1Eaton-Peabody Laboratory,
Delgutte, Bertrand,
Philip X. Joris,
Ruth Y. Litovsky, and
Tom C. T. Yin.
Receptive fields and binaural interactions for virtual-space stimuli in
the cat inferior colliculus. Sound localization depends on
multiple acoustic cues such as interaural differences in time (ITD) and
level (ILD) and spectral features introduced by the pinnae. Although
many neurons in the inferior colliculus (IC) are sensitive to the
direction of sound sources in free field, the acoustic cues underlying
this sensitivity are unknown. To approach this question, we recorded
the responses of IC cells in anesthetized cats to virtual space (VS)
stimuli synthesized by filtering noise through head-related transfer
functions measured in one cat. These stimuli not only possess
natural combinations of ITD, ILD, and spectral cues as in free field
but also allow precise control over each cue. VS receptive fields were
measured in the horizontal and median vertical planes. The vast
majority of cells were sensitive to the azimuth of VS stimuli in the
horizontal plane for low to moderate stimulus levels. Two-thirds showed
a "contra-preference" receptive field, with a vigorous response on the contralateral side of an edge azimuth. The other third of
receptive fields were tuned around a best azimuth. Although edge
azimuths of contra-preference cells had a broad distribution, best
azimuths of tuned cells were near the midline. About half the cells
tested were sensitive to the elevation of VS stimuli along the median
sagittal plane by showing either a peak or a trough at a particular
elevation. In general receptive fields for VS stimuli were similar to
those found in free-field studies of IC neurons, suggesting that VS
stimulation provided the essential cues for sound localization.
Binaural interactions for VS stimuli were studied by comparing
responses to binaural stimulation with responses to monaural
stimulation of the contralateral ear. A majority of cells showed either
purely inhibitory (BI) or mixed facilitatory/inhibitory (BF&I)
interactions. Others showed purely facilitatory (BF) or no interactions
(monaural). Binaural interactions were correlated with azimuth
sensitivity: most contra-preference cells had either BI or BF&I
interactions, whereas tuned cells were usually BF. These correlations
demonstrate the importance of binaural interactions for azimuth
sensitivity. Nevertheless most monaural cells were azimuth-sensitive,
suggesting that monaural cues also play a role. These results suggest
that the azimuth of a high-frequency sound source is coded primarily by
edges in azimuth receptive fields of a population of ILD-sensitive cells.
Sound localization is a complex process that
integrates sensory information with cognitive influences. Three main
acoustic cues contribute to sound localization: interaural disparities in time (ITD) and level (ILD) and spectral cues (Blauert
1983 Such control can be achieved in dichotic studies that deliver stimuli
through closed acoustic systems. Many studies have shown that cells in
the auditory brain stem and midbrain are sensitive to ITD and ILD
(Goldberg and Brown 1969 It is possible to simulate the sound-pressure waveforms produced in the
ear canals by free-field sound sources through closed acoustic systems.
Pioneered in the 1970s (Blauert 1983 One reason for choosing the inferior colliculus (IC) as the site for
applying VS techniques is its rich pattern of inputs from brain stem
auditory nuclei (Adams 1979 A traditional technique for assessing the relative importance of
monaural spectral cues and interaural disparity cues for sound
localization is monaural ear occlusion. This technique is popular in
human psychophysics (see Wightman and Kistler 1997 The present report focuses on a quantitative description of spatial
receptive fields in the horizontal and median vertical planes of the
frontal hemifield for cells in the inferior colliculus of anesthetized
cats using VS stimuli. Responses to VS stimuli are described for both
binaural and monaural stimulation to assess the role of binaural
interactions in shaping receptive fields. We also compare responses to
VS stimuli with responses to broadband noise stimuli that have been
used traditionally in dichotic studies. In a subsequent paper, we use
VS techniques for identifying which acoustic cues are most important
for the directional sensitivity of IC cells. A preliminary report of
these findings has appeared (Delgutte et al. 1995 The results presented in this paper are based on two separate
series of experiments: six experiments were carried out at the University of Wisconsin in Madison, whereas eight others were carried
out at the Massachusetts Eye and Ear Infirmary in Boston. Unless
otherwise noted, techniques for both series of experiments were very
similar and examination of their results revealed no substantial
differences so that both sets of data were pooled.
Recording techniques
Methods for recording from single units in the IC of
barbiturate-anesthetized cats are essentially the same as described by Yin et al. (1986) The animal was placed in a double-walled, electrically shielded,
sound-proof room. The dorsal surface of the IC was exposed on the left
side by a craniotomy anterior to the tentorium and aspiration of the
overlying cerebral cortex. Parylene-insulated tungsten microelectrodes
(Microprobe, Clarksburg, MD) with exposed tips of 8-12 µm were
mounted on a remote-controlled hydraulic microdrive and aimed at the
IC. Spikes from single units were amplified and isolated. The times of
detected spikes were measured by a custom-built timer with a resolution
of 1 µs and stored in a computer file for analysis and display.
Cells encountered in the dorsalmost millimeter of an electrode
penetration were broadly tuned to high frequencies. Further ventrally,
characteristic frequencies (CFs) rapidly dropped to low frequencies,
after which a regularly increasing sequence of CFs was encountered. The
rapid drop in CF was taken as the dorsal boundary of the central
nucleus of the inferior colliculus (ICC), and all units encountered as
the CFs increased were assumed to be in the ICC.
Recording techniques for the Boston experiments were essentially the
same as those of the Madison experiments with two exceptions. First,
dial-in urethan (75 mg/kg ip) rather than pentobarbital sodium was used
for anesthesia. Second, the posterior surface of the IC rather than its
dorsal surface was exposed via a posterior-fossa craniotomy and
aspiration of the overlying cerebellum. The electrode was oriented
nearly horizontally in a parasagittal plane, approximately parallel to
iso-frequency laminae (Merzenich and Reid 1974 Histology
Histological processing for reconstruction of the electrode
tracks was performed for nine cats. At the end of the experiment, the
brain was fixed by either perfusion or immersion in aldehyde fixatives,
and the brain stem processed for either paraffin-embedded or frozen
sections stained with cresyl violet. The vast majority of tracks
clearly traversed the ICC. Because the dorsal border of the ICC is hard
to determine in Nissl sections, some electrode tracks from the
dorsalmost horizontal penetrations may have encompassed the pericentral
nucleus. There were no obvious physiological differences between these
tracks and those that were unambiguously in the ICC so that it seems
appropriate to treat our entire sample of cells as being from the ICC.
Stimuli
Acoustic stimuli consisted of tone bursts, broadband noise, and
VS stimuli presented either binaurally or monaurally. All stimuli were
generated digitally (16 bits), then converted to analogue signals using
sampling rates of either 80 or 100 kHz and antialiasing filters.
Stimulus levels in each ear were set by custom-built programmable
attenuators having resolutions of either 1 (Madison) or 0.1 dB (Boston).
The attenuated output of the D/A converter was sent to an acoustic
assembly comprising an electrodynamic speaker (Realistic 40-1377) and
a calibrated probe-tube microphone (Larson-Davis 2530 or Brüel
and Kjaer 1/2-in). The assembly was inserted into the cut end of the
ear canal to form a closed system. The sound pressure near the tympanic
membrane was measured as a function of frequency from 50 Hz to 40 kHz,
and these measurements were used to synthesize digital filters that
equalized the response of the acoustic system. This equalization
technique gave a flat frequency response within ±2 dB for frequencies
<25 kHz.
Bursts of broadband, Gaussian noise were synthesized by a random number
generator. Noise bursts were 200 or 250 ms in duration and had
rise-fall times of either 4 or 20 ms. The same sample of pseudorandom
noise was used throughout an experiment and, when stimuli were
delivered binaurally, the same waveform was applied to both ears. These
broadband noise bursts were equalized digitally, then either directly
delivered to the acoustic systems or preprocessed by digital filters to
generate VS stimuli. In either case, the stimulus repetition rate was
normally two per second, although slower rates occasionally were used
for units that showed fatigue.
