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The Journal of Neuroscience, January 1, 2001, 21(1):300-304
Neural Correlates of Auditory-Visual Stimulus Onset
Asynchrony Detection
Khalafalla O.
Bushara2,
Jordan
Grafman3, and
Mark
Hallett1
1 National Institute of Neurological Disorders and
Stroke, 2 Human Motor Control Section, and
3 Cognitive Neuroscience Section, National Institutes of
Health, Bethesda, Maryland 20892-1428
 |
ABSTRACT |
Intersensory temporal synchrony is an ubiquitous sensory attribute
that has proven to be critical for binding multisensory inputs,
sometimes erroneously leading to dramatic perceptual illusions. However, little is known about how the brain detects temporal synchrony
between multimodal sensory inputs. We used positron emission
tomography to demonstrate that detecting auditory-visual stimulus onset asynchrony activates a large-scale neural network of
insular, posterior parietal, prefrontal, and cerebellar areas with the
highest and task-specific activity localized to the right insula.
Interregional covariance analysis further showed significant task-related functional interactions between the insula, the posterior thalamus, and superior colliculus. Based on these results and the
available electrophysiological and anatomical connectivity data in
animals, we propose that the insula, via its known short-latency connections with the tectal system, mediates temporally defined auditory-visual interaction at an early stage of cortical processing permitting phenomena such as the ventriloquist and the McGurk illusions.
Key words:
audiovisual asynchrony; temporal integration; insular
cortex; PET; multisensory; cortical processing
| |
INTRODUCTION |
A fundamental brain function is to
integrate information available to multiple sensory modalities
producing a unified representation of the external world. Although
multimodal sensory inputs from a single object or event normally
coincide both in space and time, intersensory integration mechanisms
seem to rely more critically on their temporal than spatial congruence
(e.g., the ventriloquist effect) (Bertelson and Radeau, 1981 ). Indeed,
the ability to detect and use temporal synchrony in associating
multimodal sensory stimuli (e.g., sounds and visual events) has been
demonstrated in human infants as young as 2 months (Lewkowicz, 1996,
2000), and is believed to be operational at birth providing an innate
capacity on which intermodal perception and associative learning are
based (Spelke, 1987; Bahrick, 1992). Yet, the neural correlates for
this basic process remain unknown. Using positron emission tomography
(PET), we studied normal human subjects while performing a task
requiring detection of auditory-visual stimulus onset asynchrony as
well as a matched control condition. The PET experiment was
designed for both paired image subtraction and correlational analysis
methods. Brain regions specifically involved in temporal
synchrony-asynchrony detection process were postulated where regional
cerebral blood flow (rCBF) responses during task performance are
significantly higher than during the control condition and
appropriately modulated as a function of increasing task demand.
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MATERIALS AND METHODS |
Subjects. Twelve right-handed healthy volunteers
(seven men, five women, ages 27-56 years) participated in behavioral
and PET experiments after giving written informed consent.
Behavioral tasks. Subjects' ability to detect
intermodal temporal mismatch between simple stationary auditory and
visual stimuli was assessed in two separate auditory-visual (AV) and
visual-auditory (VA) conditions. In both conditions, the number of
trials with asynchronous stimuli was equal to that of trials with
synchronous stimuli. In AV, asynchronous trials were presented with the
sound preceding the visual stimulus, whereas in VA, the visual stimulus preceded the sound. Subjects pressed one of two buttons (with the right
index or middle finger) to indicate whether tones and visual stimuli
were perceived as being synchronous or asynchronous. Each subject
performed 10 blocks in random order. Each block consisted of 50 trials:
25 trials with synchronous stimuli (zero AV delay) randomly intermixed
with 25 trials with asynchronous stimuli (AV delay of 50, 75, 100, 150, or 200 msec or VA delay of 100, 150, 200, 250, or 300 msec between
onsets of stimuli). Choice of these delays was based on the findings of
previous behavioral studies (Dixon and Spitz, 1980; Lewkowicz, 1996).
