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The Journal of Neuroscience, February 1, 1998, 18(3):1072-1084
Cross-Modal Transfer of Information between the Tactile and the
Visual Representations in the Human Brain: A Positron Emission
Tomographic Study
Nouchine
Hadjikhani1 and
Per E.
Roland1
1 Division of Human Brain Research, Institute of
Neuroscience, Karolinska Institute, 171 77 Stockholm, Sweden
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ABSTRACT |
Positron emission tomography in three-dimensional acquisition mode
was used to identify the neural populations involved in tactile-visual
cross-modal transfer of shape. Eight young male volunteers went through
three runs of three different matching conditions: tactile-tactile
(TT), tactile-visual (TV), and visual-visual (VV), and a motor
control condition. Fifteen spherical ellipsoids were used as
stimuli.
By subtracting the different matching conditions and calculating the
intersections of statistically significant activations, we could
identify cortical functional fields involved in the formation of visual
and tactile representation of the objects alone and those involved in
cross-modal transfer of the shapes of the objects.
Fields engaged in representation of visual shape, revealed in
VV-control, TV-control and TV-TT, were found bilaterally in the
lingual, fusiform, and middle occipital gyri and the cuneus. Fields
engaged in the formation of the tactile representation of shape,
appearing in TT-control, TV-control and TV-VV, were found in the
left postcentral gyrus, left superior parietal lobule, and right
cerebellum.
Finally, fields active in both TV-VV and TV-TT were considered as
those involved in cross-modal transfer of information. One field was
found, situated in the right insula-claustrum. This region has been
shown to be activated in other studies involving cross-modal transfer
of information. The claustrum may play an important role in cross-modal
matching, because it receives and gives rise to multimodal cortical
projections. We propose here that modality-specific areas can
communicate, exchange information, and interact via the claustrum.
Key words:
human; PET; claustrum; cross-modal transfer; visual
system; somatosensory system
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INTRODUCTION |
The relations between sight and
touch have been for long a matter of debate, as in 1709 the philosopher
George Berkeley in his book An Essay Towards A New Theory of
Vision concluded that there were no necessary connections between
a tactile world and a visual world. Even today there is theoretical and
experimental support for the view that there are no cortical
convergence regions, in which neuron populations integrate information
from different sensory modalities and from different submodalities
(Abeles, 1991 ; Felleman and van Essen, 1991; Young et al., 1992; Singer
1993, 1995). Information from visual submodalities seem to be processed by parallel "functional streams" (Ungerleider and Mishkin, 1982; Livingstone and Hubel, 1988; Haxby et al., 1991; Zeki et al., 1991;
Gulyas et al., 1994). Because further direct anatomical connections
between somatosensory and visual areas in primates are sparse, if at
all existing (Selemon and Goldman-Rakic, 1988; Cavada and Goldman-Rakic
1989; Neal et al., 1990), one might expect that somatosensory and
visual information is processed by segregated populations of neurons.
Still everyone recognizes a key, whether it is felt in a pocket or seen
on a table. How is this possible?
The research done on tactile-visual cross-modal performance has been
based mainly on the assumption that there must exist amodal
representations of form in so-called polysensory areas, defined as
areas activated by stimuli from more than one sensory modality.
Nevertheless, in a review on cross-modal abilities in nonhuman
primates, Ettlinger and Wilson (1990) concluded that there is no
polysensory cross-modal area, no cross-modal region "in which
representations formed in one sense would reside and be accessed by
another sense," but suggested instead a system in which the senses
can access each other directly from their sensory-specific systems. For
the present purpose, we define cross-modal-specific areas as areas
activated only when information coming from two or more different
sensory modalities is compared.
We examined tactile-visual matching of the shapes of objects. In
tactile-visual matching of three-dimensional objects, the tactile
information is of a different nature from that of visual information.
When the hand is used to palpate an object, the information is sampled
in a piecemeal manner, such that only a part of the object surface is
covered by the fingers during each sampling path (Roland and Mortensen,
1987), and information is integrated over time to form a truly
three-dimensional shape representation. In the visual system,
information about an object can be simultaneously obtained and
transferred to the visual cortex, but if it is seen from a stationary
angle of view, only a part of its surface is sampled. This difference
speaks against any common polymodal or amodal representation for the
two modalities.
We studied tactile-tactile and visual-visual intramodal matching
aiming to identify cortical fields engaged in processing and
representation of tactile and visual shape. Putative polysensory areas
thus should be activated by tactile as well as visual intramodal shape
matching. We also studied tactile-visual cross-modal matching of shape
with the purpose of identifying cross-modal-specific areas. Neither any
polymodal nor any cross-modal cortical areas were found; instead the
claustrum was specifically activated by cross-modal shape matching.
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MATERIALS AND METHODS |
Subjects
Eight young male volunteers (aged between 22 and 32 years; mean,
26 years) participated in the study. All of the subjects gave informed
consent according to the requirement of the Ethics Committee and the
Radiation Safety Committee of the Karolinska Institute. None had
previous or present history of significant medical illness, and all had
a normal magnetic resonance imaging (MRI) scan. All subjects were
right-handed, according to the Edinburgh questionnaire (Oldfield,
1971).
