1Wellcome Department of Cognitive Neurology, Institute of Neurology, University College London, London WC1N 3BG; and 2Department of Psychology, Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom
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ABSTRACT |
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Macaluso, Emiliano, Chris Frith, and Jon Driver. Selective Spatial Attention in Vision and Touch: Unimodal and Multimodal Mechanisms Revealed by PET. J. Neurophysiol. 83: 3062-3075, 2000. Two positron-emission tomography (PET) experiments explored the neural basis of selective spatial attention in vision and touch, testing for modality-specific versus multimodal activations due to attended side. In the first study, either light flashes or finger vibrations were presented bilaterally. Twelve healthy volunteers were scanned while sustaining covert attention on the left or right hemifield within each modality. The main effect for attending right minus left, across both modalities, revealed bimodal spatial attention effects in the left intraparietal sulcus and left occipitotemporal junction. Modality-specific attentional effects (again, for attending right vs. left) were found in the left superior occipital gyrus for vision, and left superior postcentral gyrus for touch. No significant activations were seen for attending left minus right. The second study presented only tactile stimuli, manipulating whether the eyes were open or closed, and including passive stimulation and rest baselines. The unimodal activation for tactile spatial attention in the left superior postcentral gyrus was replicated. The bimodal activation of the left intraparietal sulcus observed in the first study was now found for touch, but only when the eyes were open (hands visible), apparently confirming its multimodal nature. These results reveal mechanisms of sustained spatial attention operating at both modality-specific and multimodal levels.
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INTRODUCTION |
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Most research on selective attention has
considered only a single sensory modality at a time. However, in the
real word all of our different senses will typically be
stimulated simultaneously, so selective attention may need to be
coordinated across different modalities. Recent research has begun to
examine the possibility of crossmodal links in spatial attention. Many
such links have now been documented psychophysically (see Driver
and Spence 1998a,b for review). Here we present two functional
imaging studies that examine possible commonalties, and possible
differences, in the neural substrates for covert spatial selective
attention in vision and in touch.
Previous functional imaging experiments on spatial attention have been
concerned either with shifts in attention, or with sustained selective attention to one stream of relevant
stimuli in the presence of irrelevant stimuli elsewhere. Studies on
attention shifting emphasize control mechanisms of spatial attention,
by comparing conditions with active attentional shifts to those with none. Typically, such comparisons activate frontoparietal areas (Corbetta et al. 1993; Jonides et al.
1993
; Nobre et al. 1997
; Petersen et al.
1994
) and show some right-hemisphere dominance. By contrast,
functional imaging research on sustained spatial attention has
emphasized the modulatory effects of attention on sensory processing,
rather than the control processes that direct attention. Heinze
et al. (1994)
provides a typical example. Whereas fixating
centrally, subjects saw two concurrent rapid streams of visual symbols,
one in either visual field. They sustained attention either on the left
or on the right stream throughout a block, to detect repetition of
symbols in just that stream. Positron-emission tomography (PET) data
showed that when attention was sustained on the left hemifield,
activation increased in right fusiform gyrus. Conversely, attending
right during equivalent bilateral stimulation activated left fusiform gyrus.
This pattern of attentional modulations of sensory processing, within
apparently unimodal visual structures, has now been observed in many
visual sustained selective-attention tasks, using PET (e.g.,
Heinze et al. 1994), event-related potentials
(ERPs) (e.g., Mangun et al. 1993
) and functional
magnetic resonance imaging (fMRI) (e.g., Hillyard et al.
1997
). Indeed, several recent fMRI studies have suggested that
even primary visual cortex can be affected (Brefczynski and
DeYoe 1999
; Gandhi et al. 1999
; Somers et
al. 1999
). We turn now to consider any such effects of spatial attention on nonvisual modalities.
Effects of sustained selective attention in audition, and in touch
ERP (Woldorff and Hillyard 1991), magnetic
encephalographic recording (MEG) (Woldorff et al.
1993
), and PET (O'Leary et al. 1995
;
Tzourio et al. 1997
) experiments reveal that sustained
selective attention to sounds in one ear versus the other, during
dichotic stimulation, can produce enhanced activity in early
contralateral auditory areas. For touch, ERP measures reveal that
tactile evoked potentials can have greater amplitudes for stimulation
on an attended versus unattended hand (Desmedt and Robertson
1977
; Desmedt and Tomberg 1989
).
However, to our knowledge, no functional imaging experiment has
examined sustained spatial selective attention to one side versus the
other during bilateral tactile stimulation, analogously to
the Heinze et al. (1994)
prototypical visual
design. Kelley et al. (1993)
showed increased blood flow
velocity in the middle cerebral artery when subjects were engaged in a
tactile sorting task. However, the poor spatial resolution of their
Doppler imaging technique did not allow precise localization of the
brain areas involved. Pardo et al.'s (1991)
tactile PET
study activated right parietal and frontal lobes during a somatosensory
task but compared this only to a rest state without stimulation and did not present tactile distractors. Drevets et al. (1995)
observed deactivation of brain areas representing currently irrelevant parts of the body in a tactile PET study, but without stimulation, when
subjects merely expected to be touched at a particular place (see also
Roland 1981
). No PET study has examined selection
between concurrent tactile targets and distractors, analogous to that studied in previous imaging experiments on sustained spatial selective attention during bilateral visual (Heinze et al. 1994
),
or bilateral auditory stimulation (Tzourio et al. 1997
;
Woldorff and Hillyard 1991
). One aim of our
study was to do this for touch. A second aim was to look at any
crossmodal links between tactile and visual selective attention.
Crossmodal links in selective spatial attention
Recent psychophysical experiments reveal extensive crossmodal
links in spatial aspects of attention (see Driver and Spence 1998a,b for review). For example, Spence and Driver
(1996)
found that sustaining auditory attention toward one
hemispace leads to visual attention also being directed to that same
side; and vice versa. Eimer and Schroeger (1998)
reported complementary ERP results. Similar crossmodal links have been
found between visual and tactile attention. Spence et al., in
press) observed psychophysically that sustaining
tactile attention toward one hemispace induces visual attention to that
side, and vice versa. Such crossmodal links in spatial attention are
consistent with abundant electrophysiological evidence in monkeys and
cats. Multimodal links in spatial representation and attention have
been described within several structures, including inferior parietal
cortex (BA 7b) and intraparietal areas, the putamen, inferior premotor cortex (BA 6), plus the superior colliculus (Andersen et al.