The visual stimulus consisted of a circle 4 cm in diameter, green or
yellow in color (25 trials with each color, randomly intermixed),
presented against a black background at the center of a computer
monitor ~50 cm from the subjects' eyes (2° visual angle). Auditory
stimuli were 2000 Hz tones presented binaurally at 90 dB via well
fitting headphones. Both visual and auditory stimuli were 100 msec in
duration and were presented randomly every 2 or 3 sec to avoid
anticipatory responses. Reaction times (measured from onset of second
stimulus to onset of button press) >1500 or <150 msec were excluded
from analysis.
Subjects were then studied with PET while performing AV and VA
conditions. Three levels of difficulty per condition (AV1, 2, 3 and
VA1, 2, 3) were established by varying the amount of intermodal delay
while keeping other task components constant. Behavioral data from the
initial six subjects were used to construct AV and VA delays applied
during the PET experiment. Subjects performed AV1, AV2, and AV3 with
delays of 242, 142, and 56 msec and VA1, VA2, and VA3 with delays of
300, 208, and 114 msec, respectively, predicted to correspond (within
each condition) to 97, 80, and 70% correct responses, respectively. To
control for brain regions activated by the sensorimotor response and by
attention to visual and auditory stimuli, subjects also performed a
control condition during which stimuli were identical to those of AV
and VA but were always synchronous; subjects pressed one of the two
buttons to indicate the color of visual stimuli. To maintain attention to sound during the control condition, subjects were instructed to
respond only if the sound was present. Sound was omitted in approximately five trials of the control condition only during training
and during 30 sec before radioisotope injection. Thus, during active
scanning of the control condition, the number of auditory and visual
stimuli was identical to that in AV and VA conditions. Control
condition, AV 1, 2, 3, and VA 1, 2, and 3 were performed in random order.
PET methods. Scans were obtained in three-dimensional
mode using a GE Advance PET tomograph (Waukesha, WI) with an axial
field of view of 15.3 cm, covering the whole brain. Task performance began 30 sec before bolus infusion of 10 mCi of
[H215O] (half life, 2.1 min) via a left cubital vein catheter. Scanning was started when a
rising brain radioactivity count was first detected (~20-30 sec
after radioisotope injection) and continued for 60 sec thereafter.
Arterial blood was not sampled, and the radioactive counts were used as
a measure of rCBF. Interscan interval was 10 min. A transmission scan
was obtained (with headphones in place) before each session and used to
correct for radioactivity attenuation. Head movement was minimized by
using a thermoplastic mask molded to each subject's head and attached
to the scanner bed. Attenuation-corrected scans were reconstructed into
35 transaxial planes, 4.25 mm apart, with an in-plane center resolution
of 6.5 mm full width at half maximum (FWHM) in each direction. SPM99b software (http://www.fil.ion.ucl.ac.uk/spm) was used for realignment, normalization to a standard stereotactic space (Montreal Neurological Institute brain template), and smoothing with an isotropic Gaussian filter of 12 mm to accommodate individual variability in gyral anatomy.
After correcting for variations in global blood flow (normalized to 50 ml/100 ml/min) using ANCOVA, differences between experimental conditions (12 subjects, three replications per condition) were statistically tested for each voxel (search volume was from
z =  50 to z = 80) using (SPM96)
(Friston et al., 1995). The resulting whole brain statistical
parametric maps (SPMs) based on the t statistic (transformed
to normalized z scores) had a final spatial resolution of
x =10.4, y = 11.8, and z = 13.4 mm (FWHM). A statistical significance threshold of peak activity
(Z > 3.09; p < 0.05 corrected for
multiple comparisons) was used. For interregional covariance analysis,
synchrony-asynchrony detection conditions (AV1, 2, 3 and VA1, 2, 3)
were treated as one task, excluding control condition scans, thus
measuring within-task, across-subject covariance with preselected
reference regions (Horwitz, 1991).