The method for synthesizing virtual-space stimuli was similar to that
used in the human psychophysical experiments of Wightman and
Kistler (1989) Digital filters for equalization and synthesis of VS stimuli were
implemented in the frequency domain using fast Fourier algorithms (Oppenheim and Schafer 1989 Figure 1 shows waveforms and power
spectra of the VS stimuli for two azimuths along the horizontal plane
(0 and 18° to the right, respectively). Only the first 3 ms of each
noise waveform are plotted. For 0° azimuth, the waveforms and spectra
are similar in both ears, as expected for a sound source located in the
median plane. The power spectra (measured with a resolution of 1/6
octave) show prominent notches at 11.5 and 23 kHz. For +18° azimuth,
the waveform in the right ear has both a higher amplitude and a shorter latency than that in the left ear. These are the expected ILDs and
ITDs. ILDs are even more apparent in the power spectra, where the
magnitude in the right ear exceeds that in the left ear by 15-20 dB
over most of the frequency range. The power spectra show prominent
notches for 18° as they do at 0°, but first-notch frequencies differ somewhat for the two azimuths. Thus the VS stimuli possess three
different cues to the azimuth of the sound source: ITD, ILD, and
spectral notches.
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
; Searle et al. 1976
). Physiological studies
under free-field stimulation have shown that many cells in the auditory
midbrain are sensitive to the direction of sound sources (King
and Palmer 1983
; Knudsen 1982
; Knudsen
and Konishi 1978
; Semple et al. 1983
; see
Irvine 1992
for review). However, free-field studies
alone cannot determine which acoustic cues are responsible for this
directional sensitivity because they do not allow independent control
over each cue.
; Rose et al.
1966
; reviewed by Irvine 1986
, 1992
). With few
exceptions (e.g., Caird and Klinke 1987
), these studies
varied a single cue without consideration of possible interactions
between cues. Furthermore most studies have focused on pure tone
stimuli, which do not contain the spectral cues provided through
directionally dependent filtering by the pinnae.
), these "virtual-space" (VS) techniques now are used widely in human
psychophysics (Blauert and Hartung 1997
;
Bronkhorst 1995
; Wightman and Kistler 1989
, 1992
,
1997
) and also are being applied to physiological studies of
sound localization in animals (Brugge et al. 1994
; Delgutte et al. 1995
; Keller et al. 1998
;
Nelken et al. 1997
; Poon and Brugge 1993
;
Rice et al. 1995
). VS techniques provide stimuli with
multiple, realistic localization cues and also give precise control
over individual cues. In the present study, VS techniques were used for
studying how sensitivity to various localization cues contributes to
spatial sensitivity in the cat inferior colliculus. We used
head-related transfer functions (HRTFs) measured in one cat by
Musicant et al. (1990)
to synthesize VS stimuli
possessing realistic ITDs, ILDs, and spectral cues.
; Oliver and Huerta 1992
; Oliver and Shneiderman 1991
). The IC
receives inputs from nuclei specialized for processing interaural time
and level disparities such as the medial superior olive and the lateral
superior olive (LSO) (Boudreau and Tsuchitani 1968
;
Joris and Yin 1995
; Yin and Chan 1990
).
It also receives inputs from the contralateral dorsal cochlear nucleus,
which has been implicated in the processing of monaural spectral cues
for sound localization (Young et al. 1992
). Such
convergence of inputs suggests that the IC may play an important role
in cue integration, a phenomenon ideally suited to VS techniques.
Another reason for applying VS techniques to the IC is that a large
body of data are available on responses of IC neurons to both
free-field stimulation (Aitkin and Martin 1987
, 1990
;
Aitkin et al. 1984
, 1985
; Calford et al.
1986
; Moore et al. 1984a
,b
; Semple et al.
1983
) and dichotic stimuli varying in ITD and ILD (see
Irvine 1986
, 1992
; Yin and Chan 1988
for
reviews). These data can help in verifying the validity of VS
stimulation and in understanding neural mechanisms underlying
sensitivity to individual cues in VS stimuli.
for
review) and also has been applied to single-unit studies in animals
(Knudsen and Konishi 1980
; Middlebrooks
1987
; Samson et al. 1993
1994
).
While seemingly straightforward, monaural ear occlusion experiments
actually are fraught with difficulties. A major issue is the interaural
attenuation provided by ear plugs. Wightman and Kistler
(1997)
showed that even a strongly attenuated (>30 dB) input
from the plugged ear still produces interaural disparities that
contribute to sound localization. The same difficulty arises in
single-unit studies, where an additional issue is reproducibility of
the multiple plug insertions that are required to record responses of
each neuron to both monaural and binaural stimulation. VS stimuli offer
the advantage that monaural stimulation can be obtained by simply
turning off the acoustic input to one ear, providing much better
interaural attenuation than typical ear plugs.
).
METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
and Carney and Yin
(1989)
. In the Madison experiments, healthy adult cats free of
middle-ear infection were anesthetized by intraperitoneal injection of
pentobarbital sodium (35 mg/kg). A venous canula was used for injecting
additional doses of anesthetic to maintain a surgical level of
anesthesia throughout the experiment. The cat's temperature was
monitored by a rectal thermometer and maintained at 37°C with a
heating pad. A tracheal canula was inserted, both pinnae were dissected
away, and the ear canals severed to allow insertion of acoustic
assemblies. A small hole was drilled into each bulla, and a 60-cm
plastic tube (0.9 mm ID) was inserted to prevent static pressure
build-up in the middle ear.
). In these horizontal penetrations, sparse, poorly responsive units were
encountered in the posterior 500-800 µm as described by
Semple and Aitkin (1979)
, after which there was a
noticeable increase in background activity and a higher density of
sharply tuned single units.
and the physiological studies of Poon and
Brugge (1993)
and Brugge et al. (1994)
. The
equalized, pseudorandom broadband noise was processed through digital
filters constructed from HRTFs measured in one "standard" cat by
Musicant et al. (1990)
. These HRTFs (1 for each spatial
position and each ear) represent the directionally dependent
transformation of sound pressure from free field to the ear canal. Thus
the sound-pressure waveforms produced in both ear canals by the closed
systems were the same as for free-field stimuli originating from a
particular direction in the standard cat. VS stimuli were synthesized
for azimuths varying from
90 to +90° in the horizontal plane and
for elevations ranging from
36 to +90° in the median vertical
plane. Positive azimuths and elevations correspond to virtual sound
sources contralateral to the recording site and above the ears, respectively.
). Two points required
special care. First, an additional band-pass filter was introduced to
restrict stimulus components between 2 and 35 kHz, the range where the HRTFs of Musicant et al. (1990)
are the most reliable.
Thus the VS stimuli contained no energy <2 kHz where ITDs are most
useful. Second, in some animals the frequency response of the acoustic system showed a rapid roll-off at high frequencies. Attempts to digitally equalize this roll-off yielded very poor signal-to-noise ratios because virtually the entire amplitude range of the D/A converter was occupied by boosted high-frequency components. To avoid
this problem, the upper cutoff frequency of the band-pass filter was
lowered to 25 kHz for these animals.
View larger version (32K):
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Fig. 1.
Examples of virtual-space (VS) stimuli for 2 source positions along the
horizontal plane: 0° azimuth (left) and 18° toward
the right (right). Stimuli were obtained by filtering a
burst of random noise. A and B: power
spectra of the sound pressures at the tympanic membranes in each ear.
Spectra were analyzed through a 1/6-octave Gaussian filter bank.
C-E: sound-pressure waveforms at the tympanic
membranes. Only the first 3 ms of the 200-ms noise bursts are shown.
Procedure
Either broadband noise bursts or tone bursts of varying
frequency were used as search stimuli. Once a single unit was isolated, its frequency tuning curve was measured using an automatic tracking procedure (Kiang and Moxon 1974) to determine the CF. In
rare cases when the tracking procedure failed (e.g., for units with closed response areas), the CF was estimated by audiovisual criteria.
After determining the CF, a rate-level function was measured for the VS
stimulus located directly in front (0° azimuth, 0° elevation), from
which a sound level was chosen (usually 15-20 dB above threshold) for
subsequent stimuli. Responses to VS stimuli were then studied as a
function of azimuth or elevation, using 20 stimulus presentations for
each location. Azimuths were presented from 90 to +90° in 9°
steps and elevations from
36 to +90°, in ascending (Madison) or
randomized (Boston) sequences. VS stimuli were presented both
binaurally and monaurally to characterize binaural interactions, and in
some units, at more than one stimulus level.
Specification of stimulus level for VS stimuli requires special care
because the gains of the HRTFs, and therefore sound pressures at the
tympanic membranes, depend on the location of the sound source. In the
Boston experiments, we specify the SPL that a free-field stimulus would
have at the center of the cat's head in the absence of the animal.
Responses to VS stimuli were studied for free-field SPLs ranging from
20 to 60 dB in these experiments, with 65% of the measurements made at
SPLs of 40 dB. In the Madison experiments, we could not always
calculate free-field SPLs, so instead we specify a "nominal SPL"
such that 127 dB corresponds to the unattenuated output of the D/A
converter. Free-field SPLs typically would be 30-50 dB lower than
nominal SPLs, depending on the experiment.
