General introduction
Multimodal perception is how animals form coherent, valid, and robust perception by processing sensory stimuli from various modalities. Surrounded by multiple objects and receiving multiple sensory stimulations, the brain is faced with the decision of how to categorize the stimuli resulting from different objects or events in the physical world. The nervous system is thus responsible for whether to integrate or segregate certain groups of temporally coincident sensory signals based on the degree of spatial and structural congruence of those stimulations. Multimodal perception has been widely studied in cognitive science, behavioral science, and neuroscience.Stimuli and sensory modalities
There are four attributes of stimulus: modality, intensity, location, and duration. The neocortex in the mammalian brain has parcellations that primarily process sensory input from one modality. For example, primary visual area, V1, or primary somatosensory area, S1. These areas mostly deal with low-level stimulus features such as brightness, orientation, intensity, etc. These areas have extensive connections to each other as well as to higher association areas that further process the stimuli and are believed to integrate sensory input from various modalities. However, recently multisensory effects have been shown to occur in primary sensory areas as well.Binding problem
The relationship between the binding problem and multisensory perception can be thought of as a question – the binding problem, and potential solution – multisensory perception. The binding problem stemmed from unanswered questions about how mammals (particularly higher primates) generate a unified, coherent perception of their surroundings from the cacophony of electromagnetic waves, chemical interactions, and pressure fluctuations that forms the physical basis of the world around us. It was investigated initially in the visual domain (colour, motion, depth, and form), then in the auditory domain, and recently in the multisensory areas. It can be said therefore, that the binding problem is central to multisensoryHistory
Studies of sensory processing in humans and other animals has traditionally been performed one sense at a time, and to the present day, numerous academic societies and journals are largely restricted to considering sensory modalities separately ( 'Vision Research', 'Hearing Research' etc.). However, there is also a long and parallel history of multisensory research. An example is the Stratton's (1896) experiments on the somatosensory effects of wearing vision-distorting prism glasses. Multisensory interactions or crossmodal effects in which the perception of a stimulus is influenced by the presence of another type of stimulus are referred since very early in the past. They were reviewed by Hartmann in a fundamental book where, among several references to different types of multisensory interactions, reference is made to the work of Urbantschitsch in 1888 who reported on the improvement of visual acuity by auditive stimuli in subjects with damaged brains. This effect was also found later in individuals with undamaged brains by Krakov and Hartmann, as well as the fact that the visual acuity could be improved by other type of stimuli. It is also noteworthy the amount of work in the early 1930s on intersensory relations in the Soviet Union, reviewed by London. A remarkable multisensory research is the extensive work of Gonzalo Gonzalo, J. (1945, 1950, 1952, 2010, 2021). ''Dinámica Cerebral'', Open Access. Edición facsímil 2010 del Vol. 1 1945, Vol. 2 1950 (Madrid: Inst. S. Ramón y Cajal, CSIC), Suplemento I 1952 (Trab. Inst. Cajal Invest. Biol.) y 1ª ed. Suplemento II 2010. Red Temática en Tecnologías de Computación Artificial/Natural (RTNAC) y Universidad de Santiago de Compostela (USC).Example of spatial and structural congruence
When we hear a car honk, we would determine which car triggers the honk by which car we see is the spatially closest to the honk. It's a spatially congruent example by combining visual and auditory stimuli. On the other hand, the sound and the pictures of a TV program would be integrated as structurally congruent by combining visual and auditory stimuli. However, if the sound and the pictures did not meaningfully fit, we would segregate the two stimuli. Therefore, spatial or structural congruence comes from not only combining the stimuli but is also determined by our understanding.Theories and approaches
Visual dominance
Literature on spatial crossmodal biases suggests that visual modality often influences information from other senses. Some research indicates that vision dominates what we hear, when varying the degree of spatial congruency. This is known as the ventriloquist effect. In cases of visual and haptic integration, children younger than 8 years of age show visual dominance when required to identify object orientation. However, haptic dominance occurs when the factor to identify is object size.Modality appropriateness
