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Volume 17, Number 23,
Issue of December 1, 1997
Detectability Index Measures of Binaural Masking Level Difference
Across Populations of Inferior Colliculus Neurons
Dan Jiang,
David McAlpine, and
Alan R. Palmer
Medical Research Council Institute of Hearing Research, University
of Nottingham, Nottingham NG7 2RD, United Kingdom
 ABSTRACT
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- FOOTNOTES
- REFERENCES
ABSTRACT 
In everyday life we continually need to detect signals against a
background of interfering noise (the "cocktail party effect"): a
task that is much easier to accomplish using two ears. The binaural masking level difference (BMLD) measures the ability of listeners to
use a difference in binaural attributes to segregate sound sources and
thus improve their discriminability against interfering noises. By
computing the detectability of tones from rate-versus-level functions
in the presence of a suprathreshold noise, we previously demonstrated
that individual low-frequency delay-sensitive neurons in the inferior
colliculus are able to show BMLDs. Here we consider the responses of a
population of such neurons when the noise level is held constant (as
conventionally in psychophysical paradigms). We have sampled the
responses of 121 units in the inferior colliculi of five guinea pigs to
identical noise and 500 Hz tones at both ears (NoSo) and to identical
noise but with the 500 Hz tone at one ear inverted (NoS ). The result
suggests that the neurons subserving detection of So tones in No
(identical noise at the two ears) noise are those neurons with best
frequencies (BFs) close to 500 Hz that respond to So tones with an
increase in their discharge rate from that attributable to the noise.
The detection of the inverted (S) signal is also attributable to
neurons with BFs close to 500 Hz. However, among these neurons, the
presence of the S tone was indicated by an increased discharge rate
in some neurons and by a decreased discharge rate in others.
Key words:
binaural masking level difference;
inferior colliculus;
detectability index;
interaural delay sensitivity;
masked threshold;
rate level function
INTRODUCTION
When listening with two ears, the
ability to detect a target signal in a background of masking noise not
only depends on the spectral and temporal characteristics of the target
and the masker, as in monaural listening, but also on the interaural
differences in the target and the masker. With identical noises and
tones at the ears, simply inverting the waveform of the tone at one ear
can reduce the detection threshold for that tone dramatically, a
phenomenon known as the binaural masking level difference (BMLD) (Hirsh, 1948a ; Licklider, 1948). The most pronounced BMLD is obtained when a 500 Hz tone presented binaurally, fully masked by a noise identical at the ears (No), is inverted in one ear. The tone
immediately becomes audible, and its level can be decreased by 12-15
dB before it again becomes inaudible (Hirsh, 1948b). The basis of this
large psychophysical effect lies in the fact that the interaural phase of low-frequency sounds is processed by brainstem neurons to provide a
cue for azimuthal position (e.g., Goldberg and Brown, 1969; Guinan et
al., 1972; Yin and Chan, 1990; Spitzer and Semple, 1995). Thus, changes
in interaural phase that make the tone more audible are equivalent to
shifting the tone away from straight ahead (where the noise is also
located). The BMLD therefore provides a measure of our ability to
segregate sounds on the basis of their spatial position and, thereby,
to improve their detectability in the presence of interfering
sounds.
It has been shown that large BMLDs are restricted to low frequencies
and are sensitive to interaural phase (Durlach and Colburn, 1978).
These characteristics suggest that the generation of the BMLD involves
the activity of low-frequency neurons in the brainstem, which are
sensitive to interaural delay (Goldberg and Brown, 1969; Guinan et al.,
1972; Yin and Kuwada, 1984; Yin and Chan, 1990; Spitzer and Semple,
1995). In a recent neurophysiological study (Jiang et al., 1997), we
have demonstrated that, using the most common BMLD stimuli (500 Hz
tones in noise) and signal detection methods, individual
delay-sensitive low-frequency neurons show BMLDs, and the masked
threshold may be indicated by either an increase or decrease in their
discharge rate from that attributable to the noise alone. We also found
that the neurons showing the largest BMLD are not necessarily those
with the lowest signal-to-noise (S/N) ratio and thus are unlikely to
contribute to detection at the masked threshold. However, in that
study, the noise level was variable and was set relative to the noise
threshold of each neuron. This made comparisons of the S/N ratio
between neurons difficult, so that it was not possible to determine the
contribution of any one neuron to the threshold detection task.