To compare azimuth sensitivity for VS stimuli with ILD sensitivity for
stimuli devoid of spectral features, responses to broadband noise were
studied as a function of ILD. Typically, ILD was varied over a ±30 dB
range by increasing the SPL at one ear while decreasing the SPL at the
other ear so as to keep the mean binaural level (MBL, the arithmetic
mean of the SPLs in dB at both ears) constant. This "MBL-constant
method" roughly mimics the changes in SPL that occur when a sound
source is moved in the horizontal plane (Irvine 1987b).
For some cells, ILD also was varied by changing the SPL in the
ipsilateral ear while keeping the contralateral SPL constant ("contra-constant method"). Although less realistic than the
MBL-constant method, this simpler method is useful for characterizing
mechanisms of binaural interactions (Irvine 1987a
).
Positive numbers denote ILDs favoring the contralateral ear, consistent
with the convention for azimuth.
DATA ANALYSIS. Discharge rate was averaged over the entire stimulus duration (200 or 250 ms), and rate-level, rate-ILD, rate-azimuth, and rate-elevation functions were smoothed by three-point triangular filters. Summary statistics derived from these basic data are introduced in RESULTS.
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RESULTS |
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Azimuth receptive fields for VS stimuli
Our results are based on recordings from 173 single units in 14 cats. We selected cells with CFs >4 kHz because the VS stimuli had
little energy <2 kHz and the spectral features such as notches are
only found in HRTFs for frequencies >8 kHz (Musicant et al. 1990). The data presented here are from a subset of 96 units
for which we obtained responses to VS stimuli presented both binaurally and monaurally. Virtually all the cells encountered responded to VS
stimuli and, among these, a vast majority showed directional sensitivity for azimuth at moderate stimulus levels.
Figure 2 shows both temporal patterns and average rates of discharge as a function of azimuth for two cells from the same cat. Temporal discharge patterns in A and B are shown as dot rasters based on 20 stimulus presentations for each of 21 azimuths. For the cell in Fig. 2, left, the average rate was clearly directional: it was low for ipsilateral (negative) azimuths, then rose to a maximum at +9° azimuth before settling to a broad plateau on the contralateral side. The dot raster shows that discharges occurred in brief bursts at specific times during the 200-ms stimulus. Although these bursts tended to occur at the same times for wide ranges of azimuths, the temporal discharge patterns did provide some additional directional information over that available in the average rate. In interpreting these temporal patterns, it is important to keep in mind that stimulus waveforms were synthesized by filtering the same sample of pseudorandom noise through different HRTFs. Thus the preferred times of discharge are likely to reflect features of the envelope of this specific noise waveform, as seen through the frequency selectivity of the neuron.
|
For the cell in Fig. 2, right, the rate response was poorly
directional but the temporal discharge pattern still contained information about azimuth. Examples such as these are unusual, in part
because most cells in our sample had more directional rate responses
than this one. Furthermore both cells in Fig. 2 were selected because
their temporal discharge patterns showed particularly prominent
directional information. About 1/3 of the cells tested only responded
at the onset of the VS stimuli. For these cells, the only directional
information available in the temporal discharge pattern was a variation
in latency with azimuth. Nevertheless, Fig. 2 suggests that at least
some IC neurons may code sound-source location in their temporal
discharge patterns as well as their averages rates (Middlebrooks
et al. 1994). In the remainder of RESULTS, we focus
on how azimuth and elevation are coded in the average rates of
discharge of IC neurons.
Types of azimuth receptive fields
Cells were initially classified based on whether they were
sensitive to changes in azimuth using the modulation index
MI = (RMAX RMIN)/RMAX, where
RMAX and RMIN are,
respectively, the maximum and minimum discharge rates over the entire
range of azimuths (Fig. 3A,
inset). Figure 3A shows the distribution of
azimuth modulation indices for our sample of cells. The distribution is highly skewed toward large modulation indices, with nearly half the
responses (50/105) being 100% modulated. Although cells with CFs
between 6 and 15 kHz had, on the average, the highest modulation indices, fully modulated units were found in all CF regions. Thus sensitivity to azimuth of VS stimuli is a robust feature of the IC cell
population at moderate stimulus levels.
|
Cells then were classified into four groups based on their
azimuth receptive field for VS stimuli. This classification scheme is
similar to those used in free-field studies of auditory neurons (Aitkin and Martin 1987; Imig et al.
1984
; Rajan et al. 1990
). Examples of each type
of receptive field are shown in Fig. 4.
|
CONTRA-PREFERENCE UNITS.
One key element in classifying directional units is the "best
azimuth," the location where the response is maximal.
Contra-preference units (Fig. 4A) are those for which the
response falls <50% of maximum on the ipsilateral side of the best
azimuth but remains >50% on the contralateral side. These units
formed the majority (63/105, 60%) of our sample. For these units, a
characteristic feature (CF) is the half-maximal azimuth, the location
where the response reaches 50% of maximum (Fig.
5A, inset). Figure
5B shows that the distribution of half-maximal azimuths for
all contra-preference cells is bimodal, with a major mode near 9°,
and a much smaller mode at +54°. There was no obvious correlation
between CF and half-maximal azimuth, except that 2/3 of the cells with
half-maximal azimuths lying in the small mode centered at +54° had
CFs near 10-15 kHz.
|
TUNED UNITS. Tuned units (Fig. 4B), those with responses that fall <50% of maximum on both sides of the best azimuth, represent the second most common type (33/105) of azimuth receptive field in our sample. Most (20/33) had CFs between 6 and 15 kHz. Figure 6B shows the distribution of best azimuths for all tuned units. Most best azimuths were between 0 and +54° with a pronounced maximum near the midline (+9°). A measure of tuning around the best azimuth is the half-width, the range of azimuths over which the response exceeds 50% of maximum (Fig. 6B, inset). Figure 6A shows the half-widths for all tuned units. Most units are broadly tuned, with half-widths exceeding 45°; the median half-width is 64°. Unlike contra-preference units, which, together, can encode a wide range of azimuths, tuned units seem most suitable for encoding azimuths near the midline.
|
Binaural interactions for VS stimuli and broadband noise
Responses to VS stimuli were obtained both for binaural
stimulation (as naturally occurs in the free field) and for monaural stimulation of the more effective ear (usually the contralateral ear).
This monaural condition is approximated by occlusion of the less
effective ear in free-field experiments (Knudsen and Konishi
1980; Middlebrooks 1987
; Samson et al.
1993
, 1994
). In some units, we also examined binaural
interactions for broadband noise lacking spectral features.
The importance of binaural interactions for the azimuth sensitivity of
IC neurons is shown by the differences between azimuth modulation
indices for binaural and monaural stimulation (Fig. 3, A and
C). On the average, modulation indices were lower for monaural
stimulation than for binaural stimulation. A greater fraction of units
had modulation indices <50% in the monaural condition than in the
binaural condition (24 vs. 6%), and a smaller fraction of units were
100% modulated in the monaural condition (24 vs. 49%). Statistical
analysis confirms that differences in distributions of modulation
indices for the two conditions are highly significant
[2(12) = 37.8, P < 0.001]. Thus
although responses to monaural stimulation can be directional at these
moderate stimulus levels, binaural interactions do play an important
role in enhancing the azimuth sensitivity of IC neurons. Azimuth
sensitivity in the monaural condition may reflect directionally
dependent changes in the gains of the HRTFs at the contralateral ear as
well as sensitivity to spectral features of the HRTFs.
MIXED FACILITATORY/INHIBITORY INTERACTION.
Figure 7 shows detailed results
from a single unit that exemplifies a frequently observed type of
binaural interaction. Figure 7A shows responses to binaural
and contralateral stimulation with VS stimuli. When the VS stimuli were
presented binaurally, the response was clearly directional: there was
little response for azimuths on the ipsilateral side, a steep rise for
azimuths near 0°, and a broad plateau on the contralateral side. In
contrast, the monaural response was hardly directional. Thus binaural
interactions were critical for the azimuth sensitivity of this unit.
Specifically, for positive azimuths, the binaural response was greater
than the monaural response obtained with contralateral stimulation, meaning that the ipsilateral ear had a facilitatory influence. On the
other hand, for negative azimuths, the binaural response was smaller
than the contralateral response, meaning that ipsilateral stimulation
had an inhibitory effect. Such mixed facilitatory and inhibitory
binaural interactions are commonly seen in the IC
(Brückner and Rübsamen 1995;
Fuzessery et al. 1990
; Irvine and Gago
1990
; Park and Pollak 1993
; Semple and
Kitzes 1987
).
|
INHIBITORY INTERACTION.
