NEUROREPORT
AUDITORY AND VESTIBULAR SYSTEMS
Sound localization in the human brain:
neuromagnetic observations
Kalle PalomaÈki,CA Paavo Alku, Ville MaÈkinen,1,3 Patrick May2 and Hannu Tiitinen1,3
1
Laboratory of Acoustics and Audio Signal Processing, Helsinki University of Technology, PO Box 3000, Fin-02015 TKK;
Cognitive Brain Research Unit and 2 Department of Psychology, University of Helsinki; 3 BioMag Laboratory, Medical Engineering
Centre, Helsinki University Central Hospital, Finland
CA
Corresponding Author
Received 15 February 2000; accepted 1 March 2000
Acknowledgements: This study was supported by the Academy of Finland.
Sound location processing in the human auditory cortex was
studied with magnetoencephalography (MEG) by producing
spatial stimuli using a modern stimulus generation methodology
utilizing head-related transfer functions (HRTFs). The stimulus
set comprised wideband noise bursts ®ltered through HRTFs
in order to produce natural spatial sounds. Neuromagnetic
responses for stimuli representing eight equally spaced sound
source directions in the azimuthal plane were measured from
10 subjects. The most prominent response, the cortically
generated N1m, was investigated above the left and right
hemisphere. We found, ®rstly, that the HRTF-based stimuli
presented from different directions elicited contralaterally
prominent N1m responses. Secondly, we found that cortical
activity re¯ecting the processing of spatial sound stimuli was
more pronounced in the right than in the left hemisphere.
NeuroReport 11:1535±1538 & 2000 Lippincott Williams &
Wilkins.
Key words: Auditory; Head-related transfer function; HRTF; Magnetoencephalography; MEG; N1m; Sound localization
INTRODUCTION
Non-invasive measurements utilizing electroencephalography (EEG) and magnetoencephalography (MEG) have
recently been used to study how stimulus features are
represented in the human brain. These measurements have
successfully revealed how, for example, tone frequency
and intensity are encoded in tonotopic [1±3] and amplitopic maps [4], respectively. Invasive animal studies further
suggest that auditory cortex contains representations for
various dynamic features, such as stimulus periodicity [5]
and duration [6].
In addition to their spectral and temporal structure,
natural sounds are perceived as having a location in
auditory space. Behavioural studies indicate that sound
localization in humans is based on the processing of
binaural cues from interaural time and level differences
(ITD and ILD, respectively) and monaural spectral cues
from the ®ltering effects of the pinna, head and body [7].
The physiological basis of auditory space perception has
mainly been invasively studied in animal models. These
studies have revealed that the mammalian brain maps
three-dimensional sound locations [8] with neurons in
auditory cortex exhibiting tuning for stimulus location in
auditory space [9]. While the processing of spatial sound in
the human brain has remained largely unexplored, eventrelated potential (ERPs) and magnetic ®eld (EMFs) measurements of, for example, the N1(m) response (for review
0959-4965 & Lippincott Williams & Wilkins
see [10]) might offer a useful tool for studying sound
localization in the human cortex.
To date, the study of auditory spatial processing in the
human brain has relied on two stimulus delivery methods:
the use of headphones coupled with ITDs [11] and ILDs
[12] and the use of multiple loudspeakers [12±14]. However, both stimulus delivery methods have certain restrictions when addressing how the human brain processes
spatial auditory environments. On the one hand, stimuli
delivered through headphones are experienced as lateralized between the ears inside the head, rather than being
localized outside the head as in natural spatial auditory
perception [7]. On the other hand, the use of loudspeakers
introduces variables such as room reverberation, which
may contaminate response patterns. Furthermore, the use
of loudspeakers is impossible with MEG because magnetic
components can not be placed inside the magnetically
shielded measurement room.
Recent developments in sound reproduction technology
allow the delivery of natural spatial sound through headphones. These developments are based on so-called headrelated transfer functions (HRTFs), digital ®lters capable of
reproducing the ®ltering effects of the pinna, head and
body [15]. HRTFs allow one to generate stimuli whose
angle of direction can be adjusted as desired and to feed
them directly to the ear canals using sound delivery
systems with no magnetic parts. Thus, HRTFs allow us, for
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È KI ET AL.
K. PALOMA
the ®rst time, to use MEG in studying how the human
cortex performs sound localization.
