Kresge Hearing Research Institute, University of Michigan, Ann Arbor, Michigan 48109-0506
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ABSTRACT |
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Furukawa, Shigeto and John C. Middlebrooks. Sensitivity of Auditory Cortical Neurons to Locations of Signals and Competing Noise Sources. J. Neurophysiol. 86: 226-240, 2001. The present study examined cortical parallels to psychophysical signal detection and sound localization in the presence of background noise. The activity of single units or of small clusters of units was recorded in cortical area A2 of chloralose-anesthetized cats. Signals were 80-ms click trains that varied in location in the horizontal plane around the animal. Maskers were continuous broadband noises. In the focal masker condition, a single masker source was tested at various azimuths. In the diffuse masker condition, uncorrelated noise was presented from two speakers at ±90° lateral to the animal. For about 2/3 of units ("type A"), the presence of the masker generally reduced neural sensitivity to signals, and the effects of the masker depended on the relative locations of signal and masker sources. For the remaining 1/3 of units ("type B"), the masker reduced spike rates at low signal levels but often augmented spike rates at higher signal levels. Increases in spike rates of type B units were most common for signal sources in front of the ear contralateral to the recording site but tended to be independent of masker source location. For type A units, masker effects could be modeled as a shift toward higher levels of spike-rate- and spike-latency-versus-level functions. For a focal masker, the shift size decreased with increasing separation of signal and masker. That result resembled psychophysical spatial unmasking, i.e., improved signal detection by spatial separation of the signal from the noise source. For the diffuse masker condition, the shift size generally was constant across signal locations. For type A units, we examined the effects of maskers on cortical signaling of sound-source location, using an artificial-neural-network (ANN) algorithm. First, an ANN was trained to estimate the signal location in the quiet condition by recognizing the spike patterns of single units. Then we tested ANN responses for spike patterns recorded under various masker conditions. Addition of a masker generally altered spike patterns and disrupted ANN identification of signal location. That disruption was smaller, however, for signal and masker configurations in which the masker did not severely reduce units' spike rates. That result compared well with the psychophysical observation that listeners maintain good localization performance as long as signals are clearly audible.
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INTRODUCTION |
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The auditory system has evolved to process behaviorally relevant sounds in a background of competing sounds. Nevertheless most studies of spatial hearing and of its neural substrates have employed acoustic stimuli presented in a silent background. The present study examined the responses of auditory cortical neurons to signals in the presence of continuous noise presented from various locations. The results of this study bear on two important aspects of hearing: spatial unmasking and sound localization.
Spatial unmasking refers to improved detection or identification of a
signal by increasing separation of signal and competing noise sources.
Spatial unmasking has been demonstrated psychophysically in humans
(detection: Saberi et al. 1991; Terhune and
Turnbull 1989
; identification: Bronkhorst and Plomp
1988
, 1989
, 1992
; Kidd et al. 1998
; Plomp
and Mimpen 1981
) and in animals (ferrets: Hine et al.
1994
; birds: Dent et al. 1997
). Stimulus
conditions used by Saberi and colleagues (1991)
were
most comparable to those used in the present study. They measured
listeners' detection thresholds for a click-train signal in the
presence of a continuous-noise masker, varying signal, and masker
locations on the horizontal plane. The elevation of detection
thresholds by the masker tended to be greatest when the masker and the
signal sources coincided in location, and masking tended to decrease
with increasing spatial separation of the masker and the signal sources
(Saberi et al. 1991
).
Two groups have studied sound localization in the presence of a masking
noise. Good and colleagues (Good and Gilkey 1996; Good et
al. 1997
) and Lorenzi and colleagues
(1999)
measured human listeners' location judgements of
click-train signals in a free field in the presence of a masker
presented from a single source. Those studies agreed that listeners
maintained relatively accurate location judgements in the presence of a
masker as long as the signal was clearly audible (i.e., signal-to-noise
ratio more than ~10 dB). That result implies that neural mechanisms
for sound localization are fairly resistant to competing sounds.
Previous studies of neurons in the auditory cortex have examined the
impact of continuous noise on neuronal responses (Brugge et al.
1998; Phillips 1985
; Phillips and Cynader
1985
; Phillips and Hall 1986
). In those studies,
neurons showed little or no sustained response to a continuous noise,
and the presence of continuous noise tended to decrease spike rates and
to increase spike latencies in response to an added stimulus. An
increase in the level of a background noise was largely equivalent to a decrease in the level of the signal. Brugge and colleagues
(1998)
recorded the responses of neurons in the cat primary
auditory cortex to broadband signals that simulated sources at various locations in virtual auditory space. A spatially diffuse masker was
simulated by adding binaurally uncorrelated noise to the signals at the
two ears. Analysis of virtual spatial receptive fields, spike rates,
and first-spike latencies indicated that the size of the masker-induced
shift in neural sensitivity was largely independent of virtual
signal-source location.
The present study further examined the effects of continuous background
noise on the responses of cortical neurons to click trains that varied
in location in a free field. We refer to the click-train stimulus as
the signal and to the continuous background noise as the
masker. Click trains were used as signals because they were
also used in psychophysical studies reviewed above (Good et al.
1996, 1997
; Lorenzi et al. 1999
; Saberi
et al. 1991
) and because they were somewhat comparable to the
single-impulse stimuli used in the physiological study by Brugge and
colleagues (1998)
. We focused on the effects of focal maskers
presented from single loudspeakers and examined the influences of
masker and signal source locations on responses of cortical neurons in
the cat's auditory cortical area A2. Neurons in area A2 have several
response properties that invite study of sound-location coding. Those
properties include broad frequency tuning (Schreiner and Cynader
1984
), sensitivity to sound location in both horizontal and
vertical planes (Middlebrooks et al. 1998
; Xu et
al. 1998
), and spatial sensitivity that parallels psychophysical responses to sounds that produce spatial illusions (Xu et al. 1999
).
Consistent with previous studies, we found that the presence of a
masker reduced neural sensitivity to signals for the majority of units.
The size of the reduction in sensitivity varied with the relative
locations of the signal and masker sources: the effect of the masker
decreased with increasing separation of signal and the masker. That
result resembled psychophysical spatial unmasking found by
Saberi and colleagues (1991). We obtained an unexpected result for a sizeable minority of units: the masker reduced spike rates
at low signal-to-noise ratios but augmented spike rates at higher
signal-to-noise ratios. We used an artificial neural network (ANN)
algorithm to evaluate the accuracy with which neural spike patterns
signaled the locations of signal sources in the absence and presence of
the masker. For many configurations of signal and masker, addition of a
masker altered spike patterns and profoundly disrupted ANN
identification of signal location. That disruption, however, was less
severe for configurations of signal and masker in which the masker did
not severely reduce the unit's spike rate. That result resembled the
psychophysical observations by Good and colleagues (Good and
Gilkey 1996
; Good et al. 1997
) and by Lorenzi and
colleagues (1999)
that listeners localized signals accurately
under conditions in which the signals were clearly audible and showed
degraded performance when the signals were near or below audibility.
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METHODS |
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Experimental apparatus, stimulus generation, and data acquisition
Stimuli were click trains
(250-s1 rate, 80-ms
duration) presented in quiet or in the presence of a continuous
broadband background noise. Throughout the present paper, we refer to
the click trains as the signals and to the background noise as the
masker. Additional stimuli were 80-ms noise bursts used as
search stimuli and 80-ms tone bursts used for measuring units'
frequency sensitivities. The experimental apparatus for stimulus
generation was identical to that detailed previously
(Middlebrooks et al. 1998
) except for the addition of
background noise. Briefly, experiments were controlled with an
Intel-based personal computer. Maskers were generated with analog
devices (described later). All stimuli other than the masker were
synthesized digitally at a sampling rate of 100 kHz, using equipment
from Tucker-Davis Technologies (Gainesville, FL). Experiments were
conducted in a sound-attenuating chamber that was lined with acoustical
foam (Illbruck, Minneapolis, MN) to suppress reflections of sounds at
frequencies <500 Hz.