1997
; Graziano and Gross 1998
; Stein et
al. 1993
).
There have been relatively few brain imaging studies of crossmodal
links in attention. Several studies examined activations when subjects
attended one modality versus another during multimodal stimulation
(Frith and Friston 1996; Roland 1982
).
However, this only addresses nonspatial selection of one
modality versus another (see Spence and Driver 1997b
),
not crossmodal links in spatially attending to one side
versus another. O'Leary et al. (1995)
reported a
multimodal brain imaging experiment on possible crossmodal links in
spatial attention between hearing and vision. Unfortunately, the
critical test for multimodal activations due to the spatial direction
of attention (i.e., a main effect of attending in one direction vs. the
other, regardless of the modality) was not reported.
Present experiments
No imaging study has as yet examined sustained spatial attention
to tactile targets on one side or the other of the body, during
bilateral tactile stimulation. Based on findings from previous spatial
attention studies within vision (e.g., Heinze et al.
1994), and within audition (e.g., Tzourio et al.
1997
), we expected that sustaining tactile spatial attention on
one side would produce stronger contralateral activation within areas
of cortex involved in tactile processing (e.g., the postcentral gyrus)
(Kaas 1983
).
Our second aim was to compare spatial effects of sustaining tactile attention on one side versus the other, against those for visual attention. In this way, we sought to identify any commonalities between the effects of selective spatial attention in the two modalities, implying multimodal mechanisms of attention. We also tested for any differences between spatial attention in vision and touch, consistent with unimodal aspects of attention. We compared covert attention to the left with attention to the right within touch; and likewise within vision. We tested for main effects of spatial attention that held regardless of modality; and also for interactions indicative of modality-specific spatial effects (i.e., found only for one modality). The bilateral stimuli were the same regardless of the side to which attention was directed, but in some blocks these stimuli were all tactile, whereas in others they were all visual (we chose to stimulate only a single modality at a time, so that there would be no ambiguity about which stimuli the participants were attending in any block, and also to allow a test of selective-attention effects specific to touch for the 1st time).
Our design was thus a 2 × 2 factorial (covert attention to left or right, in vision or touch). This allows tests for activations within and across modalities, caused by the side to which covert attention was directed.
We used PET rather than fMRI for the functional imaging, because this
allowed visual and tactile stimulation to be presented at the same
external locations in space, in a free-field situation with the hands
directly visible. The use of common locations across the modalities has
been shown psychophysically to be of considerable importance when
studying crossmodal links in spatial attention (e.g., Driver and
Spence 1998a,b
).
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METHODS |
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Subjects
Twelve volunteers participated in the first study (mean age, 32 yr; range, 23-51). In this study and also experiment 2, all were right-handed males. None had abnormal psychiatric or neurological history, or current medication. After receiving an explanation of the procedures, subjects gave written informed consent. The study was approved by the Ethics Committee of The National Hospital for Neurology and Neurosurgery. Permission to administer radioactivity was obtained from the Administration of Radioactive Substances Advisory Committee of the Department of Health, UK.
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EXPERIMENT 1 |
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Design
The first experiment was intended to have a 2 × 3 factorial design, but became a 2 × 2 design in practice. One factor was the attended hemifield: left or right. The second was the modality of current bilateral stimulation: vision versus touch (vs. audition). This gave a total of six conditions, with two replications each. However, auditory conditions were not analyzed, because the sounds were extremely hard to localize when in the scanner, thus compromising spatial attention during auditory blocks. Therefore only visual and tactile blocks were analyzed, reducing the experiment to a 2 × 2 design. Note that the bilateral stimulation was identical for attend-left and attend-right blocks within a modality, but that the modality of this bilateral stimulation changed between visual and tactile blocks. The four analyzed conditions will be referred to as vision-attend-left (VL), vision-attend-right (VR), touch-attend-left (TL), and touch-attend-right (TR). Their order was counterbalanced within and across subjects. Before each scan, the subject saw a message informing them about the upcoming condition e.g.,"Modality: VISION. Attend to: LEFT."
Stimuli
Subjects lay in the scanner with elbows bent through 70°, and
hands visible, each resting on a wooden support 25° of visual angle
from the midline. A computer screen was located centrally between the
two supports. Each support accommodated a red light-emitting diode
(LED; 1° of visual angle; luminance, 21.3 cd/m2), and a solenoid (12 V) for delivering
tactile stimulation. These stimuli, and their peripheral locations,
closely matched those used in previous psychophysical studies
demonstrating visual-tactile links in spatial attention (e.g.,
Driver and Spence 1998a,b
; Spence et al., in
press). The index finger of each hand was restrained over the
solenoid, and the LED on that side was placed as close as possible to
the finger. The room was dimly lit, such that the hands were visible.
Experimental stimulations were always bilateral: either flashing red
lights on both sides in the visual blocks, or 30-Hz vibrations (which
could not be heard) on both index fingers in the tactile blocks. Only
one modality was stimulated within each condition. Each block of
stimulation comprised a 2-min sequence of events, half of which were
single pulses (each 200 ms) with the other half double pulses (200 ms
on, 200 ms off, 200 ms on), and with one event on each side every
2 s. The order of single and double pulses was random and
independent in the two hemifields.
Task
Our experiment required a task where spatially selective attention could be directed to one side throughout a block of bilateral stimulation, in a similar manner regardless of which modality was stimulated. We wanted subjects to succeed in this selective attention task, to avoid contamination of the neural activations by error-related processes. The task chosen required subjects to attend to the stimuli in only one hemifield, to detect double pulses among single pulses. Double-pulse targets on the attended side required a verbal response (quickly saying "bip"). Single pulses on the attended side required no response, and likewise for all the distractor events on the unattended side (whether single or double pulses). Any false positive responses to double pulses on the irrelevant side would thus indicate a failure to sustain attention on just the relevant side. A small white cross was displayed centrally on the computer screen, and fixation was maintained on this throughout. A 10-min training session allowed familiarization with the task for each modality before the experiment.
