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The Journal of Neuroscience, April 1, 2000, 20(7):2664-2672
A Positron Emission Tomographic Study of Auditory Localization in
the Congenitally Blind
Robert
Weeks1,
Barry
Horwitz3,
Ali
Aziz-Sultan1,
Biao
Tian4,
C. Mark
Wessinger4,
Leonardo G.
Cohen2,
Mark
Hallett1, and
Josef P.
Rauschecker4
1 Human Motor Control Section, and 2 Human
Cortical Physiology Section, Medical Neurology Branch, National
Institute of Neurological Diseases and Stroke, and
3 Language Section, Voice, Speech, and Language Branch,
National Institute on Deafness and Other Communication Disorders,
National Institutes of Health, Bethesda, Maryland 20892, and
4 Georgetown Institute for Cognitive and Computational
Sciences, Georgetown University Medical Center, Washington, DC 20007
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ABSTRACT |
We have used positron emission tomography (PET) to measure regional
cerebral blood flow (rCBF) in sighted and congenitally blind subjects
performing auditory localization tasks. During scanning, the spectral
and binaural cues of localized sound were reproduced by a sound system
and delivered via headphones. During tasks that required auditory
localization both the sighted and blind subjects strongly activated
posterior parietal areas. In addition, the blind subjects activated
association areas in the right occipital cortex, the foci of which were
similar to areas previously identified in visual location and motion
detection experiments in sighted subjects. The blind subjects,
therefore, demonstrated visual to auditory cross-modal plasticity with
auditory localization activating occipital association areas originally intended for dorsal-stream visual processing.
To determine the functional connectivity of pre-selected brain regions
in primary and non-primary auditory and posterior parietal cortex in
the two cohorts, we performed an inter-regional correlation analysis on
the rCBF data set. During auditory localization in the blind subjects,
rCBF activity in the right posterior parietal cortex was positively
correlated with that in the right occipital region, whereas in sighted
subjects correlations were generally negative. There were no
significant positive occipital correlations in either cohort when
reference regions in temporal or left parietal cortex were chosen. This
indicates that in congenitally blind subjects the right occipital
cortex participates in a functional network for auditory localization
and that occipital activity is more likely to arise from connections
with posterior parietal cortex.
Key words:
blindness; cross-modal plasticity; extrastriate; parietal cortex; positron emission tomography; sound
localization
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INTRODUCTION |
The effects of visual loss on the
remaining senses is a question of great interest to neuroscientists
(Rauschecker, 1995 ; Sadato et al., 1996; Cohen et al., 1999; Kujala et
al., 2000). Animal studies have shown an expansion of nonvisual at the
expense of formerly visual regions after binocular deprivation
(Rauschecker and Korte, 1993). In terms of behavioral abilities,
improved auditory spatial abilities of blind subjects have recently
been demonstrated in both animals (Rauschecker and Kniepert, 1994; King
and Parsons, 1999) and humans (Muchnik et al., 1991; Lessard et al.,
1998; de Volder et al., 1999; Röder et al., 1999). Human
neuroimaging studies have shown that in subjects blind early in life,
but not in sighted subjects, the occipital cortex is activated during Braille reading or other tactile discrimination tasks (Sadato et al.,
1996; Büchel et al., 1998). No studies have been performed so far
to examine the hypothesis that occipital (or other normally visual)
areas participate in the processing of auditory spatial information. We
have, therefore, designed an experiment to determine the functional
neuroanatomy of auditory localization in congenitally blind subjects
and sighted control subjects. In addition to conventional subtraction
analysis, we also used an interregional correlation analysis (Horwitz,
1994) of the regional cerebral blood flow (rCBF) data to determine
whether the principal nodes of activation during auditory localization
were functionally connected to other brain regions in similar or
different ways in blind compared to sighted subjects. The choice of
reference regions (bilateral primary and non-primary auditory cortices
and bilateral inferior parietal lobules) was made, a priori, after
analysis of the data in the sighted controls (Bushara et al., 1999;
Weeks et al., 1999). The two analytical techniques (subtraction and
correlation) are complementary and, when performed on the same data
set, can provide a fuller understanding of the underlying neural
changes during the task under study.