Signals were presented from multiple loudspeakers, one loudspeaker at a
time. A circular hoop held the loudspeakers in the horizontal plane at
a distance of 1.2 m from the animal's head. The speaker location
directly in front of the animal was labeled 0°, and
positive azimuths indicated speakers on the right
side of the animal, which was ipsilateral to the recorded
cortical hemisphere. Signal source locations varied between 160°
and +160° in 40° steps. Speakers were calibrated using a precision
microphone (ACO Pacific) with Golay codes as probe sounds (Golay
1961
; Zhou et al. 1992
). An inverse filter
response for each loudspeaker was stored on computer disk. The click
signal presented to a loudspeaker was the time-domain waveform of the
inverse transfer function of the particular loudspeaker, windowed to a
3-ms duration. Clicks emitted from the loudspeakers had 80% of the
power restricted to an 80-µs compressive peak and had flat spectra
between 0.5 and 30 kHz. Noise and tone bursts were 80 ms in duration,
ramped on and off with 5-ms rise/fall times. Signals and tone bursts were presented once per second.
Continuous maskers were generated by a custom broadband random noise
generator, spectrally flattened by a two-channel graphic equalizer
(Rane, Mukilteo, WA), and presented through a single loudspeaker placed
at various azimuths. The amplitude spectrum of the masker sound field
measured at the center of the chamber was low-passed <30 kHz and
showed root-mean-squared fluctuation of 3 dB from 0.5 to 30 kHz. The
center of the masker loudspeaker was positioned 5° below the circular
hoop that held the signal loudspeakers. Masker source locations varied
between 120 and +120° in 40° steps. We refer to the maskers
presented from single loudspeakers as focal maskers. An
additional, diffuse, masker condition used two uncorrelated
noise sources. In that condition, noises were generated by the two
independent random noise sources, shaped with the two channels of the
graphic equalizer, and presented through two loudspeakers at azimuths
of
90 and +90°. The resulting signals in the two ears were largely
uncorrelated. Such uncorrelated signals at two ears produce a sensation
of a spatially diffuse sound (Blauert 1997
). The diffuse
masker condition was the condition that was most similar to the masker
used in the study by Brugge and colleagues (1998)
. All
units, except 13 units recorded in a supplementary experiment
(described later), were tested with focal-masker locations of
40, 0, and +40° and masker levels of 35 dB SPL (re: 20 µPa). A subset of
units was tested with additional focal masker locations, the diffuse
masker, and/or masker levels of 15 and 25 dB SPL. In a supplementary
experiment, units were tested with the 0° focal masker and with the
diffuse masker levels of 15, 25, and 35 dB SPL.
Procedures for unit recording and for spike sorting were identical to
those detailed by Furukawa et al. (2000). Briefly, unit activity was recorded extracellularly with silicon-substrate
multi-channel probes (Anderson et al. 1989
). Each probe
had one shank along which 16 recording sites were located in 100- or
150-µm intervals. The activity at each site was amplified with custom
hardware, digitized at a rate of 25 kHz, sharply low-pass filtered <6
kHz, resampled at 12.5 kHz, and stored on computer disk for off-line spike sorting (described later). For monitoring purposes, spikes were
discriminated on-line with a simple peak-detection algorithm. On-line
monitoring was used to estimate units' threshold SPLs and frequency tuning.
Animal preparation
This report presents data from six purpose-bred adult cats of
both sexes. One additional cat was used for the supplementary experiment. The animal preparation was identical to that detailed previously (Middlebrooks et al. 1998). In brief,
isoflurane anesthesia was used during surgery, and
-chloralose was
used for unit recording. All recordings were made from the right
cortical hemisphere. A skull opening was made to reveal the middle
ectosylvian gyrus, and a plastic chamber was cemented around the
ventral margin of the opening to contain a pool of silicone oil. The
scalp was sutured closed around the plastic chamber. The animal was
positioned in the center of the sound-attenuating chamber, with its
body supported in a sling that also held a heating pad. Its head was
supported from behind by a bar attached to a skull fixture. Thin wire
supports were used to push the external ears into a forward position
(Middlebrooks and Knudsen 1987
). The position of the
ears was constant throughout each experiment.
At the end of each experiment, the animal was killed. The cortex was immersed in buffered formalin and later inspected to confirm the gyrus recorded from.
Experimental procedure
Recordings were made from cortical area A2. Electrode
penetrations passed dorsoventrally, oblique to the cortical surface near the crest of the middle ectosylvian gyrus, ventral to area A1.
Area A2 was distinguished from area A1 by the absence of tonotopic organization and by response bands that were 1 octave wide at signal
levels 40 dB above threshold (Reale and Imig 1980
;
Schreiner and Cynader 1984
). Search stimuli consisted of
broadband noise bursts, presented at 0° or contralateral 40°
azimuth. The depth of the recording probe was adjusted so as to observe
unit responses at as many recording sites as possible. Typically, unit
spike responses were observed at ~10 of 16 recording sites in each
probe penetration.
Study of units in each electrode penetration began by identifying
units' frequency sensitivities with a sound source fixed at a location
from which a noise burst produced a strong response, usually 0° or
contralateral 40° azimuth. Tone frequencies were varied in 1/3-octave
steps from 1.18 to 30 kHz. Next, responses to click trains presented
from the same location were recorded for a range of SPLs in 5-dB steps.
Units' thresholds were estimated to the nearest 5 dB by inspection of
on-line poststimulus time histograms and spike-rate-versus-level plots.
When units' thresholds differed among the multiple recording sites at
one probe position, we adopted the modal threshold SPL of units as the
representative threshold SPL for that probe position. Usually, units'
thresholds differed by 10 dB at each probe position.
The units' spatial sensitivities were measured using a stimulus set
that consisted of signals presented from nine azimuths in the
horizontal plane (160° to +160° in 40° steps). When signals were presented in quiet, tested signals ranged between 0 and 40 dB
above the units' threshold in 5-dB steps. When presented with masker,
tested signal levels ranged in 5- or 10-dB steps between 20 and 40 dB
above the units' threshold in quiet. Each series of trials consisted
of every combination of signal location and level presented once in
pseudo-random order, and each block consisted of 10 or 20 series of
trials. Blocks of trials in quiet and masker conditions were
interleaved to monitor the stability of recording throughout the
recording session. For the quiet condition, two to four blocks were
presented, interleaved with masker conditions, yielding a total of
20-40 repetitions of each stimulus. For each masker condition, one or
two blocks were presented, yielding a total of 10-20 repetitions for
each signal-masker combination. The order of blocks of masker
conditions was randomized to reduce systematic bias due to any
potential slow drift in units' response characteristics. Before
starting each block of trials, we waited
30 s to permit units to
adapt to the continuous masker or quiet. Study at each probe placement
typically lasted ~2-5 h, depending on the number of masker
conditions tested. Outside of the 2- to 5-h period, additional stimuli
often were tested at each probe placement to provide data for other
studies. Experiments typically lasted 3-5 days and yielded recordings
from 2 to 7 electrode penetrations.
Data analysis
Spikes were discriminated off-line using custom software that
employed a template-matching algorithm. Well-isolated single units were
encountered in only ~7% of recordings, so the majority of recordings
were from clusters of two or more unresolved units; examples of single
units and cluster recordings are illustrated in Furukawa et al.
(2000). We observed no systematic difference in masker effects
between well-isolated units and multi-unit clusters, so we do not
distinguish types of unit isolation in the presentation of the results.