To investigate the contribution of single neurons to detection at the
masked threshold, and to allow generalization of responses to other
standard binaural configurations, we have examined a relatively large
number of inferior colliculi (IC) units from small number of
experiments using 500 Hz tones (zero or phase) masked by identical
noise at a fixed level in the two ears.
MATERIALS AND METHODS
Many of the detailed methods have been described previously
(Jiang et al., 1997). The recordings described in this paper were made
from the inferior colliculi of five pigmented guinea pigs weighing
between 300 and 400 gm. The animals were premedicated with atropine
sulfate (0.06 mg, s.c.) and anesthetized with an intraperitoneal
injection of urethane (1.3 gm/kg in 20% solution). Further analgesia
was obtained with phenoperidine (1 mg/kg, i.m.). Supplementary doses of
phenoperidine (0.5-1 mg/kg, i.m.) were given on indication provided by
the pedal withdrawal reflex. All animals were tracheotomized, and core
temperature was maintained at 37°C with a heating blanket. The animal
was placed inside a sound-attenuating room in a stereotaxic frame with
hollow plastic speculae replacing the ear bars. Pressure equalization
within the middle ear was achieved by a narrow polythene tube sealed into a small hole in the bulla on each side. The cochlear condition was
assessed by measuring thresholds of the cochlear action potential (CAP)
to a series of short tones (0.5, 1, 2, 4, 5, 7, 10, 15, 20, and 30 kHz)
in the left ear at intervals throughout the experiment, using a silver
wire electrode on the round window (Palmer et al., 1986). There are two
causes of raised CAP thresholds that we commonly encounter: fluid
buildup in the bulla, which is promoted by the presence of the round
window electrode, and systemic cochlear deterioration. Monitoring only
the left ear allowed us to assess systemic and hence bilateral effects,
and we made the not unreasonable assumption that in the absence of the
wire electrode, fluid buildup in the right bulla would not be a serious
problem.
A craniotomy was performed on the right side, extending 2-3 mm rostral
and caudal of the interaural axis and 3-4 mm lateral from midline.
Recordings were made with stereotaxically placed tungsten-in-glass
microelectrodes (Bullock et al., 1988) advanced by a piezoelectric
motor (Burleigh Inchworm IW-700/710) into the inferior colliculus
through the intact cortex.
The stimuli were delivered through two sealed acoustic systems
identical on each side. Each system consisted of a 12.7 mm condenser
earphone (Brüel and Kjaer 4134), coupled to a damped 4-mm-diameter probe tube, which fitted into the speculum. The output
was calibrated a few millimeters from the tympanic membrane using a
Brüel and Kjaer 4134 microphone fitted with a calibrated 1 mm
probe tube. The sound system response on each side was flat to within
±5 dB from 100 to 10,000 Hz, and the left and right systems were
matched to within ±2 dB over this range.
The stimuli used in this study were tones and noises presented to the
two ears. The noise used was digitally synthesized "frozen" noise
with a bandwidth of 50 Hz-5 kHz and output at a sampling rate of 50 kHz via a digital-analog converter (TDT QDA2) and a waveform
reconstruction filter (Kemo VBF33; cutoff slope, 135 dB/octave from 5 kHz). The same frozen noise sample was used for all units. Interaural
delays of the noise were introduced by varying the time of onset of the
noise to one ear during synthesis. Tonal stimuli were either from a
Hewlett Packard 3325A waveform synthesizer or digitally synthesized and
output from a digital analog converter (TDT QDA2) and a waveform
reconstruction filter (Kemo VBF33; cutoff, slope 135 dB/octave from 5 kHz).
Single neurons were isolated using 50 msec tone and/or noise bursts as
search stimuli. The extracellularly recorded neural action potentials
were amplified (×1000), filtered (155-1800 Hz), converted to logic
pulses by an amplitude discriminator, and timed with 10 µsec
resolution (CED 1401 plus). The lowest binaural threshold to
interaurally in-phase tones and the frequency at which it was obtained
[the best frequency (BF)] were determined audiovisually.
The following analyses were performed in the present study.
Noise delay functions. Noise delay functions (NDFs) were
measured by presenting the noise with interaural time disparities over
a range equal to three times the period of the BF of the neuron, in 52 equal delay steps, starting from ipsilateral leading. The duration of
the stimulus was 333 msec, with three repetitions giving 1 sec
stimulation time at each delay. The noise level was arbitrarily chosen
at 7-15 dB above No noise threshold at which a reasonable No-driven
response and a well tuned noise delay function could be obtained. The
interaural time delay (ITD) corresponding to the maximum discharge rate
is denoted as the noise best delay (NBD). In some cases, the NDFs had
two or more large peaks situated at large positive and negative delays
with a trough at zero delay. In these cases, the NBD was designated as
the delay of the largest peak close to zero delay, in the range of
contralateral leading ITDs.
