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The Journal of Neuroscience, September 3, 2003, 23(22):8143-8151
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GABA Is Involved in Spatial Unmasking in the Frog Auditory Midbrain
Wen-Yu Lin andAlbert S. Feng Department of Molecular and Integrative Physiology and Beckman Institute, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801
Abstract
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Abstract
Introduction
Real-world listening situations comprise multiple auditory objects. Sounds originating from different objects are summated at the eardrum. The auditory system therefore must segregate the streams of sounds associated with the different objects. One listening strategy in complex environments is to attend to signals originating from one spatial location. In doing so, signal detection is compromised when a masker is present at close proximity, and detection is improved if the masker is spatially separated from the signal. A recent study has shown that, in frogs, spatial unmasking is more robust at the midbrain than at the periphery, indicating the importance of central mechanisms for this process. In this study, we investigated spatial unmasking patterns of single neurons in the frog inferior colliculus (IC) before and during iontophoretic application of bicuculline, a GABAA receptor antagonist. We found that drug application markedly decreased the strength of spatial unmasking such that even large angular separation of signal and masker sources produced only a weak masking release. Under the drug, the strength of spatial unmasking of midbrain neurons approximated that of auditory nerve fibers. These data show that GABAergic interactions in the auditory midbrain play an important role in spatial unmasking. Analysis of the effect of the drug on the direction sensitivity of the units shows that for the majority of IC units, bicuculline degrades binaural processing involved in directional coding, thereby compromising spatial unmasking. For other IC units, however, the decline in the strength of spatial unmasking is attributable to the effects of bicuculline on different central auditory processes.
Key words: inferior colliculus; torus semicircularis; stream segregation; release from masking; spatial unmasking; bicuculline; hearing; masking; signal detection
Introduction
Frogs communicate by sound in acoustically cluttered environments. Male frogs emit advertisement calls to attract females around a breeding pond that is often shared with numerous con-specific as well as sympatric males. It is generally up to the females to localize and discriminate the calls of conspecific males from calls of sympatric males to avoid interspecies breeding (Gerhardt, 1988). Despite the complexity in the calling environments, females show a high degree of success in call identification and localization. Within a chorus, conspecific males interact extensively such that their calls are conspicuous to the females (Wells, 1988
The goal of this study was to advance our understanding of the central mechanisms responsible for spatial unmasking. Lin and Feng (2001
The frog IC receives bilateral projections from the cochlear and superior olivary nuclei in the caudal brainstem (Feng and Lin, 1991
Gooler et al., 1996
Materials and Methods
The general experimental methods were as described in an earlier paper (Lin and Feng, 2001Acoustic stimuli comprised tone bursts (duration, 200 msec; rise-fall time, 5 msec), broadband noise bursts [used as the masker (M)], and a prerecorded species mating trill [used as the probe (P)]. Tone bursts were used to acquire the general response properties of a unit. The waveforms and power spectral densities of the probe and the masker, as well as the power spectrum of the probe in the masker (P + M) are shown in Figure 1. The mating trill (Fig. 1 D) was selected as the probe because it is the predominant call type in frog choruses; it has a duration of 900 msec with energy concentrated over 150, 500, 700, 1000, and 1700 Hz (Fig. 1 A). Because of limitations of the data analysis software, we used only the first half of the trill as the probe (i.e., 450 msec); the two halves of the mating trill had the same trill rate, and they differed only in the envelope of the call. The masker (Fig. 1 E) was a broadband noise with a flat power spectrum over the frog's audible range of 100-3000 Hz (Fig. 1 B). The probe and masker were both digitized such that when they were presented through the digital-to-analog (D/A) converters (see below), they had a consistent temporal relationship. Frozen noise bursts were preferred over free-running noise bursts; the latter are undesirable because they have transient fluxes of energy in different frequency bands that vary from one trial to the next and thus can themselves elicit a change in the response of a unit. The duration of the masker was 450 msec, matching that of the probe; thus, P and M overlapped in time completely. Although temporally overlapped, the response of a unit to broadband noise was generally random and thus could be distinguished from the response of a unit to the probe that typically showed time-locked firing patterns (Fig. 2). Time-locked firing was therefore a potential metric for estimation of probe detection (see below).