According to Welch and Warren (1980), the Modality Appropriateness Hypothesis states that the influence of perception in each modality in multisensory integration depends on that modality's appropriateness for the given task. Thus, vision has a greater influence on integrated localization than hearing, and hearing and touch have a greater bearing on timing estimates than vision. More recent studies refine this early qualitative account of multisensory integration. Alais and Burr (2004), found that following progressive degradation in the quality of a visual stimulus, participants' perception of spatial location was determined progressively more by a simultaneous auditory cue. However, they also progressively changed the temporal uncertainty of the auditory cue; eventually concluding that it is the uncertainty of individual modalities that determine to what extent information from each modality is considered when forming a percept. This conclusion is similar in some respects to the 'inverse effectiveness rule'. The extent to which multisensory integration occurs may vary according to the ambiguity of the relevant stimuli. In support of this notion, a recent study shows that weak senses such as olfaction can even modulate the perception of visual information as long as the reliability of visual signals is adequately compromised.Bayesian integration
The theory of Bayesian integration is based on the fact that the brain must deal with a number of inputs, which vary in reliability. In dealing with these inputs, it must construct a coherent representation of the world that corresponds to reality. The Bayesian integration view is that the brain uses a form of Bayesian inference. This view has been backed up by computational modeling of such a Bayesian inference from signals to coherent representation, which shows similar characteristics to integration in the brain.Cue combination vs. causal inference models
With the assumption of independence between various sources, the traditional cue combination model is successful in modality integration. However, depending on the discrepancies between modalities, there might be different forms of stimuli fusion: integration, partial integration, and segregation. To fully understand the other two types, we have to use causal inference model without the assumption as cue combination model. This freedom gives us general combination of any numbers of signals and modalities by using Bayes' rule to make causal inference of sensory signals.The hierarchical vs. non-hierarchical models
The difference between two models is that hierarchical model can explicitly make causal inference to predict certain stimulus while non-hierarchical model can only predict joint probability of stimuli. However, hierarchical model is actually a special case of non-hierarchical model by setting joint prior as a weighted average of the prior to common and independent causes, each weighted by their prior probability. Based on the correspondence of these two models, we can also say that hierarchical is a mixture modal of non-hierarchical model.Independence of likelihoods and priors
ForPrinciples
The contributions of Barry Stein, Alex Meredith, and their colleagues (e.g."The merging of the senses" 1993,) are widely considered to be the groundbreaking work in the modern field of multisensory integration. Through detailed long-term study of the neurophysiology of the superior colliculus, they distilled three general principles by which multisensory integration may best be described. *The spatial rule states that multisensory integration is more likely or stronger when the constituent unisensory stimuli arise from approximately the same location. *The temporal rule states that multisensory integration is more likely or stronger when the constituent unisensory stimuli arise at approximately the same time. *The principle of inverse effectiveness states that multisensory integration is more likely or stronger when the constituent unisensory stimuli evoke relatively weak responses when presented in isolation.Perceptual and behavioral consequences
A unimodal approach dominated scientific literature until the beginning of this century. Although this enabled rapid progression of neural mapping, and an improved understanding of neural structures, the investigation of perception remained relatively stagnant, with a few exceptions. The recent revitalized enthusiasm into perceptual research is indicative of a substantial shift away from reductionism and toward gestalt methodologies. Gestalt theory, dominant in the late 19th and early 20th centuries espoused two general principles: the 'principle of totality' in which conscious experience must be considered globally, and the 'principle of psychophysical isomorphism' which states that perceptual phenomena are correlated with cerebral activity. Just these ideas were already applied byDecreasing sensory uncertainty
It has been widely acknowledged that uncertainty in sensory domains results in an increased dependence of multisensory integration. Hence, it follows that cues from multiple modalities that are both temporally and spatially synchronous are viewed neurally and perceptually as emanating from the same source. The degree of synchrony that is required for this 'binding' to occur is currently being investigated in a variety of approaches. The integrative function only occurs to a point beyond which the subject can differentiate them as two opposing stimuli. Concurrently, a significant intermediate conclusion can be drawn from the research thus far. Multisensory stimuli that are bound into a single percept, are also bound on the same receptive fields of multisensory neurons in the SC and cortex.Decreasing reaction time
Responses to multiple simultaneous sensory stimuli can be faster than responses to the same stimuli presented in isolation. Hershenson (1962) presented a light and tone simultaneously and separately, and asked human participants to respond as rapidly as possible to them. As the asynchrony between the onsets of both stimuli was varied, it was observed that for certain degrees of asynchrony, reaction times were decreased. These levels of asynchrony were quite small, perhaps reflecting the temporal window that exists in multisensory neurons of the SC. Further studies have analysed the reaction times of saccadic eye movements; and more recently correlated these findings to neural phenomena. In patients studied by Gonzalo, with lesions in the parieto-occipital cortex, the decrease in the reaction time to a given stimulus by means of intersensory facilitation was shown to be very remarkable.Redundant target effects