Task design
Two similar sets of 15 spherical ellipsoids weighing all the
same but having different shapes were used as stimuli (Fig.
1).
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Figure 1.
The fifteen spherical ellipsoids. The fifteen
ellipsoids used in this experiment were made to have the same weight
and surface, differing by their shape only. Two similar sets were
used.
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The regional cerebral blood flow was measured during four different
conditions, each scanned three times. These were matching tasks in
tactile-tactile (TT), tactile-visual (TV), and visual-visual (VV)
modalities, and a control condition.
The experimenter was standing beside the subject. The stimuli were
presented as pairs. The pairs were constituted in the following way:
one-fourth were matching ellipsoids of identical shapes; another fourth
were ellipsoids having one step difference between each other; a third
fourth were ellipsoids having two steps difference between each other;
and finally one-fourth were three steps different. We define a step as
the gap between two ellipsoids having the least difference in shape
(for a detailed description of the stimuli, see Roland and Mortensen,
1987). The different pairs were presented in a random order. The
subjects had not seen the objects before the experiment, nor had they
an idea about the number of objects that were in the series. The TT
tasks were always done first, because we did not want the subjects to
see the stimuli before the experiments requiring visual exposure. The
other conditions were randomized.
Figure 2 illustrates the experimental
conditions, and Figure 3 gives a flow
chart for the different experiments.
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Figure 2.
The experimental procedure. The subjects were
lying in the camera with their stereotactic helmet fixed to the PET
scanner. They could see the ellipsoids when the experimenter presented them on a shelf placed over their head through a mirror. They could
not, however, see the ellipsoids placed in their right hand for the
tactile examination. Just above the shelf a crosshair could be seen
through the mirror, to which the subjects fixated during the TT and
control conditions. They answered if they thought that two ellipsoids
were identical in shape by raising their right thumb.
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Figure 3.
Flow chart of the different tasks during the
scanning. T1a stands for the first object in the
tactile-tactile matching, T1b for the second, and so
forth. This design balanced the number of visual and tactile
stimulations.
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TT matching. The subjects were instructed to fix a point on
the presentation shelf seen in the mirror during the whole procedure. The tactile stimuli were presented sequentially in pairs to the right
hand of the subjects. The subjects received the ellipsoids in their
palm in different orientations and explored them by palpation between
fingers and opposing thumb. The first ellipsoid in the pair was
palpated for 3-4 sec, and the second was palpated for 2-3 sec. A new
pair was presented approximately every eighth second. The subjects were
not able to see the ellipsoids. If they thought that the two ellipsoids
had identical shapes, the subjects had to raise their right thumb.
TV matching. The tactile and the visual stimuli were
presented simultaneously. The subjects had ~3 sec to palpate one
ellipsoid (without being able to see it) and three seconds to look at
the ellipsoid that was presented on a shelf placed over their head. A
new pair was presented approximately every fourth second. A mirror
allowed them to see the objects at a distance of 60 cm. The subjects
again extended their right thumb if they thought that the two
ellipsoids were identical.
VV matching. The first ellipsoid in the pair was presented
on the shelf for ~4 sec, and then the second ellipsoid was presented for ~2 sec. A new pair was presented every eighth second. The subjects answered by raising their right thumb if they thought that the
two ellipsoids had identical shapes.
Control. Subjects fixated the same fixation point as in the
TT experiment and were instructed to move their right hand in the same
way as if they were actually palpating the objects.
The monitoring of eye movement was done by a video recording on a split
screen of the subject's face. The movement of the right hand of the
subjects was recorded as well. Subjects were told not to speak during
the entire procedure, and the room was kept as quiet as possible.
Psychophysics
Before the positron emission tomographic (PET) experiment, five
additional subjects underwent psychophysical testing of the same
conditions. The only notable exception is that we tested separately
visual-tactile matching and tactile-visual matching to be sure that
there was no difference to be noted depending on the modality presented
first. Each subject went through four runs of 120 pairs of ellipsoids,
with a priori varying probabilities of matching. Receiver operating
characteristic curves and d values measuring the separation
between the means of the noise and signal distribution were calculated
for each subject in each modality (Green and Swets, 1966).
Scanning procedure
Each subject, lying in a supine position and equipped with a
stereotactic helmet (Bergström et al., 1981), had a
high-resolution MRI scan and a PET scan. The MRI scans were done using
a spoiled gradient echo sequence obtained with a 1.5 T General Electric Signa scanner [echo time, 5 msec; repetition time, 21 msec; flip angle, 50°, giving rise to a three-dimensional (3D) volume of 128 × 256 × 256 in isotropic voxels of 1 mm3]. Each subject had an arterial catheter
inserted under local anesthesia in the left radial artery for the
measurement of arterial concentration of radiotracer.