The cerebral processing of spatial sounds produced with
HRTFs has recently been investigated in two studies
applying PET, where it was found that blood¯ow increased in superior parietal and prefrontal areas during
spatial auditory tasks [16,17]. These studies, however, left
unresolved the role of auditory cortex in sound localization
as well as the differences in brain activity elicited by
sounds originating from different source direction angles.
These issues are addressed in the present study. We focus
on the role of auditory cortex in the processing of sounds
representing a natural spatial environment by analyzing
the magnetic responses evoked by spatial stimuli generated
using HRTFs.
MATERIALS AND METHODS
A total of 10 volunteers (nine right-handed, two female,
mean age 29 years) served as subjects with informed
consent and the approval of the Ethical Committee of
Helsinki University Central Hospital (HUCH). The stimuli
for the auditory localization task were produced using
HRTFs provided by the University of Wisconsin [15]. The
stimuli consisted of eight HRTF-®ltered noise sequences
(bandwidth 11 kHz, stimulus duration 50 ms, onset-to-onset
interstimulus interval 800 ms) corresponding to eight azimuthal directions (0, 45, 90, 135, 180, 225, 270 and 3158) in
the horizontal plane (see Fig. 1).
In the MEG experiment, the stimuli were played by
randomizing their direction angle. Stimulus intensity was
scaled by adjusting the sound sample from 08 azimuth to
75 dB SPL. Binaural loudness of stimuli from all directions
was equalized using the loudness model [18].
The EMFs elicited by auditory stimuli were recorded
(passband 0.03±100 Hz, sampling rate 400 Hz) with a 122channel whole-head magnetometer (Neuromag-122) which
measures the gradients äBz /äx and äBz /äy of the magnetic
®eld component Bz at 61 locations over the head. The
subject, sitting in a reclining chair, concentrated on watching a silent movie and was instructed not to pay attention
to the auditory stimuli. Brain activity time locked to
stimulus onset was averaged over a 500 ms post-stimulus
period (baseline-corrected with respect to a 100 ms prestimulus period) and ®ltered with a passband of 1±30 Hz.
Electrodes monitoring both horizontal (HEOG) and vertical
(VEOG) eye movements were used in removing artifacts,
de®ned as activity in excess of 150 ìV. Over 100 instances
of each stimulus type were presented to each subject.
Data from channel pairs above the temporal lobes with
the largest N1m amplitude were analyzed separately for
both hemispheres, and the N1m amplitude was determined as a vector sum from these channel pairs. As MEG
sensors pick up brain activity maximally directly above the
source [19], the channel pair at which the maximum was
obtained indicates the approximate location of the underlying source. Statistical analyses (ANOVA) were performed
for data obtained by MEG.
In order to determine the perceptual quality of the HRTF
stimuli, the subjects were also tested with a behavioural
match-to-sample task. The eight stimuli were ®rst played
in a clockwise sequence with the direction angle of the ®rst
sound randomized. Then a test sample from a random
direction was played three times after which the subject
Left hemisphere
N1m responses
Right hemisphere
N1m responses
08
08
458
3158
908
2708
908
2708
1358
2258
458
3158
1358
2258
40 fT/cm
1808
2100 ms
1808
500 ms
240 fT/cm
Fig. 1. N1m responses of both hemispheres (grand-averaged over 10 subjects) from the sensor maximally detecting N1m activity shown for each of
the eight direction angles. MEG measurements were conducted by using spatial sounds corresponding to eight different source locations as stimuli. The
stimulus set comprised HRTF-®ltered noise bursts whose direction angle was varied between 0 and 3158 in the azimuthal plane. The obtained magnetic
responses were quanti®ed by using the channels with the largest N1m amplitude over the left and the right hemisphere.
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Vol 11 No 7 15 May 2000
NEUROREPORT
SOUND LOCALIZATION: MEG OBSERVATIONS
indicated the direction angle of this test sample by a button
press. Hit rates were calculated for each angle.
RESULTS
The stimulus set used in the present experiment approximated the horizontal auditory plane well, with the behavioural match-to-sample task indicating that the samples
were localized correctly with 67% accuracy. The probability
of correctly performed localization increased to 86% when
errors within the so-called cones of confusion [7] (i.e.
between angles 0 and 1808, 45 and 1358, 225 and 3158) were
ignored. These cones are regions in auditory space within
which behavioural discrimination of the direction between
sound sources is weak due to ITD and ILD varying only
slightly because of the asymmetry of the head.