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Figure 1. Mating trills of Rana pipiens (or the probe) and the masker used in this study. A, Power spectrum of the probe at 63 dB SPL. B, Power spectrum of masker at 69 dB SPL. C, Power spectrum of probe and masker at respective levels, i.e., at a signal-to-noise ratio of -6 dB. D, Waveform of the probe in its digitized form. E, Waveform of the masker in its digitized form.
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Figure 2. Rate level functions (left plots), d' functions (middle plots), and composite dot histograms (right plots) of an IC unit to P alone (A) and P + M (B). In the left plots, the response of the unit at each sound level is shown by the average spike count ± SD to 10 stimulus (Stim.) epochs. In the middle plots, the y-axis represents d' (for calculation, see Materials and Methods), and the open arrows indicate the probe detection thresholds to P alone (18.3 dB SPL) and P + M (21.2 dB SPL), namely, the sound levels at which d' = 1; the corresponding levels are shown by solid arrows in the left plots and by open arrowheads in the right plots. The composite dot histograms in the right plots show the timing of trains of action potentials (each spike is represented by a single dot) at various sound levels. Time 0 represents the onset time of the acoustic stimuli. In these plots, 10 traces of spike trains are shown at each sound level.
The stimulus parameters were controlled by Tucker Davis System 2 hardware and software from a personal computer. To present the prerecorded natural call and noise bursts, each digital file that was stored on the computer hard drive was retrieved and passed through a D/A converter (sampling frequency, 12 kHz), a programmable attenuator, an audio amplifier, and a loudspeaker.
P and M were broadcast through two separate loudspeakers (ADS 200 LC) mounted on two separate hoops at 0° elevation. These hoops could be rotated independently over a 180° range in the frontal field using two separate mechanical systems (Lin and Feng, 2001
Extracellular recordings were made from single neurons in the left IC using a single-barrel glass pipette (tip diameter, 1 µm; filled with 0.2 M potassium acetate in 0.05 M Tris buffer) attached to a five-barrel glass pipette (tip diameter,
10 µm). Two of the five barrels were filled with bicuculline methiodide (BIC, 10 mM, pH 3.0; Sigma, St. Louis, MO), a GABAA receptor blocker. The central barrel was filled with 0.64% sodium chloride, pH 7.4, for maintaining electrical balance. The electrode assembly was attached to a piezoelectric microdrive and positioned stereotactically onto the dorsal surface of the optic tectum above the IC. The five-barrel pipette was connected to a six-channel iontophoresis current generator (Dagan 6400). A retaining current of -15 nA was used to prevent drug leakage at all times except during drug injection. Action potentials as picked up by the single-barrel glass pipette were amplified 10,000x by a preamplifier (Dagan 2400), filtered (passband of 100-6000 Hz), monitored audiovisually, and processed using Tucker Davis data acquisition software. The time of occurrence of action potentials was recorded using Brain-Ware, along with the waveform of action potentials. Times of spikes were registered by the software and used to construct the dot histogram off-line (Fig. 2, left plots). In the rare cases in which the electrode isolated more than one unit, responses from the individual units could be segregated on the basis of differential action potential waveforms. The recorded spike waveform was also used for identification of units during the long recording session (1.5-3 hr).
To search for auditory neurons, a series of five sequential tone bursts with five different carrier frequencies were presented at 90 dB sound pressure level (SPL) from the right 90° [corresponding to contralateral 90° (c90°)]; this represents the best azimuth for most units in the left IC (Gooler et al., 1996
After a unit was isolated, its frequency-threshold curve and best frequency were determined audiovisually using tone bursts as stimuli. Afterward, we determined the rate level function (RLF) of the unit to P alone at a fixed azimuth of c90°. We next determined the responses of the unit to M alone at a constant level (at 6 dB above the response threshold of the unit to the best frequency at c90°) at various azimuths. The masker loudspeaker was initially positioned at c90° and later moved in random order to c45°,0°, ipsilateral 45° (i45°), and i90°. The response to M alone served as a reference for the response of unit to P + M. With the masker at different azimuths, we collected a series of RLFs to P + M by changing the probe level systematically from subthreshold to suprathreshold levels in 1-2 dB increments; these RLFs will be referred to as masked RLFs (MRLFs).