The regional cerebral blood flow (rCBF) was measured in 3D acquisition
mode with a Siemens ECAT EXACT HR PET camera (for technical description, see Wienhard et al., 1994). The radiotracer used was
15O-labeled butanol, which was synthesized according to the
method of Berridge et al. (1991). Fifteen microcuries of radiotracer were injected intravenously as a bolus at the beginning of each run,
followed by a 20 ml flush with saline. The tasks began ~15 sec before
the radiotracer injection and proceeded throughout the duration of the
scan (180 sec). During this time, the subjects could match ~22 pairs
of stimuli. The rCBF was calculated by an autoradiographic procedure by
taking frames between 0 and 60 sec (Meyer, 1989). The sinograms were
reconstructed with a cutoff frequency of 0.5 cycle with a Ramp filter,
and the reconstructed image was subsequently filtered with a 4.2 mm
full-width half-maximum 3D isotropic Gaussian filter.
The individual MRI and rCBF images were standardized anatomically using
the human brain atlas of Roland et al. (1994). To reduce variance of
the rCBF measurements the global blood flow was normalized to 50 ml · 100
gm 1 · min1.
Statistical analysis
The statistical analysis tested the hypothesis that clusters of
high t values occur by chance in the standard anatomical
space and was described in detail previously (Roland et al., 1993). In
short, individual voxel-by-voxel rCBF subtraction images were calculated for each subject and averaged. For example, for a given test
repeated i times in subject k:
These images were subsequently averaged.
These individual mean images were used to calculate a group mean
image:
and eventually a t image was calculated:
The spatial three-dimensional autocorrelation was then
determined in Student's t pictures obtained from the
 rCBFi,k images of subtracting two TT matching images to
give a noise image, as described by Roland et al. (1993). The resulting
noise t pictures were thresholded at different t
values, and clusters of voxels of suprathreshold values were
identified. We simulated 2000 groups of eight subjects each for each
t threshold. From these noise t picture tables of
clusters of suprathreshold t values, exceeding a certain
number of voxels, were produced (Roland et al., 1993). The criteria
used for accepting rCBF changes in adjacent clustered voxels as
activations were set so that there was an average probability of
p < 0.1 of finding one false-positive
cluster or more within the three-dimensional space of the
standard anatomical brain format. Accordingly the descriptive
Student's t pictures were thresholded such that the
(omnibus) probability of finding one or more false-positive clusters
was p < 0.1. The resulting cluster images thus show
only the activated parts of the brain and zero elsewhere. The
significance of each cluster was also assessed by nonparametric method
of Holmes et al. (1996). For a t threshold of 2.5 this
method gave p < 0.1 for one or more false-positive
clusters of  900 mm3 in size.
These cluster images are henceforth referred to as TT-control,
TV-control, VV-control, TV-TT, and TT-VV. For the convenience of
the reader, the different significant clusters are listed in Tables 2
and 3 in accordance with the method of Roland et al. (1993). In Tables
2 and 3 the average t value of each cluster is also
calculated as the mean of the values of the voxels constituting the
cluster.
The cluster images TT-control, TV-control, VV-control, TV-TT, and
TT-VV were then used to form Boolean intersection images (Ledberg et
al., 1995), as, for example, TT-control  TV-VV. This Boolean
intersection carries no assumptions and shows the intersections or
overlaps of clusters that correspond to cortical or subcortical regions
active in both TT-control and TV-VV. For example, if a cluster in
TT-control has p < 0.05 of being a false-positive, the probability that any cluster from TV-control by chance will overlap this is p < 0.05, because the prerequisite for
overlap is that the TT-control cluster is present.
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RESULTS |
Psychophysics
The psychophysical testing showed that there is a linear
relationship between presented and chosen stimulus, regardless of the
modalities, as shown by the linear regression curves. The direction of
cross-modal information transfer (i.e., tactile to visual vs visual to
tactile) had no influence on the performance (Fig.
4).
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Figure 4.
Psychophysical experiment. This figure shows the
results of the psychophysics experiment that was done before the PET
study. Four different paradigms are presented: tactile-tactile,
visual-visual, tactile-visual, and visual-tactile. In each
graph, the responses of the subjects deciding that two objects were
identical are shown versus the actual stimuli presented by the
experimenter. Error bars indicate SD. The regression lines of chosen
versus given stimuli were calculated together with the correlation
coefficient. Even if the performance of the subjects was slightly
better in the visual-visual matching condition, the overall
performance does not depend on the mode of presentation of the
stimulus. The responses are linear. Cross-modal comparison gives the
same results as intramodal matching. Furthermore, there is no notable
difference depending on whether the ellipsoids are first presented
visually and then haptically or are presented in the reverse
order.