For simplicity of presentation, we refer to both the multi-unit
clusters and the well-isolated units as "units."
Units were screened for responsiveness and stability based on responses obtained in quiet. Responsiveness of each unit was evaluated by the mean spike rate for the stimulus that elicited the maximum number of spikes. If the mean spike rate for the best stimulus was <1 spike per trial, the unit was excluded from further analysis. Stability of a unit was determined by spike rates for the quiet condition, using a two-way ANOVA, with factors being stimulus condition (i.e., combinations of signal SPL and location) and block number. We excluded units for which the variance accounted for by series number plus the variance accounted for by interaction of block number and stimulus condition exceeded 7% of the total variance. The screen by block number eliminated units for which there was a change in unit responsiveness or in the number of neurons included in a multi-unit cluster. The screen by block number and stimulus condition eliminated units for which sensitivity to SPL or location changed. The final data set that satisfied all criteria included 117 recording sites at 21 probe placements.
Spike times were stored as latencies relative to the onset of sound at a loudspeaker. The arrival of sound at the cat's head was delayed by ~3.5 ms because of the acoustical travel time. Cortical neurons' spike latencies were >10 ms after the stimulus onset, and robust responses after 60 ms were rare. To reduce any influence of occasional unreliable late spikes, we restricted analysis to the range of spike times from 10 to 60 ms after the stimulus onset. Mean spike rates (spikes per trial) were computed within that 50-ms time window. The distribution of first spike latencies was generally highly skewed, having a long tail toward longer latencies, and the standard deviations of first-spike latencies tended to be larger for longer latencies. For that reason, mean first-spike latencies were represented by the geometric means.
Mean spike rates and first-spike latencies were sensitive to signal
levels. For the majority of units, addition of continuous background
noise tended to shift that sensitivity along the level axis. The
following procedure was used to compute the rate-versus-level-function (RLF) shift and latency-versus-level-function (LLF) shift. First, RLFs
for the quiet condition and for each masker condition were linearly
interpolated in 1-dB steps. Second, the RLF for the quiet condition was
shifted along the level axis in successive 1-dB steps. For each shift,
we computed the root-mean-square (RMS) of the difference in spike rate
between the shifted RLF for the quiet condition and the RLF for masker
condition over the range of levels for which the two functions
overlapped. The RLF shift due to the masker was defined as the dB shift
that minimized the RMS difference in spike rate. A positive shift
indicated that the masker reduced a unit's sensitivity, shifting the
RLF toward higher signal levels. Generally, shifts ranged between 0 and
20 dB, but sometimes were allowed to range between 10 and 30 dB if
that reduced the RMS difference significantly (1-tailed
t-test, P < 0.01) relative to the minimum
RMS for shift ranging between 0 and 20 dB. LLF shifts were computed in
a similar fashion to RLF shifts but on a logarithmic latency scale.
Poststimulus times of the first spikes were first converted to a
logarithmic scale, and the mean of first-spike latencies at each SPL
was computed based on all the trials with any spikes. Note that there
were SPLs at which mean latencies were not computed because of the absence of spikes on any trials. The LLF for each signal location was
constructed by interpolating among all the SPLs at which mean latencies
were computed. The LLF shift was defined as the dB shift that minimized
the RMS difference in logarithmic latency.
We examined the effects of maskers on location coding by cortical
neurons. The procedure employed an ANN algorithm that associated neuronal spike patterns with particular signal locations. Neural responses recorded on odd- and even-numbered trials were divided into
training and test sets, respectively. The training set was used to
train the ANN, then the trained network was used to estimate sound-source locations by recognizing spike patterns in the test set.
The procedure for computing averaged spike patterns, the network
architecture, and the procedures for training and testing were
identical to those detailed previously (Middlebrooks et al. 1998). Twenty and 50 spike patterns were formed for training
and testing, respectively. The ANN analysis in the present study
consisted of two stages. In the first stage, the ANN was trained and
tested with spike patterns recorded in the quiet condition. In the
second stage, the trained ANN was tested with spike patterns recorded in each masker condition. The ANN estimates of signal locations in the
quiet and masker conditions at each signal location were compared in
terms of the circular centroid and the quartiles below and
above the centroid. The centroid was formed by treating each network
location estimate as a unit vector, then computing the direction of the
vector sum of the unit vectors (Fisher 1993
; Furukawa et al. 2000
).
An additional measure of location coding was given by the best azimuth. The spatial tuning of most units broadened at high sound levels, so best azimuths were computed for the lowest tested signal level at which the maximum spike rate was >20% of the maximum across all levels. Best azimuths were computed only for units that showed >50% modulation of spike rate by signal azimuth at that sound level. The spike-rate-versus-azimuth function was interpolated linearly in 1° steps. From that interpolated function, the response peak was identified as the set of contiguous points at which spike rates were >75% of the maximum, and a vector sum was formed from all the points within the peak. The best azimuth was the direction of the resultant.
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RESULTS |
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The database consisted of 117 single units or unit clusters
recorded from cortical area A2 of six cats. An additional 13 units from
one additional cat were tested in a supplementary experiment. Units
responded to broad ranges of pure-tone frequencies (typically >2
octave) and favored high frequencies: ~90% of units responded robustly to frequencies >6 kHz, whereas only ~30% of units
responded robustly to frequencies <2 kHz. Azimuth sensitivities of the
units were similar to those found in our previous studies
(Furukawa et al. 2000; Middlebrooks et al.
1998
). The spike rates of the majority of units were broadly
tuned to contralateral signal-source azimuths, and units' azimuth
selectivity broadened with increasing signal level. Only ~27% of
units showed RLFs that were nonmonotonic in that the spike rate at the
highest tested sound level was <75% of that measured at a lower sound
level. There was no systematic qualitative difference in masker effects
among units that differed in frequency tuning, sharpness of azimuth
sensitivity, or monotonicity of RLF.
No unit showed appreciable steady-state firing in quiet or in the presence of a continuous masker. Units typically responded to the signal with a few spikes locked to the signal onset both in quiet and in the presence of a continuous masker.
Response patterns and spatial tuning in backgrounds of quiet and of masking noise
Figure 1 represents the responses of one unit. Each raster plot shows responses to click trains at a range of signal locations. Each column of raster plots represents one signal level (labeled relative to the threshold in the quiet condition). Each row of raster plots represents the quiet condition (top), one of three focal masker locations (rows 2-4) or the diffuse masker condition (row 5). The rightmost column shows plots of spike rate versus signal location; each plot shows three to five signal levels.
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In the quiet condition (top), signal levels within 20 dB of
threshold produced maximum spike rates and minimum latencies when signal sources were located around 40° (i.e., contralateral to the
recording site). The azimuth sensitivity flattened as the signal level
was increased to 40 dB above threshold. The addition of a continuous
masker (rows 2-5) tended to decrease spike rates at all but
the highest signal levels. In the masker conditions, the raster plots
at each signal level generally resembled the plots for the quiet
condition at signal levels that were 10-20 dB lower. The focal maskers
tended to show the greatest effect on responses to signal sources
located near the masker. The +40° masker, for instance, tended to
reduce spike rates and increase latencies in response to signals on the
ipsilateral side; responses to the contralateral 160° signal also
were reduced. The
40° masker, in turn, tended to reduce responses
to contralateral signals while preserving most of the response to
targets around ipsilateral 40 and 80°. The reduction of signal
sensitivity due to the 0° focal masker (row 3) and the
diffuse masker (row 5) was rather uniform across signal
locations (although the masker effect was least for signals around
40°). That is, each of the rate profiles for the 0° or diffuse
masker condition somewhat resembled a profile for the quiet condition
at a lower signal level.
