1Ashton Graybiel Spatial Orientation Laboratory and Volen Center for Complex Systems, Brandeis University, Waltham 02454-9110; 2Department of Brain and Cognitive Science and 3Research Laboratory of Electronics, Department of Electrical Engineering, Massachusetts Institute of Technology, Cambridge 02139; and 4Center for Adaptive Systems, Boston University, Boston, Massachusetts 02215
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
DiZio, Paul, Richard Held, James R. Lackner, Barbara Shinn-Cunningham, and Nathaniel Durlach. Gravitoinertial Force Magnitude and Direction Influence Head-Centric Auditory Localization. J. Neurophysiol. 85: 2455-2460, 2001. We measured the influence of gravitoinertial force (GIF) magnitude and direction on head-centric auditory localization to determine whether a true audiogravic illusion exists. In experiment 1, supine subjects adjusted computer-generated dichotic stimuli until they heard a fused sound straight ahead in the midsagittal plane of the head under a variety of GIF conditions generated in a slow-rotation room. The dichotic stimuli were constructed by convolving broadband noise with head-related transfer function pairs that model the acoustic filtering at the listener's ears. These stimuli give rise to the perception of externally localized sounds. When the GIF was increased from 1 to 2 g and rotated 60° rightward relative to the head and body, subjects on average set an acoustic stimulus 7.3° right of their head's median plane to hear it as straight ahead. When the GIF was doubled and rotated 60° leftward, subjects set the sound 6.8° leftward of baseline values to hear it as centered. In experiment 2, increasing the GIF in the median plane of the supine body to 2 g did not influence auditory localization. In experiment 3, tilts up to 75° of the supine body relative to the normal 1 g GIF led to small shifts, 1-2°, of auditory setting toward the up ear to maintain a head-centered sound localization. These results show that head-centric auditory localization is affected by azimuthal rotation and increase in magnitude of the GIF and demonstrate that an audiogravic illusion exists. Sound localization is shifted in the direction opposite GIF rotation by an amount related to the magnitude of the GIF and its angular deviation relative to the median plane.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Interaural timing, phase, and amplitude spectra
are important cues for judging the azimuth of a broadband sound
relative to the median plane of the head (cf. Blauert
1983; Colburn and Durlach 1978
; Yost and
Gourevitch 1987
). The physical transformations that a sound
waveform undergoes by interacting with the head and pinnae can be
described by linear filters called head-related transfer functions
(HRTFs) (Wightman and Kistler 1980
). HRTFs are unique
for each location around the head in humans because their ears are
immobile. Binaural acoustical patterns are not the only factors
influencing a sound source's perceived location. Proprioceptive and
somatosensory information about target location derived from hand
contact can also influence where an auditory stimulus is heard
(Lackner and Shenker 1985
). Head movements can help
resolve auditory front-back ambiguities and the elevation of an
external sound source (Wallach 1940
). Their influence
depends on relating movement-contingent auditory, proprioceptive, and vestibular signals. Head movements can also be used to re-calibrate sound localization when pseudophones are worn that alter the auditory cues at the ears from an external sound source (Held
1955
).
Rotary acceleration of the whole body also
influences the perceived auditory azimuth of a sound stimulus. A
blindfolded listener in a rotating chair will hear a head-fixed,
midline, sound source as moving and displacing relative to his or her
head, a phenomenon known as the audiogyral illusion (Clark and
Graybiel 1949). The auditory target will be heard to displace
in the direction opposite self-rotation when the chair accelerates, to
come back to the midline when constant velocity is maintained, and to
displace again during deceleration (Arnoult 1952
;
Clark and Graybiel 1949
; Lester and Morant
1970
; Munsterberg and Pierce 1894
). Thus
during clockwise acceleration to constant velocity, a midline sound
source will be heard to the left of the head's midline and then during deceleration will be heard to the right of midline.
Graybiel and Niven (1951) found that linear acceleration
influenced auditory localization as well and referred to this as the
"audiogravic illusion." If an observer is seated off-center in a
rotating room, radial centripetal forces combine with gravity to
generate a resultant linear gravitoinertial force (GIF) vector greater
than either component and oriented between the two. Graybiel and Niven
had seated observers face the center of a slow rotation room and lean
over 90° to one side. A ring of speakers was positioned in the
head's azimuthal plane at 5° separations. As the room began to spin,
the GIF was displaced in relation to the head in azimuth (see Fig.