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During the actual PET scanning, the probability of a responding match
given a matching pair, i.e., p(match | match), and the probability of a responding match given a nonmatching pair, i.e., p(match | nonmatch), was calculated for each subject. On
the basis of these probabilities a measure of the performance
d was calculated (Greens and Swets, 1966). The subjects had
d values between 0.40 and 2.88, indicating that all of them
actually performed above chance or noise level. Furthermore, this range
of d values was comparable to the range of 0.65-3.0
obtained by the five subjects performing the psychophysical test
outside of the PET camera, indicating no major differences between the
two groups. For the subjects doing PET, there were no differences in
d between conditions, indicating the same level of
difficulty between the tasks. By paired comparison of d
values, the subjects being their own control, the average intrasubject
differences in d were TV-VV,  0.66 ± 0.93 (SD); and
TV-TT, 0.08 ± 0.61.
To examine whether the motor activity of exploring the ellipsoids
tactually was balanced between the matching tasks (i.e., TV and TT),
between TV and the control condition, and between TT and the control
condition, we analyzed the frequencies of movements of the individual
fingers of the subjects doing PET. By a paired comparison, the subjects
being their own controls, the average intrasubject differences were in
TT-control for the thumb (0.05 ± 0.08 Hz) and for the index
(0.02 ± 0.12 Hz). The corresponding differences in frequencies
for TV control were for the thumb (0.02 ± 0.07 Hz) and for the
index (0.06 ± 0.13 Hz). The number of thumb and index movements
in TT, TV, and control did not vary very much for a given subject: the
intrasubject SDs were between 0.6 and 8%. The subjects fixated the
fixation point as instructed during the TT and the rest condition, and
there was no significant eye movement while the subjects were presented
the visual stimuli in TV and in VV.
Regional cerebral blood flow changes
Tale 1 shows the
rationale of the different subtractions. Somatosensory areas and
perhaps polysensory areas participating in the formation of tactile
representation of the stimuli were assumed to be active in
tactile-tactile minus control, tactile-visual minus control, and
tactile-visual minus visual-visual. By calculating the intersection
between the two independent cluster images of TV-VV and TT-control,
we expected to isolate those areas involved in the formation of the
tactile representation of the stimuli. Visual areas and perhaps
polysensory areas were expected to be activated during the visual
matching in the following paradigms: visual-visual minus control,
tactile-visual minus control, and tactile-visual minus
tactile-tactile. The overlap between TV-TT and VV-control was
expected to show areas specifically engaged in the formation of the
visual representation of the stimuli. The overlap between the two
cluster images of the cross-modal matching tasks, i.e., TV-TT and
TV-VV, would isolate areas specifically engaged in the cross-modal
matching procedure, whereas the overlap between all of the tasks minus
control would isolate polysensory areas activated regardless of the
mode of stimulation. Tables 2 and
3 show the location (i.e., center of
gravity), volume, and mean t value of the fields of
activation in the different tasks. Tables
4-6
show the location and extent of the overlaps of fields engaged in the
formation of tactile-visual representation of the stimuli and in the
cross-modal transfer of information.
Tactile-tactile minus control
Several fields of activation were found in the parietal lobe. The
biggest increase of rCBF was situated in the left postcentral gyrus,
extending posteriorly from the posterior part of the gyrus and the
cortex lining the postcentral sulcus into superior parietal lobule and
the anterior part of the intraparietal sulcus. A second focus of
activation was found in the right parietal lobe, situated in the
supramarginal gyrus (Table 2).
Other foci of activation were found in the right thalamus, the right
temporal pole, and the left anterior prefrontal cortex. The cerebellum
showed several foci of activation bilaterally.
Tactile-visual minus control
Fields of activation were found mainly in the occipital, temporal,
and parietal lobes.
The biggest activation cluster was situated on the left cuneus,
extending anteroposteriorly along the calcarine sulcus. A second
cluster was situated on the left superior occipital gyrus, on its
posterior part. A third cluster was situated on the left middle
occipital gyrus. The right occipital cortex contained one cluster of
activation that was situated on the lingual gyrus and the cortex lining
the collateral sulcus, extending anteriorly to the fusiform gyrus
(Table 3).
In the left parietal lobe, a field of activation was found in the
postcentral gyrus, extending medially onto the cortex lining the
postcentral gyrus and on the posterior parietal cortex, including the
cortex lining the anterior part of the intraparietal sulcus. A second
cluster was situated on the left superior parietal lobule. A third
cluster was found in the left precuneus and in the cortex lining the
parieto-occipital sulcus. On the right parietal lobe, we found a
cluster of activation on the superior parietal lobule that was situated
more posteriorly than the one on the left side (Table 2).
Other foci of activation were found in the right thalamus, in the
anterior prefrontal cortex bilaterally, and in the right cerebellum.
Two minor clusters at the location of the right insula-claustrum were
found of 172 and 143 mm3 with mean t
values 3.35 and 3.34, respectively. These were not statistically
significant.
Visual-visual minus control
In the occipital lobes, several clusters of activation were found
bilaterally. The most important one was situated on the left lingual
gyrus, extending anteroposteriorly along the calcarine sulcus (Table
3).