Because stimulation was bilateral throughout each block, any effects of
attending left or right should reflect just the endogenous direction of
covert attention, and not involve any of the stimulus-driven influences
that may follow lateralized stimulation on just one side (e.g.,
"inhibition of return") (Posner et al. 1985). Such stimulus-driven influences should be equivalent across the conditions compared.
Monitoring of fixation
Eye position was monitored in two ways. For the first six subjects we used electrooculographical (EOG) recording. Silver-chloride electrodes were placed on the outer ocular canthi above and below the left eye, with the ground electrode placed above the right eye, to measure horizontal and vertical eye position. To calibrate regularly for any drift in EOG, immediately before and after each scan the fixation point moved to new positions for 500 ms, first at 6 and then at 12° eccentricity, alternately in the left or right visual field. Subjects followed these movements of the cross with their eyes. This allowed calibration of the straight-ahead position, and thus confirmation that no substantial drift in the EOG had taken place during the block. For the last six subjects, eye position was monitored with a charge-coupled device (CCD) camera instead, placed closely above the left eye. An infrared LED was directed at the eye to ensure a good image. This required less preparatory work but still ensured a good measure of eye position. All subjects adhered to the central fixation instruction satisfactorily, ensuring that only effects of covert attention should be found in the regional cerebral blood flow (rCBF) data.
MRI acquisition
Before or after the PET scanning session, each subject underwent a structural MRI scan. Images were acquired using a VISION scanner operating at 2 Tesla (Simens, Erlangen, Germany). The T1 MPRAGE sequence (TE = 4 ms, TR = 9.5 s, TI = 600 ms) gives a resolution of 1 × 1 × 1.5 mm.
Acquisition of rCBF data
PET scans were performed with a CTI EXACT HR+ (CTI, Knoxville,
TN) 32-slice scanner, with retracted collimating septa covering a field
of view of 15.5 cm. Subjects received an intravenous bolus of
H215O infused over 20 s,
followed by a 20-s saline flush. There were 12 successive
administrations of H215O, each
separated by 8 min. Images were reconstructed with a Hanning filter of
0.5, full width at half-maximum (FWHM) 6.5 mm. Data were acquired in a
90-s scan frame after injection of 8-10 mCi of
H215O. Each stimulation and task
condition began 20-30 s before image acquisition, and continued for 2 min. Total counts per voxel during the build-up phase of radioactivity
served as an estimate of rCBF (Fox and Mintun 1989;
Mazziotta et al. 1985
).
Analysis of rCBF data
To facilitate intersubject pooling, rCBF data were realigned,
spatially (stereotactically) normalized and smoothed. Scans of each
subject were realigned using the first as reference. The six parameters
(3 translations and 3 rotations) of this rigid body transformation were
estimated using a least-squares approach (Friston et al.
1995a). The structural MRI of each subject was coregistrated to
the mean PET image of the same subject. The coregistrated structural
images were transformed into the Montreal Neurological Institute (MNI)
standard space (Collins et al. 1994
), using 12 linear
and quadratic 3D transformations. Residual variance was corrected using
a set of smooth basis functions (Friston et al. 1995a
).
Normalization parameters were then applied to the PET images (because
of technical problems during structural MRI acquisition, in
experiment 2 functional PET images were normalized by
estimating parameters from the mean PET image of each subject). As a
final preprocessing step the images were smoothed using an isotropic Gaussian kernel (FWHM of 16 mm).
The data were analyzed using Statistical Parametric Mapping (SPM97d,
Wellcome Department of Cognitive Neurology) (Friston et al.
1995b). Condition, subject, and global flow effects were estimated according to the general linear model at each and every voxel. A blocked one-way ANCOVA had global activity as covariate of no
interest. To test hypotheses about regionally specific condition effects, the estimated effects were compared using linear compounds (contrasts). The resulting set of voxel values for each contrast constitutes a statistical parametric map of the t statistic
SPM{t}(with uncorrected P values). The SPM{t} values
were transformed into units of the normal distribution, SPM{Z}.
Because of the high number of voxels tested, the significance of each
region was estimated using distributional approximations from the
theory of Gaussian Fields to assign corrected P
values. This tests the probability that an activation, characterized by
peak height and spatial extent, could have occurred by chance. The
spatial extent of the activations for this calculation was first
determined by thresholding all SPM-maps at P
uncorrected = 0.001.
Additional a priori criteria for rCBF analysis
Our design sought to identify brain areas showing a differential activation when subjects attended one hemifield versus the other hemifield. We also wanted to distinguish areas showing this spatial effect within only one modality (unimodal effects), versus those showing a spatial effect independent from stimulated modality (multimodal effects). To differentiate between these two categories of spatial modulation, we adopted the following criteria (see Table 1 for an overview):
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MULTIMODAL EFFECTS. These areas were defined as areas showing a main effect of attended side, with all voxels in the cluster also showing a simple effect of attended side within both modalities (i.e., tactile and visual blocks). The SPM thresholds were set at P uncorrected = 0.001 for the primary contrast (main effect) and at P uncorrected = 0.05 for the additional contrasts (simple effects in touch and in vision). Correction for multiple comparisons (P corrected = 0.05) was then applied to the set of surviving voxels.
UNIMODAL EFFECTS. These areas were defined as areas showing a simple effect of attended side in just one modality, with all voxels within the activated cluster also showing an interaction between attended side and stimulated modality. As for the characterization of multimodal areas, the SPM thresholds were set at P uncorrected = 0.001 for the contrast of primary interest (here, simple effect within one modality) and at P uncorrected = 0.05 for the additional contrast (interaction). Correction for multiple comparisons (P corrected = 0.05) was applied to the set of surviving voxels. Finally, we checked that none of the voxels within the cluster showed any simple effect of attended side in the other modality, even at P uncorrected = 0.05.