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MATERIALS AND METHODS |
Subjects. Nine congenitally blind subjects were
studied (four male and five female; mean age, 42.0 years), and their
results compared to those of nine, sighted control subjects (three male and six female; mean age, 38.2 years). In each group, eight of the
subjects were right-handed, and one subject ambidextrous. Seven of the
blind subjects were blind secondary to retinopathy of prematurity, one
had bilateral anophthalmia, and another had congenital glaucoma and
bilateral cataracts. None of the blind subjects had ever had object
vision and none had perception of light at time of scanning. All
subjects had normal neurological examinations, apart from their visual
deficits, and normal high-resolution brain MRI scans. None of the
subjects had any detectable auditory deficits or any history of
auditory disease.
Auditory localization. The practicalities of PET scanning
prevented auditory localization from being performed in a free-field situation. We, therefore, used sounds synthesized according to the
technique described by Wightman and Kistler (1989), which is based on
the assumption that if the acoustical waveforms arriving at both
eardrums are the same under headphone and free-field listening conditions, then the listener's acoustical experience should also be
the same (Wightman and Kistler, 1989). The technique requires simultaneous recording (from both ears) of sounds arriving from loudspeakers at several spatial positions in a free-sound-field using
miniature probe microphones inserted into the ear canals 1-2 mm from
the tympanic membrane. Intensity and phase transformations of sounds
recorded in the absence of the subject to those recorded from each
eardrum [the free-field-to-eardrum transfer function or head-related
transfer function (HRTF)] are incorporated into digital filters and
used for sound synthesis (Wightman and Kistler, 1989). We used
nonindividualized HRTFs (University of Wisconsin-Madison; Wenzel et
al., 1993), implemented in a Tucker-Davies Technologies (Gainesville,
FL) sound system to generate bandpassed bursts with a bandwidth of six
octaves and a center frequency of 2 kHz. These were calibrated
independently for each ear using a Brüel & Kjaer 1/2 inch
condenser microphone and sound level meter and presented binaurally via
well-fitting high-quality headphones (model HD 545; Sennheiser,
Oldlime, CT) at 25 dB above each subject's left and right
ear's sensation level threshold (average of three trials). The mean
threshold for all subjects was 10 dB SPL. Sounds were perceived as
coming from seven different directions ( 90, 60, 30, 0, +30, +60,
and +90°, where 0° is straight-ahead) within the azimuth in the
frontal interaural plane (at zero elevation). Stimulus duration was 500 msec, and interstimulus interval was 2 sec (i.e., ~40 trials per
task). Presentation of stimulus location was pseudorandomized balancing
right and left hemispaces in each task.
Experimental design. The paradigm consisted of four
conditions. Condition one was an unconstrained rest condition (R)
without sound delivered. Headphones were worn throughout and helped to reduce exposure to the ambient noise in the scanner room. Condition two
consisted of passive listening (PL) to intermittent sound with the same
characteristics as under active localization conditions three and four
but without varying binaural differences. Sound was thereby always
perceived as if coming from straight ahead or in some cases coming from
"inside their head." Subjects were requested to simply listen to
the sound and told that its location was of no significance. Conditions
three and four consisted of the randomized delivery of localized sound
from one of seven azimuth locations (+90, +60, +30, 0, 30, 60, and
90°), perceived in front of the subjects. Condition three
[auditory localization (AL)] was a modified delayed matching task
whereby subjects successively had to make a same/different
discrimination of each sound direction with that of the preceding
sound. In condition four [auditory localization with movement (AM)]
subjects were asked to immediately move the joystick with the right
hand to indicate the stimulus direction.