Masked rate level functions. Masked rate level functions
(MRLFs) were obtained by measuring tone rate level functions in the presence of a noise masker at the fixed level of 23 dB
SPL/ . Tone rate level functions were generated by
presenting tones (50 msec duration; rise-fall time, 1 msec) and noise
(5 kHz bandwidth) simultaneously gated and varying the level of the
tone pseudorandomly over a maximum range of 100 dB in 1 dB steps.
Possible order effects were minimized by ensuring that each stimulus
was never >50 dB weaker than the one preceding it. The number of
spikes elicited by each tone was counted, and the average MRLF was
computed from 10 presentations at each level at 5/sec. The frequency of
the tone used was 500 Hz either interaurally in phase (So) or out of
phase (S).
Determining the masked threshold from the MRLFs. To
determine the masked threshold for a tone from the MRLF, we used an
analysis technique derived from signal detection theory (Green and
Swets, 1966). Such techniques have already been widely used in the
analysis of the responses of auditory nerve fibers (e.g., Delgutte,
1987; Winslow and Sachs, 1987; Viemeister, 1988; Rice et al., 1995). However, here we use a modification of these methods, because the
classic detectability index (d ) metric assumes that the
responses of the neurons are normally distributed with equal variances, an assumption that does not necessary hold for the discharge
characteristic of auditory nerve fibers (Teich and Khanna, 1985; Young
and Barta, 1986) or, for that matter, other neurons in the auditory
pathway. Accordingly, we used a modified version of d, the
standard separation (D), described by Sakitt (1973).
This index gives a simple interpretation of discrimination that is
independent of any assumptions about the underlying distributions. The
calculation of D is described in the following equation:
|
(1)
|
where R(n + s) and
R(n) are, respectively, means for the
distribution of the response to the signal-plus-noise masker and to the
noise masker alone, and SD(n) and
SD(n + s) are the SDs of the
respective response distributions. Random rating would produce
D = 0, and perfect discrimination would produce an
infinite D. For our purposes, the masked threshold for a
tone in noise was defined as the lowest level at which D had
an absolute value of 1.0, and a positive BMLD is defined where the
masked threshold for S tones is lower than that for So tones.
RESULTS
To investigate the contribution of single neurons to signal
detection under the most commonly used binaural masking situation, NoSo
and NoS with signal at 500 Hz, we took the following measures to
reduce the interanimal discrepancies: (1) We used a small number of
animals (five guinea pigs) that have a similar body weight ranging from
318-394 gm (mean ± SD, 353.2 ± 27.2 gm). The CAP thresholds for 1000 Hz tone bursts was similar across the five animals
(±5 dB) and was monitored at intervals throughout each experiment. (2)
We recorded from as many units as possible in each single animal. A
total number of 121 units were recorded, and the numbers of units taken
in each animal were 22, 29, 11, 32, and 26, respectively. We used
physiological criteria (short latency, crisp nonhabituating, often
tonic responses, and delay sensitivity) to ensure that recordings were
made in the central nucleus of the inferior colliculus (ICC) and
confirmed the location of the recording site to within ICC by
histological reconstruction of the position of electrolytic lesions
made in the last recording sites. If the BF of any unit was <2500 Hz,
it was included in the analysis.
The thresholds of the units and their relationship to the masking
noise level
The BF of the 121 units ranged from 100 to 2330 Hz, and Figure
1A shows their
distribution. The majority (78.5%, 95 of 121) of units had BFs between
200 and 1000 Hz. Figure 1B compares BF tone-evoked
(filled circles) and noise-evoked (open
circles) thresholds. Tone and noise thresholds were measured
binaurally with zero interaural delay (So and No). Both thresholds are
expressed in decibels SPL with noise threshold expressed as noise
spectral density (Jiang et al., 1997). Three major features are
apparent. First, thresholds for both tones and noise decreased with
increasing BF, as expected from the audiogram of the guinea pig.
Second, at any frequency, the thresholds of different neurons are
scattered within a ±10 dB range, with some units having extremely high
thresholds for tone and/or noise. Third, there is a consistent
separation between tone and noise thresholds across frequency.
Fig. 1.