These laborious definitions were chosen to ensure that multimodal areas did show spatial modulation during both tactile and visual blocks and that unimodal areas showed an effect of attended side within only one modality, with none in the other. Note that these multiple criteria can only make our analyses more conservative than the contrasts with which they begin (main effect for multimodal modulations, and simple effect for unimodal modulations). False negative results might therefore be more likely than false positives. ![]() |
RESULTS |
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Behavioral performance
The task was performed well, with accuracy above 97% for targets on the attended side, and negligible false alarms to double pulses on the unattended side, thus indicating adherence to the spatially selective requirements of the sustained attention task. For technical reasons, verbal reaction times (RTs) to the double-pulse targets in the attended hemifield were available for only six subjects. Means ± SE were 528 ± 40 ms for vision-left (VL), 531 ± 35 ms for VR, 541 ± 44 ms for TL, and 505 ± 46 ms for TR. A two-way within-subject ANOVA found no significant terms; RT did not differ reliably between vision and touch (P > 0.72), nor between attending left or right (P > 0.43), with no interaction (P > 0.18). Attending left or right, within vision or touch, thus appears well-matched for difficulty.
rCBF in relation to stimulated modality
ACTIVITY ASSOCIATED WITH PERFORMING THE TASK ON VISUAL STIMULATION. Comparing scans acquired during the spatial attention task for visual stimuli, versus the tactile scans (i.e., [VL + VR] > [TL + TR]), revealed areas of greater rCBF bilaterally in the medial occipital gyrus, the superior occipital gyrus and the superior parietal gyrus (see Table 2). The medial occipital activations were anteriorly located, extending to the posterior part of the inferior temporal gyri and the medial temporal gyri. The activations in the superior occipital gyri extended from the superior occipital sulci and gyri into the superior part of the medial occipital gyri. The activations associated with the visual task thus all fell within cortical areas that would be expected to be involved in low-level visual judgements such as those here.
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ACTIVITY ASSOCIATED WITH PERFORMING THE TASK ON TACTILE
STIMULATION.
The reverse comparison (i.e., [TL + TR] > [VL + VR]) showed
increased regional rCBF in three areas: the left and right parietal operculi (SII), extending into the inferior postcentral gyri, plus the
left superior postcentral gyrus (see Table 2). The latter activation
extended posteriorly to the left supramarginal gyrus, postcentral
sulcus, and intraparietal sulcus. Thus the activations associated with
the tactile task all fell within cortical areas previously associated
with somatosensory processing (Coghill et al. 1994;
Kaas 1983
). The greater extent of activations in the left hemisphere will be considered later.
Effects related to the spatial direction of covert attention
The bilateral stimulation was identical when attending left versus right, so any effect on rCBF must be due to the direction of endogenous attention. Using the criteria described earlier (Table 1), we tested for multimodal effects revealed by greater activity for attending one side versus the other, independent of modality. We also tested for unimodal effects, where an effect of attended side was present only for one modality. These analyses revealed three "multimodal attention" clusters, one "tactile attention only" cluster and one "visual attention only" cluster (with a subthreshold multimodal cluster nearby).
MULTIMODAL INFLUENCES OF SELECTIVE SPATIAL ATTENTION. All areas showing significant multimodal attentional modulation were found for the main effect of attending-right minus attending-left: [VR + TR] > [VL + TL], subject to the additional criteria described above (i.e., corresponding simple effects within each modality as well, i.e., both [TR > TL] and [VR > VL]). Surprisingly, no region showed higher rCBF for the reverse spatial comparisons (attending-left minus attending-right), in either modality, a consistent finding throughout this paper that is discussed later.
One multimodal attentional activation was at the interception of the left intraparietal sulcus with the left postcentral sulcus (see Fig. 1, top, and Table 3), contralateral to the attended right side. As shown in the rCBF plot for the maxima (Fig. 1, top), the effect of spatial attention (i.e., greater flow when attending right vs. left), was present irrespective of the stimulated modality, despite higher activation for touch overall. At the maxima for the main effect of attended side (x, y, z =
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UNIMODAL INFLUENCES OF SELECTIVE SPATIAL ATTENTION.
We tested for areas showing a simple effect of attending right minus
left within just one modality (i.e., TR > TL for touch, or
VR > VL for vision), in the presence of an interaction between stimulated modality and attended side (i.e., [TR TL] > [VR
VL] for areas showing attentional modulation only in
touch; and [VR
VL] > [TR
TL] for vision), and with
no simple effect of attended side in the other modality even at low
threshold. This revealed two activations (see bottom of
Table 3). One showed an effect of attended side only for touch, the
other only for vision (but with a subthreshold multimodal cluster
nearby). All activations were in the left hemisphere, contralateral to
the attended right side once again.
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DISCUSSION |
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Experiment 1 makes several new observations. It
provides the first functional imaging evidence that sustaining
selective spatial attention to one side versus the other can modulate
activations during bilateral tactile stimulation (i.e., with
concurrent targets and distractors). This extends previous findings on
selective attention in vision (e.g., Heinze et al. 1994)
and in audition (e.g., Tzourio et al. 1997
) to the
tactile modality. The contralateral selective attention effects in
somatosensory areas accord with recent findings in monkey
electrophysiology (Burton et al. 1997
).
Second, this study demonstrates that covert spatial attention to one side versus the other has both modality-specific and multimodal influences on brain activity, within distinct brain areas. Three multimodal areas showed higher flow when attending right versus left, irrespective of the stimulated modality (i.e., for both the visual and the tactile tasks). These were the left intraparietal sulcus, the left occipitotemporal junction, and the right inferior occipital gyrus (although the latter activation was unexpectedly ipsilateral to the attended side and did not replicate in experiment 2). Two "unimodal" areas showed higher flow when attending right but only for stimuli in one modality: the left superior postcentral gyrus for touch, and the left superior occipital gyrus for vision (although we observed a subthreshold multimodal cluster near the latter).