The unit represented in Fig. 1 was typical of the majority of units in
that maskers reduced units' sensitivities to signals and in that focal
maskers had the greatest influence on signal sources located near the
masker location. For descriptive purposes, we refer to units that
showed that characteristic as type A. The remainder of units, type B,
showed less sensitivity to the location of a focal masker. The type B
unit represented in Fig. 2 showed a
preference for contralateral signals at lower SPLs and a broad range of
azimuths at higher SPLs, like the unit represented in Fig. 1. All of
the masker conditions reduced responses to signals at the lowest SPL,
with relative sparing of responses to signals away from the masker
location. At the highest signal levels, however, this unit and other
type B units showed enhancement of the response to signals,
particularly at 80 and
40°, regardless of masker location. This
is particularly clear in the spike-rate plots in Fig. 2, which show
that the maximum spike rate elicited by signals at
40° in the
+40°-masker condition was nearly three times that obtained in the
quiet condition.
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We distinguished types A and B because, as shown in a later section, masker effects on type A units could be quantified conveniently in terms of shifts in RLFs whereas that analysis proved to be invalid for type B units. Details about the differences between those two types of units will be described in later sections in which we examine rate- or latency-versus-level functions for various conditions. Before then, the following sections describe effects of maskers on spatial tuning and on the size of the population of active units; those sections pertain to both type A and type B units.
Masker effects on spatial tuning
The magnitude of masker effects tended to vary with
signal locations, as illustrated in Figs. 1 and 2. For that reason,
addition of a focal masker could change the apparent azimuth preference of a unit. In Fig. 1, for example, a masker presented at 40° selectively reduced responses to signal sources at
40° while preserving responses to signal sources at +40 and +80°. The effect was to shift the unit's best azimuth from
40 to +40°. Note that the masker did not create a response to a signal that would not have
elicited a response in quiet. Instead, the effect of the focal masker
was to carve a response peak out of an otherwise-flat azimuth function.
Figure 3 summarizes the effects of
maskers on the best azimuths of all units that showed azimuth tuning
(including unit types A and B); the procedure for computation of best
azimuths is given in METHODS. Each panel represents one
masker condition and plots units' best azimuths in the presence of a
masker against best azimuths in quiet. Each circle represents one unit,
and asterisks represent the locations of focal maskers. In the quiet
condition, the majority of units preferred contralateral signal
locations. The contralateral maskers tended to displace the best
azimuth away from the masker location toward the ipsilateral side.
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Masker effects on the size of the population of active units
The effects of maskers on the size of the population of
active units was summarized by plotting the percentage of units that were activated above a criterion level in various signal and masker conditions. Figure 4, left,
shows the percentages of the unit population that were activated by the
20-dB SPL signal at various locations. In this analysis, we defined a
unit as active when its average spike rate was 50% of that unit's
maximum rate measured across all signal locations in the quiet
condition. Each panel represents one masker condition. The
and
-
- represent the active population in the quiet and masked
conditions, respectively. Slight differences among the panels in the
plots for the quiet condition reflect differences in the numbers of
units that were tested in each masker condition.
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The plots for the quiet condition in Fig. 4 show that a signal source at any location activated a large percentage of the unit population and that the greatest percentage was activated by frontal contralateral signals. A masker from any location tended to suppress strongly the size of the population activated by rear and ipsilateral signals. Figure 4, right, shows, of the population that was active in quiet, the percentage that was suppressed by the various maskers. Maskers tended to have the greatest impact on the units activated by signal sources near the masker source, particularly for ipsilateral (+40 and +80°) maskers.
Masker effects on rate- and latency-versus-level functions
Mean spike rates tended to increase, and mean latencies tended to
decrease, with increasing signal levels. Addition of a masker tended to
shift the RLFs and LLFs of units to higher signal levels. This finding
was consistent with previous studies (Brugge et al. 1998; Phillips 1985
; Phillips and Cynader
1985
; Phillips and Hall 1986
). As stated in the
preceding text, ~27% of units showed nonmonotonic RLFs. Nonmonotonic
units tended to preserve the nonmonotonic characteristic of their RLFs
in the presence of masking noise. Figure
5, left, shows examples of
RLFs and LLFs for one unit for the 0° signal. The -
-
represent RLF (top) and LLF (bottom) for the
quiet condition. The -
- and -
- represent
corresponding plots for the
40 and +40° maskers, respectively. One
can see that the RLF and LLF in the masker conditions resembled the
quiet-condition functions shifted to the right. In the majority of
cases, masker effects could be characterized by the shift sizes of the
RLF or LLF functions.
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There were, however, cases in which masker effects could not be
characterized by shifts in RLFs. Specifically, addition of a masker
sometimes increased the spike rate, so that masker-induced RLF changes could not be accounted for by a simple shift of the RLF.
Figure 5, right, shows examples of such cases for one unit. Although the presence of the 40° (
) or 0° (
) masker
appeared to elevate signal thresholds, the spike rate for the masker
condition increased rapidly with signal SPL, reaching greater rates
than the highest rate for the quiet condition (top). One
concern was that instability of unit responses might have produced the
observed changes of RLFs for the masker conditions. In the course of
studying this unit, however, we divided the recording for the quiet
condition into four blocks of trials and interleaved those blocks with
recordings for the masker conditions. The - - - in the top
right panel show the range of the RLFs in quiet computed for the
individual blocks of trials. One can see that the RLFs for the masker
conditions generally fell out of the range of the RLFs in quiet,
indicating that changes in RLFs could not be accounted for by unit instability.
The LLF for the same cases (bottom right) showed little or no indication of facilitation (i.e., shorter spike latencies). In general, first-spike latency was bounded by a minimum poststimulus time, which was probably determined by specific axonal conduction velocity and synaptic delays.
For cases of facilitation like that shown in Fig. 5, right,
it was not appropriate to represent masker effects by RLF and LLF
shifts. Thus we excluded a group of units (the type B units) for which
the masker-induced facilitation was particularly robust and applied
analyses of RLF and LLF shifts to the rest of the unit sample (the type
A units). Types A and B were distinguished in the following way. For
each unit in each of signal-masker configurations including the quiet
condition, we found the maximum spike rate across all signal levels
tested. Then, at each signal location, we computed the ratio of the
maximum spike rates for the masker condition versus the quiet
condition. Ratios appreciably greater than unity indicated increased
maximum spike rate by the presence of the masker. A somewhat distinct
population of units showed increased rates in several signal-masker
configurations. We classified a unit sensitivity for a signal-masker
configuration as "facilitated" when the ratio of maximum spike
rates was >1.2. Across all 117 units and nine signal locations
(160-160° in 40° steps), 7.2, 6.9, and 15.4% of signal-masker
configurations showed facilitation for the
40, 0, and 40° maskers,
respectively. For the diffuse masker, 11.9% of signal-masker
configurations (41 units by 9 signal locations) showed facilitation. We
defined as type B a population of units that showed facilitation in
units in
4 of the 27 signal-masker configurations for which all the
units were tested (9 signal locations; 3 masker locations:
40, 0, and
+40°; 1 masker SPL: 35 dB). The remainder of units were classed as
type A. Of the total of 117 units, 79 and 38 units were classified as
types A and B, respectively. The proportion of units classified as type
B was fairly insensitive to the choice of the criterion for
facilitation. That is, when the criterion was varied between 1.0 and
1.4, 26 units were consistently included among the 38 units with the
highest ranks in the number of configurations with facilitation. Type B
units were recorded in 12 of 21 electrode penetrations in five of six
cats; in 6 of those 12 penetrations,
50% of units recorded were type
B. Penetrations in which both types were found did not show any
significant clustering of unit types along recording sites. We were
able to apply "runs tests" for randomness of sequence (Sokal
and Rohlf 1995
) to three of the penetrations, none of which
showed significant nonrandom sequences of unit types (P > 0.05). Type A and B units were similar in that the majority of units
showed contralateral or broad azimuth sensitivities, and the average
best azimuths showed no significant difference (type A:
50.0°, type
B:
65.1°; 2-tailed t-test, P
0.0728).