1). The observers were asked to indicate
which speaker emitted a sound in the apparent horizontal plane. When
the room was stationary, the median plane of the laterally flexed head was horizontal, and observers correctly indicated a sound from the
speaker located in that plane. When the room was spinning, the GIF was
rotated inboard, and observers felt their whole body was tilted
backward or outboard. They now identified as being in the horizontal
plane sounds emitted by a speaker physically below the median plane of
their head. Howard and Templeton (1966)
and
Howard (1982)
have argued that this effect is not an
audiogravic illusion but represents accurate auditory localization with
respect to a changed reference frame. In other words, the subject feels tilted in relation to the horizontal and thus chooses a speaker that is
displaced in relation to his or her body by the extent of the apparent
self-tilt.
|
Our goal in the present experiments was to determine whether a genuine audiogravic illusion exists such that sound localization vis a vis the head itself is altered. To do so, we measured head-centric auditory localization in azimuth during exposure to GIF transitions in a rotating room. Using head-relative instead of horizon-relative localization avoids the issue of a changed external reference frame for localization. We also used greater changes in GIF magnitude and direction and a more comfortable posture for the subjects than Graybiel and Niven. Our aims included determining whether changes in the angle of GIF, the magnitude of GIF, or a combination of the two lead to changes in head-relative auditory localization. We also wanted to observe the time course of any changes.
Whether a head-relative audiogravic illusion exists has important
theoretical implications. Binaural acoustic information such as
interaural time and spectral differences are intrinsically in a
head-centric frame of reference in humans. By contrast, neural maps in
the colliculus of cats, animals with motile ears, have receptive fields
defined in head-centric coordinates that include compensation for ear
movements (Middlebrooks and Knudsen 1987). Jay
and Sparks (1984)
have shown that the auditory receptive fields of visual-auditory units in the primate superior colliculus change as a
function of eye position so that the auditory and visual maps stay in
register. Spatially tuned auditory-visual neurons exist in the primate
parietal cortex as well (Stricane et al. 1996
).
Psychophysical experiments have shown that eye position and head
position can affect auditory localization in humans (Lewald and
Ehrenstein 1996
, 1998
). In the cat auditory cortex, the
representation of sound location is distributed over large populations
of very broadly tuned neurons that respond to multiple acoustic
parameters (Middlebrooks et al. 1998
). Our investigation
of vestibular and somatic influences on sound localization will further
identify spatial reference frames for multi-modal neural coding. In
addition, understanding audiogravic effects has potential practical
applications in instruments providing orientation cues that pilots
might use to prevent disorientation in unusual flight environments
(Teas 1993
).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experiment 1: twofold increase and 60° rotation of GIF
subjects. Fourteen subjects, nine males and five females, including two of the authors participated. Their ages ranged from 20 to 55 yr. The selection criteria included self-reports of normal hearing, balance, and posture and no general health restrictions that would make exposure to 2.0 g hazardous. The procedures used were approved by the Brandeis Human Subject Committee and were explained to subjects before they gave informed consent.
apparatus. The experiment was performed in the Graybiel Laboratory slow rotation room (SRR), a circular enclosure 6.7 m in diameter powered by electric motors. A dedicated controller with a computer interface permits the programming of desired angular velocity profiles. The on-board equipment included a "bed" that could be tilted around its long axis, provisions for subject restraint, a system for generating spatially localizable sounds, and a joystick for the subject to indicate responses. Figure 2A illustrates the experimental situation.
|
procedure. The subjects were blindfolded throughout the experiment. They were always kept earth-horizontal while the magnitude and orientation of GIF were manipulated by rotating the SRR. In the prerotation baseline phase, the SRR was stationary while auditory settings to the midsagittal plane of the head were made over a 100-s period. In phase two, the SRR was accelerated at 1°/s2 for 152 s, held at 152°/s for 100 s, and decelerated to a stop at 1°/s2. At constant velocity the resultant GIF was tilted 60° with respect to the subject's median plane and had a magnitude of 2.0 g. The third phase with the SRR stationary followed immediately and lasted for 100 s. A fourth identical phase followed after a 300-s delay. An entire run took 1,004 s. Figure 2B illustrates the SRR speed as well as GIF magnitude and direction during the rotation phase of a run. Figure 3A shows the experimental conditions during the baseline and constant velocity phases.
|
Experiment 2: twofold increase of GIF in the midsagittal plane
We again doubled GIF magnitude but arranged for it to rotate into rather than out of alignment with the subject's median plane. This allowed us to determine whether an increase in magnitude of GIF per se would elicit an audiogravic illusion or whether a displacement relative to the sagittal plane is also necessary.
Ten subjects participated. Nine had been in experiment 1, including two of the authors. All gave informed consent to the Human Subject Committee approved protocol. The apparatus and procedure were the same as in experiment 1 with one exception. The restrained subject was tilted 60° right ear down from the supine position toward the center of the rotating room (see Fig. 3B). In the no-rotation periods, the GIF equaled 1.0 g and was oriented 60° left of the subject's median plane; when the room was rotating at 152°/s constant velocity, the GIF equaled 2.0 g and was aligned with the subject's median plane. The average of the five prerotation midline settings for each subject was taken as his or her zero baseline.