One may speculate that the multimodal influences of selective attention
on rCBF could provide a possible neural substrate for the crossmodal
links in spatial attention between vision and touch that Driver
and Spence (1998b) and Spence et al. (in press) have documented psychophysically. Although the multimodal activations were not found within primary sensory cortices, it is interesting to
note that they arose in areas that typically responded more strongly to
one modality than the other overall (the left intraparietal sulcus
responded more strongly for touch, whereas the left occipitotemporal junction responded more strongly for vision; see Fig. 1, top
and bottom). These activations might in principle reflect
influences of multimodal attention on primarily unimodal areas. This
would fit previous proposals (Driver and Spence 1998b
;
Spence et al., in press) that the direction of visual
attention can influence tactile responses, and vice versa.
However, it is possible that the multimodal influences of attention found here were due to each subject undergoing both the visual and the tactile task. Due to this experience, the tactile task might come to activate structures associated with the analogous visual task, and vice versa. A further possibility arises when one considers that even though only one modality was experimentally stimulated during each block, some degree of stimulation was in fact always present within both modalities. Because subjects had their eyes open throughout, their hands were always visible in the dimly lit room, providing continuous visual stimulation even during the tactile blocks. Equally, during the visual blocks, some limited tactile stimulation would have been continuously available due to each hand resting passively on its support. It is possible that the multimodal attentional influences may have been due to spatial attention affecting neural responses to continuous background stimulation in the environment, for the second modality in which there was currently no experimental stimulation.
These possibilities were all assessed in experiment 2, by comparing attending right versus left within touch, when subjects eyes were open (with hands visible) versus closed; and by exposing subjects only to the tactile task, to avoid associations with the analogous visual task. In addition, experiment 2 tested the replicability of our results for the tactile modality, which seemed worthwhile because experiment 1 is the first imaging study to address selection of one side versus another during bilateral tactile stimulation. Finally, the next study also tested the replicability of two unexpected patterns found in experiment 1: the unpredicted activation in the right inferior occipital gyrus, ipsilateral to the attended right side; and the surprising fact that all of the attentional activations were produced for attending right minus attending left, with none reaching significance for the reverse comparison.
One possible explanation for the lack of right-hemisphere
activations when attending left versus right is that this hemisphere may have been active both when attention was directed to the left and also when it was directed to the right (cf.
Kelley et al. 1993). The design of experiment
1 could not reveal any areas activated in common for attending
left and right. Experiment 2 added two low-level
baseline conditions, with no spatial attention requirements. Subtraction of these from the attentional conditions should reveal any
activations (e.g., in the right hemisphere) that are common for
attending left and right.
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EXPERIMENT 2 |
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Design
Six new subjects (mean age 25 yr, range 20-29) were tested in a 2 × 2 factorial design, plus two additional low-level baselines. One factor in the factorial design was the attended direction (left vs. right) as before, but now always with bilateral tactile stimulation. The second factor was the presence or absence of environmental visual input (eyes open with central fixation and hands visible vs. eyes closed). In addition there were two baseline conditions: passive bilateral somatosensory stimulation during central fixation and a rest condition (no stimulation, eyes closed). These six conditions will be referred to as follows: eyes open while attending left in touch (OTL); eyes open while attending right in touch (OTR); eyes closed while attending left in touch (CTL); eyes closed while attending right in touch (CTR); passive tactile stimulation with eyes open (P); and rest with no stimulation and eyes closed (R). All six conditions were replicated twice, with the order counterbalanced within and across subjects. Instructions about the upcoming condition were given verbally before each scan.
Comparing attentional conditions to the baselines should reveal any areas activated both when attending to the left or right. Comparisons with the baselines and can also test whether the left-hemisphere structures identified in experiment 1 are not only activated when attending right, but also de-activated when attending left. Comparing the eyes-open and eyes-closed tactile attention conditions should reveal any role of visual input (including sight of the hands) in the attentional modulations produced during tactile selection. Finally, if the areas showing multimodal attention effects in experiment 1 were only activated because subjects experienced both the tactile task and a closely related visual task, they should no longer be activated in the present study, because the new subjects only underwent the tactile task.
Stimuli
The position of the subject's hands was as in the first experiment. Experimental stimuli were now only somatosensory (i.e., the flashing visual LEDs were no longer used). The stimulus sequences were as for the tactile task in experiment 1. Indeed, the left-attention and right-attention conditions with eyes open (hands visible) were identical in every respect to that task. The eyes-closed conditions had the same somatosensory inputs and task, but now without any visual stimulation (e.g., no sight of the hands). In the passive stimulation condition, bilateral tactile stimulation again took place, but the subject had only to maintain central fixation, with no requirement to attend covertly toward one side or the other. In the rest condition, no stimulation was given: the subject simply lay in the scanner with eyes closed.
Tasks
During the attention conditions, subjects again had to detect targets (double pulses among nontarget single pulses) in the attended hemifield with a verbal response, while ignoring distractors (both single and double pulses) in the other hemifield, as in the first experiment. When the eyes were open, the subject had to maintain central fixation, monitored with the CCD camera as before. During the eyes-closed condition, eye position could not be assessed. The attention conditions were again practiced for 10 min before the experiment.
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RESULTS AND DISCUSSION |
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Behavioral performance
Accuracy was 98%, with negligible false positive to double pulses on the ignored side. RT data were available for four subjects. Means ± SE were 650 ± 31 ms for OTL, 638 ± 45 ms for OTR, 639 ± 40 ms for CTL, and 651 ± 45 ms for CTR. A two-way ANOVA found no significant terms; no difference when attending left versus right (P > 0.9), no effect of eyes open versus closed (P > 0.69), and no interaction (P > 0.21). Overall tactile RT was slower than in experiment 1, perhaps because an analogous task was no longer performed in vision.
Effects of spatially selective tactile attention on rCBF
Because after experiment 1 we had specific hypotheses for the location of any activations, we no longer corrected for multiple comparisons, but in all other respects criteria for significance were as before. Voxel level threshold was set at P-uncorrected and a cluster extent threshold of P-uncorrected = 0.05 was applied. As in experiment 1, no areas were activated for attending left minus attending right (which we discuss later). Once again, only the reverse subtraction revealed attentional modulations, and all were in the left hemisphere, contralateral to the attended right side.