The inferior part of the middle occipital gyri was bilaterally
activated, and the left superior part of the middle occipital gyrus
also showed a cluster of activation. The right fusiform gyrus was
activated in its posterior part.
The parietal lobes showed two foci of activation on the right side. One
was situated in the superior parietal lobule and extended to the cortex
lining the intraparietal sulcus, and another was in the angular
gyrus.
We found bilateral fields of activation in the anterior and posterior
cingulate cortex and in the anterior part of the middle frontal gyrus.
The left anterior insula was also activated.
Tactile-visual minus visual-visual
According to our hypothesis, this subtraction should reveal the
areas engaged in the tactile exploration of the stimuli and in
cross-modal matching. Clusters of activation were found in the parietal
lobes, with a big cluster of activation centered on the left
postcentral gyrus, extending anteriorly to the cortex lining the
central sulcus and posteriorly to the postcentral sulcus and the
anterior part of the intraparietal sulcus as well as going more
medially on the superior parietal lobule; a second cluster was situated
on the right postcentral gyrus. Another cluster was found at the bottom
of the left central sulcus. The left middle cingulate and the left
thalamus were activated. The cerebellum showed bilateral foci of
activation. Finally, a cluster of activation was situated in the right
insula-claustrum region.
Tactile-visual minus tactile-tactile
This subtraction image was hypothesized to reveal the areas
engaged in the visual perception of form as well as in cross-modal matching. Fields of activation were found in the occipital and parietal
cortex as well as in the thalamus and in the right insula-claustrum region (Table 3).
In the occipital cortex, the middle occipital gyri were activated
bilaterally; other foci of activation were found in the left lingual
gyrus extending on to the collateral sulcus and in the left posterior
and anterior fusiform gyrus.
The parietal cortex showed areas of activation in the left precuneus,
in the right superior parietal gyrus, and in the cortex lining the
intraparietal sulcus as well as in the right supramarginal and angular
gyri.
The pulvinar nucleus of the thalamus was activated bilaterally, and a
cluster of activation was found in the left hippocampus. At a more
liberal level of significance (p < 0.6) a small
cluster (t = 6.3) was found in the left superior
colliculus (Talairach and Tournoux, 1988; coordinate 6, 30, 2).
Fields of activation were found in the left cerebellum.
A cluster of significant activation was found in the right
insula-claustrum region, with a center of gravity situated in the claustrum.
TT-control  TV-VV
This intersection of two independent cluster images was supposed
to reveal the areas specifically activated in the formation of the
tactile representation of the stimuli (Fig.
5). A cluster of activation was found in
the left parietal lobe, on the left postcentral gyrus, which was
extending into the cortex lining the postcentral sulcus and the
anterior intraparietal sulcus, and in the posterior parietal cortex. A
second one was situated more anteriorly on the postcentral gyrus,
extending to the cortex lining the central sulcus (Table 4).
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Figure 5.
Illustration of the tactile representation of the
stimuli. Shown are the fields consistently active in two independent
conditions, which both involved tactile representations of the
ellipsoids, i.e., TT-control TV-VV. Five different slices are
presented here: a-d are on the left hemisphere;
e is on the right hemisphere. The levels of the slices
are shown on the superior view of a 3D reconstruction on the
bottom right (a, x = 48; b, x = 43; c,
x = 38; d, x = 29; e, x = 18).
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Two clusters of activation were found in the right cerebellum.
That two activated fields,
Xi,A and
Xi,B, originating from
the respective cluster images A and B, reflect
activity in approximately the same synaptic cortical field can be
addressed in a forward way. Let the estimated volumes and centers of
gravities of a cluster in TT-control and a cluster in TV-VV be
Vi,TT and Vi,TV-VV and TTi,cog
and TV-VVi,cog, respectively. In this case,
VTT < VTV-VV (Table 2). A reasonable
criterion of judging whether two clusters reflect activation in the
same location is that the overlap, Q, produced by the two
clusters is equal to or greater than half of the volume of the smallest
of the two clusters, and the centers of gravity of the two clusters are
included in the overlap (Ledberg et al., 1995). i.e.:
This was fulfilled for all three intersections (overlaps) as seen
by comparing Tables 2 and 4.
VV-control TV-TT
This intersection of two independent cluster images was supposed
to show the areas specifically engaged in the formation of the visual
representation of the stimuli (Fig. 6).
We found all the clusters of activation in the occipital lobes. (Table
5). The lingual gyri and collateral sulci were activated bilaterally, as were the fusiform gyri. Other foci of activation were found in the
right hemisphere in the superior occipital gyrus and in the left
hemisphere in the middle occipital gyrus, the left cuneus, and the
cortex lining the parieto-occipital sulcus, and in the cortex lining
the calcarine sulcus. Of these overlaps the centers of gravity and the
volume of overlap in the middle occipital gyri produced by the two
clusters was greater than half of the volume of the smallest of the two
clusters, and the centers of gravity of the two clusters were included
in the overlap.
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Figure 6.