A, Histogram of the BF distribution
of 121 units. B, Threshold levels for binaurally
presented BF signals and No noise. C, Difference between
No level and noise threshold plotted against the BF of the units.
D, Histogram showing the level of the No noise with
respect to noise threshold for the 121 units.
[View Larger Version of this Image (27K GIF file)]
In this study, when the binaural configurations NoSo or NoS were
used, the noise level was set at a fixed value of 23 dB SPL/, regardless of the No threshold of the single unit.
Figure 1C plots the difference between the masking noise
level and the No threshold against the BF of each unit. The majority of
units had No thresholds below the level of the noise masker, as
indicated by a positive value in Figure 1C. Only 9% of
units had their No threshold  3 dB above the noise-masker level (Fig.
1D), and most of these units had BFs <300 Hz. Thus, the majority of neurons were activated by the level of No noise presented.
The response characteristics to NoSo and NoS
An example of the analyses for a single neuron, with a BF of 950 Hz, is shown in Figure 2. The neuron
responded best to noise (NBD; Fig. 2A) and to 500 Hz
tones (Fig. 2B) when the interaural delay was close
to zero. When driven with identical noises at each ear (zero
interaural delay, No), this unit showed very different responses to
increasing levels of the 500 Hz tone, as can be seen in its MRLFs in
Figure 2, C and D. In response to 500 Hz tones with identical phase (So), the discharge rate increased as the tone
level was increased, once a threshold level was exceeded. In contrast,
when the phase of the 500 Hz tone in one ear was inverted (S), the
discharge rate decreased steadily as the tone level was increased
beyond a threshold value and then increased again at higher tone
levels. For this unit the first indication of the presence of the 500 Hz tone was, therefore, an increased discharge rate for So signals and
a decrease for S signals.
Fig. 2.
Complete profile of responses of a single inferior
colliculus neuron. A, Noise delay function.
B, Interaural phase difference histogram for 500 Hz
tones measured using binaural beats (Kuwada et al., 1979).
C, Masked rate-versus-level function for NoSo. D, Masked rate-versus-level function for NoS. The
binaural configurations are linked to the delay functions in
A and B by arrows.
[View Larger Version of this Image (27K GIF file)]
The masked threshold at 500 Hz was estimated by applying the standard
separation D metric to the MRLFs. Figure
3 shows examples of two units. The full
MRLFs to So and S 500 Hz tones are illustrated in Figure 3,
A and B. The unit in Figure 3A showed
an increase in discharge rate for So and a decrease followed by an
increase for S as the level of the tones were increased. The unit in
Figure 3B showed increases in discharge for both So and S
tones. Figure 3, C and D, shows the standard
separation (D) as a function of tone level, and the
arrows indicate the tone levels at which a value of ±1.0
was obtained. These "masked thresholds" are also indicated by
arrows in Figure 3, A and B, and are
plotted in the insets. These insets show that, despite the
differences in their rate level functions, a BMLD was measurable for
each of these units, and that in both cases the S tones were
detectable at a lower sound level than So tones.
Fig. 3.
Use of the standard separation analysis to
determine the masked thresholds for two inferior colliculus neurons
(A, B). Rate-versus-level functions are shown for So
(filled circles) and S (open
squares) 500 Hz tones in the presence of noise in the same
phase (No) at the two ears. The discharge rates over the first 10 dB of
the rate-versus-level function were used to estimate the mean and SD of
the discharge rates attributable to the noise alone. The standard
separation values are plotted for each 1 dB step in tone level in
(C, D). The criterion of a D value of 1.0 was used to determine the minimum sound level at which a response to
the tone (either an increase or a decrease in the discharge rate) could be detected (i.e., the masked threshold). The masked thresholds are
shown by the arrows in C and
D, and these are replotted in the insets
of A and B.
[View Larger Version of this Image (38K GIF file)]
As illustrated in Figure 3, we have divided MRLFs into two groups,
based on whether increases or decreases in discharge rate were first
observed as the tone level was increased. Type P MRLFs showed an
increase in discharge rate as the tone level was increased and gave a
Positive D value of 1 at masked threshold (Fig. 3, MRLF for NoSo in A, MRLFs in B). Type N MRLFs
showed a reduction in discharge rate as tone level was increased and
gave a Negative D value of  1 (Fig. 3A,
MRLF for NoS). This classification is independent of whether the
signal was So or S; in other words, in different units we have found
that the presence of the tone was indicated by discharge rate increases
for both So and S (type P/type P), decreases for both (type N/type
N), decreases for So and increases for S (type P/type N), or
decreases for S and increases for So (type N/type P). In the present
study, for NoSo, 61.2% of units showed type P MRLF, 28.9% showed type
N MRLF, and 9.9% of units showed no significant increase or decrease
in the discharge rate from those evoked by noise alone even at highest signal level. In contrast to NoSo, for NoS, the type P, type N, and
unchanged MRLFs accounted for 36.4, 57.9, and 5.8% of the total number
of units, respectively. We have previously demonstrated that the type
of MRLF is entirely consistent with the delay sensitivity of the neuron
(Jiang et al., 1997).