Behavioral data of the accuracy of auditory localization were
determined before and during scanning by a comparison of the direction
of sound produced by the sound system with the direction to which the
subject moved the joystick. Before scanning each subject underwent 10 trials, each consisting of 72 consecutively presented sounds to
determine a prescanning mean angular error for each subject. Similar
data were collected for each subject during condition four of the PET
experiment. Subjects were requested not to make eye movements to the
perceived sound location. Initially during training, subjects made
saccadic eye movements to the perceived direction of the sound, but
after a short time subjects stopped making such eye movements. To
further document eye movements during auditory localization, horizontal
electro-oculograms (EOGs) were recorded for three subjects after their
PET scans (outside of the scanner). Saccadic eye movements were not
detected in EOG recordings during the localization tasks in any of
these subjects.
Scanning details and data acquisition. Each subject
underwent eight sequential rCBF PET scans, two scans for each
condition, in a randomized order, using the tracer
H215O. Scans were
obtained using a Scanditronix PC 2048-15b PET camera with data
acquired in two-dimensional (2-D) mode. The axial field of view of the
scanner is 9.75 cm with an in-plane resolution at the center of the
field of view of 6.1 mm. For each scan, a bolus intravenous injection
of 37.5 mCi of H215O in
6-8 cc of normal saline was administered. After an ~20 sec delay,
emission data were acquired in a 60 sec time frame, with an interval of
10 min between each successive
H215O administration.
Subjects were positioned within the scanner so that the lowermost
detectors covered the most inferior temporal regions. A 10 min
transmission scan using rotating rods of
68Ge/68Ga was
performed for attenuation correction before the rCBF scans and used to
reconstruct a 2-D attenuation map. The attenuation-corrected emission
data were reconstructed as 15 contiguous axial planes of slice
thickness 6.5 mm. The reconstructed image planes contained 128 × 128 pixels, each measuring 2.09 × 2.09 mm.
Data analysis. All calculations and image manipulations were
performed on Sun SPARC computers using Analyze version 7.1 image display software (BRU; Mayo Foundation) and Matlab (MathWorks, Natick, MA). Data analysis was performed using statistical parametric mapping (SPM95; Functional Imaging Laboratory, Queen Square, London, UK) (Friston, 1995) and "in-house" correlation programs written in Matlab.
To correct for any head movement between scans, all head images were
aligned on a voxel-by-voxel basis using a three-dimensional automated
image registration algorithm (Woods et al., 1992). The intercommissural
(AC-PC) line was identified, and the volume was transformed into
standard stereotactic space (Talairach and Tournoux, 1988). Each
image was smoothed with an isotropic Gaussian filter of 12 mm to
increase the signal-to-noise ratio. Further data processing was
performed separately for the subtraction and correlation analyses and
is described below.
Subtraction analysis. The SPM analysis is an implementation
of the General Linear Model of statistics (Winer, 1971; Friston, 1995),
equivalent to an ANOVA applied on a voxel-by-voxel basis, in
which global activity and subject variability are confounding effects,
and the task effect is the parameter of interest. The model was applied
on a single-subject basis, and the images were scaled to a global mean
rCBF of 50 ml per 100 mg/min. The resulting set of voxel values for
each contrast constitute a statistical parametric map of the
t statistic SPM{t}. The SPM{t}
values were transformed to the unit normal distribution
(SPM{Z}) and thresholded at Z > 3.09 (equivalent to an uncorrected p value > 0.001). The resulting foci were then characterized in terms of peak height with a
Bonferroni-like correction for the number of independent voxels giving
a final Z score for peak height significance of >4.2. We
performed three groups of contrasts: group 1 consisted of three
within-group comparisons in the blind subjects: (1) passive listening
versus rest (PL-R), (2) delayed matching auditory localization versus
rest (AL-R), and (3) auditory localization with joystick movements
versus rest (AM-R). Groups 2 and 3 comprised between-group comparisons
of the same three contrasts (PL-R, AL-R, and AM-R), revealing areas of
relatively increased rCBF in the blind subjects and regions of
relatively increased rCBF in the sighted subjects.
Correlation analysis. We used an analytical technique that
assesses the within-task, across-subject, inter-regional correlations with a specified reference region (Horwitz, 1994). We chose six, a
priori, reference regions from the within-group analysis of the control
group data: that of a left and right primary auditory region [Brodmann
areas (BA) 41/42], nonprimary auditory "association" cortex within
the superior temporal gyri (BA 22), and the inferior parietal lobules
(BA 40; Bushara et al., 1999; Weeks et al., 1999).