Experiment 3: tilt of the median plane in a normal 1.0 g environment
Six subjects who had participated in the prior experiments took part. The rotating room was always stationary so that the GIF was always 1.0 g. The subject's orientation to gravity was set to 1 of 11 bed angles around the z-axis between 75° right and left at 15° increments (see Fig. 3C). Subjects made auditory settings to center a sound in the head's median plane as in the earlier experiments. The bed angles were presented in random order and each angle was repeated six times within a session. A position was held long enough for the subject to make one setting and then the bed was manually moved to a new position.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experiment 1
Figure 4A shows the averaged sequential auditory midline settings for subjects exposed to rightward rotation of the GIF relative to the midsagittal plane. During acceleration, auditory settings shifted to the right relative to the 1.0 g baseline and then plateaued at constant velocity (GIF equal 2.0 g, tilted 60° right re the head). In the six trials done at constant velocity, subjects indicated as being straight ahead auditory stimuli 7.3 ± 4.17° (mean ± SD) right of the baseline settings. During deceleration, settings shifted back toward prerotation baseline, reaching their resting level before the room came to a stop. In the immediate postrotation period, the average auditory setting was 2.98 ± 6.031° left of prerotation. This value was virtually unchanged five minutes later, 3.01 ± 5.4° left of baseline.
|
ANOVA (SPSS MANOVA procedure) revealed significant differences
[F(3,30) = 4.73, P = 0.008] among the
four steady GIF periodsprerotation, constant velocity, immediate
postrotation, and delayed postrotation. Pairwise contrasts indicated
that auditory settings in the constant velocity phase differed
significantly from each of the no-rotation conditions
(P < 0.026 at least), but the no-rotation conditions did not differ from one another.
An ANOVA was also performed to test for differences in trial-to-trial variability across the steady GIF periods. The standard deviation of each subject's settings in each GIF period was used as a measure of variability. The overall test was significant [F(3,30) = 4.02, P = 0.034]. The constant velocity condition was significantly more variable (7.19° standard deviation) than the three no-rotation conditions collectively (5.28°), P < 0.05. It took on average of 6.9 s to complete an auditory setting. There was no effect of rotation on the time to make a setting.
Figure 4B shows the auditory midline settings of the subjects who were exposed to a leftward shift of the GIF during rotation. Their results were directionally opposite to those tested with rightward GIF rotation. During acceleration, auditory settings shifted leftward relative to baseline and at constant velocity rotation peaked at 6.8° leftward. During deceleration, the settings shifted back toward prerotation baseline and were at baseline by the time the room fully stopped. As with the subjects exposed to rightward displacement of the GIF, a MANOVA indicated that auditory settings varied significantly across the prerotation, constant velocity, immediate postrotation, and final postrotation periods [F(3,13) = 34.6, P = 0.004]. Only the constant velocity period settings differed significantly from the other conditions in pairwise comparisons. The trial-to-trial variability (standard deviation) was also greater in the constant velocity period compared with the other three periods.
Experiment 2
The results are plotted in Fig. 5. There was very little shift relative to prerotation baseline during acceleration, settings averaged 2.3° right of baseline during constant velocity, 0.37° right immediately postrotation and 1.66° left in the delayed postrotation period. Analysis of variance revealed no significant difference among the four periods [F(3,27) = 1.74, P = 0.182].
|
Experiment 3
The results are presented in terms of angles of the GIF relative to the subject's median plane with positive angles representing rightward displacement of the GIF in relation to the median plane. The midline settings at zero tilt angle were used as the baseline reference value. Each subject's six repeated settings at the same tilt angle were averaged and linear regression lines were fit to the auditory settings versus GIF tilt. Statistical comparisons were made of the average slopes. Figure 6 summarizes the results.
|
In tilted conditions, the settings shifted slightly but systematically
in the direction that the GIF rotated. The average slope was only 0.05, but this was significantly different from 0 (t = 6.497, P < 0.001) because the results were very
consistent from subject to subject.
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experiment 1
The observations in experiment 1 unequivocally confirm the existence of an audiogravic illusion when the GIF vector is increased in magnitude and rotated away from the median plane of the head. Sounds must be shifted in the same direction as the rotation of the GIF relative to head azimuth to be perceived in the head's median plane.
Experiment 2
The results in experiment 2 indicate that an audiogravic illusion does not occur when the GIF doubles and rotates into the median plane of the head and body. The absence of an auditory shift in this condition and the significant shifts seen in experiment 1 indicate that an increase in GIF magnitude in the sagittal plane is not sufficient to cause an audiogravic illusion but that a rotation of the GIF vector is necessary for the shift in localization to be induced. The final experiment determined how auditory localization would be affected by the direction of the GIF vector when its magnitude was always 1 g.
