with feedback of interoceptive (cardiac) information. We show that both subjective and objective measures of virtual-hand ownership are enhanced by cardio-visual feedback in-time with the actual heartbeat,as compared to asynchronous feedback. We further show that these measures correlate with individual differences in interoceptive sensitivity,and are also modulated by the integration of proprioceptive signals instantiated using real-time visual remapping of finger movements to the virtual hand.Our results demonstrate that interoceptive signals directly influence the experience of body ownership via multisensory integration,and they lend support to models of conscious selfhood based on interoceptive predictive coding
Audiovisual temporal correspondence modulates human multisensory superior temporal sulcus plus primary sensory cortices
The brain should integrate related but not unrelated information from different senses. Temporal patterning of inputs to different modalities may provide critical information about whether those inputs are related or not. We studied effects of temporal correspondence between auditory and visual streams on human brain activity with functional magnetic resonance imaging ( fMRI). Streams of visual flashes with irregularly jittered, arrhythmic timing could appear on right or left, with or without a stream of auditory tones that coincided perfectly when present ( highly unlikely by chance), were noncoincident with vision ( different erratic, arrhythmic pattern with same temporal statistics), or an auditory stream appeared alone. fMRI revealed blood oxygenation level-dependent ( BOLD) increases in multisensory superior temporal sulcus (mSTS), contralateral to a visual stream when coincident with an auditory stream, and BOLD decreases for noncoincidence relative to unisensory baselines. Contralateral primary visual cortex and auditory cortex were also affected by audiovisual temporal correspondence or noncorrespondence, as confirmed in individuals. Connectivity analyses indicated enhanced influence from mSTS on primary sensory areas, rather than vice versa, during audiovisual correspondence. Temporal correspondence between auditory and visual streams affects a network of both multisensory ( mSTS) and sensory-specific areas in humans, including even primary visual and auditory cortex, with stronger responses for corresponding and thus related audiovisual inputs
Distortions of Subjective Time Perception Within and Across Senses
Background: The ability to estimate the passage of time is of fundamental importance for perceptual and cognitive processes. One experience of time is the perception of duration, which is not isomorphic to physical duration and can be distorted by a number of factors. Yet, the critical features generating these perceptual shifts in subjective duration are not understood.
Methodology/Findings: We used prospective duration judgments within and across sensory modalities to examine the effect of stimulus predictability and feature change on the perception of duration. First, we found robust distortions of perceived duration in auditory, visual and auditory-visual presentations despite the predictability of the feature changes in the stimuli. For example, a looming disc embedded in a series of steady discs led to time dilation, whereas a steady disc embedded in a series of looming discs led to time compression. Second, we addressed whether visual (auditory) inputs could alter the perception of duration of auditory (visual) inputs. When participants were presented with incongruent audio-visual stimuli, the perceived duration of auditory events could be shortened or lengthened by the presence of conflicting visual information; however, the perceived duration of visual events was seldom distorted by the presence of auditory information and was never perceived shorter than their actual durations.