Standardized rCBF for each subject and each scan was evaluated as the
ratio of rCBF in each voxel to global CBF. For each subject, the
relationship between standardized rCBF in a reference voxel and
standardized rCBF in all other brain voxels was calculated. The
strength of the inter-regional relationship was assessed by an
across-subject correlation, a high correlation coefficient indicating
that a region is likely to be functionally connected with the reference
region. The inherent assumption in this technique is that a homogenous
group of subjects use a similar regional network for a task, but that
each subject performs the task with a different level of rCBF change
whether that be a hemodynamic effect or related to attention or task
difficulty. The resulting subject-to-subject variation results in
strong covariances in activity between the nodes of the network.
Thresholds of significance for the within-group correlations were set
at p < 0.01 and displayed as statistical maps in
standard stereotactic space. To allow statistical comparisons between
the correlations in the sighted and blind subjects, the correlation
maps were converted into a Gaussianized data set by a Fisher
transformation followed by conventional univariate statistics to
calculate Z scores. Data from the between-group comparison
of correlation maps were considered significant if Z scores
were >4.0. These data were then displayed in another statistical map
showing regions of significant difference between the correlation maps
of the sighted and blind subjects. Subjects performed each condition
twice and within-task correlations were corrected for the
nonindependence of the two data sets from each subject (Horwitz et al.,
1998).
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RESULTS |
The behavioral data collected before scanning showed a mean
angular error during auditory localization with joystick movements of
23.8° (SD, 4.4) in the sighted subjects and 22.2° (SD, 4.3) in the
blind subjects. During scanning the mean error was 21.1° (SD, 1.9) in
the sighted subjects and 21.6° (SD, 4.5) in the blind subjects. There
were no significant differences between the blind and sighted cohorts
in terms of angular error.
Subtraction analysis
Tables 1-3 list the within-group comparisons in the sighted and
blind cohorts. The data from the sighted subjects have been documented
fully in a previous paper (Weeks et al., 1999) and will only be
discussed in relation to the data from the blind subjects.
Table 1 lists the areas of activation in
the passive listening versus rest comparison in sighted and blind
subjects. In general, levels of activation were not high in this
comparison in either of the studied cohorts. Because of interest in
superior temporal gyral activation, we have listed all peaks of
activation in this area irrespective of significance levels.
In Table 2 are listed the results of the
within-group comparison of the auditory localization and delayed
matching task compared to rest in the two cohorts. The blind subjects
activated a number of areas in this task, including right inferior
parietal lobule (IPL; BA 40), bilateral parieto-occipital cortex (BA
19), right dorsal occipital cortex (BA 18), right dorsal and ventral
premotor areas (BA 6), and a right prefrontal area (BA 46). The areas
of activation in the blind subjects for the within-group comparison AL-R are illustrated in Figure
1A. The sighted
subjects activated bilateral IPL (BA 40), left auditory association
cortex (BA 22), right inferior temporal cortex (BA 20), and areas in
the right prefrontal cortex (BA 11 and 9/46). The sighted subjects did
not activate parieto-occipital cortex or dorsal occipital visual
association areas.
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Figure 1.
Statistical parametric maps of increased regional
cerebral blood flow in the blind subjects compared to rest. All areas
shown are significant at Z > 4.2 after Bonferroni
correction for multiple comparisons (see "Subtraction analysis" in
Materials and Methods). A illustrates the within-group
comparison of auditory localization and delayed-matching compared to
rest, and B shows the comparison of auditory
localization with movement versus rest.
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Table 3 documents the results of the
within-group comparison of auditory localization with joystick movement
against rest. The blind subjects activated bilateral IPL (BA 40),
bilateral parieto-occipital areas (BA 19), contralateral (to the moving hand) sensorimotor cortex (BA 1, 2, 3, and 4) and anterior cingulate cortex (BA 24), and bilateral cerebellar hemispheres and ipsilateral ventral premotor areas (BA 6). The sighted subjects activated bilateral
IPL (BA 40) and movement-related areas in similar locations to the
blind cohort but did not activate parieto-occipital cortices. The areas
of activation in the blind subjects for the within-group comparison
AM-R are illustrated in Figure 1B.