Illustration of the visual representation of the
stimuli. Shown are the areas active in the overlap between two
independent conditions, which involved the visual representation of the
stimulus, i.e., VV-control TV-TT. Five different slices are
presented here: a-d are situated on the left
hemisphere; e is on the right hemisphere. The levels of
the slices are shown on the superior view of a 3D reconstruction on the
bottom right (a, x = 48; b, x = 31; c,
x = 21; d, x = 9; e, x = 17).
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TV-TT TV-VV
This intersection image was supposed to show the areas engaged in
cross-modal transfer of information (Fig.
7). Only one cluster of activation was
found, which was situated in the right insula-claustrum, with a center
of gravity situated toward the claustrum (Fig.
8, Table 6). Here also the centers of
gravity of the two clusters were included in the overlap.
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Figure 7.
Activation in the cross-modal paradigms.
Shown are the areas of activation in the two different paradigms
involving cross-modal transfer of information. On the
left is the cluster image of TV-TT, which shows areas
involved in the formation of the visual representation of the stimulus
and in the cross-modal transfer of information (coronal slice,
y = 8; horizontal slice, z = 9); on the right is the cluster image of TV-VV, which
shows areas engaged in the formation of the tactile representation of
the stimulus and in the cross-modal transfer of information (coronal
slice, y = 8; horizontal slice,
z = 13).
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Figure 8.
Activation of the isolated cross-modal component.
Shown is the intersection between the two cluster images of TV-VV and
TV-TT, i.e., TV-VV TV-TT, on the mean MRI of the subjects after
the standardization with the human brain atlas (discussed by Roland et
al., 1994). A, Horizontal slice at the level
z = 8, B, Coronal slice at the level
y = 4. One cluster of activation is constantly present in those two tasks, situated in the right insula-claustrum region, with a center of gravity situated in the claustrum.
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TT-control TV-control VV-control
This intersection image could isolate the polysensory areas
engaged by processing of somatosensory and visual shape information, regardless of the modality. We did not find any significant cluster of
activation by performing these intersections.
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DISCUSSION |
This experiment, designed for each subject with three runs of four
different tasks, gave the opportunity to study, within the same group
of subjects, different aspects of the somatosensory and visual
processing of shape and to isolate the structures involved in
cross-modal transfer of shape.
The motor measurements showed that the matching conditions were
mutually balanced and balanced against the control condition for motor
activity of the right hand. Accordingly, no activations appeared in any
of the motor cortices in any of the subtractions.
In addition, the signal energies for the somatosensory and visual shape
stimulation (Roland and Mortensen, 1987) were also balanced across the
three matching conditions. Accordingly, we observed no changes in
visual cortices in TV-VV and no changes in somatosensory cortices in
TT-TV. One might argue that the attention in TV was divided between
the somatosensory and the visual modalities, whereas it was allocated
to the visual modality in VV and the somatosensory modality in TT.
However, to balance the allocation of attention toward the
somatosensory and the visual modality between conditions TV and TT and
TV and VV, the number of matchings in TV were twice the number during
TT and VV.
The performance of the subjects, reflected by their d
values, were balanced across matching conditions. This made it unlikely that differences between conditions could be interpreted as differences in attention and/or task difficulty. The attentional effects or rCBF
may vary between TT and VV. Cross-modal attentional effects in visual
tasks tend to decrease the rCBF in somatosensory areas, and
somatosensory tasks tend to decrease rCBF in visual areas (Haxby et
al., 1994; Kawashima et al., 1995). It is not unlikely that the greater
pace of the TV compared with the TT condition and the VV condition
might imply a higher rate of switching attention from the tactile to
the visual modality and vice versa. This could be a possible
explanation for the pulvinar activation seen in TV-TT and TV-VV
(Petersen et al., 1985, 1987).
Tables 2 and 4 show the fields activated every time the subjects
perceived the ellipsoids tactually. Fields specifically engaged in the
haptic processing of the ellipsoids were found by computing the
intersection of the cluster images of TT-control and TV-VV. They were
located to the contralateral postcentral gyrus, superior parietal
lobule, and the cortex lining the anterior part of the intraparietal
sulcus. The cortex lining the postcentral sulcus, anterior part of the
intraparietal sulcus, and the cortex of the anterior part of the
superior parietal lobule have in other studies been activated
specifically during haptic processing of shape and length of objects
(Roland and Larsen, 1976; Seitz et al., 1991; O'Sullivan et al., 1994;
Roland et al., 1996). Together with the present results, this strongly
indicates that neurons in these regions are engaged in the formation of
the haptic shape. We use the expression haptic processing of shape to
note that although the experimental design attempted to balance
allocation of attention between the somatosensory and visual
modalities, we cannot exclude that in the intersection TT-control TV-VV, the effect of somatosensory attention to shape might not be
separable from the processing of shape information.