Also, there was no significant association of unit type with
monotonicity of the RLFs (as defined earlier in RESULTS,
2 test P
0.2286). The only
reliable difference between types A and B was the absence or presence
of increases in maximum spike rate by the masker. We focus on type A
units in the following paragraphs, then return to type B units at the
end of RESULTS.
RLF and LLF shifts in type A units provided single values to represent
masker effects across a range of signal levels and provided a
consistent unit (i.e., dB) for comparing masker effects between two
aspects of neural responses: spike rate and latency. Also, the RLF
shift permits a comparison of the present results with psychophysical
studies of spatial unmasking (e.g., Saberi et al. 1991)
and with other physiological studies that represented masker effects
with threshold shifts (Jiang et al. 1997
;
Ramachandran et al. 2000
; Ratnam and Feng
1998
). The RLF shift adopted in the present study was
conceptually similar to the "dynamic range shift" defined by
Phillips and Hall (1986)
, which was the difference between quiet and masker RLFs in signal SPLs that elicited a spike rate
of 50% of the maximum rate. The details of the procedure for
computation of RLF and LLF shift are given in METHODS. For most cases, masker effects could be modeled well by the RLF shifts. That is, for >89% of RLFs and for >84% of LLFs (across 79 type A
units; 9 signal locations:
160,
120, ... , +120, and +160°; 3 masker locations:
40, 0, and +40°; 1 masker SPL: 35 dB), the RMS
difference between the quiet and the masked RLFs or LLFs was reduced by
50% by the optimal shift. For the remainder of units, RLFs and LLFs
were measured at only the lower or upper end of the units' dynamic
range, so the RLF and LLF shifts were less well defined. Nevertheless
even for those units the RLF or LLF shift provided a useful indicator
of masker effects on units' sensitivities to signal.
Despite the qualitatively different nature of mean spike rates and
first-spike latencies as attributes of neural response patterns, RLF
and LLF shifts tended to show similar sensitivity to signal and masker
locations. We compared the RLF and LLF shifts for 2,000 pairs (across
79 units; 9 signal locations: 160,
120, ... , +120, and
+160°; 3 masker locations:
40, 0, and +40°; 1 masker SPL: 35 dB;
except for 133 signal-masker configurations for which LLF shifts were
unavailable due to too few spikes). On average, RLF shifts were only
0.8 dB greater than LLF shifts (standard deviation of the difference:
9.2 dB), although the difference was statistically significant (paired
t-test, P < 0.0001, df = 1,999). There
was a modest but statistically significant correlation between RLF and
LLF shifts (r = 0.442; P < 0.0001). A
possible source for the differences between RLF and LLF shifts might
have been due to statistical differences between (linear) spike rate and (logarithmic) latency. Also, note that the spike rate is a measure
that represents responses over the entire 50-ms recording time window,
whereas the first-spike latency represents only the first spike. Thus
it is also possible that the differences between the RLF and LLF shifts
reflected effects of the masker on later spikes in the spike pattern.
Effects of signal and masker locations on RLF and LLF shifts
Figure 6 shows RLF and LLF shifts
for the type A unit that was represented in Fig. 1. That unit had broad
spatial sensitivity, a broad frequency response area, and monotonic
RLFs, as was typical of our sample of units. The three panels of the
figure show plots for three masker-source locations: 40, 0, and
+40°. RLF and LLF shifts showed similar sensitivity to signal- and
masker-source locations. Masker sources located at
40 and +40° had
the strongest effects on responses to signal sources located near the
maskers. The effects of a masker at 0° were less sensitive to
signal-source location. Note that the negative LLF shift obtained for
the
40° signal and the +40° masker likely was a result of
imprecise shift estimation due to our sampling from shallow parts of
the unmasked and masked LLFs around the shorter extreme of the dynamic
range.
|
Figure 7 shows RLF and LLF shifts
averaged across the type A population as a function of signal-source
locations. The mean data confirm the impression given by individual
examples. Both RLF and LLF shifts generally were greatest when signal
and masker sources coincided in location, with LLF shifts showing
somewhat greater modulation by signal location than RLF shifts,
particularly for ipsilateral maskers. The modulation of the profile for
the 0° focal masker was relatively small: the difference between the maximum and minimum of the shift profile was ~5 dB for the 0° masker for both RLF and LLF shifts, whereas the differences for the
80° masker were ~10 and 14 dB for RLF and LLF shifts,
respectively. The shift profile for the diffuse masker was quite flat
for the RLF shift and was somewhat irregular for the LLF shift.
|
The cat's external ear has the greatest gain for sound sources in
front of the ear, along the "acoustic axis" (e.g.,
Middlebrooks and Pettigrew 1981). Thus we considered the
possibility that the directional dependence of the masker effects in
Fig. 7 might be determined simply by the signal-to-noise ratio (SNR) in
a single ear. Here, we consider the SNR in power integrated across a
broad frequency range, and do not regard the detailed
frequency-by-frequency SNR due to the location-dependent transfer
functions of the external ears (Musicant et al. 1990
;
Rice et al. 1992
; Xu and Middlebrooks 2000
). In each panel of Fig. 7, the masker was fixed in
location and in level, so in each panel the decrease in SNR
within each ear relative to the quiet condition was constant across
signal locations (here, "noise" in the quiet condition refers to
the internal noise). If masker effects were due exclusively to changes in SNR at only one ear, one would predict that RLF and LLF shifts would
be insensitive to signal-source location. The plots in Fig. 7 clearly
contradict that prediction, and thus we conclude that the SNR in a
single ear could not account for the signal-location dependence of the
masker effects.
Cortical neurons in the present study, as in previous reports, tended to be most sensitive to sound sources located near the acoustic axis of the contralateral ear. Thus we expected the masker effect to be greatest when the masker source was located on the contralateral side. This expectation was tested by averaging RLF and LLF shifts across signal locations and then plotting the averages as a function of masker location (Fig. 8). The figure also shows the directional gain of the contralateral ear (- - -), represented by the pressure gain averaged over frequencies from 3 to 30 kHz. That range of frequency covered frequency response areas of the majority of units in our sample. The physiological data roughly paralleled the acoustical data; this suggests a dominance of contralateral ear inputs in determining the overall reduction in sensitivity induced by maskers. The shift sizes for the diffuse masker were as great as the shift sizes for the most effective focal maskers.
|
Effects of masker level
So far, we have described the results for a masker fixed at 35 dB
SPL. We tested two additional masker levels (15 and 25 dB SPL) at
masker locations of 40, 0, and +40°, for 29 type A units. Figure
9 represents average RLF or LLF shifts
(left and right, respectively) at three masker
levels as a function of signal location. Each row of panels represents
one masker location (- - -). The data for the 35-dB masker (
and
) generally followed the trends shown in Fig. 7, which is based on
all of the 79 type A units including the units represented in Fig. 9.
