Free-field binaural unmasking in budgerigars ( Melopsittacus undulatus )

Behavioral Neuroscience Copyright 1997 by the American Psychological Association, Inc. 1997, Vol. l l l , No. 3, 590-598 0735-7044/97/$3.00

Free-Field Binaural Unmasking in Budgerigars (Melopsittacus undulatus)

Micheal L. Dent University of Maryland College Park

Ole N. Larsen Odense University

Robert J. Dooling University of Maryland College Park

The detection of signals in noise is important for understanding both the mechanisms of hearing and how the auditory system functions under more natural conditions. In humans, the auditory system gains some improvement if the signal and noise are separated in space (binaural masking release). Birds with small heads are at a disadvantage in separating noise and signal sources relative to large mammals, because interaural time differences are much smaller. Two binaural phenomena in budgerigars related to the detection of tones in noise were examined. Budgerigars show 8 dB of free-field binaural masking release when signal and noise are presented to their right side and correlated noise is presented to their left side. Budgerigars also show a spatial masking release of 9 dB when a signal and noise are separated in azimuth by 90 ° . These results are similar to those found in humans and other mammals with much larger heads.

The auditory system is constantly faced with the task of detecting biologically important sounds against a background of environmental noise. Masking occurs when the threshold of audibility of one sound is raised by the presence of another (masking) sound. In a few cases, for example, close to running water, this environmental noise is domi- nated by a single, relatively time-invariant, broad-band source. Under free-field conditions, both experimental and anecdotal evidence in humans shows that signal detection and speech intelligibility are improved as the biologically important signal is spatially separated from such a masker (Saberi, Dostal, Sadralodabai, Bull, & Perrott, 1991; Santon, 1986, 1987). For pure-tone signals as well as for trains of clicks, the improvement in detectability can be as large as 15 dB. This spatial release from masking is one of several well-known effects that are characteristic of the binaural auditory system. The well-known "cocktail party effect" is another example in which detection is improved when the binaural phase difference of the signal is made different from the binaural phase difference of the masking noise. A similar effect can be obtained with monaural masked thresholds by adding noise in phase to the contralateral ear (Gulick, Gescheider, & Frisina, 1989). The binaural masking level

Micheal L. Dent and Robert J. Dooling, Department of Psychol- ogy, University of Maryland College Park; Ole N. Larsen, Center for Sound Communication, Institute of Biology, Odense Univer- sity, Odense, Denmark.

This work was supported by the Danish National Research Foundation and National Institutes of Health Grants DC-00198 and MH-00982. Special thanks to Catherine Carr, Satoshi Amagai, Kevin O'Grady, and Kathy Nepote for assistance.

Correspondence concerning this article should be addressed to Robert J. Dooling, Department of Psychology, University of Maryland, College Park, Maryland 20742. Electronic mail may be sent via Internet to [email protected].

difference (BMLD) refers to the general condition in which signals masked by a noise at one ear become unmasked (i.e., threshold improves) by sounds reaching the other ear (for a discussion, see Yost, 1988).

One of the interesting aspects of the BMLD is that the physiological processes producing masking release in mammals are not well understood. It is likely that the mechanisms involved are related to the coding of interaural time differences (ITD) in the lower levels of the auditory system as those proposed for sound localization (Jeffress, Blodgett, & Deatherage, 1962). In mammals, for instance, delay sensitivity of low-frequency neurons is established by a coincidence mechanism at the level of the medial superior olive (Yin & C h a n , 1990). In humans, perceived lateral position is not greatly influenced by interaural phase or interaural time differences for frequencies above 1200 Hz (Yost, 1981)--about the frequency where phase coding begins to break down. Cells sensitive to ITDs have been found in the inferior colliculus of mammals, where they act as binaural correlators (Caird, Palmer, & Rees, 1991). Studies on the precedence effect in cats show that inferior colliculus cells will discharge at the perceived, not actual, location of a sound source (Yin, 1994). Many comparative studies, especially on mammals, show that animals with large heads such as cattle, horses, and goats potentially generate more prominent directional cues than those with small heads but do not always have smaller localization thresholds (H. E. Heffner & R. S. Heffner, 1984; R. S. Heffner & H. E. Heffner, 1983, 1986, 1992).

In barn owls, the nucleus laminaris (NL) has been shown to be the first site of binaural timing computations (Sullivan & Konishi, 1984; Takahashi, Moiseff, & Konishi, 1984). This timing information (for frequencies up to 8 kHz) is preserved throughout the brainstem and up to the midbrain auditory area (Konishi, 1993; Moiseff & Konishi, 1983).