Masked threshold for NoSo and NoS
Figure 4A shows
the masked thresholds for So and S tones obtained from 121 single
units in five guinea pigs. Two features are clear from this plot: (1)
the lowest masked thresholds for both So and S 500 Hz tones were
obtained in the frequency region at ~500 Hz; and (2) the S masked
thresholds (open squares) were generally lower than the So
masked thresholds (filled circles). To emphasize this
latter point, we have averaged separately the masked thresholds for the
So and S populations and plotted these averages in Figure
4B. On average, S masked thresholds were 5.5 dB
lower than So masked thresholds. However, in any detection task
subjects presumably respond at the lowest signal level that evokes a
detectable change in the neural output. In the BMLD task, the lowest
estimate of the masked threshold will be provided by the neurons at
~500 Hz. We have, therefore, averaged the masked thresholds for So
and S from the 300-800 Hz region (Fig. 4A, dashed
lines) and plotted them in Figure 4C. These masked
thresholds are somewhat lower than those obtained by averaging the
whole population, but the S threshold remained lower than the So
threshold (by 6.6 dB).
Fig. 4.
Masked thresholds for So and S 500 Hz tones in
No noise as a function of the neuron BF. A, Masked
thresholds across a population of low-frequency inferior colliculus
neurons pooled from five guinea pigs for 500 Hz tones in So
(filled circles) and S (open squares) configurations in the presence of a fixed level (23 dB SPL/) of No noise. The dashed lines indicate the region from 300-800 Hz centered around the tone frequency of 500 Hz, which is marked by an arrow. B, The
average of all of the masked thresholds across this population is
plotted for So (filled circles) and for S
(open squares). The difference between these values is
significant at the p < 0.001 level by Student's
t test. C, The average of the masked
thresholds from the frequency range 300-800 Hz, indicated by the
dashed lines in A, is plotted for So
(filled circles) and for S (open
squares). The difference between these values is significant at
the p < 0.001 level by Student's t
test.
[View Larger Version of this Image (32K GIF file)]
The relationship between the type of MRLF and the masked threshold is
shown in Figure 5. The relative
proportions of units giving type P, type N, and unchanged MRLFs are
shown by the histogram of Figure 5A. The average masked
thresholds for So and S tones among units yielding type P and type N
MRLFs are plotted in Figure 5B. Taking first the responses
to the So tones shown by the black bars and dots,
units that demonstrated a type P MRLF led to a lower average masked
threshold (65 dB SPL) than did those yielding type N MRLF (69 dB SPL).
The average masked threshold for S signals (white bars
and squares), among units yielding type P MRLF, is only 1 dB
lower (64 dB SPL) than for the lowest So masked threshold. The average
masked threshold for 500 Hz S tones, among those units yielding a
type N MRLF (60 dB SPL), is the lowest of all conditions.
Fig. 5.
Proportions of neurons showing increases or
decreases in discharge rate at masked threshold and their average
masked thresholds. A, Histogram of the number of units
in our population that yielded positive (type P) or negative (type N)
D values at the masked threshold in response to So
(filled bars) or S (open bars)
500 Hz tones. B, Averages of the masked thresholds for
So (filled circles) and S (open
squares) tones computed separately for units yielding positive
and negative D values, as indicated by the
arrows from the histogram bars to the corresponding
masked thresholds.
[View Larger Version of this Image (19K GIF file)]
Detecting the So and S under the masking conditions
Although the averaged masked threshold for each binaural condition
and the magnitude and direction of the BMLD are indicative of the
encoding ability of IC neurons for NoSo and NoS, it is obvious that
those units with high masked threshold for one of the two
configurations will not contribute to the signal detection of the
configuration concerned. Instead, for a fixed level of masking noise,
the relative masked thresholds of the units would be more indicative of
their contribution to the detection of the tonal signal. The units with
the lowest masked thresholds presumably mediate the detection of the
tone. However, the S/N ratio at which guinea pigs can detect the tones
masked by a noise is unknown. Thus, we have arbitrarily taken the S/N
ratio at which 5-8% of neurons were responding to the signals as a
likely indication of the behavioral masked threshold.