For each cell, we collected the responses of the unit to 10 epochs of a stimulus and calculated the average spike count and SD of it. The detection thresholds for P alone and for P + M, were estimated from the RLFs and MRLFs of the unit, respectively, using d' analysis from the signal detection theory, taking the firing variance into account (Sakitt, 1973
where RP + M and RM are the mean responses to P + M and M alone, and SDP + M and SDM are the SDs of the respective responses. The detection threshold for P + M at a specific azimuth was defined as the lowest probe level at which d' = 1, with the condition that d' at the next level was greater than at the threshold (Fig. 2). As shown in the composite raster dot histograms (Fig. 2, right plots), units fired more vigorously at the threshold level than at subthreshold levels, as expected, with evidence of time-locked discharges to the amplitude modulations in the probe at suprathreshold levels. Note that for P alone, there was no masker in the stimulus; thus, for calculation of d', we used the spontaneous firing of the unit as RM and the response of the unit to P alone as RP + M.
Because the experimental protocol was very long, to ensure timely completion of the experimental protocol, instead of measuring RM directly, we used RP + M at very low probe levels (subthreshold) to estimate this value. A similar procedure was used in previous binaural masking level difference (BMLD) studies (Jiang et al., 1997
In addition to rate-based d' analysis, we also measured the synchronization coefficients from responses to P alone, P + M, and M alone, taking advantage of the differences in the firing synchrony to the signal envelope (Fig. 2). We found that the time-locking data could be used as a second metric for assessing the detection thresholds of a unit for >60% of IC neurons. For the rest of IC neurons, however, their response to even P alone showed little or no statistically significant time locking, yet probe detection was easily determined using rate-based d' analysis. Also, for the first population of IC neurons, the cutoff points for the synchronization coefficient (wherein the coefficient was significantly different from the background value) were variable, without a single standard that could be used for all neurons. In light of these findings, we used rate-based d' analysis exclusively for determining probe detection.
Masking by noise originating from the same azimuth typically elevated the probe detection threshold of the unit (Ratnam and Feng, 1998
To test the working hypothesis, we compared the strengths of spatial unmasking for IC neurons before (i.e., control condition) and during (i.e., experimental condition) drug application. Drug application was performed by applying a positive current of 10-30 nA. During continuous drug application, the response of a unit to P alone was studied at a fixed sound level to observe the progressive increase in response with time. When the drug-induced increase in the firing rate of a unit had saturated, usually after bicuculline had been injected for 15-20 min, we began collection of experimental data by studying the RLF of the unit to P alone and the MRLFs of the unit to P + M at various masker azimuths. After the experimental protocol was completed, bicuculline application was withdrawn. Then, after a waiting period of
A previous study in the frog IC (Zhang et al., 1999
Results
Complete spatial unmasking data were obtained from 28 IC neurons (and partial data were obtained from 59 IC neurons) under the control and experimental conditions, i.e., before and during drug application. As reported previously (Ratnam and Feng, 1998The spatial unmasking response characteristics of a representative IC unit are shown in Figure 3. This unit showed no spontaneous firing during the predrug control period, and the probe was detected at 23.6 dB SPL at which d'= 1 (Fig. 3A, open arrow, G, diamond). The response of the unit to P + M is shown by the MRLF (Fig. 3B, solid line). The MRLF was shifted upward (and also slightly rightward) from the RLF of the unit because of higher background firing, as shown by the response of the unit to M alone (Fig. 3B, open triangle). This shift elevated the probe detection threshold of the unit by 3.5 dB (shift is shown as X in Fig. 3G). A change in the masker azimuth to c45° lowered the response of the unit to M alone (Fig. 3C, open triangle) and produced a downward and leftward shift in the MRLF, thereby lowering the probe detection threshold (Fig. 3C, solid arrow). Further spatial separation of probe and masker sources produced only a slight change in the probe detection threshold (Fig. 3G). The maximum masking release of 5.1 dB (Fig. 3G, Y) was obtained with the masker located at i90°.