In general, one can see a monotonic increase of RLF and LLF shift with
increasing masker level. The profiles of shifts versus signal locations
were relatively flat for the lowest masker level; the somewhat distinct dip of the RLF-shift profile for the 0° masker and the 0° signal was a result of imprecise shift estimation due to our sampling from
shallow parts of the RLFs. The rate of increase in RLF or LLF shifts
with increasing masker level depended on the signal-masker configuration. For the 0° masker, the growth rate was generally constant across signal locations: each 10-dB increment in masker level
resulted in an increase of 8.5 ± 2.8 (SD) dB in the RLF shift and
an increase of 6.3 ± 1.5 dB in the LLF shift. For lateral maskers, however, the growth rate of shifts was generally greater for
signals ipsilateral to the masker. For the
40° masker, the average
growth rate of shifts was 9.7 dB (RLF shift) and 9.2 dB (LLF shift) for
the
40° signal compared with 2.6 dB (RLF shift) and 3.2 dB (LLF
shift) for the +40° signal. Similarly, for the +40° masker, the
average growth rate of shifts was 7.9 dB (RLF shift) and 7.3 dB (LLF
shift) for the +40° signal, versus 2.4 dB (RLF shift) and 2.6 dB (LLF
shift) for the
40° signal. A floor effect could account in part for
the small growth rate for signals contralateral to the masker since
shift sizes for those signals were generally small (e.g., signals
contralateral to the recorded side, for the +40° masker). The small
growth rate, however, was also observed for configurations in which the
shift size at the lowest masker level was well above zero (e.g.,
signals ipsilateral to the recorded side, for the
40° masker). The
results indicate that the effect of masker level depends on the
relative locations of signal and masker sources.
|
For 13 units obtained in a supplementary experiment, we compared the effects of masker level between the focal 0° and the diffuse masker (data not shown). The effect of masker level was similar between the two masker conditions. The average increase of RLF shift by a 10-dB increment of masker SPL was 6.5 and 6.6 dB for the 0° and the diffuse masker, respectively (P = 0.44; paired t-test; df = 226). Similarly, the average increase of LLF shift was 6.6 and 5.5 dB for the 0° and the diffuse maskers, respectively (P = 0.037; paired t-test; df = 223).
Masker effects on accuracy of location coding
We examined the effects of a continuous masker on the coding of
sound-source location by cortical units. As detailed in
METHODS , the approach was to train an ANN to recognize the
spike patterns associated with particular signal-source locations in
the quiet condition and then to test the trained network with spike
patterns recorded in various masker conditions. Results presented in
previous sections have indicated that addition of a masker was somewhat like reducing the signal level, so it seemed obvious that maskers would
influence spike patterns and thus influence the ANN estimate of
signal-source location. Nevertheless our previous studies have demonstrated that estimation of source location by this ANN procedure is fairly robust to changes in stimulus level as long as the ANN is
trained with cortical responses to stimuli that varied in level (e.g.,
Middlebrooks et al. 1998). For that reason, we
anticipated that an ANN that was trained with spike patterns obtained
for multiple signal levels in the quiet condition could estimate
signal-source locations based on spike patterns obtained in a masked
condition. In the present analysis, we trained and tested the ANN for
signal levels between 20 and 40 dB above the unit thresholds obtained in the quiet condition.
Figure 10 represents ANN results for
one unit for the quiet condition and in the presence of focal maskers
at 40, 0, and +40°. The distribution of ANN estimates of
signal-source location is represented by lines that show the centroids
and the ranges of second and third quartiles. The results for the quiet
condition (the leftmost plot) are repeated by gray shading
in all the other plots. The top row of plots shows data for
all the tested signal-source locations and levels. Location accuracy
was markedly degraded in the masker condition compared with the quiet
condition. In the
40° masker condition, for example, most cortical
responses to signal sources in front of the animal were incorrectly
assigned to rear locations. In that case, spike rates elicited by
frontal targets were strongly reduced by the masker, thereby causing
them to resemble spike rates that were elicited by rear targets in the
quiet condition.
|
The degradation of location estimates in Fig. 10, top, could
have been due at least in part to large RLF and LLF shifts. That is,
the masked signal levels at some signal locations fell below the
"operating range" of the ANN. That would be analogous to the localization errors shown by human listeners when masked signal are
near the limits of audibility (Good and Gilkey 1996; Good et al.
1997
; Lorenzi et al. 1999
). We addressed this
problem by expressing masked signal levels as the signal level relative
to threshold in quiet shifted by the mean of the RLF and LLF shifts computed for each signal- and masker-source location; these shifted levels are referred to as "effective signal levels." The ANN
analysis was repeated using only the conditions for which effective
signal levels fell in the range of 20-40 dB above the unit threshold in quiet. The results are shown in Fig. 10, bottom. Signal
locations with missing points are locations at which the RLF and LLF
shifts were so large that no data were available for computing the
statistics, which was often the case for locations around the masker.
Compared with the results in the top panels, the ANN
estimates of locations in the masker conditions were closer to the
estimates in the quiet condition. There were, however, configurations
for which ANN estimates for the masker condition deviated greatly from
those for the quiet condition, even after the adjustment by the
effective signal level; that was most apparent for the 0° masker.
This indicates that the masker had effects on features in the spike
patterns that could not be accounted for by the RLF or LLF shifts and
that the trained ANN was somewhat sensitive to those features.
The illustrated results were generally representative of the population of type A units. The accuracy of location coding was characterized for each unit by the centroid error (defined in METHODS). Centroid errors were computed for all available units, signal locations, and masker locations. The average centroid error for the quiet conditions was 42.8°. The error increased to 80.1° averaged across the three masker conditions (P < 0.001; t-test of mean; df = 1,700). The error was significantly reduced to 62.9° by removing responses for stimuli with out-of-range effective signal levels (P < 0.001; t-test of means 62.9 vs. 80.1°; df = 1,762).
Units exhibiting facilitation by maskers (type B units)
In this section, we briefly consider the cases in which a masker produced facilitation of unit responses. Here, we limit our analyses to type B units, which exhibited facilitation of their responses in the presence of a masker for a greater number of signal-masker configurations than did type A units. Most type A and B units were similar to each other in that they tended to show contralateral or broad spatial preference in the quiet condition: examples of A and B units were shown in Figs. 1 and 2, respectively.
We noted that facilitation, as defined earlier, was most often observed
for signals around 80 and
40°, regardless of masker location.
Figure 11 plots the number of type B
units that exhibited facilitation by >20% as a function of signal
location for masker locations of
40, 0, and +40°. Generally
facilitation occurred most often for the +40° masker, but within all
masker conditions, facilitation was most common for a signal location
of
40°.
|
Maskers generally had two effects on RLFs of type B units: elevation of response threshold and increased maximum spike rate. These effects resulted in a steepening of the slope of the RLF. The influence of the masker on threshold and maximum spike rate varied across signal-masker configurations and across units, so we were not able to draw general conclusions. Figure 12 shows examples of RLFs for three units, each of which was tested with three masker levels. In the top panel, a masker with increasing level gradually elevated the response threshold and increased the maximum spike rate. In the middle panel, a masker at the two lowest levels substantially increased the maximum spike rate, while the threshold level was relatively unaffected. Threshold elevation was observed only for the highest masker level. In contrast, the unit represented in the bottom panel showed an elevation of threshold without an increase in the maximum spike rate for the lowest masker levels; an increased maximum spike rate occurred only for the highest masker SPL.
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DISCUSSION |
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In the present study, we examined the responses of cortical neurons to signals at various source locations in the presence of continuous diffuse maskers or of focal maskers at various locations. Consistent with previous physiological results, the continuous masker elicited no sustained cortical spike activity and generally reduced responses to signals, although a sizeable minority of units showed facilitated spike rates in some masker conditions. The principal new finding of the study was that masker effects were sensitive to the locations of signal and masker sources. The majority of units showed greatest masker effects when signal and masker sources coincided in location, and the effects decreased with increased separation of signal and masker sources. Masking noise tended to degrade the accuracy of cortical coding of signal-source location, at least in the range of signal and masker sound levels that were tested in this study. Location-coding accuracy improved when the analysis was restricted to conditions in which signal levels were well above masked thresholds.
Comparison with previous studies
We are aware of two groups of researchers that have examined the
effects of a continuous masker on unit responses in the auditory cortex. Phillips and Cynader (1985), Phillips
(1985)
, and Phillips and Hall (1986)
tested
characteristic-frequency tone bursts presented against continuous
broadband maskers with both signal and the masker presented monaurally
to the ear contralateral to the recorded cortical hemisphere.