Figure 8A shows results for a
cell showing another frequently observed type of binaural interaction.
In this case, both binaural and monaural responses to VS stimuli were
sensitive to azimuth. The binaural response was smaller than the
monaural response to contralateral stimuli over the entire range of
azimuths, indicating that stimulation of the ipsilateral ear had a
purely inhibitory effect. Cells showing this type of binaural
interaction are formally classified as EO/I (Irvine
1986) and commonly referred to as EI. This type of binaural
interaction also predominates for broadband noise, as shown in Fig.
8B: the response to contralateral noise exceeds the binaural
response measured at a constant MBL of 60 dB over a wide range of
contralateral SPLs. Only at the lowest ipsilateral level (30 dB) is the
binaural response clearly greater than the contralateral response,
indicating weak facilitation.
|
FACILITATORY INTERACTION.
While most cells in our sample showed either purely inhibitory or mixed
inhibitory/facilitatory binaural interactions, some showed prominent
facilitatory interactions. An example of such a cell is shown in Fig.
9. The cell did not respond to
stimulation of the ipsilateral ear alone (not shown) and was weakly
responsive to contralateral stimulation with VS stimuli. In contrast,
the response to VS stimuli presented binaurally showed a prominent maximum for azimuths near +18° (Fig. 9A). This maximum
resulted from powerful binaural facilitation because the binaural
response exceeded the response to contralaterally presented VS stimuli over a broad range of azimuths. While facilitation was the dominant binaural interaction for this cell, there was also weak inhibition for
azimuths between 63 and
36°. Facilitation is also apparent for
responses measured when varying the azimuth for the ipsilateral ear
while holding the contralateral ear at an azimuth of 0°: these responses exceeded the monaural response to the contralateral, 0°-azimuth stimulus for virtually all azimuths.
|
MONAURAL CELL.
Not all cells sensitive to azimuth showed binaural interactions. An
example of a primarily monaural cell with a CF of 22 kHz is shown in
Fig. 10. The responses to VS stimuli
presented binaurally and contralaterally were very similar (Fig.
10A). Moreover, when azimuth in the ipsilateral ear was
varied while holding the azimuth in the contralateral ear constant at
0°, the cell response remained nearly constant, confirming that
ipsilateral stimulation has a minimal effect. A similar pattern of
results is apparent for broadband noise (Fig. 10B), where
varying ILD by the MBL-constant method gives a response similar to the
rate-level function for contralateral noise. However, when ILD
sensitivity was assessed by the contra-constant method, the response
dropped for ILDs more negative than 15 dB, indicating an inhibitory
effect of intense ipsilateral stimulation. This inhibition was not
apparent for VS stimuli, possibly because the effective range of ILDs
achieved by varying azimuth did not extend below
15 dB. Nevertheless
the overall pattern of responses was similar for VS stimuli and
broadband noise for this primarily monaural cell.
|
Quantification of binaural interactions
To summarize results such as those of Figs. 7-10 for the entire
unit population, two quantitative measures of binaural interactions were derived from responses to VS stimuli (Fig.
11A). When the binaural and
monaural responses are plotted together as a function of azimuth on the
same coordinates, the two curves define three regions: an area of
facilitation AF where the binaural response is greater than the
monaural response; an area of suppression AS where the binaural
response is smaller than the monaural response; a common area A0
located below both curves. From these three areas, two dimensionless
measures of binaural interactions were defined, the binaural
interaction strength, BIS = (AF + AS)/(A0 + AF + AS), and the
binaural interaction type, BIT = (AF AS)/ (AF + AS). BIS is a number
between 0 and 1 characterizing how much the monaural and binaural
responses differ regardless of how they differ. Thus a zero BIS means
that the monaural and binaural responses are identical for all azimuths
(implying a monaural cell), whereas a BIS near 1 means that either the
binaural or the monaural response is large compared with the other one
for all azimuths, implying strong binaural interactions. BIT, on the
other hand, is a number between
1 and +1 expressing whether binaural
interactions are primarily inhibitory or facilitatory regardless of
their strength. A positive BIT means that, on the average, the binaural
response exceeds the monaural response, implying a facilitatory
interaction, whereas a negative BIT means the opposite, as occurs for
an EI cell. A large BIS with a BIT near 0 implies mixed facilitatory and inhibitory interactions.
|
To help interpret these measures, Fig.
12 shows further examples of binaural
interactions for VS stimuli. Each panel shows the response of one cell
as a function of azimuth for both binaural and contralateral
stimulation. The cells are arranged in a matrix so that the horizontal
position along each row corresponds to the value of BIS and the
vertical position along each column to the value of BIT. Cells in the
leftmost column have BISs <0.2 and are therefore primarily
monaural. Moving toward the right (increasing BIS), monaural
and binaural responses increasingly differ. Units in the top
row have strongly positive BITs (>0.7) and show predominantly
facilitatory interactions. In contrast, units in the bottom
row have strongly negative BITs (less than 0.4) and show
predominantly inhibitory interactions. Finally, units in the
middle row have BITs near 0 and show a mix of facilitation and inhibition.
|
Figure 11B shows BIT plotted against BIS for the entire
sample of cells in which VS responses were studied both binaurally and
monaurally. This display was used to classify cells into four broad
categories of binaural interactions (separated by - - -). These
boundaries were drawn to encompass clear instances of each category,
and attempts were made to place boundaries at troughs in the
distributions of BIT and BIS. Monaural units are defined as having BISs
<0.18. Among the other (binaural) units, facilitatory (BF) units have
BITs >0.65, inhibitory (BI) units have BITs less than 0.30, and
mixed (BF&I) units have BITs between
0.30 and 0.65. Although these
divisions are largely arbitrary, there does seem to be a firm
distinction between BI and BF&I units in that very few units have BITs
between
0.40 and
0.15. There is also a high density of units with
BITs near
1 and +1, providing some justification for the BI and BF
categories. Units from all four categories were found throughout the
range of CFs.
Table 1 gives a cross-classification of
our IC cells according to azimuth sensitivity and binaural interactions
for VS stimuli.1 To a large
extent, the type of azimuth receptive field can be predicted from
binaural interactions. With few exceptions, contra-preference units
have either BI (25/63) or BF&I (23/63) interactions, consistent with
their weak response for ipsilateral azimuths where ILD is negative.
Tuned units are most frequently BF (15/33). These cells respond
maximally near the midline and, correspondingly, show the greatest
facilitation for ILDs near 0 dB. Nevertheless, monaural factors also
play a role in azimuth sensitivity. A high proportion (10/11) of
monaural units were azimuth-sensitive at these relatively low sound
levels. Even for binaural units, variations in SPL at the contralateral
ear seem to contribute to tuning around a best azimuth. Specifically, a
significant fraction (9/33) of tuned units showed EI interactions. For
these units, the decrease in response for azimuths farther
contralateral than the best azimuth cannot be due to inhibition from
the ipsilateral ear, which is minimum at these azimuths. Instead, this
decrease in response may reflect the decrease in the gain of the HRTFs
at the contralateral ear for azimuths more contralateral than the pinna
axis at +45° (Calford et al. 1986; Musicant et
al. 1990
) or nonmonotonicities in the contralateral rate-level
function.
|
Effect of overall SPL
To examine the stability of azimuth receptive fields with respect
to changes in stimulus level, responses to VS stimuli were measured at
two or more sound levels in a few cells. Figure
13 shows results from one unit where VS
responses were measured at three different levels in both monaural and
binaural conditions. At the lowest sound level (60 dB), the unit had a
tuned response with a best azimuth at +36° in both conditions.
Because this level was very close to threshold, these responses
probably reflect the directional sensitivity of the contralateral
pinna, which has its acoustic axis near the best azimuth
(Calford et al. 1986). At 80 and 100 dB, responses in
the binaural condition changed to a contra-preference pattern with a
half-maximal azimuth near the midline. The half-maximal azimuth moved
only slightly when the level was increased from 80 to 100 dB. This
relative stability contrasts with responses to monaural stimulation of
the contralateral ear, which progressively invaded the ipsilateral
hemifield as stimulus level was increased. Thus for this unit, although
responses are directional for both binaural and monaural stimulation at stimulus levels near threshold, inhibitory binaural interactions play
an important role in creating a level-tolerant azimuth receptive field
at suprathreshold levels.
|
Among 20 units for which responses were studied at two or more stimulus levels, half had only relatively small (<1.5°/dB) changes in half-maximal azimuth with stimulus level. For most (7/10) of the remaining units, half-maximal azimuths moved toward the ipsilateral side at a rate >1.5°/dB with increases in stimulus level. Only three units showed large movements toward the contralateral side. Thus on the basis of this small sample, there is a trend for receptive fields to expand toward the ipsilateral side when stimulus level is increased, but some units have relatively level-tolerant sensitivity.