| |
RESULTS |
Behavioral tasks
As expected, the longer the delay between visual and auditory
stimuli the more readily their temporal synchrony-asynchrony was
detected (Fig. 1). Similar thresholds
were obtained in previous behavioral studies using various audiovisual
bimodal presentations (e.g., speech, colliding, or moving-sounding
objects) (Dixon and Spitz, 1980; Lewkowicz, 1996), indicating that,
regardless of stimulus characteristics, humans are less sensitive to
temporal mismatch between heteromodal than between same-modality
auditory or visual stimuli (for review, see Nichelli, 1993). Subjects
were faster and more accurate in AV than VA conditions (Fig. 1), a finding consistent with previous studies showing that humans
characteristically tolerate greater temporal discrepancies between
visual and auditory events when sight precedes sound than when the
sound occurs first (Dixon and Spitz, 1980; Lewkowicz, 1996).
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Figure 1.
Subjects' performance while detecting
auditory-visual synchrony-asynchrony at different intermodal delays.
Means (± SEM) of percentage of correct responses
(a) and response times (b)
of 12 subjects. AV (open circles), Sound leading; VA
(solid circles), light leading. Percentage of correct
responses significantly increased (F(4,11) = 45.4;
p < 0.0001 and 61.7; p < 0.0001) while response time decreased (F(4,11) = 9.9; p < 0.0034 and 18.7; p < 0.0001), as a function of intermodal delay for AV and VA, respectively.
At delays of 100, 150, and 200 msec, subjects were faster and more
accurate in AV than VA conditions (t test,
p < 0.006).
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During PET, percentage of correct responses and reaction times were:
96.8 ± 0.7 and 467.1 ± 26.0 for control condition;
91.8 ± 2.3 and 423.3 ± 28.9 for AV1; 84.0 ± 3.2 and
470.0 ± 32.5 for AV2; 69.8 ± 2.9 and 530.5 ± 38.0 for
AV3; 87.7 ± 2.8 and 427.8 ± 33.8 for VA1; 81.0 ± 2.8 and 491.3 ± 41.6 for VA2; 67.9 ± 3.9 and 545.0 ± 38.1 for VA3; respectively.
PET results
Using voxel-based image subtraction, AV and VA were compared with
the control condition (C) yielding two contrasts: (AV C) and
(VA C), where AV and VA are the average of rCBF responses to
AV1, 2, and 3 and VA1, 2, and 3, respectively (Table
1). With either contrast, no significant
activation was detected in the sensorimotor, occipital, or temporal
regions (p > 0.05 uncorrected), indicating that
responses to sensorimotor, visual, and auditory stimulation were
adequately controlled for. AV C contrast showed significant
activation of the right anterior insular cortex, right ventrolateral
prefrontal cortex, right inferior parietal lobule, and left cerebellar
hemisphere (Table 1). Highly similar activation clusters were obtained
by the contrast (VA C) (Table 1). Both contrasts also activated
a homologous area in the left insular region; however, this activation
was below statistical significance. Figure
2 shows areas significantly activated in
common to both (AV C) and (VA C) without significant
interaction between the contrasts (p > 0.05),
i.e., independent of whether the sound or visual stimulus occurred
first.
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Table 1.
Brain regions activated during auditory-visual
synchrony-asynchrony detection (AV and VA) relative to control
condition (C)
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Figure 2.
Brain regions activated in common to both
auditory-visual and visual-auditory synchrony-asynchrony detection
conditions. Statistical parametric maps were superimposed on axial
views of a normalized representative subject's brain.
a, Right inferior parietal lobule (46, 54, 48;
z = 5.15; p < 0.006);
b, right ventrolateral prefrontal cortex (48, 34, 18;
z = 5.60; p < 0.001);
c, right anterior insular cortex (36, 24, 4;
z = 6.57; p < 0.0001); and
d, left cerebellar hemisphere (28, 58, 48;
z = 5.43; p < 0.002).
p values corrected for multiple comparisons.
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We then applied regression analysis to identify voxels with rCBF
responses that positively correlate with increasing task demand, i.e.,
decreasing intermodal delay. These were found only in the right insular
region with the voxel of maximal correlation lying precisely within the
activation cluster shown independently by subtraction analysis (Fig.