Table 4 lists the results of the
between-group contrasts showing regions of relatively increased
activation in the blind and in the sighted cohort. There were no
significant between-group differences, either increases in blind or
sighted subjects, in the PL-R comparison. The regions of increased
activation in the blind in the AL-R task are listed in Table
4a and in the AM-R task in Table 4b. The results
of both contrasts indicate two regions of statistically increased
activation in the blind subjects both in the right occipital cortex,
one situated in the dorsal occipital cortex (comprising parts of BA 18 and 19) and another in the ventral occipital cortex (BA 19). The
normalized rCBF values for each task show that the changes are a
composite of a deactivation in the sighted subjects of ~2-3% of the
initial resting rCBF value and an additional 5-6% increase in rCBF in
the blind subjects, when compared to the initial resting rCBF level.
The data from Table 4a, showing relatively increased
activation in the blind cohort in the AL-R contrast, are illustrated in
Figure 2A (the results
listed in Table 4b are very similar and are not
illustrated).
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Figure 2.
Statistical parametric maps from the between-group
contrasts showing regions of relatively increased activation in the
blind and regions of enhanced activation in the sighted cohort.
A shows relatively increased activation in the blind
cohort compared to the sighted in the auditory localization and delayed
matching compared to rest contrast. The rCBF increases in the sighted
subjects compared to the blind in the same task are shown in
B.
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The rCBF increases in the sighted subjects compared to the blind in the
AL-R task are listed in Table 4c and illustrated in Figure
2B. The sighted subjects had relatively increased
activation during the AL task in left inferior temporal areas (BA 20).
The area of activation extends superiorly into posterior parietal areas
with separate subpeaks in this region, but none of them reached
significance. There were no areas of relatively increased activation in
the sighted cohort in the AM-R contrast.
Correlation analysis
Six reference regions were chosen, as described in Materials and
Methods. The results for the within-condition, inter-regional correlations for the right and left IPL reference regions in the delayed-matching auditory localization condition (AL-R) are shown in
Tables 5 and
6. The tables indicate the significant
(p < 0.01) positive and negative correlations
for blind and sighted subjects and any significant differences between
the inter-regional correlation maps of the two cohorts.
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Table 5.
Local maxima in occipital and temporal lobes for regional
correlations of standardized rCBF during auditory localization for a
reference voxel in the right inferior parietal lobule (Talairach
coordinates: 42, 48, 32)
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Table 6.
Local maxima in occipital and temporal lobes for regional
correlations of standardized rCBF during auditory localization for a
reference voxel in the left inferior parietal lobule (Talairach
coordinates: 42, 48, 36).
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When the right IPL was used as the reference region in the sighted
subjects, there were highly significant positive correlations with
right auditory cortex (BA 41/42) and left IPL (BA 40) and negative
correlations with bilateral dorsal occipital (BA 18), left peristriate
cortex (BA 18), right ventral occipital cortex (BA 18), and two regions
in the right inferior temporal cortex (BA 20/37). The same reference
region in the blind subjects revealed positive correlations with right
superior temporal gyrus (BA 42), right inferior and middle temporal
cortex (BA 20 and 21), left IPL (BA 40), right parieto-occipital (BA
7/19), right dorsal occipital (BA 19), right peristriate cortex (BA 18)
and two areas in ventral occipital cortex (BA 19) without any
significant negative inter-regional correlations. The comparison
between the two sets of correlations revealed that in the blind
subjects there were significantly greater inter-regional correlations
than the sighted subjects between the right IPL and the right
parieto-occipital (BA 7/19), right ventral and dorsal occipital (BA
19), right peristriate (BA 18), and right superior and inferior
temporal cortices (BA 20 and 22). There were no significantly increased
inter-regional correlations in the sighted cohort compared to the blind subjects.