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Figure 3. Spatial unmasking response patterns of unit 28-2 (best frequency, 700 Hz). A, RLF of the unit to P alone at c90° (this RLF is also shown in B-F as a dotted curve); the open arrow indicates the probe detection threshold to this stimulus as determined by d' of 1. B-F, MRLFs to P + M (solid curve) at various masker azimuths; for each plot, the filled arrow indicates the probe detection threshold for P + M (i.e., the sound level for which d'= 1). G, Change in the probe detection threshold as a result of masking and spatial unmasking (through angular separation of P and M sources) during the control period before drug application; the diamond represents the probe detection threshold for P alone; X, amount of threshold elevation attributable to masking; Y, maximum masking release attributable to source separation. H-N, Response characteristics of the unit during the period when bicuculline was applied iontophoretically (15 nA). O, Spatial unmasking response pattern of the unit 40 min after withdrawal of bicuculline.
Drug application increased the probe responses across a wide range of sound levels (Fig. 3, compare A, H). For this unit, the increase in firing rate lowered the probe detection threshold to 19.2 dB SPL (Fig. 3N, diamond). Under bicuculline, the response of the unit to M alone at c90° (Fig. 3I, open triangle) was also more robust (Fig. 3, compare B, I), thereby elevating its MRLF (Fig. 3I, solid curve). As a result, the probe detection threshold was raised to 23.5 dB SPL (Fig. 3N, X). Unlike the control condition, however, this threshold increase was only partially rescued by spatial separation of probe and masker sources (Fig. 3N). Moving the masker to c45, 0, i45, and i90° lowered the probe detection threshold, but only slightly (Fig. 3J-M). The maximum masking release, obtained with the masker at i90°, was a mere 2.1 dB (Fig. 3N), which was 3 dB less than the control condition.
Forty minutes after withdrawal of the drug, the probe responses returned to the levels observed during the predrug period, and the responses to P + M at various masker azimuths also closely approximated those shown during the initial control period. Thus, the spatial unmasking pattern of the unit (Fig. 3O) resembled the pattern shown during the control period (Fig. 3G). Specifically, an angular separation of 45° released the masking effect completely.
Figure 4 shows the spatial unmasking patterns of four other IC units during the control and experimental periods. Unit 27-1 (Fig. 4A) showed a graded spatial unmasking pattern during the control period (top plot). The probe detection threshold was elevated by 7.5 dB because of masking at c90° (top plot, X). Spatial separation of P and M sources conferred a progressive increase in masking release that was maximal (5.8 dB) at a masker azimuth of i45° (top plot, Y). Under bicuculline, the masker at c90° produced a threshold shift of 10.3 dB (bottom plot, X); this was slightly greater than during the control period, but spatial unmasking was noticeably weaker, with a maximum masking release of 2.3 dB only (bottom plot, Y).
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Figure 4. Spatial unmasking response patterns of four representative IC neurons. See legend to Figure 3 for the different symbols. A, B, Data from two units with graded spatial unmasking patterns under the control (i.e., predrug) and experimental (i.e., when BIC was applied iontophoretically) conditions. C, D, Responses of two units with J-type spatial unmasking patterns under the control condition.
Similarly, for unit 30-2 (Fig. 4B), the masker at c90° respectively elevated the probe detection threshold by 11.7 and 14.1 dB during the control and experimental periods (top, bottom plots, X). The strengths of spatial unmasking in both periods were once again different. The maximum masking release values were 11.3 dB during the control period and only 3.8 dB during the experimental period.
Units 18-1 and 19-1 showed J-type spatial unmasking patterns during the control period (Fig. 4C,D). For these units, angular separation of 45-90° rescued much of the masking effect, with additional spatial separations having little or no further masking release. Drug application weakened the masking release (bottom plots, smaller Y), even though the elevation in threshold attributable to masking was smaller than that of the control period.
The spatial masking and unmasking data from the entire sample (n = 28) is summarized in Figures 5 and 6. Masking-induced threshold shifts varied greatly among IC units, irrespective of the best frequency of the unit, during both the control and experimental periods. During the control period, the threshold shift ranged from 1 to 20.9 dB, with a mean ± SD of 8.38 ± 4.95 dB (Fig. 5A; these data are in agreement with the results of Lin and Feng, 2001
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Figure 5. Distributions of threshold shift attributable to masking and the maximum masking release attributable to spatial separation for 28 IC units studied under two different experimental conditions. The mean ± SD of each data set are shown above each graph. The results of two-tailed Student's t tests between the same data set from two different experimental conditions are shown in B and D. N.S., Not statistically significant. **Statistically significant difference.
