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Multisensory integration, also known as multimodal integration, is the study of how information from the different sensory modalities (such as sight, sound, touch, smell, self-motion, and taste) may be integrated by the nervous system.
A coherent representation of objects combining modalities enables
animals to have meaningful perceptual experiences. Indeed, multisensory
integration is central to adaptive behavior because it allows animals to
perceive a world of coherent perceptual entities.
Multisensory integration also deals with how different sensory
modalities interact with one another and alter each other's processing.
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 multisensory perception.
However, considerations of how unified conscious representations
are formed are not the full focus of multisensory Integration research.
It is obviously important for the senses to interact in order to
maximize how efficiently people interact with the environment. For
perceptual experience and behavior to benefit from the simultaneous
stimulation of multiple sensory modalities, integration of the
information from these modalities is necessary. Some of the mechanisms
mediating this phenomenon and its subsequent effects on cognitive and
behavioural processes will be examined hereafter. Perception is often
defined as one's conscious experience, and thereby combines inputs from
all relevant senses and prior knowledge. Perception is also defined and
studied in terms of feature extraction, which is several hundred
milliseconds away from conscious experience. Notwithstanding the
existence of Gestalt psychology schools that advocate a holistic approach to the operation of the brain,
the physiological processes underlying the formation of percepts and
conscious experience have been vastly understudied. Nevertheless,
burgeoning neuroscience research continues to enrich our understanding
of the many details of the brain, including neural structures implicated
in multisensory integration such as the superior colliculus (SC) and various cortical structures such as the superior temporal gyrus (GT)
and visual and auditory association areas. Although the structure and
function of the SC are well known, the cortex and the relationship
between its constituent parts are presently the subject of much
investigation. Concurrently, the recent impetus on integration has
enabled investigation into perceptual phenomena such as the ventriloquism effect, rapid localization of stimuli and the McGurk effect; culminating in a more thorough understanding of the human brain and its functions.
History
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 brain. This effect was also found latter in normals 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 thirties on intersensory relations in Soviet
Union, reviewed by London. A remarkable multisensory research is the extensive work of Gonzalo
in the forties on the characterization of a multisensory syndrome in
patients with parieto-occipital cortical lesions. In this syndrome, all
the sensory functions are affected, and with symmetric bilaterality, in
spite of being a unilateral lesion where the primary areas were not
involved. A feature of this syndrome is the great permeability to
crossmodal effects between visual, tactile, auditive stimuli as well as
muscular effort to improve the perception, also decreasing the reaction
times. The improvement by crossmodal effect was found to be greater as
the primary stimulus to be perceived was weaker, and as the cortical
lesion was greater (Vol I and II of reference).
This author interpreted these phenomena under a dynamic physiological
concept, and from a model based on functional gradients through the
cortex and scaling laws of dynamical systems, thus highlighting the
functional unity of the cortex. According to the functional cortical
gradients, the specificity of the cortex would be distributed in
gradation, and the overlap of different specific gradients would be
related to multisensory interactions.
Multisensory research has recently gained enormous interest and popularity.
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, 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
For Bayesian model,
the prior and likelihood generally represent the statistics of the
environment and the sensory representations. The independence of priors
and likelihoods is not assured since the prior may vary with likelihood
only by the representations. However, the independence has been proved
by Shams with series of parameter control in multi sensory perception
experiment.
Principles
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 by Justo Gonzalo
in his work of brain dynamics, where a sensory-cerebral correspondence
is considered in the formulation of the "development of the sensory
field due to a psychophysical isomorphism" (pag. 23 of the English
translation of ref.).
Both ideas 'principle of totality' and 'psychophysical isomorphism'
are particularly relevant in the current climate and have driven
researchers to investigate the behavioural benefits of multisensory
integration.
Decreasing 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 end 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
Ventriloquism
has been used as the evidence for the modality appropriateness
hypothesis. Ventriloquism is the situation in which auditory location
perception is shifted toward a visual cue. The original study describing
this phenomenon was conducted by Howard and Templeton, (1966) after
which several studies have replicated and built upon the conclusions
they reached. In conditions in which the visual cue is unambiguous, visual capture reliably occurs. Thus to test the influence of sound on perceived location, the visual stimulus must be progressively degraded.
Furthermore, given that auditory stimuli are more attuned to temporal
changes, recent studies have tested the ability of temporal
characteristics to influence the spatial location of visual stimuli.