The inter-regional correlations for the right IPL region are
illustrated as statistical maps in standard stereotactic space in
Figure 3A-C.
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Figure 3.
Inter-regional correlations for the right IPL
region (Talairach coordinates, 42, 48, 32) in the delayed-matching
auditory-localization condition for sighted (A)
and blind (B) subjects. Correlations are
displayed as statistical maps in standard stereotactic space
(left side of the image corresponds to the left side of
the brain). The values of the correlation coefficients are given by a
gray scale, with positive correlations in white and
negative correlations in black; significant positive
correlations (p < 0.01) are shown in
red, and significant negative correlations are shown in
blue. Nine representative horizontal sections are shown,
from left to right, at 16, 12, 8, 4, 0, 4, 8, 12, and 16 mm
relative to the AC-PC line, covering the majority of the occipital
lobe. C shows regions with significantly different
correlation coefficients (p < 0.05) between
the sighted and blind cohorts. Correlations significantly larger in
sighted subjects are displayed in red, and those greater
in blind subjects are displayed in yellow.
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When the left IPL was used as the reference region, the sighted
subjects had positive correlations with left superior temporal gyrus
(STG) (BA 22), right STG (BA 41/42), and right IPL (BA 40). There were
negative correlations with bilateral parieto-occipital (BA 7/19), left
ventral occipital areas (BA 19), and middle temporal gyrus (BA 21). In
the blind subjects, left IPL was positively correlated with right IPL
(BA 40) and two areas in the right STG (BA 41/42 and 22) and negatively
correlated with left parieto-occipital (BA 7/19), left peristriate (BA
18), and left dorsal occipital cortex (BA 18). When the two sets of
inter-regional correlations were compared, in the blind subjects, there
were greater positive correlations between the left IPL and two regions
in the right STG (BA 42 and 22) and a region in the right fusiform
gyrus (BA 19). There were no areas with significantly increased
inter-regional correlations in the sighted cohort compared to the blind
subjects for the left IPL reference region. The correlation maps
for the auditory localization and joystick movements condition (AM-R) revealed a very similar pattern of inter-regional correlations to that
discussed above for both IPL foci.
We also placed reference regions in superior temporal areas whose
location were identified from the subtraction analysis in the sighted
subjects. The results showed positive correlations withcontralateral
STG and posterior parietal areas but not with other cortical regions.
There were no significant differences between the inter-regional
correlations of the sighted and blind cohorts for reference regions in STG.
After the results of the subtraction and correlation analysis revealed
extensive occipital activation in the congenitally blind subjects, we
placed another reference region in right occipital cortex. Using this
reference region there were significant negative correlations with IPL
regions in the sighted subjects and positive correlations with the
right IPL in the blind subjects. However, apart from these regions
there were very few other significant areas of inter-regional
correlation, and the analysis did not add further information to that
provided already.
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DISCUSSION |
The behavioral data collected during PET scanning show
that the sighted and blind cohorts perform similarly, in terms of
angular errors, during the auditory localization task with joystick
movement (AM), and thus performance differences cannot readily explain any differences in the activation patterns of the two cohorts. Because
of the use of nonindividualized HRTFs the mean errors in localization,
as measured by joystick movements, are relatively large in both groups.
However, the size of the localization errors is smaller than the
angular distance between the (virtual) sound sources and, therefore,
does not impact on the interpretation of our data. Eye movements are
also unlikely to be a confounding factor, because electro-oculographic
recordings clearly showed that after a period of training subjects did
not make such movements. Furthermore, even if subjects had only learned
to suppress their overt eye movements while still making eye movement
plans, this should not influence activation in parietal cortex, because
neuronal responses in this brain region are independent of the
intention to perform specific motor acts (Colby and Goldberg, 1999).
Congenitally blind subjects, in particular, are unlikely to perform
many more eye movements that could explain the increased activation in
parietal and occipital cortex found in our study.