Sensitivity to elevation
Neural representation of sound sources located in the median vertical plane are interesting because interaural disparity cues are minimal for these stimuli so that their localization must be based primarily on spectral features. In 49 neurons, we studied responses to VS stimuli varying in elevation in the median vertical plane. Here, we report results for a subset of 24 neurons for which elevation sensitivity was studied in both monaural and binaural conditions.
Figure 3, B and D, shows the distribution of
modulation indices for elevation for both binaural stimulation and
monaural stimulation of the more effective ear. In the binaural
condition (Fig. 3B), modulation indices for elevation were,
on the average, lower than those for azimuth (Fig. 3A). Some
neurons that were strongly sensitive to azimuth were much less so to
elevation. Unlike the situation for azimuth, modulation indices for
elevation were similar in the monaural and binaural conditions. Indeed,
differences in the distributions of elevation modulation indices for
monaural and binaural stimulation were not statistically significant
[2(6) = 3.15, P = 0.79]. Thus as
expected binaural interactions are less important for the elevation
sensitivity of IC neurons than they are for azimuth sensitivity.
Figure 14 shows examples of monaural and binaural elevation sensitivities for VS stimuli in three units. One (Fig. 14A) was classified as monaural based on its azimuth sensitivity shown in Fig. 10. Consistent with this classification, the elevation sensitivity for VS stimuli was similar for binaural and monaural stimulation, with prominent tuning to elevations near +27°. Figure 14B shows elevation sensitivity for the BF&I unit, for which azimuth sensitivity is shown in Fig. 7. This unit was poorly sensitive to elevation in the binaural condition and somewhat more sensitive for contralateral stimulation. The binaural response exceeded the monaural response for all elevations, consistent with the slight binaural facilitation seen for VS stimuli at 0° azimuth in Fig. 7A and for broadband noise at 0 dB ILD in Fig. 7B. Figure 14C shows elevation sensitivity for the BF unit, for which azimuth sensitivity is shown in Fig. 9A. In the binaural condition, the unit showed broad tuning to elevation around a maximum at 0°. Responsiveness to stimuli varying in elevation was markedly lower when these stimuli were delivered to the contralateral ear only. This observation is consistent with the powerful binaural facilitation exhibited by this unit in response to VS stimuli varying in azimuth. Thus for all three units in Fig. 14, binaural interactions measured with VS stimuli varying in elevation are consistent with those for VS stimuli varying in azimuth.
|
Units were classified into four categories based on their receptive
field for elevation (Fig. 15). Two of
these categories, nondirectional units (Fig. 15A) and tuned
units (Fig. 15B), are defined in the same manner as the
homonymous types of azimuth receptive fields. The fraction of units
classified as nondirectional was considerably higher for elevation
(11/24) than for azimuth (6/105). Best elevations of the four tuned
units ranged between 9 and +27°. A third type of elevation
sensitivity was trough units (Fig. 15C), for which elevation
functions showed a pronounced minimum, with the response rising to
50% of maximum on both sides of the minimum. Trough units formed
25% (6/24) of our sample, and their troughs were restricted to
elevations between +27 and +54°. One of the tuned units also showed a
trough so that it could fit into either category (Fig. 15B).
Finally three elevation-sensitive units showed neither a simple peak
nor a trough and were left unclassified (Fig. 15D).
|
There was no obvious relationship between the elevation and azimuth exhibited by a given unit. For example, among the most numerous class of units that showed a contra-preference pattern for azimuth, 9 were classified as nondirectional for elevation, whereas the other 10 were distributed among trough, tuned, and other units. Interestingly, two of three units that were classified as nondirectional for azimuth were sensitive to elevation. On the other hand, 9 of 10 units nondirectional for elevation had contra-preference patterns for azimuth. No systematic correlations between elevation sensitivity and binaural interactions were apparent either. This general lack of correlation is consistent with the view that azimuth and elevation sensitivities largely depend on separate localization cues and neural mechanisms.
RELATION TO SPECTRAL FEATURES IN HRTFS.
Most (10/13) elevation-sensitive units had CFs in the >8 kHz frequency
region where HRTFs show prominent spectral features. One hypothesis is
that troughs in neural elevation functions for VS stimuli are due to
the prominent spectral notches found in HRTFs for sound sources located
in the frontal hemifield (Musicant et al. 1990;
Rice et al. 1992
). However, not every HRTF spectral notch necessarily will be reflected in neural responses, depending on
how the notch frequency varies with elevation. When seen through 1/6-octave filters, HRTFs in the median plane typically show two prominent spectral notches (Fig. 1). The first notch frequency increases systematically from 8 kHz at
36° to 19 kHz at +54°. Thus neurons tuned to frequencies in the first-notch region are expected to show a trough in their rate-elevation function at the
elevation for which the notch frequency is near the cell's CF. In
contrast, because the second notch frequency stays nearly constant at
22-24 kHz regardless of elevation, neurons having CFs near the second
notch frequency are not expected to show a trough as elevation is
varied. Instead they might show a broad maximum near +20-30°
elevation, reflecting the slight upward tilt of the pinna axis
(Calford et al. 1986
; Musicant et al.
1990
).
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DISCUSSION |
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Spatial receptive fields of IC neurons in free field and VS
We have studied the directional sensitivity of IC cells for VS stimuli synthesized by filtering broadband noise through HRTFs from a standard cat. For a vast majority of cells, average discharge rates varied appreciably with the azimuth of VS stimuli along the horizontal plane for moderate stimulus levels. About 2/3 of azimuth-sensitive cells showed a contra-preference receptive field with a pronounced edge near their half-maximal azimuth. The other third showed a tuned receptive field around a best azimuth. Although half-maximal azimuths of contra-preference units had a broad distribution, best azimuths of tuned units were restricted to positions near the midline. About half the cells tested were sensitive to the elevation of VS stimuli placed in the median vertical plane. Most elevation-sensitive cells showed either a peak or a trough at a particular elevation that could be related to features of the HRTFs.
Two obvious limitations of the study are the synthesis of VS stimuli from nonindividualized HRTFs and the use of low to moderate stimulus levels (usually 15-20 dB above neural thresholds). Discussion of these issues is deferred until our results have been compared with those of both free-field studies of directional sensitivity and dichotic studies of ILD sensitivity in the IC.
Most free-field studies of IC neurons in the cat (Aitkin et al.
1984, 1985
; Calford et al. 1986
;
Moore et al. 1984a
,b
; Semple et al. 1983
)
were concerned primarily with mapping the entire spatial receptive
field for tonal stimuli and did not give detailed characterizations of
neural responses in the horizontal and median vertical planes. The two
studies most comparable with ours are those of Aitkin and Martin
(1987
, 1990
) because they focus on high-CF (>3 kHz) neurons,
give detailed characterizations of azimuth and elevation sensitivity,
and describe responses to broadband noise as well as CF tones.
Aitkin and Martin (1987) report that 44% of IC units in
their sample were "azimuth selective" for broadband noise. At
first sight, this seems to be a much lower proportion than the 94%
azimuth-sensitive units that we found. However, to be called azimuth
selective, the units studied by Aitkin and Martin (1987)
not only had to meet our 50% response modulation criterion, but in
addition their half-maximal azimuth had to change by <0.5°/dB when
overall intensity was varied. Among the units the responses to VS
stimuli of which were studied at more than one stimulus level, most
showed changes in half-maximal azimuth >0.5°/dB, so that they would
not be considered "azimuth selective" according to the criteria
of Aitkin and Martin (1987)
. Moreover, our sample is
biased toward azimuth-sensitive units because insensitive units
sometimes were skipped with no further study. These differences in
sampling techniques and criteria for azimuth selectivity may account
for differences in the proportion of sensitive units between the
Aitkin and Martin (1987)
study and our own.
As in our study, a majority of azimuth-sensitive units studied by
Aitkin and Martin (1987) showed a contra-preference
receptive field, whereas a smaller fraction of units were tuned around
a best azimuth. From their Fig. 6, half-maximal azimuths of most contra-preference cells were between
20 and +20° with a skew toward
ipsilateral (negative) azimuths. This result is consistent with our own
distribution, which is somewhat broader (Fig. 5B). Best
azimuths of tuned units studied by Aitkin and Martin
(1987)
were centered at +20°, again consistent with our
results (Fig. 6B). Thus azimuth receptive fields for high-CF
IC neurons shows striking similarities between the free field and our
virtual acoustic space. This result suggests that our VS stimuli
contained the essential cues for the azimuth sensitivity of IC neurons.