Figure 6 plots the D
values of 121 units against their BFs for NoSo (Fig.
6A) and NoS (Fig. 6B). In each
case, the signal level was 50 dB SPL. The S/N ratio within the
frequency channel at 500 Hz is 0 dB, calculated according to the
effective bandwidth of 200 Hz with a center frequency at 500 Hz (guinea
pig data; Evans et al., 1992), or 37 dB by merely taking the difference between the tone level and the noise spectral density at 500 Hz. For
NoSo, 6.6% units (8 of 121) showed significant changes in their
discharge rate, as illustrated by their D values (1). Two features are noteworthy: (1) all of the significant changes were attributable to increases in discharge rate from those evoked by the No
noise alone, i.e., units with type P MRLFs for NoSo; and (2) the BFs of
the units that showed significant changes in their discharge rate were
close to 500 Hz (the signal frequency). For the same S/N ratio, the
response of same group units to NoS is shown in Figure
6B. In contrast to NoSo, more units (14%) showed a
significant change in their discharge rate, and among them, half showed
an increase (D 1, type P MRLF) and half showed a decrease (D  1, type N MRLF) in their discharge
rate. If we assume that this S/N ratio is close to the threshold for
NoSo, Figure 6 would be consistent with the psychophysical paradigm in
which the signal becomes detectable again when the phase of the signal
at one ear is inverted. In Figure 6B, the BFs of
units that showed significant changes in their discharge rate are also close to 500 Hz.
Fig. 6.
Population profiles of detectability. Here we have
taken two arbitrary signal-to-noise ratios, which are likely to provide an indication of the activity in the IC when signals are close to the
behavioral threshold for the guinea pig. The standard separation D is plotted against BFs for 121 units for NoSo and
NoS for within-channel S/N ratios of 0 (A,
B) and 5 dB (C, D) (see Materials and
Methods for details).
[View Larger Version of this Image (32K GIF file)]
In Figure 6, C and D, the signal level was 5 dB
lower than in Figure 6, A and B (i.e., 45 dB SPL)
to give a within-channel S/N ratio of 5 dB. For NoSo, only two units
had D values slightly >1 (Fig. 6C). For NoS,
8.3% of units (10 of 121) still showed the significant change in their
discharge rate. Interestingly, both increase in discharge rate (five
units) and decrease in discharge rate (five units) were observed.
Relationship between signal detection and delay sensitivity
In the discussion of our previous study (Jiang et al., 1997), we
suggested that the detection of So and S signals may be attributed
to different units, and the role of individual neurons in a specific
detection task (NoSo or NoS) was related to their delay sensitivity.
However, because in that study we optimized the noise level to obtain
data from each and every unit, we were unable to make definitive
statements about the relative contribution of units to detection for
the So and S signals. Here by the use of a single noise level we are
able to assess properly the contribution of each unit to detection.
As illustrated in Figure 6, for an S/N ratio of 0 dB, when S tones
were presented, 17 units (14%) showed significant changes (increase or
decrease) in the discharge rate evoked by the No noise alone. At this
same tone level eight units increased their No evoked discharge when
presented with So signals. Of the eight units that increased discharge
to So signals, only two of these were also among the 10 units
responding to S with a decrease, and three were among those units
responding to S with an increase in discharge. This result indicates
that few of the units that respond to low-level S signals also
contribute to So signal detection.
At a within-channel S/N ratio of 5 dB, the three units still
responding to the S signal with increases in their discharge rate
did not respond to So signals (even at 0 S/N ratio). Two units that
responded to both the So and S signals at a within-channel S/N ratio
of 0 dB were still among the six units showing significant decreases in
discharge rate to low levels of S signal. This is attributable to
the fact that both units had a low masked threshold for the S
signal, although one of them showed only a small BMLD.