Brugge and colleagues (1998)
used single-impulse signals
presented from various locations in a "virtual acoustic space." The
masker in that study was diffuse, produced by presenting binaurally
uncorrelated noise to the two ears. Both groups studied neurons in
cortical area A1 of anesthetized cats.
Consistent with both those groups, the present study showed that the presence of a masker tended to elevate units' thresholds. The previous studies showed an overall depression of responses. That was also the case for type A units in the present study, although type B units showed spike-rate facilitation under some masker conditions. The Brugge group demonstrated that the magnitude of the sensitivity shift induced by a diffuse masker was relatively uniform across signal locations. Similar results were shown in the present study for the comparable, diffuse-masker condition: RLF shifts (and LLF shifts to a lesser degree) were relatively constant across signal locations (Fig. 7). Another finding common to both those groups was that the presence of a masker decreased units' signal sensitivity such that an increase in the level of the masker was roughly equivalent to an equal-magnitude decrease in the level of the signal. That reciprocal trading of masker and signal levels was seen in RLFs and LLFs in both studies and in the structure of virtual-space receptive fields in the Brugge study. For the focal 0° masker condition in the present study, the increase in RLF and LLF shift resulting from a 10-dB increment of masker level was ~6-12 dB, which was not far from the decibel-for-decibel trading of signal and masker levels reported previously. Note that the focal 0° condition was similar to the diffuse masker condition in the Brugge study and in the present study in that the diffuse and focal 0° maskers produced nearly equal spectra and equal overall sound levels at the two ears. The maskers differed mainly in temporal fine structure, which probably had little influence on the high-frequency neurons that we studied, and in short-term interaural level differences. In fact, the supplementary experiment showed little difference between the focal 0° and the diffuse conditions in shift increase per 10-dB increment of masker level.
The novel findings of our study derived from presentation of focal
maskers from locations off the midline. For the majority of units, RLF
and LLF shifts by a focal masker located away from the midline were
greatest when signal and masker sources coincided in location.
Conversely, the strength of masking could be decreased by separating
signal and masker sources. That observation has a counterpart in
psychophysical studies that have demonstrated that the detectability of
a signal improves if it is separated in location from a continuous
noise source (Saberi et al. 1991). Furthermore we
observed a signal-location dependence of the reciprocal trading between
signal and masker sound levels. When signal sources were located near
masker sources, a 10-dB increase in masker level tended to produce a
nearly 10-dB increase in the masker-induced shift in RLFs or LLFs. That
is consistent with the previous study by Brugge and colleagues
(1998)
and with our results for the focal 0° and the diffuse
maskers. In contrast, signal sources located contralateral to
off-midline masker sources showed a much smaller growth of masking, as
low as 2-3 dB per 10-dB masker increase. This small growth of masking
could be explained by a floor effect for some conditions, e.g.,
contralateral signals for the +40° masker (Fig. 9). There were,
however, instances of small growth rates for signal-masker conditions
that produced sufficiently large RLF and LLF shifts even for the lowest
masker level (ipsilateral signals for the
40° masker). This result
suggests that a near-reciprocal relationship between masker and signal
level holds only for a limited set of conditions.
A facilitative effect of the masker like that found in the present
study was not formally reported in studies by Phillip's or Brugge's
groups, who studied units in area A1. Thus it is possible that
masker-induced facilitation was a phenomenon that is true for units in
area A2 but not in area A1. An example of RLFs by Phillips and
Hall (1986, Fig. 2b), however, did demonstrate increased maximum spike rate accompanied by elevated response thresholds in the
presence of masker, as often found in the facilitation cases in the
present study (cf. Figs. 5 and 12). Thus it is possible that previous
studies have overlooked a population of A1 neurons that show
facilitation by background noise. Clearly, more extensive studies are
required to understand masker-induced facilitation across the cortex.
Significance of multi-unit cluster recording
We used multi-channel recording probes that permitted us to record from as many as 16 cortical sites simultaneously. That made it possible to test a sizeable sample of units with a large number of signal and masker conditions. The disadvantage of the multi-channel probe was that it generally did not permit reliable isolation of single units. It is a concern that the multi-unit clusters that were studied might have contained neurons that differed from each other in their detailed response properties. Any averaging of differing response characteristics that resulted from multi-unit cluster recording would have blunted differences among various unit types. That is, we might have failed to detect rare response types that could only be seen by recording from individual neurons. Moreover, the two response types that we defined, types A and B, might have demonstrated quantitatively greater differences if single units had been isolated. Perhaps finer differences among neurons will be discovered in later studies. Nevertheless the major conclusions in the present study about effects of signal and masker locations on the responses of unit populations are based on data averaged over multiple recording sites and are unlikely to reflect an artifact of multi-unit cluster recording.
One serious concern about the interpretation of multi-unit cluster recordings is that it is not possible to guarantee that a cluster studied over 2-5 h contained the same units. For that reason, one must be concerned that apparent masker-related changes in responses might be confounded by changes in the recorded population. We guarded against this in two ways. First, we tested the various masker conditions in blocks that differed in order among animals and probe placements. That prevented the association of particular masker condition with the beginning, middle, or end of study at each recording site. Second, we repeated measures of sensitivity to azimuth and signal level in the quiet condition in two to four repeated blocks of trials distributed among the blocks of masker trials. As detailed in METHODS, any systematic change in the sensitivity of units at a particular recording site to azimuth or signal level led to rejection of data from that site. It is possible that data were included in cases in which the members of a unit cluster changed during a lengthy recording session. If so, however, units that left the cluster were replaced by units with similar responsiveness and similar azimuth and level specificity.
Underlying mechanisms for the masker effects
Ramachandran and colleagues (2000) reported the
effects of continuous background noise on neurons in the cat inferior
colliculus (IC) that generally paralleled the effects on cortical
neurons: the dynamic range of the RLF shifted to higher signal SPLs,
and 1-dB increases in noise level tended to result in near 1-dB
increases in the shift size. Thus it is possible that the reduced
signal sensitivity of cortical neurons due to continuous background
noise can be attributed in part to the reduced excitatory inputs from brain stem pathways. In the IC, however, the presence of a background noise generally resulted in the compression of the dynamic range of
spike rate due to elevated background spike rate and reduced maximum
signal-driven spike rate for neurons with monotonic RLFs (Ramachandran et al. 2000
). Such a compression effect
was not observed in the cortex. Cortical neurons do not respond to a
continuous background noise in a sustained fashion (Brugge et
al. 1998
; Phillips and Hall 1986
; present
results), and generally there is no indication of reduced maximum
signal-driven spike rate (Phillips and Hall 1986
). In
certain conditions, the maximum rate even was increased by the presence
of the masker, as found for the type B units in the present study.
Short-term adaptation in cortical neurons might play a role in the
reduction of the masker-driven background spike rate (Volkov and
Galazyuk 1992
). The maintenance or facilitation of the maximum
spike rate might be explained in terms of the balance of excitatory and
inhibitory inputs from ascending pathways that converge on single
cortical neurons. The maximum spike rate could be maintained in the
presence of masker if a reduction of excitatory inputs is accompanied
by reduced inhibitory inputs. Similarly facilitation would occur if the
attenuation of inhibitory inputs exceeds that of excitatory inputs.
A major finding of the present study was the dependence of RLF and LLF
shifts on the locations of signal and masker in the free field.