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Figure 6. Amount of threshold shift (A) and maximum masking release (B) for each of the 28 IC units under the normal (left side) and experimental (right side) conditions. Open circles in B represent the data from five IC units that were minimally affected by drug application.
Drug application consistently reduced the strength of masking release (Fig. 6B). As shown in Figure 5, C and D, the maximum masking release during the control period ranged from 3.1 to 14.6 dB, with a mean of 8.57 ± 3.19 dB (this agrees well with the result of Lin and Feng, 2001
Additionally, for units with J-type spatial unmasking patterns (n = 14; Fig. 4C,D), the angular separations required for achieving 75% of the maximum masking release were on average 77° during the control period and 135° during the experimental period. These two means were significantly different (p < 0.0003). However, for the remaining IC units with graded and complex spatial unmasking patterns, the angular separations required for achieving 75% of the maximum masking release during the control (i.e., 140°) and experimental (i.e., 122°) periods were not significantly different (p > 0.1).
For five IC units (Fig. 6B, open circles), application of bicuculline had very small effects over the strength of spatial unmasking; spatial unmasking remained robust under the experimental condition, and the maximum masking release was reduced by <1.5 dB. These neurons presumably have inherited their spatial unmasking properties from lower brainstem neurons and auditory nerve fibers.
To gain further insight into the particular GABAergic processing that was responsible for spatial unmasking, we determined the extent to which the sensitivity of a unit to sound direction contributed to spatial unmasking. For this, we plotted the directional responses of IC units to M alone under the control and experimental conditions. We found that, although bicuculline consistently increased the auditory response of a unit to M alone, its influence over the directional sensitivity of a unit was variable. Figure 7A shows a representative effect of bicuculline on the directional response of a unit. This unit showed a sigmoidal directional response pattern, responding maximally to M alone from c90°, and its response decreased progressively when the masker azimuth was changed toward i90°. Bicuculline elevated the responses of the unit at all azimuths, leaving its directional response pattern unchanged; i.e., it remained sigmoidal. However, for this neuron, application of bicuculline reduced its directional sensitivity (Fig. 7B); the directional sensitivity of the unit was represented by the change in the normalized response between c90 and i90° (see Materials and Methods).
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Figure 7. Directional responses of two IC units to M alone at a suprathreshold level during the control (open circle) and experimental (filled circle) conditions. A, B, Directional responses from a unit whose directional sensitivity was reduced by application of BIC, using the absolute spike count and normalized response (with regard to the maximum spike count for the respective response curve) as a metric. C, D, Similar data from a unit whose directional sensitivity was increased by application of BIC.
Results from all 28 IC units showed that, during the control period, the percent change in firing rate with an 180° change in azimuth was on average 90.5%. Under bicuculline, the average percent change was only 68.5%. These averages were significantly different (p < 0.0004).
The above population data indicated that a reduction in the strength of spatial unmasking resulting from drug application was likely attributed to a reduction in the directional sensitivity of a unit. Analysis of individual data (Fig. 8), however, showed that such a correlation was applicable to only a population of IC units. Specifically, for 15 of the 28 units studied (bottom plot bounded by dashed, dotted oval), bicuculline gave rise to a wide range of reduction in directionality (range, 10-90%). For these, a large reduction in the directionality is accompanied by a marked weakening of spatial unmasking. For 10 cells (bounded by dotted oval), however, bicuculline produced only a small change (<20%) in directionality, yet most of these cells showed a noticeable reduction in the strength of spatial unmasking. For two IC neurons (Fig. 8, top half), bicuculline actually increased the directionally sensitivity of the unit, i.e., by 28 and 67%, respectively. As shown for one of these cells (Fig. 7C), the increase in directional sensitivity was attributable to a pronounced increase in the response of the unit at c45-c90° and a decrease in response at i45-i90°. Despite the increase in directional sensitivity, the strength of spatial unmasking for these two neurons was either unchanged or totally abolished.