The findings in experiment 3 point to small but systematic changes in perceived azimuth of an acoustic stimulus when a subject is reoriented in a normal terrestrial force background. A rightward rotation of GIF relative to the median plane requires a rightward shift of auditory settings for a sound to be heard in the subject's median plane. The direction of this effect is consistent with what was observed in amplified fashion at 2.0 g in experiment 1.
General discussion
We conclude that a true audiogravic illusion exists in the form of
a head-relative shift in auditory localization during exposure to a
changing linear GIF resultant. The apparent direction of an auditory
target shifts in the same plane but in the opposite direction to the
displacement of the GIF resultant. In other words, increasing the
magnitude of the GIF resultant and changing its direction relative to
the head and torso induces an apparent displacement of a sound source
relative to the head in the opposite direction. In their original
study, Graybiel and Niven (1951) used ambient sound
sources and had subjects make localization judgments relative to the
apparent horizontal. They observed changes in auditory settings that
corresponded to about 80% of the angular displacement of the GIF
resultant. Howard (Howard 1982
; Howard and
Templeton 1966
) argued that this shift does not represent an
illusion but is a change attributable to using a new reference frame,
that what needs to be explained is why the shift is not 100%. The head relative shifts we have observed in the present study correspond to
about 20% of the shift of the GIF resultant. The Graybiel and Niven (1951)
results thus reflect a reference frame shift and a
true audiogravic illusion.
We have found that a shift in sound lateralization is produced if the
GIF resultant rotates away from the median plane and simultaneously
increases in magnitude from 1.0 to 2.0 g. There is little or
no bias if the GIF rotates into alignment with the median plane during
the transition from 1.0 to 2.0 g. The auditory shifts are
tightly coupled to temporal changes in GIF, and they return to baseline
without significant aftereffects on return to a 1 g GIF. The
small change in auditory localization associated with rotating the GIF
relative to the sagittal plane of the head complements and is
consistent with the findings of Lewald and Ehrenstein
(1998), who found that turning the head relative to the torso
without changing gravitoinertial orientation induces the same direction
of auditory shift.
The existence of an audiogravic illusion indicates an additional level
of representation or analysis in computational neural maps subserving
auditory localization. HRTF pairs encode target location in an
intrinsic head-centric coordinate system. Psychophysical mappings of
HRTF information to perceived azimuth have been established empirically
(Wightman and Kistler 1989). However, the relationship between physical acoustic information (HRTFs) and perceived spatial location is remapped by alterations in GIF. This means the neural computations underlying sound localization interrelate binaural auditory HRTF information about the acoustic target with vestibular, proprioceptive, and somatosensory representations of GIF direction and magnitude.
The GIF influence on auditory localization may act at a level that
affects sensory localization in multiple modalities. For example, a
comparison of the audiogravic and oculogravic illusions suggests that
alterations in GIF may have parallel effects on auditory and visual
localization. The oculogravic illusion is a change in the perceived
position or orientation of an object that is physically stationary in
relation to an observer when the observer is exposed to a change in
direction and magnitude of the GIF vector (Corriea et al.
1968; Graybiel 1952
; Miller and Graybiel
1968
). The audiogravic and oculogravic illusions are
similar
stationary auditory and visual targets appear to move and
displace in the direction opposite the rotation of a supra-1 g GIF resultant. The audiogravic illusion we have
demonstrated is with respect to the head's azimuthal plane while the
oculogravic illusion has been tested primarily in the sagittal and
frontal planes. Nevertheless, the similarity between the oculogravic
and audiogravic illusions raises the possibility of parallel changes in
visual and auditory spatial representations or of a common change
altering multisensory localization. We have, in fact, completed studies
of the oculogravic illusion during changes of GIF in azimuth and find
that it matches the audiogravic illusion in amplitude and timing
(DiZio, Lackner, and Held, unpublished data) This implies a common
mechanism subserving both illusions, one in which the assignment of
spatial direction relative to the head involves signals specifying body
orientation in relation to the resultant GIF vector. Parietal cortex
contains representations of the necessary reference frames for
implementing such a transformation (cf. Andersen et al.
1997
; Colby and Duhamel 1996
; Kalaska et
al. 1997
; Stein and Meredith 1993
).
![]() |
ACKNOWLEDGMENTS |
---|
This work was supported by Air Force Office of Scientific Research Contract F49620110171.
![]() |
FOOTNOTES |
---|
Address for reprint requests: P. DiZio, Ashton Graybiel Spatial Orientation Laboratory, Brandeis University-MS033, Waltham, MA 02454-9110 (E-mail: dizio{at}brandeis.edu).
Received 18 September 2000; accepted in final form 16 February 2001.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
Visit Other APS Journals Online |