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The Journal of Neuroscience, 2002, 22:RC207:1-5
RAPID COMMUNICATION
Role of the Posterior Parietal Cortex in Spatial Hearing
Jörg
Lewald1, 2,
Henrik
Foltys3, and
Rudolf
Töpper3
1 Institute for Occupational Physiology, D-44139
Dortmund, Germany, 2 Department of Cognitive and
Environmental Psychology, Ruhr University, D-44780 Bochum, Germany, and
3 Department of Neurology, University Hospital of Aachen,
D-52074 Aachen, Germany
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ABSTRACT |
The human posterior parietal cortex (PPC) is well known to be
involved in various functions of multisensory spatial perception. However, the specific role of the PPC in hearing has, up to now, remained unclear. To allow more reliable conclusions to be drawn on
this issue, we have used repetitive transcranial magnetic stimulation in healthy subjects. Focal stimulation of the PPC induced a systematic shift in the lateralization of interaural time differences (ITDs, a
main cue for auditory azimuth), whereas the acuity of ITD
discrimination was unaffected. We propose that the PPC is specifically
involved in relating azimuthal angles of sound to the body coordinates and is part of a "where" stream in cortical processing of auditory information.
Key words:
posterior parietal cortex; repetitive transcranial
magnetic stimulation; interaural time differences; sound localization; space perception; psychophysics; human
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INTRODUCTION |
Unlike
visual spatial perception, spatial hearing is based not on the
representation of sensory stimuli on a receptor epithelium but on the
evaluation of specific cues of the sound received by the two ears. In
particular, interaural differences in time of arrival and level as well
as spectral cues are used to derive azimuthal and elevational
coordinates of the position of a sound source with respect to the ears.
Neural correlates of these basic processes, synthesizing
representations of acoustic space, have been located in the subcortical
auditory pathway up to the primary auditory cortex (Masterton, 1992 ;
Middlebrooks, 2000). The role of brain regions beyond the primary
auditory cortex in higher-order perceptual processes of spatial hearing
is, however, poorly understood. Anatomical and physiological results
obtained recently in the monkey have suggested that the spatial
component of auditory information is processed within a "dorsolateral
stream", which includes the caudal superior temporal cortex,
posterior parietal cortex (PPC), and dorsolateral prefrontal cortex,
and is anatomically distinct from a "ventrolateral stream",
processing nonspatial acoustic features (Rauschecker, 1998; Romanski et
al., 1999; Rauschecker and Tian, 2000). This seems to be analogous to
the widely held view of parietal "where" and temporal "what"
processing streams for transmission of visual spatial and object
information, respectively (Mishkin et al., 1983). Starting from this
hypothesis, the present study focused on the functional
characterization of the human PPC in auditory localization. For this
purpose, we aimed to selectively affect neural processing in this area
by repetitive transcranial magnetic stimulation (rTMS). With this
technique, high-current pulses, generated in a coil of wire placed
above the scalp, produce magnetic fields that induce electric fields
(Hallett, 2000; Walsh and Cowey, 2000). The repetitive electric-field
changes during rTMS stimulate neurons of the underlying cortical
surface in an uncoordinated manner, thus interrupting normal brain
activity. Transient alterations of the activity of the stimulated area
have been shown to persist for several minutes after application of rTMS (Pascual-Leone et al., 1994; Chen et al., 1997; Mottaghy et al.,
1999; Töpper et al., 1999). In the present study, sound lateralization was tested during this rTMS after-effect to minimize interference between the auditory stimuli used and the sound pulses accompanying rTMS pulses, as well as those between magnetic stimulation and peripheral hearing functions.
