Transcript different sensory modalities

Stein, B., Meredith, M., The merging of the
senses, Cambridge, Mass., MIT Press, 1993
Part III, IV
Representation of the sensory space in
the superior colliculus
Alignement of sensory and motor maps
Sensory and motor representations are
distributed in map-like form
Segregation
• Map-like recreation of the receptor epithelium, and thus of the sensory space it
serves
• In the cns the visual, auditory, somatosensory representations occupy spatially
distinct regions, functionally and anatomically defined
• In the sensory cortex and thalamus the representations of the different sensory
modalities are organized in maps which are segregated one from another
(segregation between modalities in order to avoid confusion between
modalities )
• Submodality features separate maps within each modality (segregation within
each modality to facilitate recognition of certain stimulus characteristics
Integration
• No distinct regions for single sensory representation or single submodality
feature in the superior colliculus
Superior colliculus
Anatomical organization:
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Cerebral tissue organized in layers, with a significant distinction between
superficial and deeper ones
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superficial layers: dense visual innervation (the entire colliculus was long considerd an
exclusively visual structure)
deeper layers receive inputs from different sensory modalities (visual, auditory,
somatosensory; ascending and descending) and from motor-related structures
deeper layers send their outputs to areas of the brain stem and spinal cord involvend in
positioning the peripheral sensory organs and in the transformation of incoming
sensory information into motor commands (sensorimotor transduction)
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most descending output neurons are the sites of multisensory convergence (multimodal
efferent neurons): each of the sensory representations has access to at least some of the same
efferent circuitry  the different sensory systems can initiate the same behaviors via some of
the same neurons
Consequences of ablation:
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disturbances in visual attention (visual neglect) and orientation behaviors (« where »
system), lost of the ability to respond appropriately to contralateral (to the lesion) touch
and auditory stimuli
bilaterally symmetrical lesions are far less disruptive to visual auditory and
somatosensory behavior than unilateral ones
Behavioral function:
• Attentive and orientation roles
Specific role:
• Integrating the modalities:
– associates the sensory inputs to redirect the organs the input originates from
– in order to localize (capture-avoid) the source of the stimulus
• Sensorimotor transduction:
– transforms incoming sensory inputs into motor commands
– by virtue of the convergence and intermixing of sensory inputs and motor circuits
(different sensory modalities access to the same output motor circuits)
• many neurons have sensory and motor properties and are involved in a variety of
circuits and functions
Realization:
– alignement of the different sensory and motor maps (receptive fields and
movement fields in register)
– sometimes with use of multisensory neurons which can have also a premotor role
Sensory maps in the colliculus
• sensory neurons of the colliculus are organized in visuotopic, somatotopic,
auditory maps
– visual maps in superficial layers: nasal-temporal meridians (horizontal medians) run rostralcaudal, vertical meridians run medial-lateral; in deeper layers: similiarity of the overall
pattern, with close alignement of the representation of central visual space, but larger
receptive fields, including far periphery of the visual space : maps are not the simple
extension of the superficial ones
– somatosensory neurons in the deeper layers have large receptive fields and are organized in
maps which show a regular relationship with visual maps: the front of the animal is
represented rostral while the hindparts are caudal, the upper surface is represented medial and
its lower aspects lateral. The blocks of tissues devoted to regions of the body surface are not
exclusive: considerable overlap among the representations
– auditory neurons are organized in a computated spatial map oriented very much like the
visual and somatosensory maps: the auditory horizontal meridian is represented rostrallycaudally and the vertical one median-laterally
• register between superficial visuotopic and deeper visual, auditory,
somatosensory maps
– the same axes are used to represent all three sensory modalities:
– the fact that the visual maps in the superficial layers and the visual, auditory and
somatotopic maps of the deeper layers are aligned indicate an intimate interaction.
But there is no evidence that superficial neurons influence deeper visual,
somatosensory or motor neurons
spatial characteristics of the visual
somatosensory and auditory systems
In both the visual and somatosensory systems each peripheral nerve
fiber responds to a stimulus in a restricted (generally contralateral)
spatial domain, regardless of stimulus intensity, nd this defines the
cell’s receptive field.
For this reason is easy to understand how the cns constructs a spatial
map of the contralateral visual field and the contralateral body surface
In contrast, there is no spatial map at the peripheral receptors of the
auditory system, which is organized both at the thalamic and cortical
levels according to frequencies or tones (tonotopic, not spatiotopic).