Structures involved in visual processing of the shape of the
ellipsoids, revealed in VV-control, TV-control, and TV-TT, showed similar patterns of activation of the visual cortex. Fields solely engaged in visual processing of the shapes of the objects, and to some
extent attention to visual object shape, were isolated in the
intersection of the two independent cluster images of VV-control with
TV-TT, which revealed several areas in the occipital cortex. All
areas lips of the calcarine sulcus, cuneus, lingual gyrus, and
the cortex lining the collateral sulcus, fusiform gyrus, and the middle
occipital gyrushave been described with different methods as being
visual areas (Clarke and Miklossy, 1990, Zilles and Schleicher, 1993,
Clarke, 1994a,b; Hadjikhani et al., 1994; Hadjikhani, 1995, Clarke et
al., 1995; Sereno et al., 1995; Van Essen et al., 1995a,b). Of these
regions, the lingual, fusiform, and occipital gyri have been activated
by perception or discrimination of visual form and geometrical patterns
(Gulyas and Roland, 1994; Gulyas et al., 1994; Roland and Gulyas,
1995).
We did not find any polymodal areas, i.e., fields of activation present
consistently in tactile-tactile, tactile-visual, and visual-visual
matching versus control. But we found an area consistently activated in
the two subtractions of task involving cross-modal transfer, i.e.,
TV-TT and TV-VV, that was situated in the right insula-claustrum.
The neural structures participating in cross-modal transfer have been
for a long time matters of debate, because lesion studies were never
able to point to a particular structure consistently involved when
cross-modal deficits were present. With notable exceptions (Ettlinger
and Wilson, 1990), cross-modal research has been generally based on the
assumption that there must be a special process to deal with
the confluence of different sensory input in "polysensory convergence
areas" (Pandya and Kuypers, 1969; Jones and Powell, 1970; Petrides
and Iversen, 1976). The earliest attempts to study the effects of brain
lesions on cross-modal performance used the cross-modal recognition
method of Cowey and Weiskrantz (1975). Sahgal et al. (1975) and
Petrides and Iversen (1976) reported impairment in cross-modal
(tactile-visual) matching abilities after posterior temporal and
prestriate removal and after lesions of the arcuate sulcus cortex. In
more recent studies, authors have used a different cross-modal
recognition paradigm (Jarvis and Ettlinger, 1977) in which monkeys
learn cross-modality (vision or touch) discrimination tasks. Cortical
lesions involving the superior temporal sulcus and the lateral
prefrontal region in monkeys did not produce deficits (Ettlinger and
Garcha, 1980). Streicher and Ettlinger (1987) examined cross-modal
performance for entirely new and unfamiliar objects. Lesions in the
frontal, temporal, and parietal cortex gave rise to impairment of
cross-modal recognition of unfamiliar objects, despite normal
performance on familiar objects.
Thus lesions to the cortex claimed as polymodal, e.g., the cortex
lining the superior temporal sulcus, the intraparietal sulcus, the
amygdala, and the lateral prefrontal cortex, have failed to abolish
cross-modal matching consistently and specifically (Cowey and
Weiskrantz, 1975; Sahgal et al., 1975; Petrides and Iversen, 1976;
Jarvis and Ettlinger, 1977; Ettlinger and Garcha, 1980; McNally et al.,
1982; Murray and Mishkin, 1984; Streicher and Ettlinger, 1987; Nahm et
al., 1993). With the exception of the prefrontal cortex, none of these
areas was activated by TV, and neither was the superior colliculus,
also claimed a polymodal structure (Stein et al., 1976). The amygdala
and the cortex lining the superior temporal sulcus were not activated
in cross-modal matching (i.e., TV-TT TV-VV), even if the
threshold was set quite liberally. Ettlinger and Wilson (1990)
suggested an alternative model for the mechanism of cross-modal
performance, claiming a so-called "leakage" between perceptual and
memory systems. On the basis of a 2-deoxyglucose study in monkeys
trained to a high level of cross-modal performance, they suggested that
one pathway for such leakage may be through the ventral claustrum
(Hörster et al., 1989).
Then how does the brain match visual shape with somatosensory shape? Is
it possible that the cortical fields representing visual shape
communicate with the cortical fields representing somatosensory shape?
From studies in monkeys there seems to be no support for such
anatomical arrangement. The possible candidates, areas 7a and 7b, are
not interconnected to any significant extent (Cavada and Goldman-Rakic,
1989; Andersen et al., 1990; Neal et al., 1990), and we do not know
where the homologs of areas 7a and 7b are in humans. Neurophysiological
studies in monkeys support the notion of parallel processing of visual
and tactile shape, because neurons in a TV task in the somatosensory
cortex react only to the tactile components immediately and during the
short delay, and neurons in the visual association cortex react only to
the visual components (Maunsell et al., 1991; Zhou and Fuster, 1996).
The left lateral prefrontal cortex was activated in TT-control, in
VV-control, and in TV-control as the only consistent example of
activations in nonsomatosensory nonvisual cortex (Tables 3, 4).