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MATERIALS AND METHODS |
Ten right-handed male subjects (27-36 years of age)
participated in this study. The experimental room was silent and
darkened, with only a fixation target (dim light spot) straight ahead
of the subject. The subject was seated, with the head fixed in a straight-ahead position by a stabilizing rest for the occiput. Dichotic
pure-tone pulses (frequency, 1 kHz; sound pressure level, 70 dB;
plateau time, 30 msec; rise/fall time, 10 msec) were presented via
insert earphones (ER-1; Etymotic Research Co., Elk Grove Village, IL) that were worn in combination with hearing-protection
earmuffs. The interaural time difference (ITD) of the sound stimulus
was varied between trials following a quasi-random order over a range from  112.5 µsec (sound leading at the left ear) to +112.5 µsec (leading at the right ear), in steps of 22.5 µsec. Within 1 sec after
stimulus presentation, subjects were required to indicate the perceived
intracranial position of the sound with respect to the median plane of
the head by pressing a "left" or "right" key. Sound stimuli
were presented with intervals of 3 sec. After a few practice trials,
two subsequent blocks, each composed of 220 trials (equaling 11 min),
were conducted as the pre-rTMS reference condition.
rTMS was applied with a magnetic stimulator (Magstim Rapid Stimulator;
Magstim Co., Spring Gardens, UK) connected with a figure-eight coil
(outer diameter, 9 cm). The magnetic stimulator was triggered by an
external device (Master 8 Trigger unit; AMPI, Jerusalem, Israel)
with a frequency of 1 Hz for 10 min (total number of stimuli was 600).
The intensity of magnetic stimulation was set to 60% of the stimulator
output (maximum output, 2.2 tesla). All stimulation parameters were in
accordance with the safety guidelines for repetitive magnetic
stimulation (Wassermann, 1998). rTMS was delivered to the posterior
parietal cortex of the left or right hemisphere, and the stimulation
sites P3 and P4 were determined according to the 10-20 EEG system.
Immediately after rTMS application, two blocks of the psychophysical
task were completed as for the reference condition. After a rest of at
least 2 h, this procedure was repeated with rTMS of the subject's
other hemisphere. For each block, the subject's judgments were
determined as a function of ITD and data were fitted to the
following sigmoid equation: f = 100/[1 + e  k(ITD AMP)], where f is the frequency of
judgments "right", given as a percentage; the "auditory median
plane" (AMP) is the ITD for which f is 50%; k
is the slope of the function at 50%; and e is the base of
the natural logarithm (compare Fig.
1A). The fit was
significant in each case (coefficient of determination:
r2 > 0.92; p < 0.0001). The values k and
r2 obtained from the fit were
used here as measures for the subject's acuity of sound
lateralization, whereas the AMP values indicated systematic shifts in
lateralization. AMPs were normalized such that values obtained with the
pre-rTMS blocks 1 and 2 were assigned 0 µsec. Negative displacements
of the AMP with the post-rTMS blocks 1 and 2 thus indicate shifts in
auditory lateralization (with respect to the corresponding pre-TMS
blocks) to the right, and positive AMP displacements indicate shifts to
the left (Fig. 1B). This normalization procedure was
conducted because subjects usually exhibited a slight bias of the AMP
to the left or right in the pre-TMS reference condition. In particular,
as is obvious from the leftward shift of the mean pre-TMS AMP in Figure
1A, the majority of subjects may have had a
preference to press the "right" key in cases in which they
perceived the sound to be exactly on the median plane or were uncertain
whether it had been to the left or right.
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Figure 1.
Effects of rTMS of the PPC on
lateralization of interaural time differences. A, Mean
psychometric functions for all subjects before (pre-rTMS) and after a
10 min period of rTMS of the right PPC (post-rTMS; block 1). Original
judgements (symbols, mean ± SEM) were fitted with
sigmoid functions. The AMP of the head was defined as that interaural
time difference at which the frequency of left and right judgements was
50% (indicated by the points of intersection of the dotted
lines). B, Mean shift of the AMP for the periods
of 0-11 min (Block 1, closed symbols,
mean ± SEM) and 11-22 min (Block 2, open
symbols, mean ± SEM) after rTMS of the left or right PPC.
Data are normalized with respect to the pre-rTMS reference condition.