The situation is less clear for elevation sensitivity. Aitkin
and Martin (1990) estimate that 35% of high-CF IC units are sensitive to the elevation of broadband noise stimuli in free field.
Considering the small sample sizes, this proportion is consistent with
our 54% for VS stimuli. Most elevation-sensitive units studied by
Aitkin and Martin (1990)
were tuned around a best
elevation. Best elevations ranged from 0 to +40° (their Fig. 4),
consistent with our findings in tuned units (Fig. 15B).
However, an obvious difference between the two studies is that trough
units were at least as common as tuned units in our sample, whereas Aitkin and Martin (1990)
did not report observing trough
units. A majority of troughs in neural responses to VS stimuli
coincided with either a trough or, for nonmonotonic units, a peak in
the pattern of HRTF gain against elevation at the CF. Although the Aitkin and Martin (1990)
data included neurons having
CFs in the first-notch region of HRTFs (8-18 kHz), where trough
responses would be expected, none of the examples shown in their
figures are from this CF region. One methodological difference between the two studies is that Aitkin and Martin (1990)
measured elevation sensitivity of neurons at their best azimuth,
whereas we always varied elevation for VS stimuli in the median
vertical plane (0° azimuth). However, because HRTFs show similar
features for typical best azimuths near +20° as they do at 0°, one
would expect to find trough responses at these azimuths as well. Thus
both the lack of trough responses in the Aitkin and Martin
(1990)
study and the minority of our trough responses that did
not obviously correspond to HRTF features remain unexplained. Because
both studies investigated elevation sensitivity in only small numbers
of neurons, the question needs further investigation.
Binaural and monaural factors underlying azimuth sensitivity in the IC
Because VS stimuli contain multiple sound localization cues, the azimuth sensitivity of IC neurons for VS stimuli might be based on monaural spectral cues, on interaural disparities such as ILD and ITD, or on a combination of binaural and monaural cues. To assess the relative importance of monaural and binaural cues, we measured the azimuth sensitivity of IC neurons to VS stimuli for both normal binaural stimulation and monaural stimulation of the more effective ear (usually contralateral). This monaural technique offers substantial advantages over monaural ear occlusion in free-field experiments.
Four broad types of binaural interactions were defined based on a quantitative comparison of responses to VS stimuli presented binaurally and monaurally. A majority of cells showed either purely inhibitory (BI) or mixed facilitatory/inhibitory (BF&I) interactions. Some cells showed either purely facilitatory (BF) or no interactions (monaural). Binaural interactions for VS stimuli were generally consistent with those for broadband noise lacking spectral features. Binaural interactions also were correlated with azimuth sensitivity. Most contra-preference cells had either BI or BF&I interactions, whereas tuned cells were most often BF (Table 1). These correlations demonstrate the importance of binaural interactions for azimuth sensitivity in most cells. Nevertheless monaural cues also play a role, as shown by the observations that most monaural cells were azimuth sensitive and that 2/3 of binaural cells retained some azimuth sensitivity for monaural stimulation.
Our binaural classification scheme obviously is related to the
traditional EO-EE-EI scheme (see Irvine 1986 for
review), but differs in that it emphasizes binaural interactions rather
than monaural responses to each individual ear. Our scheme represents an effort to define binaural interactions based on quantitative and
explicit criteria. Because VS stimuli approximate the free field, it
may be more functionally meaningful than the traditional one based on
pure-tone stimuli. On the basis of the fairly uniform distribution of
the binaural interaction measures BIS and BIT in Fig. 11B,
there is no justification for further dividing IC cells into finer
categories. In fact, some of the category boundaries are arbitrary, and
it would be more accurate to describe the difference between monaural
and binaural units as a continuum of BIS and that between BF and BF&I
units as a continuum of BIT. Nevertheless the boundary between BI and
BF&I units is less arbitrary because few units had BITs near the
border. In any case, discrete categories are convenient for linguistic reference.
Despite these classification issues, all four types of binaural
interactions have been reported in previous studies of ILD sensitivity
in high-CF IC neurons (cat: Benevento et al. 1970; Caird and Klinke 1987
; Geisler et al.
1969
; Irvine and Gago 1990
; Rose et al.
1966
; rat: Stillman 1972
; gerbil:
Brückner and Rübsamen 1995
; Semple
and Kitzes 1987
; mustache bat: Fuzessery and Pollak 1985
; Fuzessery et al. 1990
;
Wenstrup et al. 1988
). In general, our results with VS
stimuli show a greater proportion of BF&I neurons and a lower
proportion of monaural units than previous studies with tones and noise
(with the exception of Semple and Kitzes 1987
). The low
proportion of BF&I neurons in some studies may be due to a failure to
adequately sample the ILD continuum, in the extreme, testing for 0 dB
ILD only. Because BF&I cells show different interactions depending on
ILD, their identification requires a fine sampling of ILD. Furthermore
coarse samplings may miss interactions limited to certain ranges of
ILDs and thereby exaggerate the proportion of monaural cells. On the
other hand, we may have underestimated the number of monaural cells by
focusing on azimuth-sensitive cells.
IC cells showing purely inhibitory interactions resemble cells in the
lateral superior olive (LSO). Binaural neurons in LSO are excited by
ipsilateral stimulation and inhibited by contralateral stimulation and
are classified as IE in the traditional scheme (Boudreau and
Tsuchitani 1968; Joris and Yin 1995
;
Tsuchitani 1988a
,b
). Thus a simple hypothesis is that EI
cells in the IC receive predominant excitatory inputs from the
contralateral LSO (Fuzessery and Pollak 1985
;
Irvine and Gago 1990
; Semple and Kitzes 1987
). However, evidence from pharmacological studies with
neurotransmitter antagonists (Klug et al. 1993
),
chemical lesion studies (Sally and Kelly 1992
), and
intracellular recordings from IC neurons (Kuwada et al.
1997
) strongly suggest that not all EI cells in the IC result
from this simple circuitry and that some inhibitory binaural
interactions are formed at supraolivary levels, including the IC and
the dorsal nucleus of the lateral lemniscus (DNLL).
Facilitatory interactions require more complex neural circuitry
than purely inhibitory interactions because facilitation has not been
reported in the LSO. Both BF&I and BF interactions have been reported
in the DNLL of the big brown bat (Covey 1993), and BF&I
cells have been found in the DNLL of the mustache bat as well
(Markovitz and Pollak 1994
). However, in the mustache
bat, the proportion of facilitated units is considerably smaller in DNLL than in the IC (Markovitz and Pollak 1994
). Pollak
and his colleagues (Markovitz and Pollak 1994
;
Park and Pollak 1993
) have hypothesized neural circuits
consistent with brain stem anatomy and pharmacology that qualitatively
account for observed binaural interactions in the IC and DNLL. In their
scheme, binaural facilitation in the IC is actually disinhibition from
presumed inhibitory interneurons in the DNLL that have different
half-maximal ILDs than excitatory inputs from the contralateral LSO.
Our results clearly show that facilitatory binaural interactions play
an important role in azimuth sensitivity of high-CF IC neurons. For
every BF&I unit in our sample, facilitation always occurred on the
contralateral side of the half-maximal azimuth, whereas inhibition
always occurred on the ipsilateral side. The net result is that BF&I
cells show greater azimuth sensitivity than would be achieved through
either monaural cues or purely inhibitory interactions alone. Similar
observations have been made in studies of ILD sensitivity in the IC
(Fuzessery et al. 1990; Irvine and Gago
1990
; Semple and Kitzes 1987
). Binaural facilitation plays an even more important role for BF cells, which often show pronounced tuning around a best azimuth usually (but not
always) located near the midline. Such cells, which respond poorly to
monaural stimulation, have been referred to as "predominantly binaural" in studies of ILD sensitivity (Fuzessery et al.
1990
; Semple and Kitzes 1987
).
ILD SENSITIVITY IN THE CAT IC.