The redundant target effect is the observation that people typically respond faster to double targets (two targets presented simultaneously) than to either of the targets presented alone. This difference in latency is termed the redundancy gain (RG). In a study done by Forster, Cavina-Pratesi, Aglioti, and Berlucchi (2001), normal observers responded faster to simultaneous visual and tactile stimuli than to single visual or tactile stimuli. RT to simultaneous visual and tactile stimuli was also faster than RT to simultaneous dual visual or tactile stimuli. The advantage for RT to combined visual-tactile stimuli over RT to the other types of stimulation could be accounted for by intersensory neural facilitation rather than by probability summation. These effects can be ascribed to the convergence of tactile and visual inputs onto neural centers which contain flexible multisensory representations of body parts.Multisensory illusions
McGurk effect
It has been found that two converging bimodal stimuli can produce a perception that is not only different in magnitude than the sum of its parts, but also quite different in quality. In a classic study labeled the McGurk effect, a person's phoneme production was dubbed with a video of that person speaking a different phoneme. The result was the perception of a third, different phoneme. McGurk and MacDonald (1976) explained that phonemes such as ba, da, ka, ta, ga and pa can be divided into four groups, those that can be visually confused, i.e. (da, ga, ka, ta) and (ba and pa), and those that can be audibly confused. Hence, when ba – voice and ga lips are processed together, the visual modality sees ga or da, and the auditory modality hears ba or da, combining to form the percept da.Ventriloquism
Double-flash illusion
The double flash illusion was reported as the first illusion to show that visual stimuli can be qualitatively altered by audio stimuli. In the standard paradigm participants are presented combinations of one to four flashes accompanied by zero to 4 beeps. They were then asked to say how many flashes they perceived. Participants perceived illusory flashes when there were more beeps than flashes. fMRI studies have shown that there is crossmodal activation in early, low level visual areas, which was qualitatively similar to the perception of a real flash. This suggests that the illusion reflects subjective perception of the extra flash. Further, studies suggest that timing of multisensory activation in unisensory cortexes is too fast to be mediated by a higher order integration suggesting feed forward or lateral connections. One study has revealed the same effect but from vision to audition, as well as fission rather than fusion effects, although the level of the auditory stimulus was reduced to make it less salient for those illusions affecting audition.Rubber hand illusion
In the rubber hand illusion (RHI), human participants view a dummy hand being stroked with a paintbrush, while they feel a series of identical brushstrokes applied to their own hand, which is hidden from view. If this visual and tactile information is applied synchronously, and if the visual appearance and position of the dummy hand is similar to one's own hand, then people may feel that the touches on their own hand are coming from the dummy hand, and even that the dummy hand is, in some way, their own hand. This is an early form ofBody transfer illusion
Neural mechanisms
Subcortical areas
Superior colliculus
The superior colliculus (SC) or optic tectum (OT) is part of the tectum, located in the midbrain, superior to the brainstem and inferior to the thalamus. It contains seven layers of alternating white and grey matter, of which the superficial contain topographic maps of the visual field; and deeper layers contain overlapping spatial maps of the visual, auditory and somatosensory modalities. The structure receives afferents directly from the retina, as well as from various regions of the cortex (primarily the occipital lobe), thePutamen
Single neurons in the macaque putamen have been shown to have visual and somatosensory responses closely related to those in the polysensory zone of the premotor cortex and area 7b in the parietal lobe.Cortical areas
Multisensory neurons exist in a large number of locations, often integrated with unimodal neurons. They have recently been discovered in areas previously thought to be modality specific, such as the somatosensory cortex; as well as in clusters at the borders between the major cerebral lobes, such as the occipito-parietal space and the occipito-temporal space. However, in order to undergo such physiological changes, there must exist continuous connectivity between these multisensory structures. It is generally agreed that information flow within the cortex follows a hierarchical configuration. Hubel and Wiesel showed that receptive fields and thus the function of cortical structures, as one proceeds out from V1 along the visual pathways, become increasingly complex and specialized. From this it was postulated that information flowed outwards in a feed-forward fashion; the complex end products eventually binding to form a percept. However, via fMRI and intracranial