We demonstrated in our earlier paper (Jiang et al., 1997), that
the response of an individual neuron to BMLD signals was consistent with their delay sensitivity. Here we are able to extend this result to
show that the contribution of a neuron to detection in BMLD tasks is
also consistent with their delay sensitivity. Figure
7 shows the masked thresholds for NoSo
and NoS plotted against the NBD for those units, showing significant
changes in their discharge rate at 0 dB S/N ratio. The different
response characteristics are indicated by different symbols. Each unit provides a pair of symbols and is marked by a number. Three
features can be observed: (1) although the units with type P response
at low So signal levels (filled round symbols on or
below dashed line) had widely distributed NBDs [from 180 µsec (unit 6) to 2300 µsec (unit 14)], most of their NBDs were
within 650 µsec; (2) the units with type P response to low S
signal levels (open round symbols on or below dashed
line) had relatively long NBDs (from 600 µsec to 2300 µsec);
units 12 and 13 showed large, positive BMLDs and responded to S
signal at a within-channel S/N ratio of 5 dB but did not respond to
So signal at a within-channel S/N ratio of 0 dB; and (3) the units with
type N responses to low S signal levels (open squares on
or below dashed line) had relatively short NBDs (from 0 to
200 µsec). Many of these units had a type P-type N response to NoSo
and NoS and a large, positive BMLD (units 1-4 and 8). Two units
showed significant changes for both NoSo and NoS (units 6 and 7),
and each had a small, positive BMLD.
Fig. 7.
Masked thresholds for NoSo and NoS
plotted against the NBD for those units in Figure 6 with significant
changes in their discharge rate. Thresholds for NoSo and NoS for a
single unit are indicated by the same number.
Dashed line, S/N ratio = 0 dB; dotted
line, S/N ratio = 5 dB.
[View Larger Version of this Image (23K GIF file)]
DISCUSSION
Generality of results
We set out to determine the contribution of single IC neurons to
the detection of 500 Hz tones masked by identical noise at the two ears
(No). The results suggest that (1) the neurons involved in both So and
S threshold detections were those with their BFs close to 500 Hz,
the signal frequency; (2) detection of the So signal and S signals
is largely attributable to different populations of units; (3)
detection of So signals was mainly by those units with a type P
response and with a relatively short best delay (NBD within 650 µsec); and (4) S signals were detected by two groups of units:
units with a type P response and a relatively long best delay (NBD > 600 µsec) and units with a type N response and a relatively short
best delay (NBD < 400 µsec).
Even restricting the analyses to the bare minimum, we needed to pool
across animals to obtain sufficient data to make the points about the
ensemble response. The alternative approach is to measure the responses
of each individual unit extensively. This we reported in earlier
studies (McAlpine et al., 1996; Jiang et al., 1997), in which we were
able to measure the responses to different levels of noise masker, to
different noise interaural configurations, and to different tone
frequencies. The data from both the present population study and the
earlier single-neuron studies are consistent in linking responses to
the sensitivities of individual neurons, and thus it seems likely that
the present data should provide a basis for predicting the responses to
other binaural configurations.
The implications of these results for current theories of binaural
processing in the higher central auditory system are discussed below.
Comparison with models of the BMLD and previous
physiological studies
One major class of models that describe the processes underlying
the BMLD consists of equalizing the amplitude of the waveforms at the
two ears and then performing a differencing operation. This results in
a cancellation of the components identical at the two ears, leaving the
nonidentical components (Durlach, 1963). Although this approach
accounts for many of the properties of the BMLD, it is not firmly
anchored in the known physiology. A more physiological approach
involves filtering the waveforms at each ear into a series of frequency
channels based on psychophysical measures of auditory filters (Stern
and Colburn, 1978). The outputs of the channels at the same frequency
from the two ears are then cross-correlated (replicating the action of
coincidence detectors known to exist in the brainstem). The second
dimension of the model is the interaural delay. The signal is detected
as a change in the correlation in any frequency channel at any point
along the delay axis. For a wide-band noise presented binaurally, the cross-correlation model produces the largest response at zero interaural delay across all the frequency channels. The addition of 500 Hz tones presented in identical phase at the masked threshold produces
a small increase around zero interaural delay in the 500 Hz channel.
Adding a low-level So signal does not disrupt the interaural phase
difference established by No noise; rather, the signal is detected as
an increased correlation in the signal frequency channel. In contrast,
an additional S signal causes variations in the interaural phase
differences established by the No noise. This variation in interaural
phase difference results in a desynchronization and thus a reduction in
the correlation attributable to the No noise, as indicated by a
decrease in the output at approximately zero interaural delay and an
increase in the output at interaural delays of ~1000 µsec (half of
the signal period). In this model, the BMLD results from an asymmetry in the effects of the So and S signals. Because the S signals have a larger effect in reducing the correlated activity than the So
signal has in increasing the correlation, it is more detectable. Note
that the BMLD results from computations within a single frequency channel at the signal frequency.