The quantitative data of Irvine and Gago (1990) on ILD
sensitivity for tones and noise in the cat IC can be compared in detail with our results for VS stimuli. Using the MBL-constant method for
studying ILD sensitivity, Irvine and Gago (1990)
found
that most cells show a pronounced edge centered at a half-maximal ILD. This pattern is similar to our contra-preference azimuth receptive field. To make the comparison quantitative, we note that, when seen
through 1/6-octave filters, the HRTFs of Musicant et al. (1990)
show a nearly linear relationship between azimuth and
ILD between
45 and +45°. Using the median rate of change in ILD of 0.34 dB/° for frequencies >3 kHz, our median half-maximal azimuth of
7° translates into an ILD of
2.4 dB, which closely corresponds to
the
3.4 dB median half-maximal ILD of Irvine and Gago
(1990)
. Moreover, the 60-dB range of half-maximal ILDs in their
Fig. 5 is consistent with our 90° range of half-maximal azimuths
(Fig. 5B) providing that rates of change of ILD reach 0.6 dB/°. Such high rates indeed occur near 10-20 kHz in the HRTFs of
Musicant et al. (1990)
. Thus the distribution of
half-maximal ILDs in the cat IC is consistent with the distribution
half-maximal azimuths. In particular, both distributions show a slight
but definite skew toward the ipsilateral side. Such a skew also has
been observed in a study of ILD sensitivity in the IC of the
unanesthetized mustache bat (Wenstrup et al. 1988
).
Validity of VS stimulation
Most of our data were collected for relatively low stimulus
levels, typically 15-20 dB above threshold for 0° azimuth. When free-field SPLs could be estimated, these ranged from 20 to 60 dB, with
two thirds of the neural measurements being made at 40 dB
SPL.3 Thus most of our data were obtained at
sound levels typical for psychophysical studies of sound localization.
Nevertheless our results on receptive fields and binaural interactions
for VS stimuli may only hold over a limited range of levels. On the
basis of our small sample of neurons that were studied at two or more
levels, as well as the more extensive free-field data of Aitkin
and Martin (1987)
, azimuth receptive fields of most neurons
tend to expand with increasing stimulus level, but some neurons are
relatively level tolerant and could encode sound location at higher
sound levels. In general, the contrast between the stability of
psychophysical performance over wide ranges of levels and the tendency
for neural receptive fields to expand with stimulus level remains a
nagging issue not only for sound localization but for other behavioral tasks such as intensity and spectral-shape discrimination.
Because we used HRTFs from one cat of Musicant et al.
(1990) for synthesizing VS stimuli in all of our experiments,
the sound-pressure waveforms of our VS stimuli in the ear canals did
not exactly match those that would occur in the free field for each
individual animal. Acoustic measurements from cats (Musicant et
al. 1990
; Rice et al. 1992
) show that although
certain features of HRTFs are stable across individuals, there also can
be significant individual differences. Human psychophysical experiments
show that although most listeners can accurately localize VS stimuli
synthesized using someone else's HRTFs, front-back confusions and
localization errors in the median vertical plane are more common than
when using individual HRTFs (Bronkhorst 1995
;
Møller et al. 1996
; Wenzel et al. 1993
).
Thus it is important to assess the effect of nonindividualized HRTFs on
our results. Given the paucity of physiological data directly relevant
to the issue in mammals (Blauert and Hartung 1997
;
Sterbing and Hartung 1998
), this assessment must rely on indirect arguments.
Measuring HRTFs in animals with moving pinnae such as cats is not
straightforward because the positions of the pinnae are not easily
standardized. There may be as much variability in HRTFs due to
placement of the pinna in an individual cat as there are individual
differences in HRTFs at the same pinna position (Rice et al.
1992). Despite this difficulty, both low-frequency (<8 kHz)
ILD cues and the prominent midfrequency (8-20 kHz) spectral notches in
HRTFs are relatively stable across animals, although the exact notch
frequency for a given source location may vary somewhat (Rice et
al. 1992
). Large individual variations are limited to high
frequencies (>20 kHz), where HRTFs show a complicated pattern of
spectral peaks and notches. When HRTFs are analyzed through a
1/6-octave filter bank, the most prominent of these high-frequency
features is a notch that stays nearly constant at 22-24 kHz throughout
the horizontal and median vertical planes. Thus high-frequency HRTFs
features appear to be poor candidates for precise encoding of either
azimuth or elevation.
Several arguments suggest that the use of nonindividualized HRTFs may
not be a severe limitation for studying the azimuth sensitivity of IC
neurons. We have shown that azimuth receptive fields of high-CF neurons
for our VS stimuli closely resemble those in free-field studies of the
cat IC (Aitkin and Martin 1987). This result suggests
that our VS stimuli based on nonindividual HRTFs contain the essential
acoustic cues for azimuth sensitivity. Moreover we found pervasive
similarities between azimuth sensitivity for VS stimuli and ILD
sensitivity for tones and noise. These findings suggest that ILD is the
primary cue for the azimuth sensitivity of high-CF IC neurons and that
neural mechanisms underlying ILD sensitivity may not depend on the
exact shape of the stimulus spectrum. Because ILD cues are more stable
across animals than high-frequency features of HRTFs (Rice et
al. 1992
), this further suggests that individual differences in
HRTFs may not be a major factor for azimuth sensitivity in the
horizontal plane.
The situation is more complex for elevation sensitivity because there
were differences in the proportions of tuned and trough units between
VS and free-field stimulation (Aitkin and Martin 1990).
These differences are based on small data samples and might be
accounted for partly by methodological differences. Furthermore it is
hard to see how interindividual differences in the frequency of the
first notch in HRTFs could transform a tuned unit into a trough unit.
Nevertheless it is possible that some of the differences in neural
responses to free-field and VS stimuli reflect the use of
nonindividualized HRTFs.
In summary, although individualized HRTFs may be important in some cases, nonindividualized HRTFs suffice to address many questions regarding sound localization particularly in the horizontal plane. The use of nonindividualized HRTFs is not the only difference between our experimental model and sound localization in natural conditions. Anesthesia, acoustic reflections (echoes), head and pinna movements, and visual and proprioceptive cues are also likely to affect the directional sensitivity of auditory neurons. As such, the present study should be seen as one of many steps required to understand the neural mechanisms for sound localization in natural environments. This study clearly shows that, for the most part, results of traditional dichotic studies of sensitivity to interaural disparities also apply to neural responses in a situation that better approximates the free field.
Neural codes for sound localization in the IC
Most IC neurons show either of two prominent features in their azimuth receptive fields for VS stimuli: a peak at the best azimuth or an edge centered at the half-maximal azimuth. Which of these two features is most likely to code the azimuth of a sound source?
Neural codes for sound localization based on neurons tuned to specific
spatial locations have been proposed for the external nucleus of the IC
of the barn owl (Knudsen and Konishi 1978;
Konishi 1986
) and for the superior colliculus (SC) of
both birds (Knudsen 1982
) and mammals (King and
Hutchings 1987
; King and Palmer 1983
; Middlebrooks and Knudsen 1984
). This type of code is
appealing when, as in the case of these nuclei, best locations are
arranged topographically to form a map of auditory space because, in
principle, the location of the sound source can be identified from the
place of maximum activity in the map. Unlike the SC and the barn owl IC, however, there is no compelling evidence for a map of azimuths in
the mammalian IC. On the other hand, codes such as the population vector (Fitzpatrick et al. 1997
; Georgopoulos et
al. 1986
) can provide accurate directional information based on
best azimuths without requiring topographic maps. For either neural
maps or population-vector codes to be effective, the distribution of
best azimuths must encompass the behaviorally relevant range. This requirement is not met for tuned neurons in the mammalian IC where best
azimuths are rarely more contralateral than +18° (Fig. 6). Thus the
class of high-CF IC cells that show a tuned response to azimuth is not
likely to provide a general code for azimuth and seems most suitable
for enhancing azimuth acuity near the midline where psychophysical
performance is the best (Heffner and Heffner 1988
;
Huang and May 1996b
; May and Huang 1996
).
Alternatives to neural codes based on best azimuths are those based on
the edge centered at the half-maximal azimuth. Such "edge codes"
have been proposed for the mammalian superior colliculus (Wise
and Irvine 1985), inferior colliculus (Wenstrup et al.
1986
), and auditory cortex (Rajan et al. 1990
).
One possibility is that edge azimuths are organized topographically so
that the azimuth of the sound source can be determined by detecting the
location of a sharp increase in neural activity along a neural map.
Evidence for such edge maps is available for both the cat superior
colliculus (Middlebrooks and Knudsen 1984
; Wise
and Irvine 1985
) and the expanded 60-kHz CF region of the
mustache bat IC (Wenstrup et al. 1986
) but is lacking
for the cat IC. Alternatively one can conceive of schemes similar to
the population vector that would provide accurate directional
information based on edges without requiring neural maps.