The contruction of spatial auditory maps in the superior colliculus is
the result of a computation based on the differences in intensity and
timing of suond as it reaches the two ears
Motor maps in the colliculus
• Premotor or motor efferent neurons of the colliculus are connected
through many circuits with other motor areas in the the brain stem and
spinal cord
• these motor connections are organized in maps
• motor maps overlap sensory maps:
– the electrical stimulation of a site representing superior temporal visual
space will move the eyes temporally and superiorly, as if to center the
fovea on the visual location represented at the stimulation site;
stimulation of the medial aspects of the structure where upper visual field
is represented will elicit upward eye movements, while lateral stimulation
downward movements
– the representation of a region of sensory space and the representation of
the signals required to move the eyes toward that region are in the same
colliculus location: sensory and motor maps covary
• eye and ear movement maps are in register
interspecies constancy of register between
sensory maps
• Details presented above are drawn from data gathered in the cat
• There are important differences between animal species
• What remains constant is the general plan of overlapping (register) of
the different sensory representations, of the movement representations
and of sensory and movement representations
• The differences reflect the sensory modality a species depends on most
for exploring and responding to environmental stimuli
• From reptiles, to birds to mammalians, the register of sensory and
movement representations in the midbrain is a constant presence,
presumably because it is an efficient solution to the problem of using
different sensory cues to move one and the same body
multisensory integration at the superior
colliculus level
topographic register and convergence on
multisensory neurons
From the examination of individual
sensory maps to the examination of
individual multisensory neurons
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The integration of a multisensory multimotor maps can be done in two ways:
– stimuli originating from the same locations in sensory space activate neighboring unimodal
neurons from different modalities which have acces to at least one of the output neurons
– different modalities converge on the same neurons and these same multisensory neurons
produce a coordinated series of premotor signals
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We have just seen that multisensory integration in the superior colliculus depends on the
alignement of sensory representations
But there is evidence that the interrelationship among different sensory representations
is more intimate than a simple parallel among individual organizations
The largest group of the sensory neurons in the deep layers is multisensory  an
effective sensory stimulus activates many of the same neurons, enhancing its salience
Visual-multisensory and somatosensory-multisensory neurons are not clustered in one
region of the superior colliculus representing one region of visual or somatosensory
space: they cover the entire structure, so that the the majority of neurons from which the
visual map, or the somatosensory map, is constructed are multisensory
multisensory neurons
• there are many areas in the brain in which multiple sensory
afferents converge
• there are colliculus neurons that respond vigorously to low
intensity auditory stimulus, but if the animal can’t see the
visual stimulus the response is suppressed
• the colliculus is an apt structure to study interactions
between sensory modalities, and in particular multisensory
integration at the level of a single neuron
Multisensory integrated maps
• Since the different sensory maps in the colliculus are
composed of many of the same neurons, it is more
appropriate to consider them as three components of a
multisensory integrated map, rather than three parallel
independent maps
• And since this « multisensory map » is in register with
motor maps, we should speak of a « multisensorymultimotor map » which coordinates th movement of
eyes, ears, head, body
• It is not to be forgotten for the understanding of the
functioning of the superior colliculus that i ntegrated
multisensory maps coexist with unimodal maps (unimodal
neurons) that preserve modality specificity and modality
specific activation of premotor neurons
multisensory neurons in the colliculus
Method:
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estimates are based on all neurons ecountered in the superior colliculus, including those that doesn’t
respond to sensory stimuli
quantitative evaluation of the effects of presenting two stimuli from different modalities
independently and concertedly in every neuron ecountered
permits to evaluate the effect of a stimulus (auditory) in biasing one other (visual), even if it itself
doesn’t generate impulses
Results (cat):
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over ½ of the the neurons of the deeper layer of the colliculus are influenced by stimuli from more
than one sensory modality = are multisensory
neurons with visual inputs predominate (somatosensory in rodents)
the most frequent category is visual-auditory multisensory (visual-somatosensory in rodents)
the ¾ of the neurons having descending efferent projections are activated by multisensory stimuli;
tha majority of neurons that fail to demonstrate a descending projection are unimodal
multisensory neurons are the most significant contributors to the behavior mediated by
the superior colliculus
the outputs of the superior colliculus are mostly the products of the synthesis of
different sensory inputs
it is the presence of integrate multisensory messages that determine colliculis mediated
behaviors
colliculus multisensory neurons characteristics
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unimodal and multimodal neurons are very similar for what regards the
properties of their receptive fields, but for their dimension (bigger receptive
field for multisensory neurons): unimodal and multisensory neurons have
acces to the same modality specific information and synthetize it in the same
way
multisensory convergence takes place directly in the colliculus (doesn’t derive