Positive values indicate shifts of the AMP to the right or shifts of
the auditory percept to the left; negative values are vice versa.
Asterisks indicate significant differences between the
reference and post-rTMS condition (n.s.,
nonsignificant). C, Schematic illustration of the main
effect. An intracranial sound image (gray-shaded area),
which was originally centered to the AMP with the reference condition,
was perceived as shifted to the left after application of rTMS to the
PPC of the right hemisphere.
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Two additional control experiments were conducted to yield estimates of
nonspecific effects of rTMS on sound lateralization. Apart from the
locus of rTMS, conditions were as in the main experiment. In one
control experiment, rTMS was applied to the occipital cortex (2 cm
above and 2 cm lateral of the inion). Stimulation of this cortical
area, which is not involved in auditory processing, had no effect on
sound lateralization. In the other control experiment, the facial nerve
(2 cm above and 2 cm ventral of the tragus) was stimulated, because
stimulation of parietal areas leads to a considerable contraction of
the ipsilateral facial muscles. No shift in sound lateralization could
be recorded in this control experiment (see Fig. 3).
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RESULTS |
Subjects made two-alternative forced-choice (left/right)
judgements on the intracranial position of sound images, which were evoked by the presentation of dichotic tone pulses with variable ITDs. Four blocks of the task, each lasting 11 min, were
conducted, two of them before a 10 min period of low-frequency rTMS (1 Hz) of the PPC (reference, pre-TMS blocks 1 and 2), and two identical blocks immediately after rTMS (post-TMS blocks 1 and 2).
In the post-rTMS block 1, the subject's AMP (point of equal
numbers of left and right judgements) was, with respect to the pre-TMS
block 1, significantly shifted toward the side of rTMS. That is, a
sound image, evoked by a constant ITD, appeared more to the left after
rTMS of the right PPC (p = 0.010) and more to the right after rTMS of the left PPC (p = 0.027;
Fisher randomization test for matched pairs) (Fig. 1). The mean
auditory shift obtained in the first block after rTMS was slightly
stronger for stimulation of the right hemisphere (12.0 µsec; SEM,
±2.8 µsec) compared with left rTMS (6.3 µsec; SEM, ±3.6 µsec).
However, this tendency did not reach the level of statistical
significance. Intersubject variability was relatively large in these
experiments: although the maximum shifts obtained after left or right
rTMS were more than ±25 µsec, in some subjects, rTMS appeared to be
less efficient, so that auditory shifts were close to zero.
Only insignificant displacements of the AMP were obtained in the
post-rTMS block 2, indicating the decrease of the rTMS after-effect as
a function of time. As shown in Figure 2,
analyses of the psychometric functions revealed no significant changes
in the acuity of auditory lateralization after rTMS. Rather, a
significant reduction in the mean reaction times of the subjects'
judgements after rTMS (block 1; right rTMS, 39.3 msec; left rTMS,
35.1 msec; p < 0.0001 in both cases; t
test) was found, although subjects were instructed merely to respond
within 1 sec after presentation of the sound stimulus. Because this
latter effect was also observed in control experiments using rTMS of
the occipital cortex, it is likely caused by an enhancement of
general vigilance. Apart from this effect, control experiments with
application of rTMS to either the occipital cortex or the facial nerve
gave no hint of nonspecific effects of rTMS on the subject's
performance. This can be taken as evidence that the effects of rTMS to
the PPC are indeed specific (Fig. 3).
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Figure 2.
Acuity of the discrimination of interaural time
differences. A, Mean coefficients of determination
(r2, mean ± SEM) resulting from
the fit of individual data to a sigmoid function. B,
Mean slopes (k) of the individual fitted
functions. Dark gray columns indicate mean values
(mean ± SEM) for block 1 of the pre-rTMS or post-rTMS conditions;
light gray columns indicate values for block 2. Differences between corresponding pre-rTMS and post-rTMS data are
nonsignificant in each case.
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Figure 3.