As we mentioned for codes based on tuned neurons, a requirement for
both edge-map or population-edge codes is that edges encompass the
behaviorally relevant range of azimuths. Figure 5 shows that this
condition is approximately met in the IC in that the distribution of
half-maximal azimuths extends from 54 to +54° with a small gap near
+36°. Figure 5 only shows data for the IC on one side; the overall
distribution of half-maximal azimuths for both ICs would show a broad
maximum at the midline. This overrepresentation of central azimuths is
consistent with psychophysical observations in both cats
(Heffner and Heffner 1988
; Huang and May
1996b
; May and Huang 1996
) and humans
(Makous and Middlebrooks 1990
; Mills 1958
) that sound localization is more accurate near the midline than for lateral positions. This midline advantage is particularly strong in cats, where the direction toward which animals turn their
head severely undershoots actual source position for azimuths more
lateral than ±45° (May and Huang 1996
). If this
finding is not a limitation of the head-turning paradigm, this
undershoot is consistent with the paucity of IC cells having
half-maximal azimuths more lateral than 45°.
Huang and May (1996a) found that cats more accurately
localize noise bands when the noise encompasses the 5-18 kHz region than when it consists entirely of higher frequency components. They
interpreted their result as evidence that the sharp spectral notches in
HRTFs between 8 and 18 kHz play a key role in sound localization
(Musicant et al. 1990
; Rice et al. 1992
).
Although their interpretation seems appropriate for elevation, the
first notch in the HRTFs of Musicant et al. (1990)
remains nearly constant at 11-13 kHz throughout the horizontal plane
so that it is not likely to provide a robust cue for azimuth. Indeed
azimuth receptive fields for VS stimuli never showed a trough that
could be unambiguously accounted for by the first notch. A more likely
explanation for the Huang and May (1996a)
result lies in
the frequency dependence of ILDs. Azimuth modulation indices of IC
neurons were maximal for units with CFs between 6 and 15 kHz. This
frequency region is that where the rate of change of ILD with azimuth
is maximal and where localization is the most accurate. Thus edge codes
are consistent with the frequency dependence as well as the azimuth dependence of sound localization in the horizontal plane.
One difficulty with edge codes is the ipsilateral bias in the
distribution of half-maximal azimuths (Fig. 5). This bias is not unique
to VS stimuli in anesthetized cats but also is found for free-field
stimuli in the cat IC (Aitkin and Martin 1987) and in
the IC of the unanesthetized mustache bat (Wenstrup et al.
1988
). Thus it seems to be a robust result. This ipsilateral bias seems inconsistent with observations that unilateral ablation of
the IC causes severe deficits in sound localization on the contralateral side (Casseday and Neff 1975
;
Jenkins and Masterton 1982
). Two hypotheses might
explain this inconsistency. The first one is that contralateral
sound-localization deficits induced by unilateral ablation primarily
reflect a loss of sensitivity to ITD, which only plays a weak role with
our high-frequency VS stimuli. Consistent with this hypothesis, best
ITDs of IC neurons do show a contralateral bias (Fitzpatrick et
al. 1997
; Yin and Chan 1988
). A second
hypothesis is that IC cells with ipsilateral half-maximal azimuths may
not play a primary role in sound localization. Because the IC is
essentially an obligatory way station in the auditory pathway, the
population of IC neurons must support all forms of auditory behaviors
in addition to sound localization. Cells with ipsilateral half-maximal
azimuths give a robust response for azimuths near the midline, so that
they are well suited for representing stimulus properties (such as
spectral features) that are not primarily directional in the natural
situation when the listener is facing the sound source.
Our results on neural responses to monaural stimulation of the
contralateral ear are relevant to psychophysical studies of "monaural" sound localization achieved by ear occlusion. Despite some inconsistencies attributable to incomplete occlusion
(Wightman and Kistler 1997), most studies conducted with
low-level, broadband, free-field stimuli report a severe reduction in
azimuth acuity, with only minor impairments in elevation discrimination
(Butler et al. 1990
; Oldfield and Parker
1986
; Slattery and Middlebrooks 1994
). These
findings are consistent with our observation that IC neurons show
significantly less response modulation as a function of azimuth for
monaural stimulation than for binaural stimulation, whereas modulation
indices for elevation are similar in the two conditions (Fig. 3).
Psychophysical studies with monaural ear occlusion consistently report
a strong bias in azimuth judgments toward the side of the unoccluded
ear. This behavior is also consistent with a neural code based on edge
azimuths because a vast majority of our contra-preference units
responded vigorously to monaural stimuli located near the midline, as
would occur for a binaural stimulus located well on the contralateral side.
Although the preceding discussion focused on edges and peaks in
receptive fields, azimuth might be coded by the overall pattern of
activation in the neural population without an explicit dependence on
peaks or edges. One such "population-pattern" code was proposed by Wise and Irvine (1985) for the cat superior
colliculus SC. In their scheme, ILD (and, by implication, azimuth) is
coded by the relative proportions of activated neurons in three groups corresponding roughly to our BF, BI, and BF&I neurons. Although this
exact scheme may not work for the IC because differences in best
azimuths among the three groups are not as clear-cut as they are in the
SC, other similar schemes might be workable. A general issue with
population-pattern codes is the potential complexity of the neural
circuitry needed to decode stimulus information.
Yet another alternative are codes based on temporal discharge patterns.
Figure 2 suggests that temporal discharge patterns of IC cells may
contain directional information that is not available in the average
rates of discharge. In this respect, the situation in the IC resembles
that found by Middlebrooks et al. (1994) in the anterior
ectosylvian sulcus of the cat auditory cortex. However, one important
difference between the two studies is that Middlebrooks et al.
(1994)
used random noise stimuli, whereas our VS stimuli were
synthesized by filtering the same exactly reproducible waveform through
every HRTF. Thus temporal discharge patterns for VS stimuli may reflect
fluctuations in the envelope of this particular noise waveform as well
as a code for sound localization. On the other hand, many IC cells have
sustained response patterns and therefore a richer opportunity for
encoding directional information in their temporal discharge pattern
than cortical cells that only respond to stimulus onset. A systematic
study of directional information available in temporal patterns for
various stimulus waveforms is needed.
In summary, we have discussed four classes of neural codes for localization of high-frequency stimuli in the horizontal plane: edge codes based on half-maximal azimuths of contra-preference cells, codes based on best azimuths of tuned neurons, population pattern codes, and codes based on temporal discharge patterns. Although none of these codes can be ruled out and all may play a role in certain conditions, edge codes seem to be the most promising for representing azimuth in high-CF IC neurons. Edge codes can account for both the frequency and azimuth dependence of sound localization in the horizontal plane and for the effects of monaural ear occlusion but have difficulties accounting for the effects of unilateral ablation of the IC. Although our results favor edge codes for localization of high-frequency stimuli in the horizontal plane, localization of low-frequency stimuli and localization in the median vertical plane probably rely on different codes. How these codes are integrated to subsume the wide range of sound localization behavior is a key question for future research.
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ACKNOWLEDGMENTS |
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We thank R. Kochhar for invaluable assistance with software for synthesizing VS stimuli and D. T. Flandermeyer, B. R. Cranston, and C. Atencio for expert figure preparation and histological processing. J. J. Guinan, S. Kalluri, C. C. Lane, and D. J. Tollin made incisive comments on the manuscript.
This research was supported by National Institute of Deafness and Other Communications Disorders Grants DC-00119 and DC-00116.
Present addresses: P. X. Joris, Division of Neurophysiology, University of Leuven Medical School, B-3000 Leuven, Belgium; R. Y. Litovsky, Dept. of Biomedical Engineering, Boston University, Boston, MA 02215.
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FOOTNOTES |
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Address for reprint requests: B. Delgutte, Eaton-Peabody Laboratory,
Massachusetts Eye and Ear Infirmary, 243 Charles St., Boston, MA
02114.
E-mail: bard{at}epl.meei.harvard.edu
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.
1 Binaural interactions for two of three ipsi-preference cells were not quantitatively characterized (and are excluded from the table) because a full azimuth function for ipsilateral stimulation was not measured. In the one ipsi-preference cell for which an ipsilateral azimuth function was measured, binaural interactions were of the IE type.
2 These 10 neurons include the 6 trough neurons of Fig. 15 as well as 4 others that had smaller troughs.
3 For frontal sound sources, sound-pressure levels at the tympanic membranes would be even higher due to the amplificatory action of the pinnae.
Received 13 July 1998; accepted in final form 8 February 1999.
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REFERENCES |
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