3). Because only three levels of task
difficulty were examined for linear rCBF correlation, this finding does
not exclude task-related response modulation in other brain regions.
However, the results of this analysis preclude any interpretation that
insular response shown in subtraction analysis is caused by
"de-activation" induced by some component of the control condition.
The location of peak voxel in both analyses was within the stereotaxic
coordinates of the insula as identified in previous PET and functional
magnetic resonance imaging studies (Calvert et al., 1997; Buchel
et al., 1998).
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Figure 3.
Statistical parametric map (thresholded at
z > 4.63; p < 0.05 corrected
for multiple comparisons) showing voxels with significant incremental
rCBF response to increasing task demand superimposed on sagittal
(a) and axial (b) views of
a normalized representative subject's brain. Voxel with highest
covariance: x = 38, y = 24, z
= 4; z = 6.42; p < 0.0001.
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Finally, we further examined nonsubtracted rCBF data for interregional
covariance as an estimate of functional connectivity between brain
regions activated during synchrony-asynchrony detection conditions
(Horwitz, 1991). Normalized rCBF values (72 scans) at peak insular,
prefrontal, posterior parietal, and cerebellar activation clusters
(Fig. 2) were used as covariates of interest. Positive rCBF
correlations with the right insula were found in the posterior midbrain
(in the region of the superior colliculus), right posterior thalamus,
right precuneus, right prefrontal cortex, and left insula (Fig.
4). Areas with significant rCBF
correlation with the right prefrontal, posterior parietal, and left
cerebellar areas are listed in Table 2.
We specifically examined the occipital and superior temporal regions
for rCBF correlations with the right insula, right prefrontal,
posterior parietal, and left cerebellar areas, but no significant
correlations were found (Fig. 4, Table 2).
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Figure 4.
Brain regions with significant functional
interactions with the right insula during synchrony-asynchrony
detection. Correlations are displayed as statistical maps
(z > 3.09) superimposed on sagittal views of a
normalized representative subject's brain. Coordinates (x, y,
z) of voxels of maximal positive rCBF correlation with the
reference voxel (36, 24, 4): a, left insula (36, 12, 0); b, posterior midbrain (in the region of the superior
colliculus; 2, 28, 12); c, right precuneus (12, 80, 48); d, right posterior thalamus (18, 22, 8);
and e, right prefrontal cortex (32, 48, 20).
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| |
DISCUSSION |
The results demonstrate that visual-auditory temporal
synchrony-asynchrony detection predominantly activates a large-scale neural network of multisensory cortical areas in the insular, posterior
parietal, and prefrontal regions. Both cognitive subtraction and
task-demand correlational analyses concur that the right insula is more
actively involved in this process than the classical association cortices in the prefrontal and posterior parietal regions. This function has not been previously assigned to the human insula and would
have not been readily predicted given the traditionally proposed
insular functions (Penfield and Faulk, 1955; Mesulam and Mufson, 1984;
Augustine, 1996). These have been derived mainly from brain lesion and
epilepsy studies that have implicated the insula in autonomic,
visceral, somatosensory, vestibular, smell, taste, and language
processing (Penfield and Faulk, 1955; Mesulam and Mufson, 1984;
Augustine, 1996). Similarly, functional neuroimaging studies showed
activation of the insula under a wide variety of behavioral conditions
and mostly emphasized its role in visceral and limbic functions. These
included pain perception, anticipatory anxiety, reflex conditioning,
and associative learning (Buchel et al., 1998; Fischer et al., 1998;
Ploghaus et al., 1999). Although many of these studies applied
behavioral tasks requiring association of visual and auditory
information and in that respect, generally agree with our findings,
none of previous functional imaging studies specifically investigated
intersensory temporal synchrony as the basis for insula activity
(Calvert et al., 1997; Buchel et al., 1998).