To relate the model to the physiological measurements, the internal
delay axis could be regarded as an array of binaural delay-sensitive neurons with different best interaural delays (Yin et al., 1987). The
increase or decrease in the output of the cross-correlation model
predicts increases or decreases in the discharge rate, caused by the
addition of the signal.
The predictions made by the model are qualitatively consistent with our
current data. Both the cross-correlation model and our data have shown
that the detection at threshold is restricted to a single frequency
region: the units with BFs of <250 and >800 Hz did not contribute to
the detection of 500 Hz signals. For some of these low-BF units the
noise was below threshold (Fig. 1). Our data also show that the So
signal was detected by IC units with a type P response, equivalent to
an increase in the number of coincidences, as predicted by the
cross-correlation model. Both type P and type N responses were observed
for NoS; neurons giving type N responses had NBDs close to zero,
whereas those giving type P responses had relatively long NBDs (Fig.
7). This is equivalent to the model prediction of a decrease in the
number of coincidences around zero interaural delay and an increase at longer delays at the masked threshold for NoS.
There have been surprisingly few studies of the neural basis for the
BMLD. Neither Langford (1984) at the medial superior olive nor Caird et
al. (1989) at the IC provided convincing evidence for differential
responses to the So and S tones in No noise, although both provided
indications that the unit responses were linked to their delay
sensitivities and that S tones could decrease the noise evoked
discharge. Later studies (Caird et al., 1991; McAlpine et al., 1996)
using methods to estimate No masked thresholds for So and S did
indicate binaural unmasking in single-unit responses, but the methods
were flawed and did not generalize well to tones other than at BF.
Finally, Jiang et al. (1997), using the same signal detection approach
as we have used in the present study, provided good evidence of
binaural unmasking that was entirely consistent with the unit delay
sensitivity and was evident for signals not at the BF (i.e., 500 Hz
tones). This latter study suggested that different populations of
neurons contributed to detection of So and S tones, but was not
appropriately designed to directly test this hypothesis.
In that study, although we were able to demonstrate the magnitude,
direction, and value of the masked threshold for single units, we were
not able to show unequivocally the role of each single unit in signal
detection. However, the results did show that the lowest S/N ratio for
detectability of So was shown by units with best delays close to zero,
and the threshold was indicated by an increase in discharge rate from
that to the No noise. For S, the lowest S/N ratios among type P
responses corresponded to those neurons with relatively long NBDs,
whereas, for type N responses, the lowest S/N ratios were among those
neurons with NBDs close to zero. We predicted that units that showed
large BMLDs would only be involved in signal detection for the
configuration for which its masked threshold was lowest. This
prediction is supported by the current study. The only units that were
involved in both So and S detection were those that showed
small-magnitude BMLDs (Fig. 7, units 6 and 7), although the direction
was still consistent with the psychophysics.
Possible physiological mechanisms for detecting signals masked by
noise and the basis of the BMLD
In the computational models of the BMLD (as described above)
detection of either So or S tones in No noise requires only a
significant alteration in the response anywhere in the ensemble of
units with different delay sensitivities and best frequencies. The S
signals generate a larger change than equal level So signals and thus
are more detectable. Our data indicate that the alterations in neural
discharge necessary for such a detection mechanism do occur.
However, a second possibility, also consistent with the present data,
is that the reduction in the discharge rate of the majority of neurons
to S signals and the increased activity of the relatively fewer
neurons act in concert to enhance detection. The effective contrast in
neuronal activation between these two populations contributes to the
S signal audibility. The relatively small population of neurons that
produce an increased discharge would have more salience against a
background of neuronal activation that is lower than that evoked by the
noise alone; i.e., the internal S/N ratio is higher. For So signals the
vast majority of neurons show an increase in discharge rate with
increasing signal level, which becomes detectable when the discharge
rate is increased significantly above the noise-evoked rate; i.e., the
internal S/N ratio is smaller than for S signals.
FOOTNOTES
Received May 23, 1997; revised Aug. 22, 1997; accepted Sept. 15, 1997.
Correspondence should be addressed to Alan Palmer, Medical Research
Council Institute of Hearing Research, University of Nottingham, University Park, Nottingham NG7 2RD, UK.
Dr. Jiang's present address: Department of Otorhinolaryngology, Derby
Royal Infirmary, Derby DE1 2QY, UK.
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