In both sighted and blind subjects, the PL task evoked only modest
bilateral activation of primary and secondary auditory areas in the STG
compared to the R condition, as evident from lower levels of
significance (Table 1). Similar lack of STG activation during PL has
been reported in other auditory imaging studies (Griffiths and Brown,
1991; Grady et al., 1997). The reason for this is unclear but
may be related to the stimulus specificity of neurons in the STG, for
which broad-band noise bursts, as used here, are not the optimal
stimuli (Rauschecker et al., 1995). Alternatively, the apparent lack of
STG activation in the PL-R comparison could be attributable to STG
activation in the unconstrained "rest" state.
Highly significant STG activation was also not a striking feature in
the other contrasts (Tables 2, 3). However, during both experimental
tasks that required auditory localization (AL and AM) the correlation
analysis identified regions within the STG as highly correlated with
the posterior parietal reference region. This suggests that during the
AL and AM tasks, areas in the STG are important components of a
functional network for the localization of sounds but that overall
activation levels in the STG, at least when measured against a rest
state, may not necessarily be high.
The between-group contrasts of AL-R and AM-R both identified two
regions of increased activation in the blind subjects, one situated in
dorsal right occipital cortex (Talairach coordinates 20, 84, 12, and
22, 76, 24 for the AL-R and AM-R contrasts, respectively) and another
in lateral ventral right occipital cortex (Talairach coordinates 34, 76, 0 and 40, 68, 4 for the AL-R and AM-R contrasts,
respectively). There were no significant differences in activation
between the sighted and blind cohorts in the PL-R task. This indicates
that the increased occipital activation of blind subjects in the AL and
AM conditions is task-related and dependent on additional processing of
auditory spatial information.
Correlation analysis provides further information regarding the
function of the right occipital cortex during auditory localization in
the blind. Activity in the right posterior parietal region was
positively correlated with right occipital cortex in the blind subjects
and negatively correlated in the sighted subjects. The between-group
differences in the inter-regional correlations between IPL and right
occipital cortex were highly significant. This confirms that in the
blind a major reorganization of pathways has taken place between the
right occipital area and the right IPL region (the two becoming
functionally connected to each other) and demonstrates that the right
occipital cortex in the blind has become part of the functional network
for auditory localization. This constitutes important additional
information, as regional activation alone, in terms of increased
activity relative to a control state, does not necessarily indicate
functional involvement in a task, and could theoretically represent
processes not under experimental control or incidental to the
experimental task (Horwitz and McIntosh, 1993).
It seems, therefore, that during auditory localization the congenitally
blind subjects recruit extrastriate occipital areas normally used for
visual processing, and thus they demonstrate visual-auditory
cross-modal plasticity. Such recruitment of additional cortical areas
for auditory localization in the blind may provide a neural basis for
the corresponding behavioral improvement reported in congenitally blind
humans (Muchnik et al., 1991; Lessard et al., 1998; Röder et al.,
1999) and in visually deprived experimental animals (Rauschecker and
Kniepert, 1994; King and Parsons, 1999). Extensive reorganization of
the occipital cortex during an early period of life (Cohen et al.,
1999), which cannot be reversed later, may also help to explain why
congenitally blind humans and experimental animals who regain their
sight later in life may not regain their vision even after years of
training (von Senden, 1932; Hubel and Wiesel, 1970; Jay et al., 1987).
Cross-modal cortical reorganization has also been demonstrated by
neuroimaging studies in deaf subjects (Levänen et al., 1998;
Neville et al., 1998).
Inspection of the activation patterns in the AL-R and AM-R within-group
comparisons in the blind subjects indicate that the peaks of right IPL
activation are shifted posteriorly, compared to the sighted controls (8 and 16 mm for the AL-R and AM-R comparisons, respectively), and that
the blind subjects activate a large area of cortex extending
posteriorly from the IPL region, including parieto-occipital and dorsal
occipital regions. Conventional subtraction analysis is insensitive
toward detecting shifts in peak activation and consequently, in the
blind versus sighted between-group comparisons of the AL-R and AM-R
contrasts, there were no significant differences in activation in the
right IPL and right parieto-occipital regions. However, the correlation
method clearly showed that inter-regional correlations between the
right IPL and parieto-occipital regions in the blind were significantly
different to those in sighted subjects, whereas correlations between
reference regions in STG and occipital areas were not significant. This
may tentatively be interpreted in the sense that auditory information
from the STG reaches the occipital areas only indirectly via the IPL region.