Interregional covariance analysis was complementary to conventional
cognitive subtraction showing task-related functional interactions
between the insular, the dorsolateral prefrontal, and posterior
parietal areas. In addition, the posterior thalamus and superior
colliculus also showed significant functional interaction with the
right insula; the region with the highest and task-specific activity,
indicating the involvement of the tectal system in auditory-visual temporal synchrony-asynchrony detection (Fig. 4). Electrophysiological and anatomical connectivity studies in primates and other mammals indicate that the insular cortex may receive auditory and/or visual inputs via multiple parallel pathways from the auditory cortex, the
temporal, prefrontal, and posterior parietal multisensory regions as
well as via subcortical projections from the superior colliculus
through the posterior group of thalamic nuclei (magnocelluar medial
geniculate and suprageniculate nuclei) (Graybiel, 1973; Guldin and
Markowitsch, 1984; Hicks et al., 1988) (Mesulam and Mufson, 1984).
Compatible with the direct tecto-thalamo-insular pathways are the short
insular neuronal latencies reported for visual and auditory stimulation
in electrophysiological studies (Sudakov et al., 1971; Benvento and
Loe, 1975; Hicks et al., 1988). Similar subcortical pathways from the
superior colliculus via the posterior thalamus are known to project to
the amygdala and are believed to mediate limbic processes such as
reflex conditioning to subconsciously perceived visual and auditory
inputs (Morris et al., 1999). Based on our results and the available
anatomical and electrophysiological data from animal studies, we can
specifically propose that intersensory temporal processing is similarly
mediated via subcortical tecto-thalamo-insular pathways. These would
allow detection of temporal correspondence between visual and auditory inputs and their interaction at an early level of cortical processing, perhaps in parallel with the primary sensory and parasensory
association cortices. In support of this hypothesis, are the results of
single unit studies showing that both insular and superior collicular neuronal responses to combinations of visual and auditory stimuli are
characteristically modulated by the amount of intermodal temporal delay
(Loe and Benevento, 1969; Benevento et al., 1977; Meredith et al.,
1987).
At the behavioral level, early interaction of visual and auditory
inputs has been proposed by several studies to explain two perceptual
illusions (the McGurk and ventriloquist effects) that result from
binding of conflicting multimodal information based on their temporal
synchrony (McGurk and MacDonald, 1976; Driver, 1996). The McGurk
illusion occurs when a sound of a syllable (e.g., "ba") is
temporally synchronized with lip movements silently uttering a
different syllable (e.g., "ga") producing the perception of another
syllable (typically "da"). According to the early (or prelabeling)
integration models of audiovisual speech perception, the McGurk effect
is evidence that voice and lip-movement cues are combined before the
unimodal acoustic and visual information are assigned to a phoneme or
word category (McGurk and MacDonald, 1976; Schwartz et al., 1998). A
similar mechanism has also been proposed to explain the ventriloquist
effect in humans [and a similar phenomenon in animals, e.g., cats
respond to temporally synchronous but spatially disparate auditory and
visual stimuli by moving to a position halfway between the two sources
(Stein and Meredith, 1993)] in which audiovisual integration is
believed to occur early in the course of cortical processing, before
the process of spatial selective attention is complete (Driver,
1996).
| |
FOOTNOTES |
Received Aug. 4, 2000; revised Oct. 13, 2000; accepted Oct 17, 2000.
We thank Devera Schoenberg for skillful editing, Dr. Elizabeth Murray
and Dr. Josef Rauschecker for useful comments on this manuscript, and
Nugyet Dang for technical assistance.
Correspondence should be addressed to Dr. Mark Hallett, National
Institutes of Health, National Institute of Neurological Disorders and
Stroke, Building 10, Room 5N226, 10 Center Drive MSC1428, Bethesda, MD
20892-1428. E-mail: hallettm{at}ninds.nih.gov.
Dr. Bushara's present address: 4B135, Minneapolis Veterans Affairs
Medical Center, Minneapolis, MN 55417.
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TOP
ABSTRACT
INTRODUCTION
Nuclear Scans