Conclusions/Significance: These results support the existence of multisensory interactions in the perception of duration and, importantly, suggest that vision can modify auditory temporal perception in a pure timing task. Insofar as distortions in subjective duration can neither be accounted for by the unpredictability of an auditory, visual or auditory-visual event, we propose that it is the intrinsic features of the stimulus that critically affect subjective time distortions
Investigating the Neural Basis of Audiovisual Speech Perception with Intracranial Recordings in Humans
Speech is inherently multisensory, containing auditory information from the voice and visual information from the mouth movements of the talker. Hearing the voice is usually sufficient to understand speech, however in noisy environments or when audition is impaired due to aging or disabilities, seeing mouth movements greatly improves speech perception. Although behavioral studies have well established this perceptual benefit, it is still not clear how the brain processes visual information from mouth movements to improve speech perception. To clarify this issue, I studied the neural activity recorded from the brain surfaces of human subjects using intracranial electrodes, a technique known as electrocorticography (ECoG). First, I studied responses to noisy speech in the auditory cortex, specifically in the superior temporal gyrus (STG). Previous studies identified the anterior parts of the STG as unisensory, responding only to auditory stimulus. On the other hand, posterior parts of the STG are known to be multisensory, responding to both auditory and visual stimuli, which makes it a key region for audiovisual speech perception. I examined how these different parts of the STG respond to clear versus noisy speech. I found that noisy speech decreased the amplitude and increased the across-trial variability of the response in the anterior STG. However, possibly due to its multisensory composition, posterior STG was not as sensitive to auditory noise as the anterior STG and responded similarly to clear and noisy speech. I also found that these two response patterns in the STG were separated by a sharp boundary demarcated by the posterior-most portion of the Heschl’s gyrus. Second, I studied responses to silent speech in the visual cortex. Previous studies demonstrated that visual cortex shows response enhancement when the auditory component of speech is noisy or absent, however it was not clear which regions of the visual cortex specifically show this response enhancement and whether this response enhancement is a result of top-down modulation from a higher region. To test this, I first mapped the receptive fields of different regions in the visual cortex and then measured their responses to visual (silent) and audiovisual speech stimuli. I found that visual regions that have central receptive fields show greater response enhancement to visual speech, possibly because these regions receive more visual information from mouth movements. I found similar response enhancement to visual speech in frontal cortex, specifically in the inferior frontal gyrus, premotor and dorsolateral prefrontal cortices, which have been implicated in speech reading in previous studies. I showed that these frontal regions display strong functional connectivity with visual regions that have central receptive fields during speech perception
Audio-visual detection benefits in the rat
Human psychophysical studies have described multisensory perceptual benefits such as enhanced detection rates and faster reaction times in great detail. However, the neural circuits and mechanism underlying multisensory integration remain difficult to study in the primate brain. While rodents offer the advantage of a range of experimental methodologies to study the neural basis of multisensory processing, rodent studies are still limited due to the small number of available multisensory protocols. We here demonstrate the feasibility of an audio-visual stimulus detection task for rats, in which the animals detect lateralized uni- and multi-sensory stimuli in a two-response forced choice paradigm. We show that animals reliably learn and perform this task. Reaction times were significantly faster and behavioral performance levels higher in multisensory compared to unisensory conditions. This benefit was strongest for dim visual targets, in agreement with classical patterns of multisensory integration, and was specific to task-informative sounds, while uninformative sounds speeded reaction times with little costs for detection performance. Importantly, multisensory benefits for stimulus detection and reaction times appeared at different levels of task proficiency and training experience, suggesting distinct mechanisms inducing these two multisensory benefits. Our results demonstrate behavioral multisensory enhancement in rats in analogy to behavioral patterns known from other species, such as humans. In addition, our paradigm enriches the set of behavioral tasks on which future studies can rely, for example to combine behavioral measurements with imaging or pharmacological studies in the behaving animal or to study changes of integration properties in disease models
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Spatial grouping resolves ambiguity to drive temporal recalibration.
Cross-modal temporal recalibration describes a shift in the point of subjective simultaneity (PSS) between 2 events following repeated exposure to asynchronous cross-modal inputs-the adaptors. Previous research suggested that audiovisual recalibration is insensitive to the spatial relationship between the adaptors. Here we show that audiovisual recalibration can be driven by cross-modal spatial grouping. Twelve participants adapted to alternating trains of lights and tones. Spatial position was manipulated, with alternating sequences of a light then a tone, or a tone then a light, presented on either side of fixation (e.g., left tone-left light-right tone-right light, etc.). As the events were evenly spaced in time, in the absence of spatial-based grouping it would be unclear if tones were leading or lagging lights. However, any grouping of spatially colocalized cross-modal events would result in an unambiguous sense of temporal order. We found that adapting to these stimuli caused the PSS between subsequent lights and tones to shift toward the temporal relationship implied by spatial-based grouping. These data therefore show that temporal recalibration is facilitated by spatial grouping. (PsycINFO Database Record (c) 2011 APA, all rights reserved)