The two foci of enhanced right occipital activation in the congenitally
blind are in a similar location as those reported in PET studies of
visual spatial (Talairach coordinates 24, 76, 24) (Haxby et al.,
1994) and visual motion processing (Talairach coordinates 40, 68, 0)
(Watson et al., 1993) in sighted subjects. The similarity between the
foci of occipital activation during visual spatial processing in
sighted subjects and auditory localization in the blind suggests that
in the latter these extrastriate areas retain a similar functional role
and similar principles of neuronal coding, albeit in a different modality.
Auditory areas in the posterior parietal cortex have previously been
shown to be involved in the spatial processing of sounds (Griffiths et
al., 1998; Bushara et al., 1999; Weeks et al., 1999) and are thought to
be part of a dorsal stream in auditory processing (Rauschecker, 1998;
Romanski et al., 1999), analogous to the dorsal stream in visual
spatial processing (Ungerleider and Mishkin, 1982; DeYoe and Van Essen,
1988; Haxby et al., 1994). It is conceivable that during a sensitive
period of early postnatal development extensive remodeling occurs in
the blind via a succession of local synaptic changes beginning in
posterior parietal cortex and linking IPL with parieto-occipital,
dorsal occipital cortex, and other extrastriate areas. In support of
cross-modal plasticity of parietal cortex, auditory responses in
parietal areas of nonhuman primates seem to depend on experience and
training (Stricanne et al., 1996; Grunewald et al., 1999). In cats
visually deprived from birth, visual areas in the anterior ectosylvian
sulcus (possibly the cat's homolog of parietal cortex in primates) are
taken over by auditory input (Rauschecker and Korte, 1993). It has been
suggested that such cortical plasticity is caused by cross-modal
competition for synaptic space on target neurons of multimodal
association cortex and is implemented via Hebbian changes of synaptic
efficacy (Hebb, 1949; Rauschecker, 1995).
We have shown an exaggerated right hemispheric dominance in the
congenitally blind subjects, not only for occipital but also parietal
and temporal regions. An indication of this was given in the
subtraction analysis when greater activation of left temporal and
parietal areas was observed in sighted compared to blind subjects in
the AL-R contrast (Table 4c). This was even more clearly
shown in the correlation data, where the left IPL in blind subjects has
functional connectivity with right temporal and parietal areas without
significant correlation with regions in the left STG. The blind
subjects also had positive correlations between the right IPL reference
region and right midtemporal and inferior temporal regions, whereas in
sighted subjects the inferior temporal areas were negatively correlated
with the IPL foci. This suggests that the right midtemporal and
inferior temporal gyri in the blind subjects participate in the
circuitry for auditory localization in the blind. In sighted subjects,
the right hemisphere has for a long time been recognized to have a
greater role in the processing of spatial information (Critchley,
1953). Lesions of the right posterior parietal region in humans have a
predilection for causing deficits of auditory spatial processing
(Heilman and Valenstein, 1972). In blind subjects, exocentric space is
dominated by the auditory modality and may, therefore, involve a
greater internal construct of external space than in sighted subjects
(Thinus-Blanc and Gaunet, 1997).
| |
FOOTNOTES |
Received Oct. 18, 1999; revised Jan. 20, 2000; accepted Jan. 21, 2000.
This work was supported by National Institutes of Health Grant
R01-DC03489 (J.P.R.), Department of Defense Grant DAMD17-93-V-3018 (J.P.R.), and the National Institute of Neurological Diseases and
Stroke Intramural Research Program.
Correspondence should be addressed to Josef P. Rauschecker, Institute
for Cognitive and Computational Sciences, Georgetown University Medical
Center, WP15 NRB, 3970 Reservoir Road, NW, Washington, DC 20007. E-mail: rauscheckerj{at}giccs.georgetown.edu.
| |
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TOP
ABSTRACT
INTRODUCTION