Individual psychometric functions of one
subject obtained in the main experiment (rTMS of the posterior parietal
cortex) and in two control experiments with rTMS of the occipital
cortex or of the facial nerve. Fitted functions are computed from block
1 data with the pre-rTMS reference conditions or after
right-hemispheric rTMS and are normalized with respect to the pre-rTMS
curve. The positions of the auditory median plane are indicated by the
points of intersection of the dotted lines. Data are
from a subject who exhibited relatively large auditory shifts in the
main experiment (compare Fig. 1A). Apart from
that fact, the psychometric functions of the other subjects were
similar to those shown here.
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DISCUSSION |
The primary finding of the present study is that focal magnetic
stimulation of the right or left PPC results in a systematic shift of
sound lateralization but does not affect the precision of ITD
discrimination. Because the ITD is a main cue for sound azimuth, this
auditory shift may correspond to an azimuthal shift of auditory space.
Thus, the PPC may play a specific role in the localization of absolute
sound-source positions but may not be involved in discrimination of the
relative positions of different sound sources.
The direction of the auditory shift toward the side contralateral to
rTMS application (Fig. 1C) can be explained on the basis of
two considerations. First, previous studies that have used rTMS at low
frequencies have suggested an inhibitory rather than an activating
influence on neural processing in the underlying cortical surface (Chen
et al., 1997). Second, neurophysiological recordings of spatially
selective auditory neurons in the monkey parietal cortex have
demonstrated preferential tuning to sounds located in the contralateral
hemispace (Mazzoni et al., 1996; Stricanne et al., 1996). Thus, the
present auditory shift may not be induced by mere inhibition of
auditory afferents from the contralateral ear, which would have
resulted in an opposite shift. A more likely interpretation is that
rTMS has specifically affected processes of neural coordinate
transformations, such as those recently demonstrated in the monkey
parietal cortex for the visual domain. In the monkey lateral
intraparietal area, visual receptive fields of single neurons
have been shown to be referenced to the body (Brotchie et al., 1995),
and a world-referenced coding of visual space was found in the adjacent
parietal area 7a (Snyder et al., 1998). Although there is as of yet no
direct experimental evidence, it seems reasonable to assume that this
also holds true for the auditory modality: a substantial proportion of
monkey parietal neurons is known to have a spatial selectivity not only for visual but also for acoustic stimuli (Mazzoni et al., 1996; Stricanne et al., 1996). Assuming homology with the monkey parietal cortex, auditory space may thus be transformed in the human PPC from
the originally head-centered into body- and/or world-centered coordinates. That is to say, when the head is rotated under normal conditions to, for example, the right, auditory receptive fields in the
PPC may systematically shift, with respect to the head, toward the
left, in a manner such that they remain stationary with respect to
external space. Inhibition of the PPC of one hemisphere by rTMS should
thus result in an interhemispheric imbalance of this neural mechanism
of coordinate transformation, as may, under normal conditions, occur
with body motion. That is, the cortical representation of auditory
space may be biased toward the nonstimulated, contralateral hemisphere.
A perceptual correlate of this bias may be that the auditory spatial
frame of reference, namely the AMP, is displaced toward the ipsilateral
hemispace. Consequently, sounds physically centered to the median
sagittal plane should be heard displaced to the side contralateral to
rTMS, as was the case in the present experiment.
Coordinate transformations such as those hypothesized above must
integrate auditory spatial information with head-to-trunk position and
vestibular (head-in-space position) signals. In this context, it is
interesting that an auditory shift that is virtually identical to that
demonstrated here after rTMS of, for example, the right PPC can be also
found when the subject's head is oriented to the right (Lewald and
Ehrenstein, 1998), when the muscle spindles of the left neck muscles
are stimulated by vibration (Lewald et al., 1999), during rotatory
acceleration of the subject's whole body to the left (Lewald and
Karnath, 2001), and after right-sided, cold-caloric vestibular
stimulation (Lewald and Karnath, 2000). In other words, direct
inhibition of the PPC of one hemisphere by rTMS may be equivalent to
(1) neck-proprioceptive afferent signals, conveying head positions to
the ipsilateral side, or (2) vestibular afferent signals, conveying
rotations to the contralateral side. These similarities further support
the view that rTMS of the PPC may have specifically affected neural
coordinate transformations, integrating auditory with
neck-proprioceptive and vestibular inputs.