Being first matters: topographical representational similarity analysis of ERP signals reveals separate networks for audiovisual temporal binding depending on the leading sense
In multisensory integration, processing in one sensory modality is enhanced by complementary information from other modalities. Inter-sensory timing is crucial in this process as only inputs reaching the brain within a restricted temporal window are perceptually bound. Previous research in the audiovisual field has investigated various features of the temporal binding window (TBW), revealing asymmetries in its size and plasticity depending on the leading input (auditory-visual, AV; visual-auditory, VA). We here tested whether separate neuronal mechanisms underlie this AV-VA dichotomy in humans. We recorded high-density EEG while participants performed an audiovisual simultaneity judgment task including various AV/VA asynchronies and unisensory control conditions (visual-only, auditory-only) and tested whether AV and VA processing generate different patterns of brain activity. After isolating the multisensory components of AV/VA event-related potentials (ERPs) from the sum of their unisensory constituents, we run a time-resolved topographical representational similarity analysis (tRSA) comparing AV and VA ERP maps. Spatial cross-correlation matrices were built from real data to index the similarity between AV- and VA-maps at each time point (500ms window post-stimulus) and then correlated with two alternative similarity model matrices: AVmaps=VAmaps vs. AVmaps≠VAmaps. The tRSA results favored the AVmaps≠VAmaps model across all time points, suggesting that audiovisual temporal binding (indexed by synchrony perception) engages different neural pathways depending on the leading sense. The existence of such dual route supports recent theoretical accounts proposing that multiple binding mechanisms are implemented in the brain to accommodate different information parsing strategies in auditory and visual sensory systems
Sight and sound out of synch: Fragmentation and renormalisation of audiovisual integration and subjective timing
The sight and sound of a person speaking or a ball bouncing may seem simultaneous, but their corresponding neural signals are spread out over time as they arrive at different multisensory brain sites. How subjective timing relates to such neural timing remains a fundamental neuroscientific and philosophical puzzle. A dominant assumption is that temporal coherence is achieved by sensory resynchronisation or recalibration across asynchronous brain events. This assumption is easily confirmed by estimating subjective audiovisual timing for groups of subjects, which is on average similar across different measures and stimuli, and approximately veridical. But few studies have examined normal and pathological individual differences in such measures.
Case PH, with lesions in pons and basal ganglia, hears people speak before seeing their lips move. Temporal order judgements (TOJ) confirmed this: voices had to lag lip-movements (by ~200ms) to seem synchronous to PH. Curiously, voices had to lead lips (also by ~200ms) to maximise the McGurk illusion (a measure of audiovisual speech integration). Thus PH’s timing was still veridical on average across measures. Similar kinds of discrepancies were also found in age-matched control participants. Most surprisingly, normal individual differences in TOJ and McGurk timing correlated negatively: subjects needing an auditory lag for subjective simultaneity needed an auditory lead for maximal McGurk, and vice versa. This generalised to the Stream-Bounce illusion. Such antagonism seems opposed to good sensory resynchronisation, yet average timing across tasks was still near-veridical.
Our findings reveal surprising disunity of subjective timing within and between subjects. To account for this we propose that the neural timing within different mechanisms is perceived relative to the average timing across mechanisms. Such renormalisation fully explains the curious antagonistic relationship between disparate timing estimates in PH and healthy participants, and how they can still perceive the timing of external events correctly, on average
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Optimal integration of auditory and vibrotactile information for judgments of temporal order
Recent research that assessed spatial judgments about multisensory stimuli suggests that humans integrate multisensory inputs in a statistically optimal manner by weighting each input by its normalized reciprocal variance. Is integration similarly optimal When humans judge the temporal properties of bimodal stimuli? Twenty-four participants performed temporal order judgments (TOJs,) about 2 spatially separated stimuli. Stimuli were auditory, vibrotactile, or both. The temporal profiles of vibrotactile stimuli were manipulated to produce 3 levels of precision for TOJs. In bimodal conditions, the asynchrony between the 2 unimodal stimuli that comprised it bimodal Stimulus was manipulated to determine the weight given to touch. Bimodal performance on 2 measures-judgment uncertainty and tactile weight-was predicted With unimodal data. A model relying exclusively on audition wits rejected on the basis of both measures. A second model that selected the best input on each trial did not predict the reduced judgment uncertainty observed in bimodal trials. Only the optimal Maximum-likelihood-estimation model predicted both judgment uncertainties and weights the model's validity is extended to TOJs. Alternatives for modeling the process of event sequencing based on integrated multisensory inputs are discussed
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