Although these functional fields were located near each other, they did
not overlap. Thus the lateral prefrontal cortex may be engaged in
matching of two stimuli, but stimuli originating from different
modalities do not engage the same prefrontal functional field. However,
that the active fields did not overlap does not exclude that they might
communicate. Indeed, bilateral cooling of a larger lateral prefrontal
region in monkeys reversibly hampers not only TV and VT cross-modal
matchings but also TT matchings (Shindy et al., 1994).
Direct communication between cortical fields representing visual shape
and cortical fields representing somatosensory shape or the
communication of each of these sets of representative fields with a
third common cortical field might not be necessary for the matching.
However, if one wants to advocate a fully parallel processing of
somesthesis and vision, it is difficult to envisage how the matching is
actually achieved. On the basis of our results, a speculative solution
is that the populations of neurons associated with somatosensory
processing of shape synchronize their activity with the populations
associated with the visual processing (Singer, 1995). If this is so,
then communication must exist at at least one location to facilitate
this synchronization.
In previous experimental studies, short-term memory components have
been a confounding factor. In our approach the TV did not contain any
memory component, whereas TT and VV had short delay between the first
and second object. Because we observed no changes or decreases in the
claustrum-insula region in TT-control or in VV-control, the
consistent activation of the claustrum-insula cannot be attributed to
this. Although unlikely, it cannot be excluded that the
claustrum-insula activation may be partly attributable to the fact
that the number of matchings were twice those of TT and VV. Against
this is the fact that the claustrum-insula was not active in
TT-control and VV-control.
Other studies may support the idea of the involvement of the claustrum
in cross-modal transfer of information. The claustrum is best developed
in primates, cetaceans, and carnivores. Its size is roughly in
proportion with cortical volume. The claustrum is connected with
virtually all of the cerebral cortex. Its connections have been studied
mostly in cats and nonhuman primates (Neal et al., 1986; Hinova-Palova
et al., 1988; Hörster et al., 1989; Cortimiglia et al., 1991;
Boussaoud et al., 1992; Clasca et al., 1992; Morecraft et al., 1992;
Baizer et al., 1993; Steele and Weller, 1993; Tokuno and Tanji, 1993;
Updyke, 1993; Webster et al., 1993) (for review, see Sherk, 1986). The
different studies show that the claustrum receives and gives rise to
direct cortical projections and that it contains maps of different
sensory (visual, auditory, and somatosensory) and motor systems.
A recent study of projection by retrograde labeling from claustrum to
S1 and V1 done by Minciacchi et al. (1995) in the cat shows a clear
topographic organization, composed of two parts. In the somatosensory
claustrum, there is a progression of cells projecting to hindpaw,
forepaw, and face representation. The visual claustrum has a
retinotopical organization, and claustral neurons project in a
retinotopical manner to corresponding parts of V1. A second pattern of
claustrum projections is composed of neurons distributed diffusely
throughout the nucleus. In both somatosensory and visual claustrum,
they intermingle with the topographically projecting cells.
In the monkey, Webster et al. (1993) demonstrated that portions of the
claustrum connected with TEO and TE appear to overlap portions
connected with other cortical areas, including V1, V2, V4, MT, MST,
inferior prefrontal cortex, frontal eye fields, and posterior parietal
cortex. Tokuno et al. (1993) showed reciprocal connections between the
primary motor area in the monkey and the claustrum, and Baizer et al.
(1993) demonstrated in the monkey that cells in the claustrum project
both to temporal and parietal cortex, and that there are two
representations of face and hand.
Conclusion
We found the insula-claustrum consistently active only when
somatosensory shape representations were compared with visual shape
representations, whereas we did not find any polymodal areas active
during the processing of somatosensory as well as visual shape
information. This and other studies support the involvement of the
insula-claustrum in cross-modal transfer of information. The claustrum
may be a site of organized and direct interaction between
modality-specific areas. Because only the somatosensory areas were
specifically active in the formation of the somatosensory representation of shape, and because only visual areas were
specifically active in the formation of the visual representation of
shape, we propose here that, instead of being based on
modality-nonspecific representations in polysensory areas, cross-modal
transfer takes place between modality-specific areas, and that those
modality-specific areas can communicate via the claustrum. This does
not, however, exclude that communications for the purpose of matching
may exist at other locations, for example, in the prefrontal cortex.
Because the claustrum is a small nucleus difficult to distinguish from the insula with PET, more studies are needed with more sensitive techniques to confirm our hypothesis that the claustrum plays a crucial
role in cross-modal transfer of information.
| |
FOOTNOTES |
Received Aug. 13, 1997; revised Oct. 17, 1997; accepted Nov. 17, 1997.
This work was supported by the Swiss National Foundation for Scientific
Research, the Societé Académique Vaudoise, and the Volvo
foundation.
Correspondence should be addressed to Dr. Nouchine Hadjikhani,
Massachusetts General Hospital-Nuclear Magnetic Resonance Center, Building 149, 13th Street, Charlestown, MA 02129.
| |
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Top
Abstract
Introduction