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Figure 8. Effects of drug application on the directional sensitivity and spatial unmasking of IC units. Directional sensitivity was measured by the total percent change in normalized directional responses between c90 and i90° (see Fig. 7). The x-axis shows the difference in the maximum masking release (see Figs. 3, 4, Y) between the control and experimental conditions, with negative values indicating a decrease in masking release resulting from drug application. The y-axis shows the difference in the percent change in the directional sensitivity of the unit between the control and experimental conditions; negative and positive values indicate, respectively, a decrease and increase in directional sensitivity resulting from drug application.
Discussion
The present study shows that application of bicuculline significantly reduces the strength of spatial unmasking in the IC such that even a large angular separation of probe and masker sources produces only a weak masking release. Under bicuculline, the spatial unmasking patterns of IC neurons are mostly flat or slowly graded, and the maximum masking release occurs primarily with a large spatial separation of 135-180°, similar to the patterns observed at the auditory periphery (Lin and Feng, 2001Whereas bicuculline weakens spatial unmasking of IC units, angular separation still produces some masking release. The weak masking release that remains is likely attributed to acoustic shadowing of the head, as observed in the auditory periphery (Lin and Feng, 2001
For five IC neurons, the drug-induced change in the strength of spatial unmasking was small, i.e.,
1.5 dB (Fig. 6B, open circle). For these units, central processing occurring at lower brainstem nuclei and the auditory nerve are likely responsible for spatial unmasking.
Previous studies have shown that GABA plays many different roles in auditory processing in the IC, monaural and binaural (Faingold et al., 1991
In humans, psychophysical studies are based mostly on dichotic experiments and use the BMLD paradigm. A dominant model for explaining the BMLD results is a running cross-correlation model of binaural interaction that includes a network of coincidence detectors used for processing the interaural time difference cue (Colburn, 1996
For frogs, neurons in the superior olivary nucleus and the auditory midbrain show poor phase-locking ability (Condon et al., 1995
We note, however, that there are exceptions to the general trend described above. For one-third of IC units, bicuculline has a small to moderate effect on the directional sensitivity of the units, yet their strength of spatial unmasking is markedly compromised (Fig. 8). The strongest counterexample is from one IC unit that becomes directionally more sensitive under the experimental condition (Fig. 7C,D), but its strength of spatial unmasking is essentially completely abolished. Clearly, for these IC units, different GABAergic-based processing is responsible for the observed weakening of spatial unmasking.
In crickets and katydids, the
neurons in the nerve cord have been shown to be responsible for spatial unmasking (Pollack, 1988
It is possible that a similar attention-based mechanism operates in the frog CNS and that such selective response to the mating trill of the species is independent of binaural processing but dependent on GABAergic interactions nonetheless. We speculate that although bicuculline increases IC unit responses to acoustic stimuli in general, it may abolish the response selectivity of the unit to the mating trill of the species, at least for a subset of IC units. There are two indirect lines of evidence that support this tenet. First, Klug et al. (2002
At present, the actual binaural inhibitory circuitry responsible for spatial unmasking in the frog IC is unclear. It is unknown whether the circuit involves ascending, descending, or commissural afferents or local interactions. As mentioned earlier, many neurons in the frog caudal brainstem nuclei exhibit binaural facilitation and binaural inhibition (Feng and Capranica, 1976
For this study, the probe was stationed at c90°, which represents the best azimuth for most IC neurons, but frogs likely can tune to listen to sound from various directions during their acoustic interactions, from the lateral as well as frontal sound fields. The benefit of central processing to spatial unmasking for sound located in the frontal field may be different from what is reported in this study and needs to be determined empirically. At this time, it is also unclear whether the strength of spatial unmasking in the IC varies with sound direction. Previously, Ratnam and Feng (1998
Footnotes
Received April 10, 2003; revised June 23, 2003; accepted June 30, 2003.This work was supported by National Institute on Deafness and Other Communication Disorders Grant R01DC-00663 from the National Institutes of Health. We thank Alexander Galazyuk, David Gooler, Mario Penna, and Rama Ratnam for commenting on previous versions of this manuscript.
Correspondence should be addressed to Dr. Wen-Yu Lin, Beckman Institute, University of Illinois, Urbana, IL 61801. E-mail: w-lin5{at}uiuc.edu.
Copyright © 2003 Society for Neuroscience 0270-6474/03/238143-09$15.00/0
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