In the MEG recordings, all eight stimuli elicited prominent N1m responses, as can be seen in the grand-averaged
responses of Fig. 1. Both hemispheres exhibited tuning to
the direction angle, with a contralateral maximum (direction angles 908 and 2708 for the left and right hemisphere,
respectively) and an ipsilateral minimum (direction angles
2708 and 908 for the left and right hemisphere, respectively)
in the amplitude of the N1m. The amplitude variation as a
function of azimuthal degree was statistically signi®cant
over both the left (F(1,7) ˆ 3.09, p , 0.01) and the right
(F(1,7) ˆ 7.74, p , 0.001) hemisphere.
Fig. 2 shows the grand-averaged N1m amplitude over
the eight stimulation conditions. The results indicate a
right-hemispheric preponderance in the processing of the
HRTF-®ltered noise stimuli: The N1m responses were considerably larger in amplitude over the right than over the
left hemisphere. The mean N1m amplitude across the eight
direction angles was 39.1 fT/cm in the right and 24.5 fT/
cm in the left hemisphere (F(1,9) ˆ 17.76, p , 0.01). Further,
the N1m amplitude variation (i.e. the difference between
the maximum and mimimum across azimuthal angle) was
larger in the right (28.6 fT/cm) than in the left (14.8 fT/cm)
hemisphere.
DISCUSSION
The present results demonstrate that it is possible to extend
non-invasive MEG research to studies of cortical processes
in complex auditory environments by using HRTF-based
stimuli. Our results show that both cortical hemispheres
are sensitive to the location of sound in three-dimensional
sound space. The amplitude of the N1m exhibited tuning
to the sound direction angle in both hemispheres, with
response maxima and minima occurring for contralateral
and ipsilateral stimuli, respectively. This contralateral preponderance of the amplitude of the N1m response is not
surprising, given that connections between the ear and
cortical hemisphere are crossed [20] and that previous
brain research has demonstrated contralaterally larger
auditory evoked electric [21] and magnetic [22±24] responses.
The present results also seem to suggest a degree of
right-hemispheric specialization in the processing of auditory space. Firstly, the N1m of the right hemisphere was,
on the average, of a considerably larger magnitude than
that of the left hemisphere. Secondly, the right hemisphere
appeared to be more sensitive to changes in the direction
angle, with the variation of the amplitude of the N1m
across direction angle being almost twice as large in the
right hemisphere than in the left.
Previous behavioural studies have shown that naturalsounding spatial auditory environments can be created by
using non-individualized HRTFs [25]. This is supported by
our behavioural test, which showed that the HRTF-stimuli
were localized relatively well by the subjects in all eight
directions. Hence, already the use of non-individualized
HRTFs provide realistic enough spatial sound conditions
for MEG measurement purposes.
Sound localization is known to be easy for sound
sources of wide frequency bandwidth [7]. Therefore, noise
bursts with a frequency band of 11 kHz were used in the
present study. This is in contrast to several previous
experiments applying sinusoidal stimuli [12,22±24], which
contain poor spectral cues for sound localization. Our
future aim is to analyse the behaviour of the N1m in sound
localization using different types of stimuli (e.g. periodic
signals and speech, as well as sounds generated with
individualized HRTFs).
CONCLUSION
Auditory localization in the human cerebral cortex as
indexed by the N1m response was studied with MEG
Right hemisphere
N1m amplitude
50
65
45
60
N1m amplitude (fT/cm)
N1m amplitude (fT/cm)
Left hemisphere
N1m amplitude
40
35
30
25
20
15
10
0
45
90
135 180 225 270 315
angle (deg)
55
50
45
40
35
30
25
0
45
90
135 180 225 270 315
angle (deg)
Fig. 2. The N1m amplitude (grand-averaged over 10 subjects) calculated as the vector sum from the channel pair maximally detecting N1m activity
over the left and right hemisphere. The behaviour of the N1m amplitude reveals contralateral and right-hemispheric preponderance of brain activity
elicited by stimuli from the different directions angles (error bars indicate s.e.m.).
Vol 11 No 7 15 May 2000
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NEUROREPORT
measurements using HRTF-®ltered wideband noise bursts
as stimuli. The amplitude behaviour of the N1m revealed
that spatial stimuli elicited predominantly contralateral
activity in the auditory cortex. Moreover, the N1m amplitude, as well as its variation across direction angle of
stimulation, was larger in the right than in the left hemisphere, which suggests right-hemispheric speci®city in the
cortical processing of spatial auditory information.
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