from multisensory neurons somewhere else)  corticotectal and peripheral
inputs are unimodal and converge on a single colliculus neuron
Assembling the stimuli: enhancement
and depression
• Since sensory channels separate the stimuli, the brain must then relate
stimuli one to another
• In assembling the stimuli from different modalities the brain acts on
the base of the significance of the stimuli, determined by:
– intrinsic circuitry
– postnatal experience
• Some combinations of stimuli enhance the activity of neural responses
and so they become more salient; other combinations depress the
activity and they remain less salient
• Enhancement and depression in activity produced by combinations of
stimuli is characteristic of superior colliculus neurons
• Enhancement and depression generally signal the presence or absence
of meaningful relations among the stimuli
Enhancement: the potent effect of
combinations of sensory stimuli
• Responses evoked by combinations of stimuli are stronger
(at all levels: response reliability, number of impulses
evoked, peak impulse frequency, duration of the discharge
train) than responses evoked by a single sensory cue
• Response enhancements are present in every multisensory
combination
• The multisensory activity of a neuron sometimes reveals
only when multiple sensory cues are present (ie: two
apparently uneffective stimuli produce action potentials
only as a combined stimulus)
Depression
• Responses evoked by combined stimuli are sometimes
weaker (fewer impulses, shorter discharge train duration,
lower peak frequencies, lower response reliability) than
one stimulus alone
• Response depression is less common than enhancement; it
depends on some specific properties as spatial inhibition,
inhibitory surrounds, inhibitory inputs that are not common
to all multisensory receptive fields
• The inhibitory effect of the ineffective stimulus becomes
apparent only when coupled with another stimulus
Rules for multisensory integration: causality
• Multisensory enhancement and depression are determined by the spatial and
temporal characteristics of the stimuli
• Multisensory assembly depends on whether or not the stimuli are like to have
common causality
– stimuli that occur at the same time in the same place are likely to be interrelate
because they are likely to have common causality
– so this combination of stimuli is likely to produce enhancement
– stimuli that occur at different places and times are unlikely to be related and they
will product depression
• Experience is not effective in changing the interaction of a stimulus
combination from enhancement to depression
• The role of experience is in aligning the different sensory maps in the superior
colliculus
• Once the maps are aligned neuronal enhancement or depression becomes
dependent on the spatial and temporal relationship among stimuli
Rules for multisensory integration: space
• Multisensory enhancement and depression are determined by the
spatial and temporal characteristics of the stimuli:
– Space: spatially coincident multisensory stimuli tend to produce response
enhancement; spatially disparate stimuli produce depression or no
interaction:
• varying the position of the different sensory stimuli, it is evident that the
enhancement is present only if the visual and auditory stimuli fall in the visual
and auditory receptive field of the multisensory neuron
• the different unimodal receptive fields of a multisensory neuron overlap
• it is in virtue of this overlap that stimuli located near one another in space
enhance one another’s effects
• it is not question of an identity of position in the external space (or visual and
somatosensory stimuli would never be integrated: it is a question of
representational axes, which are common (see register, alignement of the
maps)
• the alignement of the maps is then a prerequisite for multisensory integration
and enhancement
• enhancement and depression depend on the falling of a stimulus in the
zones of excitation or of inhibition of the receptive field of a
multisensory neuron: the receptive field and not space is the proper
referent for multisensory integration
receptive fields
• Receptive fields are the regions in which limits a stimulus produces an
excitation
• Sometimes these regions are bordered by inhibitory areas the
excitation of which produces the suppression of the excitation in the
entire receptive field
• A stimulus is never excitatory or inhibitory in itself
• Receptive fields characteristics are robust
Rules for multisensory integration: time
• Multisensory enhancement and depression are determined
by the spatial and temporal characteristics of the stimuli:
– Time: multisensory stimuli within a certain “temporal window”
interact in a way that enhances responses
– Overlapping the peak activity (excitatory or inhibitory) periods of
two unimodal stimuli maximizes their interactions
Other rules for multisensory integration
• Response enhancement is not effective when two stimuli come from
the same modality (despite the fact that multisensory intgration
depends on unimodal receptive field properties)
• Combinations of weak unimodal stimuli produces the greatest results
Summary
• The construction of a multisensory space at the superior
colliculus level
– parallel alignement (register)
• alignement of the sensory representations (sensory maps register)
• alignement of the sensory and movement representations (sensory and
motor maps register)
– convergence on a single neuron (integrated multisensory maps)
• multisensory neurons
• multisensory and premotor neurons
– coordinating different modalities (different spaces) and
movement (sensorimotor transduction)
– in order to position the sensory organ in relation with the
stimulus to reach-avoid (attention-positioning)
Questions
• Enhancement-depression paradigm :
– ROLE OF SPACE AND TIME FOR SENSORY INTEGRATION
– CAUSALITY: IS IT TRUE THAT TWO STIMULI BEING
ASSEMBLIED FOR TEMPORAL AND SPATIAL REASONS (WHERE
TIME AND SPACE ARE RELATIVE TO THE RECEPTIVE FIELD
CHARACTERISTICS, AND NOT TO THE OBJECT THEY
ORIGINATE IN) ARE LIKELY TO HAVE A COMMON CAUSALITY?
AND THAT COMMON CAUSALITY IS THE RELEVANT
PARAMETER?
• Existence of unimodal informations:
– EXISTENCE OF UNIMODAL SPATIAL INFORMATIONS IN THE
FORM OF RECEPTIVE FIELD EXCITATIONS
• Alignement of the sensorimotor maps as a prerequisite for integration