In obvious alignment with our findings, previous neuroimaging studies
have demonstrated bilateral activation of the PPC with sound-localization tasks (Griffiths et al., 1998; Bushara et al., 1999;
Weeks et al., 1999). The pronounced right-hemispheric predominance obtained in those studies may correspond to the present observation that the mean auditory shift was larger after right rTMS than after
left rTMS (Fig. 1B). This tendency, although
statistically nonsignificant, is in accord with the view of a
preferential role of the right PPC for sound localization.
Previous studies on patients with brain lesions including
the PPC have also reported shifts in auditory localization or
lateralization compared with healthy subjects. The majority of those
studies, although not all (Vallar et al., 1995), have demonstrated more or less pronounced systematic errors toward the right after lesions of
the right hemisphere, and either nonsignificant or dispersed errors
after left-hemispheric lesions (Bisiach et al., 1984; Pinek et al.,
1989; Pinek and Brouchon, 1992; Tanaka et al., 1999; Bellmann et al.,
2001). In general, this seems to be in agreement with the present
results. However, the directions of the auditory shifts found after
rTMS and after brain lesions are apparently opposite if rTMS is
supposed to induce transient "virtual lesions" (Walsh and Cowey,
2000). One must nevertheless consider that actual brain damage
usually involves larger parts of several cortical and subcortical brain
regions, so that conclusions on the specific role of the PPC are
difficult to draw. A critical point in the studies mentioned above may
be that most patients suffered from a hemispatial neglect (a lack of
awareness of space on the side of the body contralateral to a brain
injury). This disorder has been attributed recently to lesions of the
right superior temporal cortex (Karnath, 2001; Karnath et al., 2001),
which is known to be involved in neural processing of auditory space
(Rauschecker, 1998; Romanski et al., 1999; Rauschecker and Tian, 2000;
Tian et al., 2001). But whereas absolute localization may be the domain
of the parietal cortex in spatial hearing, the human right superior
temporal cortex may rather be important for auditory spatial
discriminative abilities (Zimmer et al., 2001).
In contrast to studies on patients with brain lesions, the present
method may have reversibly affected a relatively restricted area of
intact cortex, so that our results may be more reliable to interpret
than those obtained from brain-damaged patients. Another major
difference between the "virtual", short-lasting lesions induced by
TMS and structural lesions is the fact that compensatory mechanisms do
not play a role in TMS-induced lesions. In conclusion, the present
study suggests that the human PPC represents the neural substrate of
transformations of auditory spatial coordinates that may be the
prerequisite for the perceptual stability of auditory (and
multisensory) space during motion (Thier and Karnath, 1997).
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FOOTNOTES |
Received Sept. 21, 2001; revised Nov. 5, 2001; accepted Nov. 27, 2001.
This work was supported by Grants Gu 261/7-1, Eh 91/4-2, and To 190/2-3
from the Deutsche Forschungsgemeinschaft. We thank P. Dillmann for
preparing the software and parts of the electronic equipment and
W. H. Ehrenstein, S. J. Fellows, and H.-O. Karnath for
valuable comments on the manuscript.
Correspondence should be addressed to Jörg Lewald, Fakultät
für Psychologie, Ruhr-Universität, D-44780 Bochum, Germany. E-mail: joerg.lewald{at}ruhr-uni-bochum.de.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2002, 22:RC207 (1-5). The
publication date is the date of posting online at
www.jneurosci.org.
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B. Roder, A. Kusmierek, C. Spence, and T. Schicke
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TOP
ABSTRACT
INTRODUCTION