SPATIAL ATTENTION EFFECTS APPLYING BOTH WITH EYES OPEN AND EYES CLOSED. As in the first experiment, we identified common activations due to one factor (attending right vs. left) across the levels of the other factor (in this case, eyes open vs. closed) by testing for a main effect of the former spatial factor (i.e., [OTR + CTR] > [OTL + CTL]), in the presence of two corresponding simple effects, here for attending right with both eyes open and eyes closed (i.e., [OTR > OTL] and [CTR > CTL]).
Only one area was activated by attending right minus attending left irrespective of whether the eyes were open or closed (Table 4; Fig. 3A). As expected after experiment 1, which found a purely tactile attentional modulation within the left postcentral gyrus, this new activation was also in left postcentral gyrus, in its anterior part. The maxima fell more medially than in experiment 1, but still within similar anatomic areas. The medial extension of the activation meant that it now included the left central sulcus (see Fig. 3A; and compare with Fig. 2A from experiment 1).
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EFFECTS OF TACTILE SPATIAL ATTENTION ONLY WITH EYES OPEN.
As for the first experiment, effects of one factor (attending
left vs. right), which applied only for one level of the
other factor (here eyes open or eyes closed), were determined by
testing for a simple effect of attended side (at a threshold of
P-uncorrected = 0.001) with eyes open or with eyes closed,
in the presence of an interaction (at P-uncorrected = 0.05),
plus a check that no simple effect was present for the other level of
eyes open/closed even at low threshold. No region showed attentional
modulation only with eyes closed. However, two regions showed increased
rCBF for attending right minus attending left only in the
eyes-open condition {i.e., passing both [OTR > OTL] and
[(OTR OTL) > (CTR
CTL)], whereas showing no
effect for [CTR > CTL]}. These areas were the left
intraparietal sulcus and the left superior occipital gyrus, both
contralateral to the attended right side once again (see Fig.
3B and Table 4), and both of which had also been activated in experiment 1. The rCBF plots for these two areas clearly
show that attentional modulation was present with eyes open (bar
1 vs. 2 in the histograms of Fig. 3B) but
not with eyes closed (bar 4 vs. 5).
Activations and deactivations in the left hemisphere
As can be seen for all the rCBF plots in Fig. 3, every area that showed modulation by spatial attention in experiment 2 also showed the following intriguing pattern. During the attend-right condition, activity was higher than both baselines; whereas activity was lower than both baselines when attending left. We tested the significance of this pattern by imposing the following multiple constraints: for eyes-open conditions ([OTR] > [P] and [P] > [OTL] and [OTR] > [R] and [R] > [OTL]), and for eyes-closed ([CTR] > [P] and [P] > [CTL] and [CTR] > [R] and [R] > [CTL]). The left intraparietal sulcus and the left superior occipital gyrus survived the first set of constraints (i.e., with eyes-open) when each contrast contributed to the multiple constraints at P = 0.05. Although the left superior postcentral gyrus showed a similar pattern with both eyes-open and eyes-closed, this did not pass our test, perhaps because of the excessive number of constraints.
Attentional tasks versus baseline controls
As already emphasized, one of the most surprising but consistent
observations across our tasks and experiments was that all the
attentional modulations found were for the contrast attending right
minus left, none for the reverse subtraction. With only one exception,
all these activations were in the left hemisphere, contralateral to the
attended right side. It seemed possible that the right hemisphere may
have failed to activate for the direct comparison of attending left
versus right because it may be involved in attending both
contralaterally and ipsilaterally (Corbetta et al. 1993;
Kelley et al. 1993
). Comparing the eyes-open attentional conditions (OTL, OTR) with the passive eyes-open stimulation baseline (P) in experiment 2 should reveal any area commonly
activated when attending left or right.
The contrast [OTL + OTR] > 2[P] showed numerous activations (see
Table 5), although some may relate to
producing and hearing the verbal response (which did not arise in the P
condition). Increased rCBF was found bilaterally in the cerebellum,
thalamus, superior temporal gyrus, putamen, globus pallidus, inferior
precentral sulcus gyrus, and also in the right inferior frontal gyrus.
Given previous evidence on the role of anterior right-hemisphere
structures in controlling spatial attention (Weintraub and
Mesulam 1987), the inferior frontal activation may reflect the
attentional demand of the task, rather than merely the verbal response.
Note that the contrast did not activate any of the superior frontal or
parietal areas that have been associated with attention
shifting (e.g., Corbetta et al. 1993
;
Nobre et al. 1997
), presumably because our task required
selective attention to be sustained on one side, rather than shifted
between locations.
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The reverse contrast (2[P] > [OTL + OTR]) showed bilateral
deactivation of occipitotemporoparietal junction when
attention was focused on the somatosensory task. The areas implicated
fell between the middle occipital gyrus, the inferior parietal lobe, and the posterior middle temporal gyrus: the left hemisphere maximum was at x, y, z = 38,
78, 32, with Z = 3.9, and the right hemisphere at x, y, z = 50,
82,
32, with Z = 5.0. The same areas continued to show
deactivation during the tactile task even when we compared the
eyes-open tactile attention conditions with eyes-closed rest (i.e., 2 × [R] > [OTL + OTR], with x, y, z =
38,
74, 36, Z = 4.6 in the left hemisphere, and
x, y, z = 46,
74, 28, Z = 5.6 in the
right hemisphere). Hence these regions, traditionally considered as
visual areas, were more active when subjects rested with eyes closed
than during the tactile attentional task when subjects had their eyes
open. This may be due to vision being suppressed when concentrating on
the tactile task (Kawashima et al. 1995
), although note
that Shulman et al. (1997)
have observed similar deactivations when comparing several active versus passive visual tasks, all with eyes open.