recording technologies, it has been observed that the activation time of successive levels of the hierarchy does not correlate with a feed-forward structure. That is, late activation has been observed in the striate cortex, markedly after activation of the prefrontal cortex in response to the same stimulus. Complementing this, afferent nerve fibres have been found that project to early visual areas such as the lingual gyrus from late in the dorsal (action) and ventral (perception) visual streams, as well as from the auditory association cortex. Feedback projections have also been observed in the opossum directly from the auditory association cortex to V1. This last observation currently highlights a point of controversy within the neuroscientific community. Sadato ''et al.'' (2004) concluded, in line with Bernstein ''et al.'' (2002), that the primary auditory cortex (A1) was functionally distinct from the auditory association cortex, in that it was void of any interaction with the visual modality. They hence concluded that A1 would not at all be effected byFrontal lobe
Area F4 in macaques Area F5 in macaques Polysensory zone of premotor cortex (PZ) in macaquesOccipital lobe
Primary visual cortex (V1) Lingual gyrus in humans Lateral occipital complex (LOC), including lateral occipital tactile visual area (LOtv)Parietal lobe
Ventral intraparietal sulcus (VIP) in macaques Lateral intraparietal sulcus (LIP) in macaques Area 7b in macaques Second somatosensory cortex (SII)Temporal lobe
Primary auditory cortex (A1) Superior temporal cortex (STG/STS/PT) Audio visual cross modal interactions are known to occur in the auditory association cortex which lies directly inferior to the Sylvian fissure in the temporal lobe. Plasticity was observed in the superior temporal gyrus (STG) by Petitto ''et al.'' (2000). Here, it was found that the STG was more active during stimulation in native deaf signers compared to hearing non signers. Concurrently, further research has revealed differences in the activation of the Planum temporale (PT) in response to non linguistic lip movements between the hearing and deaf; as well as progressively increasing activation of the auditory association cortex as previously deaf participants gain hearing experience via a cochlear implant. Anterior ectosylvian sulus (AES) in cats Rostral lateral suprasylvian sulcus (rLS) in catsCortical-subcortical interactions
The most significant interaction between these two systems (corticotectal interactions) is the connection between the anterior ectosylvian sulcus (AES), which lies at the junction of the parietal, temporal and frontal lobes, and the SC. The AES is divided into three unimodal regions with multisensory neurons at the junctions between these sections. (Jiang & Stein, 2003). Neurons from the unimodal regions project to the deep layers of the SC and influence the multiplicative integration effect. That is, although they can receive inputs from all modalities as normal, the SC can not enhance or depress the effect of multisensory stimulation without input from the AES. Concurrently, the multisensory neurons of the AES, although also integrally connected to unimodal AES neurons, are not directly connected to the SC. This pattern of division is reflected in other areas of the cortex, resulting in the observation that cortical and tectal multisensory systems are somewhat dissociated. Stein, London, Wilkinson and Price (1996) analysed the perceived luminance of an LED in the context of spatially disparate auditory distracters of various types. A significant finding was that a sound increased the perceived brightness of the light, regardless of their relative spatial locations, provided the light's image was projected onto the fovea. Here, the apparent lack of the spatial rule, further differentiates cortical and tectal multisensory neurons. Little empirical evidence exists to justify this dichotomy. Nevertheless, cortical neurons governing perception, and a separate sub cortical system governing action (orientation behavior) is synonymous with the perception action hypothesis of the visual stream. Further investigation into this field is necessary before any substantial claims can be made.Dual "what" and "where" multisensory routes
Research suggests the existence of two multisensory routes for "what" and "where". The "what" route identifying the identity of things involving areaDevelopment of multisensory operations
Theories of development
All species equipped with multiple sensory systems, utilize them in an integrative manner to achieve action and perception. However, in most species, especially higher mammals and humans, the ability to integrate develops in parallel with physical and cognitive maturity. Children until certain ages do not show mature integration patterns. Classically, two opposing views that are principally modern manifestations of the nativist/empiricist dichotomy have been put forth. The integration (empiricist) view states that at birth, sensory modalities are not at all connected. Hence, it is only through active exploration that plastic changes can occur in the nervous system to initiate holistic perceptions and actions. Conversely, the differentiation (nativist) perspective asserts that the young nervous system is highly interconnected; and that during development, modalities are gradually differentiated as relevant connections are rehearsed and the irrelevant are discarded. Using the SC as a model, the nature of this dichotomy can be analysed. In the newborn cat, deep layers of the SC contain only neurons responding to the somatosensory modality. Within