Some types of EVP – electronic voice phenomenon,
mainly the ones using sound bubbles are considered a kind of modern
ventriloquism technique and is played by the use of sophisticated
software, computers and sound equipment.
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 of body transfer illusion. The RHI is an illusion of vision, touch, and posture (proprioception), but a similar illusion can also be induced with touch and proprioception.
It has also been found that the illusion may not require tactile
stimulation at all, but can be completely induced using mere vision of
the rubber hand being in a congruent posture with the hidden real hand. The very first report of this kind of illusion may have been as early as 1937 (Tastevin, 1937).
Body transfer illusion
Body transfer illusion
typically involves the use of virtual reality devices to induce the
illusion in the subject that the body of another person or being is the
subject's own body.
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), the spinal cord and the inferior colliculus. It sends efferents to the spinal cord, cerebellum, thalamus and occipital lobe via the lateral geniculate nucleus
(LGN). The structure contains a high proportion of multisensory neurons
and plays a role in the motor control of orientation behaviours of the
eyes, ears and head.
Receptive fields from somatosensory, visual and auditory
modalities converge in the deeper layers to form a two-dimensional
multisensory map of the external world. Here, objects straight ahead are
represented caudally and objects on the periphery are represented
rosterally. Similarly, locations in superior sensory space are
represented medially, and inferior locations are represented laterally.
However, in contrast to simple convergence, the SC integrates
information to create an output that differs from the sum of its inputs.
Following a phenomenon labelled the 'spatial rule', neurons are excited
if stimuli from multiple modalities fall on the same or adjacent
receptive fields, but are inhibited if the stimuli fall on disparate
fields.
Excited neurons may then proceed to innervate various muscles and
neural structures to orient an individual's behaviour and attention
toward the stimulus. Neurons in the SC also adhere to the 'temporal
rule', in which stimulation must occur within close temporal proximity
to excite neurons. However, due to the varying processing time between
modalities and the relatively slower speed of sound to light, it has
been found the neurons may be optimally excited when stimulated some
time apart.
Putamen
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 by cross modal plasticity.
This concurs with Jones and Powell's (1970) contention that primary
sensory areas are connected only to other areas of the same modality.
In contrast, the dorsal auditory pathway, projecting from the
temporal lobe is largely concerned with processing spatial information,
and contains receptive fields that are topographically organized. Fibers
from this region project directly to neurons governing corresponding
receptive fields in V1.
The perceptual consequences of this have not yet been empirically
acknowledged. However, it can be hypothesized that these projections may
be the precursors of increased acuity and emphasis of visual stimuli in
relevant areas of perceptual space. Consequently, this finding rejects
Jones and Powell's (1970) hypothesis and thus is in conflict with Sadato et al.'s (2004) findings.
A resolution to this discrepancy includes the possibility that primary
sensory areas can not be classified as a single group, and thus may be
far more different from what was previously thought.
The multisensory syndrome with symmetric bilaterality, characterized
by Gonzalo and called by this author `central syndrome of the cortex',
was originated from a unilateral parieto-occipital cortical lesion
equidistant from the visual, tactile, and auditory projection areas
(the middle of area 19, the anterior part of area 18 and the most
posterior of area 39, in Brodmann terminology) that was called `central
zone'. The gradation observed between syndromes led this author to
propose a functional gradient scheme in which the specificity of the
cortex is distributed with a continuous variation, the overlap of the specific gradients would be high or maximum in that ` central zone'.
Further research is necessary for a definitive resolution.
Frontal lobe
Area F4 in macaques
Area F5 in macaques
Polysensory zone of premotor cortex (PZ) in macaques
Occipital 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 cats
Cortical-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
area Brodmann area 9 in the right inferior frontal gyrus and right middle frontal gyrus, Brodmann area 13 and Brodmann area 45 in the right insula-inferior frontal gyrus area, and Brodmann area 13 bilaterally in the insula. The "where" route detecting their spatial attributes involving the Brodmann area 40 in the right and left inferior parietal lobule and the Brodmann area 7 in the right precuneus-superior parietal lobule and Brodmann area 7 in
the left superior parietal lobe.
Development 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.
Another study found that cross-modal integration of touch and vision for distinguishing size and orientation is available from at least 8 years of age. For pre-integration age groups, one sense dominates depending on the characteristic discerned (see visual dominance).