Previous studies have demonstrated both binaural and monaural processes
that might contribute to the masker effects. As an example of a
binaural process, Jiang and colleagues (1997) found a
population of neurons in the guinea pig IC that showed differential
sensitivities between in-phase and anti-phase signals between the ears
in the presence of anti-phase noise masker. Also, Ramachandran
and colleagues (2000)
studied the effects of interaural level
difference of signal and masker in the cat IC neurons. The sensitivity
of their type I units to a signal with contralaterally dominant
interaural level difference (ILD) (i.e., level in the contralateral ear higher than in the ipsilateral ear) was greater when
presented against a masker with ipsilaterally dominant ILD than when
presented against a masker with contralaterally dominant ILD. Thus it
is possible that the binaural processes found in those IC studies
contribute to cortical sensitivity to relative locations of signal and
masker. We also note a demonstration in an amphibian IC of neurons that
showed effects of signal and masker locations equivalent to spatial
unmasking, i.e., decreased response thresholds for signals by
increasing spatial separation of a masker from the signal
(Ratnam and Feng 1998
).
Regarding monaural processes, the responses of individual cortical
neurons are influenced by location-dependent spectral details of the
acoustical inputs to each eardrum (Samson et al. 1993; Xu et al. 1999
). The transfer function of each external
ear varies with the angle of incidence of sound, so the spectral
envelope of a sound at each eardrum varies with the sound-source
location (Musicant et al. 1990
; Rice et al.
1992
; Xu and Middlebrooks 2000
). For that
reason, the frequency-by-frequency SNR is determined by an interaction
of the signal and masker locations. A single neuron's responses could
be determined by a further interaction of the frequency-dependent SNR
and the neuron's frequency sensitivity. Thus the across-neuron and
-subject variances of the masker-signal interaction in masker effect
may be partly accounted for by the fact that frequency sensitivities
varied somewhat across neurons and that the directional transfer
functions varied among cats (Xu and Middlebrooks 2000
).
Relationship to psychophysical spatial unmasking
Saberi and colleagues (1991) demonstrated spatial
unmasking in human listeners, using stimulus configurations comparable
to the present study. That study showed the highest detection threshold for signals around the masker location and decreasing threshold for
increasing separation of signal and masker. The present results in
cortical physiology (Fig. 7) mirrored the results by Saberi et al.: the
RLF and LLF shifts tended to be largest when the signal location
coincided with the masker location and became smaller for increasing
separation between the signal and the masker. This effect can be seen
clearly for the lateral maskers and to a lesser degree for the 0°
masker. The present findings differed in two ways from those of the
Saberi study. First, we found smaller overall spatial-unmasking effects
than in the previous study. For example, the RLF shifts and LLF shifts
in the present study were no more than 10 and 14 dB, respectively, for
the
80° masker, whereas Saberi and colleagues observed threshold
shifts as large as 17 dB for a 90° masker (Fig. 4 of Saberi et
al. 1991
). Second, compared with the lateral maskers, the 0°
masker showed only a small spatial unmasking, only ~5 dB. The Saberi
study, on the other hand, demonstrated threshold shifts of as much as
15 dB for the 0° masker. The generally smaller modulation size in the
present study was partly due to our procedure for computation of RLF
and LLF shifts, which forces shifts to take a limited range (
10-+30
dB), resulting in compressed profiles of average shifts. The relatively
small modulation size for the 0° masker in the present study might be
accounted for by the insensitivity of A2 neurons to low frequencies.
Unlike neurons in cat A2, human listeners integrate information across a broad range of frequencies. For human listeners, the magnitude of
spatial-unmasking effect is greater for frontal maskers than for
lateral maskers when the signal is restricted to low frequencies (<1
kHz); but the reverse is true when the signal is restricted to mid
(1-5 kHz) or high (>5 kHz) frequencies (Good et al.
1997
). Quantitative differences between the two studies might
also reflect spatial attention effects that could have been present in
the human listeners but not in the anesthetized cats.
Listeners can improve signal detection by attending to the ear at which
the SNR is greater. This "better-ear" listening is a process that
accounts at least partly for spatial unmasking (Bronkhorst and
Plomp 1988, 1989
, 1992
; Kidd et al. 1998
;
Terhune and Turnbull 1989
). In the presence of a lateral
focal masker, the noise level is greater in the ear ipsilateral to the
masker than in the contralateral ear, because of shadowing by the head. Separating the signal from the masker location would increase the SNR
in the ear contralateral to the masker, and thus attention to that ear
would improve detection. Although the better-ear listening is feasible
for psychophysical listeners, who in principle could base their
judgements on populations of neurons in both cortical hemispheres, such
a strategy could not account entirely for the signal-masker interaction
found in the present study. This is because the two ears have
asymmetrical influences on each cortical hemisphere. Most neurons in
area A2 are excited by stimulation of the contralateral ear, but a
smaller proportion of neurons (~40%) are excited by ipsilateral
stimulation (Schreiner and Cynader 1984
). Thus according
to the better-ear listening hypothesis, we would expect weaker
unmasking of ipsilateral signals (smaller modulation of
shift-vs.-signal-location function) with a contralateral (
80 and
40°) masker than of contralateral signals with an ipsilateral (+40
and +80°) masker. The results in Fig. 7 conflict with this expectation. Furthermore the noise levels in the two ears were nearly
equal for the 0° masker condition, so the hypothesis of better-ear
listening would predict no spatial unmasking by separation of signal
and masker. In fact, the 0° masker condition in Fig. 7 showed a
slight dependence of RLF and LLF shifts on signal location, the
greatest shift being found for signals near 0°. Therefore other
mechanisms are needed to explain the signal-masker interaction found in
the present study.
Implications for sound localization
The results of the present study and of the study by Brugge
and colleagues (1996) suggest that the masker effects on spike rates and first-spike latencies are in many cases equivalent to the
effects of a reduction in signal level. This implies that the
perturbation by maskers of the neural coding of sound location would be
equivalent to the perturbation by varying signal level. It is known
that cortical neurons can signal location-related information by their
spike patterns and that this signaling is robust to variation in
stimulus levels (Brugge et al. 1996
; Middlebrooks et al. 1998
). Therefore we predicted that location signaling by cortical neurons would also be fairly robust to the presence of masker.
In the present study, location estimates by an ANN trained with spike
patterns recorded in the absence of a masker were severely disrupted
when presented with spike patterns in the presence of a masker. That
disruption, however, was reduced significantly under conditions in
which the effective levels of signals remained within the operating
range of the ANN. This result was comparable to the psychophysical
result that a continuous masker has relatively little impact on the
accuracy of localization judgement by human listeners at least when the
signal level is above a modest (~10 dB) sensation level (Good
et al. 1996
, 1997
; Lorenzi et al. 1999
). Nevertheless considerable errors in ANN location estimates under masker
condition remained even after adjustment by the effective signal level
(see, for example, the panel for the 0° masker in Fig. 10). This
indicates that some features of spike patterns are sensitive to signal
locations in quiet (thus captured by the ANN as information-bearing
features) but are disrupted by the presence of a masker. Further
studies will be necessary to identify information-bearing features in
spike patterns that are robust to perturbations by maskers.
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ACKNOWLEDGMENTS |
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We thank Z. Onsan and C. Ellinger for technical assistance. B. Mickey, E. Macpherson, and D. Wu helped to collect experimental data. B. Mickey, E. Macpherson, and two anonymous reviewers gave constructive comments on earlier versions of the manuscript.
This work was supported by National Institutes of Health (NIH) Grants PO1-DC-00078 and R01-DC-00420. Multi-channel recording probes were graciously provided by the University of Michigan Center for Neural Communication Technology, which is supported by NIH Grant P41-RR-09754.
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FOOTNOTES |
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Address for reprint requests: J. C. Middlebrooks, Kresge Hearing Research Institute, University of Michigan, 1301 E. Ann St., Ann Arbor, MI 48109-0506 (E-mail: jmidd{at}umich.edu).
Received 16 October 2000; accepted in final form 2 April 2001.
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REFERENCES |
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