a week, auditory neurons begin to occur, but it is not until two weeks after birth that the first multisensory neurons appear. Further changes continue, with the arrival of visual neurons after three weeks, until the SC has achieved its fully mature structure after three to four months. Concurrently in species of monkey, newborns are endowed with a significant complement of multisensory cells; however, along with cats there is no integration effect apparent until much later. This delay is thought to be the result of the relatively slower development of cortical structures including the AES; which as stated above, is essential for the existence of the integration effect. Furthermore, it was found by Wallace (2004) that cats raised in a light deprived environment had severely underdeveloped visual receptive fields in deep layers of the SC. Although, receptive field size has been shown to decrease with maturity, the above finding suggests that integration in the SC is a function of experience. Nevertheless, the existence of visual multisensory neurons, despite a complete lack of visual experience, highlights the apparent relevance of nativist viewpoints. Multisensory development in the cortex has been studied to a lesser extent, however a similar study to that presented above was performed on cats whose optic nerves had been severed. These cats displayed a marked improvement in their ability to localize stimuli through audition; and consequently also showed increased neural connectivity between V1 and the auditory cortex. Such plasticity in early childhood allows for greater adaptability, and thus more normal development in other areas for those with a sensory deficit. In contrast, following the initial formative period, the SC does not appear to display any neural plasticity. Despite this, habituation and sensititisation over the long term is known to exist in orientation behaviors. This apparent plasticity in function has been attributed to the adaptability of the AES. That is, although neurons in the SC have a fixed magnitude of output per unit input, and essentially operate an all or nothing response, the level of neural firing can be more finely tuned by variations in input by the AES. Although there is evidence for either perspective of the integration/differentiation dichotomy, a significant body of evidence also exists for a combination of factors from either view. Thus, analogous to the broader nativist/empiricist argument, it is apparent that rather than a dichotomy, there exists a continuum, such that the integration and differentiation hypotheses are extremes at either end.Psychophysical development of integration
Not much is known about the development of the ability to integrate multiple estimates such as vision and touch. Some multisensory abilities are present from early infancy, but it is not until children are eight years or older before they use multiple modalities to reduce sensory uncertainty. One study demonstrated that cross-modal visual and auditory integration is present from within 1 year of life. This study measured response time for orientating towards a source. Infants who were 8–10 months old showed significantly decreased response times when the source was presented through both visual and auditory information compared to a single modality. Younger infants, however, showed no such change in response times to these different conditions. Indeed, the results of the study indicates that children potentially have the capacity to integrate sensory sources at any age. However, in certain cases, for example visual cues, intermodal integration is avoided.Applications
Prosthesis
Prosthetics designers should carefully consider the nature of dimensionality alteration of sensorimotor signaling from and to the CNS when designing prosthetic devices. As reported in literatures, neural signaling from the CNS to the motors is organized in a way that the dimensionalities of the signals are gradually increased as you approach the muscles, also called muscle synergies. In the same principal, but in opposite ordering, on the other hand, signals dimensionalities from the sensory receptors are gradually integrated, also called sensory synergies, as they approaches the CNS. This bow tie like signaling formation enables the CNS to process abstract yet valuable information only. Such as process will decrease complexity of the data, handle the noises and guarantee to the CNS the optimum energy consumption. Although the current commercially available prosthetic devices mainly focusing in implementing the motor side by simply uses EMG sensors to switch between different activation states of the prosthesis. Very limited works have proposed a system to involve by integrating the sensory side. The integration of tactile sense and proprioception is regarded as essential for implementing the ability to perceive environmental input.Visual Rehabilitation
Multisensory integration has also been shown to ameliorate visual hemianopia. Through the repeated presentation of multisensory stimuli in the blind hemifield, the ability to respond to purely visual stimuli gradually returns to that hemifield in a central to peripheral manner. These benefits persist even after the explicit multisensory training ceases.See also
*References
Further reading
* * *{{cite book , author1=Wallace, Mark , author2=Murray, Micah Middelmann , title=The Neural Bases of Multisensory Processes (Frontiers in Neuroscience) , publisher=CRC Press , location=Boca Raton , year=2012 , isbn=978-1-4398-1217-4 , oclc=707710852, url=https://www.ncbi.nlm.nih.gov/books/NBK92848/External links