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GENERAL DISCUSSION |
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We tested for modality-specific and multimodal attentional modulations with two experiments. The first study used bilateral stimulation in either vision or touch. Subjects had to attend to the stream of stimuli in one hemifield while ignoring distractors in the other hemifield. PET data revealed several areas showing modulation due to the attended side, independently of the modality stimulated (multimodal effects; e.g., in the intraparietal sulcus). A further area was modulated only by the direction of tactile attention (in the postcentral gyrus), and another (in the superior occipital gyrus) by visual attention (albeit with a subthreshold multimodal activation nearby).
The second experiment tested whether the multimodal attentional activations depend on the presence of visual input (and sight of the hands) during the tactile task. The tactile task was repeated with eyes open versus closed. The results confirmed that the multimodal attentional activations in the intraparietal sulcus require visual input (which included sight of the hands) during tactile attention. By contrast, the unimodal effect for tactile attention in the postcentral gyrus, which had been shown in experiment 1, was replicated regardless of whether the eyes were open or closed.
Unimodal effects of sustained spatial attention
Previous experiments using either visual (e.g., Heinze et
al. 1994; Vandenberghe et al. 1997
) or
auditory (e.g., Tzourio et al. 1997
) bilateral
stimulation showed that selective attention to on one side modulates
contralateral representations in the brain, at relatively early stages
of sensory processing. Our experiments demonstrate for the first time
that attention can produce similar contralateral modulation during
bilateral stimulation within the human somatosensory system
also (albeit with an unexpected hemisphere asymmetry, discussed later).
Both experiments found this for attending right versus left within the
postcentral gyrus, an early somatosensory area. Our results thus extend
previous observations in nonhuman primates (Burton et al.
1997
; Hsiao et al. 1993
; Hyvaerinen et al. 1980
) and humans (Desmedt and Tomberg 1989
;
Drevets et al. 1995
; Roland 1981
),
suggesting that the somatosensory system can be endogenously modulated
at relatively early stages of processing. Experiment 2 further showed that modulation by tactile attention in the postcentral
gyrus does not depend on any visual input.
During the bilateral visual stimulation we observed
contralateral attentional modulation of two distinct extrastriate
areas: a lateral occipitotemporal cluster, close to an area recently activated during similar visuospatial selective attentional tasks (Hillyard et al. 1997; Mangun et al.
1998
), plus a more dorsal area. Unlike Heinze et al.
(1994)
and Vandenberghe et al. (1997)
, we did
not observe activations in the fusiform gyrus, but those studies used
shape stimuli that are more likely to activate the ventral visual
stream. Our stimuli were small lights placed near the hands, as in
previous psychophysical studies of tactile-visual links in attention
(e.g., Driver and Spence 1998a
,b
). The fact that dorsal
and lateral occipital areas showed attentional modulation, rather than
ventral areas (or primary visual cortex), may be due to the use of such
stimuli, which were chosen to emphasize the spatial (peri-personal)
properties of the visual stimuli placed by the hands, rather than their form.
Multimodal effects of sustained spatial attention
The central aim of experiment 1 was to identify brain
areas showing modulation by the direction of spatial attention (left or
right) independently of the stimulated modality. Such areas may be good
candidates for representing space across modalities (Andersen et
al. 1997; Graziano and Gross 1998
), as already
suggested by single-cell findings for regions in monkey intraparietal
sulcus (Graziano and Gross 1993
). Multimodal attentional
activations were indeed found in human intraparietal sulcus, for both
experiments. The possibility of learned, artificial associations
between analogous tactile and visual tasks seems unlikely to explain
this multimodal intraparietal activation, because only the tactile task
was experienced by the subjects of experiment 2.
Single-cell recordings from monkeys in and around the intraparietal
sulcus have revealed multimodal units, typically with corresponding
spatial receptive fields across different modalities (e.g.,
Andersen et al. 1997; Colby and Duhamel
1991
; Graziano and Gross 1993
; Snyder et
al. 1998
). Further single-cell studies indicate that areas
around the intraparietal sulcus are also involved in spatial attention
(e.g., Bushnell et al. 1981
; Robinson et al.
1995
). Moreover, previous functional imaging (Corbetta
et al. 1993
; Nobre et al. 1997
;
Wojciulik and Kanwisher 1999
) and neuropsychology
(Posner et al. 1984
) in humans agrees with this, at
least for the case of visual attention.
The results of experiment 1 appear to confirm the multimodal
nature of spatial representation in the human intraparietal sulcus, and
the influence of attention on it. Stronger activation when attending
right versus left was found regardless of the stimulated modality. This
attentional modulation was replicated in experiment 2, which
used only the tactile task, but the effect of attended tactile side was
now observed only in the eyes-open conditions. By contrast, the purely
tactile attentional modulations in the postcentral gyrus were observed
regardless of whether eyes were open versus closed. Visuotactile links
that depend on sight of the hand have previously been demonstrated
physiologically (Graziano and Gross 1993) in monkey
areas 7b and VIP. Moreover, Ladavas et al. (1998)
recently reported a group of right-hemisphere patients, with lesions
centered on the parietal lobe, whose attentional deficits in touch
could be modulated by visual stimulation near the hands, provided the
hands were visible. Taken together, these findings accord with the
present observations, in suggesting that intraparietal regions may
provide spatial representations that incorporate both tactile and
visual information in an integrated manner and can be modulated by
spatial attention.