A study investigating sensory integration within a single modality (vision) found that it cannot be established until age 12 and above. This particular study assessed the integration of disparity and texture
cues to resolve surface slant. Though younger age groups showed a
somewhat better performance when combining disparity and texture cues
compared to using only disparity or texture cues, this difference was
not statistically significant. In adults, the sensory integration can be mandatory, meaning that they no longer have access to the individual sensory sources.
Acknowledging these variations, many hypotheses have been
established to reflect why these observations are task-dependent. Given
that different senses develop at different rates, it has been proposed
that cross-modal integration does not appear until both modalities have reached maturity. The human body undergoes significant physical transformation throughout childhood. Not only is there growth in size and stature (affecting viewing height), but there is also change in inter-ocular distance and eyeball length. Therefore, sensory signals need to be constantly re-evaluated to appreciate these various physiological changes.
Some support comes from animal studies that explore the neurobiology
behind integration. Adult monkeys have deep inter-neuronal connections
within the superior colliculus providing strong, accelerated visuo-auditory integration. Young animals conversely, do not have this enhancement until unimodal properties are fully developed.
Additionally, to rationalize sensory dominance, Gori et al.
(2008) advocates that the brain utilises the most direct source of
information during sensory immaturity. In this case, orientation is primarily a visual characteristic. It can be derived directly from the object image that forms on the retina, irrespective of other visual factors. In fact, data shows that a functional property of neurons within primate visual cortices' are their discernment to orientation. In contrast, haptic
orientation judgements are recovered through collaborated patterned
stimulations, evidently an indirect source susceptible to interference.
Likewise, when size is concerned haptic
information coming from positions of the fingers is more immediate.
Visual-size perceptions, alternatively, have to be computed using
parameters such as slant and distance.
Considering this, sensory dominance is a useful instinct to assist with
calibration. During sensory immaturity, the more simple and robust
information source could be used to tweak the accuracy of the alternate
source.
Follow-up work by Gori et al. (2012) showed that, at all ages,
vision-size perceptions are near perfect when viewing objects within the
haptic workspace (i.e. at arm's reach). However, systematic errors in perception appeared when the object was positioned beyond this zone.
Children younger than 14 years tend to underestimate object size,
whereas adults overestimated. However, if the object was returned to the
haptic workspace, those visual biases disappeared.
These results support the hypothesis that haptic information may
educate visual perceptions. If sources are used for cross-calibration
they cannot, therefore, be combined (integrated). Maintaining access to
individual estimates is a trade-off for extra plasticity over accuracy, which could be beneficial in retrospect to the developing body.
Alternatively, Ernst (2008) advocates that efficient integration
initially relies upon establishing correspondence – which sensory
signals belong together. Indeed, studies have shown that visuo-haptic integration fails in adults when there is a perceived spatial separation, suggesting sensory information is coming from different targets. Furthermore, if the separation can be explained, for example viewing an object through a mirror, integration is re-established and can even be optimal.
Ernst (2008) suggests that adults can obtain this knowledge from
previous experiences to quickly determine which sensory sources depict
the same target, but young children could be deficient in this area.
Once there is a sufficient bank of experiences, confidence to correctly
integrate sensory signals can then be introduced in their behaviour.
Lastly, Nardini et al. (2010) recently hypothesised that young
children have optimized their sensory appreciation for speed over
accuracy.
When information is presented in two forms, children may derive an
estimate from the fastest available source, subsequently ignoring the
alternate, even if it contains redundant information. Nardini et al.
(2010) provides evidence that children's (aged 6 years) response
latencies are significantly lower when stimuli are presented in
multi-cue over single-cue conditions.
Conversely, adults showed no change between these conditions. Indeed,
adults display mandatory fusion of signals, therefore they can only ever
aim for maximum accuracy.
However, the overall mean latencies for children were not faster than
adults, which suggests that speed optimization merely enable them to
keep up with the mature pace. Considering the haste of real-world
events, this strategy may prove necessary to counteract the general
slower processing of children and maintain effective vision-action
coupling. Ultimately the developing sensory system may preferentially adapt for different goals – speed and detecting sensory conflicts – those typical of objective learning.
The late development of efficient integration has also been investigated from computational point of view.
Daee et al. (2014) showed that having one dominant sensory source at
early age, rather than integrating all sources, facilitates the overall
development of cross-modal integrations.
Applications
Prosthesis
Prosthetics
designers should carefully consider the nature of dimensionality
alteration of sensorimotor signaling from and to the CNS
when designing prothesitic 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.