Hemispheric asymmetries
One surprising but consistent finding was that significant attentional modulations were observed only for attending right minus left, primarily within the left hemisphere. Unexpectedly, no right-hemisphere activations were observed for attending left versus right. This pattern was replicated in four entirely separate datasets (i.e., for both the visual and the tactile blocks in experiment 1; and for both eyes-open and eyes-closed blocks in experiment 2). However, finding a reliable effect in one hemisphere but not the other does not of course guarantee that there is a reliable difference between hemispheres; for instance, the right hemisphere might conceivably show a pattern below our threshold, which did not reach significance due to lack of power. To assess this, we carried out a further analysis comparing the attentional effects in the two hemispheres directly. This showed that the contralateral attentional modulations in the left-hemisphere were significantly greater than any subthreshold trends that might have existed in symmetrical right-hemisphere regions. We assessed this with paired t-tests comparing the magnitude of contralateral attentional modulations in the two hemispheres. These attentional modulations correspond to the difference in brain activity when attending contralaterally minus ipsilaterally. These modulations were compared for the maxima in the left hemisphere, versus the voxel showing the largest contralateral effect in the right hemisphere within a 14-mm cubic search region (chosen to match the smoothing) centered symmetrically with respect to the left-hemisphere maxima. These tests confirmed that all regions for which we reported left-hemisphere attentional modulations in experiments 1 and 2 showed stronger modulation for that hemisphere than in the right hemisphere. This between-hemisphere difference was reliable for five of the seven areas (at P < 0.05 or better), the exceptions being the occipital clusters in experiment 1. The ability to detect significant interactions between attentional modulations and hemispheres provides qualitative indication that the lack of spatial modulation in the right hemisphere was not merely due to lack of power.
It is possible that both hemisphere might have shown modulation by
attention to the contralateral side, if a more demanding task had been
used. However, mere task difficulty seems unable to explain why the
left-hemisphere modulations were significantly larger than any trends
in the right hemisphere. One possible explanation for this unexpected
lateralized pattern could be that right-hemisphere structures are
active both when attending left and attending right (cf.
Corbetta et al. 1993; Kelley et al. 1993
;
Weintraub and Mesulam 1987
) and therefore do not show
any effect of attended side. Activations for selectively attending to
one side, regardless of direction, should be revealed by the comparison
between attentive task and passive stimulation in experiment
2. This comparison did not reveal activation of right
intraparietal, postcentral, or occipital areas, symmetrical to those
found in the left hemisphere for attending right minus left. Instead,
common activity for attending in either direction was found in frontal
and temporal regions. These activations must be interpreted with
caution, because the baselines did not include verbal responding.
Nevertheless, the right inferior frontal gyrus activation seems
unlikely to be due to verbal responses alone and may play a role in
controlling the direction of attention.
Because the lateralized pattern (modulation by attended side only in
the left hemisphere) was not predicted, we can only speculate on its
cause. Previous associations of spatial attention with right-hemisphere
structures in functional imaging have primarily concerned tasks where
attention must be shifted between locations (e.g.,
Corbetta et al. 1993; Nobre et al. 1997
),
rather than sustained on one side as here. The present
results might be taken to suggest left-hemisphere specialization for
sustained attention. However, this seems unlikely given the bilateral
activations reported by Heinze et al. (1994)
, and the
right-lateralized results of Vandenberghe et al. (1997)
,
in their purely visual studies of sustained attention.
A further possibility is that the present left lateralization relates
somehow to our attention task requiring a verbal (presumably left
hemisphere) response. However, the Vandenberghe et al.
(1997) visual study also used a verbal response, yet found
right lateralization. Moreover, several ERP studies have shown
contralateral attentional modulations within both hemispheres, while
using a verbal response (e.g., Eimer and Driver, in press).
The present laterality could conceivably relate to all our subjects being right handed, and to the task specifically requiring that attention be directed to spatial positions immediately adjacent to the hands. The level of activity for just the dominant hand (projecting to the left hemisphere for right handers) may be most important for determining which hand will be attended. Left handers provide the obvious test for this.
Finally, the explanation that we favor is that the left laterality of
the present attentional modulations may be due to the particular
discrimination task used (temporal discrimination of single vs. double
pulses). This might fit with prior work on left-hemisphere dominance
for temporal discriminations (Brown and Nicholls 1997; Papcun et al. 1974
). Moreover, it receives some initial
support from an fMRI study we ran recently, which compared effects of sustained spatial attention for different visual tasks (Macaluso and Frith 1999
). One of the tasks in this study was closely
similar to the visual task in the present experiment 1 (i.e., detection of double pulses on the attended side during bilateral
stimulation), except that responses were now manual. Once again,
contralateral attentional modulations were stronger for attending right
minus left, within the left hemisphere, than for the reverse contrast in the right hemisphere. This was replicated despite the change from
verbal responding to manual. Furthermore, using a different visual task
(orientation discrimination, similar to Vandenberghe et al.
1997
) led to the opposite pattern for contralateral attentional modulations (i.e., now right-lateralized, as in Vandenberghe et al. 1997
), thus indicating a role for the particular
discrimination required in determining the laterality of attentional activations.
Conclusions
Whatever the ultimate resolution of the laterality issue, several
clear conclusions can still be drawn from the present experiments, regardless of laterality considerations. Our findings show that spatial
attention to one side versus the other during bilateral stimulation has
both modality-specific and multimodal consequences for brain activity,
at separate sites. The postcentral gyrus shows modulation only by
tactile attention, and does so regardless of whether the eyes are open
or closed. By contrast, the intraparietal sulcus shows attentional
modulation during both visual and tactile tasks, but only when visual
inputs are available (including sight of the hands) for the latter
tactile case. These results seem in accord with physiological findings
from single-cell recordings in animals on the representations present
within postcentral gyrus (Hsiao et al. 1993)
and intraparietal sulcus regions (Graziano and Gross
1993
). One might speculate that our findings may also suggest a possible neural basis for the crossmodal links in spatial attention between vision and touch that have recently been documented psychophysically in both normal (Driver and Spence
1998a
,b
; Spence et al., in press) and
brain-damaged (Ladavas et al. 1998
) human populations.
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ACKNOWLEDGMENTS |
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The Functional Imaging Laboratory was supported by the Wellcome Trust. E. Macaluso and J. Driver were supported by a Program Grant from the Medical Research Council of the United Kingdom. E. Macaluso was also supported by Research Training Grant 83EU-048816 from The Swiss National Research Foundation (Switzerland) and a personal grant from the Janggen-Poehn-Stiftung (Switzerland).
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FOOTNOTES |
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Address for reprint requests: E. Macaluso, Wellcome Department of Cognitive Neurology, 12 Queen Square, London WC1N 3BG, UK.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 28 May 1999; accepted in final form 31 January 2000.
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REFERENCES |
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