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BINAURAL UNMASKING IN BUDGERIGARS 591

Recent evidence from single-unit recordings in budgerigars to binaural stimulation using a closed sound system shows that these small birds have NL neurons that are sensitive to ITDs (Amagai, Carr, & Dooling, 1996). The absolute localization thresholds of barn owls as measured behaviorally are much smaller than the localization abilities of the budgerigar for noise bursts (about 2 ° vs. 20 °) (Knudsen, Blasdel, & Konishi, 1979; Park & Dooling, 1991). It is not known whether ITD-tuned cells for small birds, apparently unspecialized for sound localization, provide an adequate support for BMLDs.

Since budgerigars (and birds in general) have a fairly narrow range of hearing (Dooling, 1991) and small interaural distances, it is an interesting question as to whether binaural-masking release could occur in birds at any frequency. The existence of binaural-masking release at the frequency ranges typically used in mammalian studies would suggest that small birds are extraordinarily sensitive to ITDs. (Because their ears are so close together, the ITD must be very small.) Or, as Calford and Piddington (1988) suggest, interaural t ime cues may be prominent at certain frequencies due to interactions in the interaural canal.

Binaural-masking release has usually been studied under closed-field conditions with earphones, so there has always been a concern as to whether it is possible to generalize the results to real-world masking situations. For example, there are several reports showing that masking was not always largest when the signal and maskers were coincident (Gate- house, 1987; Santon, 1987).

In this study, we examined binaural-masking release in the budgerigar under free-field conditions. Budgerigars have proven to be excellent subjects for psychoacoustic tests and, consequently, much is known about heating and auditory discrimination in this species in both quiet and in noisy backgrounds (Dooling, 1986; Dooling & Saunders, 1975; Dooling & Searcy, 1979; Okanoya & Dooling, 1987). In contrast to the wealth of comparative free-field data on sound localization (see, for example, Heffner & Heffner, 1986, 1987, 1988), there has been only one recent study of binaural-masking release in an animal (the ferret) under free-field conditions (Hine, Martin, & Moore, 1994). Ferrets showed a significant binaural masking release at 500 Hz, consistent with masking release found in humans (Gate- house, 1987; Saberi et al., 1991; Santon, 1986, 1987).

We address spatial release from masking in budgerigars in two behavioral experiments. First, we measured the effect of masking to the ipsilateral ear when adding correlated noise to the contralateral ear at several different test frequencies. In a second experiment, we measured the effect of spatially separating the signal from the noise masker (at 0 °, frontal direction) on masked thresholds. In this experiment, the tone signal was moved from 0 ° (same location as the noise) to 360 ° in 30 ° intervals.

E x p e r i m e n t 1

The first experiment follows a recent study by Hine et al. (1994) in the ferret. In this experiment, we measured masking under free-field conditions, in which the signal plus

noise is presented from a speaker mounted to one side of the bird 's head (unilateral condition) and when correlated noise is presented from a second speaker mounted on the other side of the bird 's head (bilateral condition). We then compare masking under a binaural condition (both ears unplugged) and under a monaural condition (ear contralateral to the signal plugged). If budgerigars experience masking release, we would predict that presenting correlated noise from both speakers (bilateral condition), but the signal from only one speaker, will result in lower masked thresholds than presenting the noise and signal from only one speaker (unilateral condition). This effect should be reduced or disappear when noise is presented bilaterally but the contralateral ear is plugged (monaural listening condition).

M e t h o d

Subjects. Four adult female budgerigars were used in the experiment. Two of the birds were bred from commercial stock in a vivarium at the University of Maryland, and the other two were caught in the wild in Queensland, Australia, and housed in the same vivarium. The birds were well-trained and had previously partici- pated in a study of absolute and masked thresholds for pure tones, in which they revealed normal hearing capabilities (Farabaugh, Dent, & Dooling, in press). They were kept on a normal light-dark cycle correlated with the season, at approximately 90% of their free-feeding weights.

Apparatus. The apparatus and procedure for testing the birds have been described previously (Okanoya & Dooling, 1987, 1991). The birds were tested in a wire cage (23 X 25 X 16 cm) that was placed in an anechoic chamber (57 X 60 x 78 cm). A response panel consisting of two sensitive microswitches with light-emitting diodes (LEDs) was mounted on the wall of the test cage just above the food hopper. The microswitch was tripped by the bird pecking the LED. The left microswitch and LED served as the observation key, and the fight microswitch and LED served as the report key. The behavior of the animals during test sessions was monitored at all times by a video camera system.

The experiment was controlled by an IBM 486 microcomputer operating Tucker-Davis modules. Sine-wave bursts with a duration of 400 ms and a rise-fall time of 10 ms were stored in digital form and output at a sampling rate of 20 kHz by a digital-analog converter (Tucker-Davis, Type DD1) to a 10 kHz anti-aliasing low-pass filter (Tucker-Davis, Type PF1) and from there to a digital attenuator (Tucker-Davis, Type PA4) and into a power amplifier (Crown, Model D-75). Continuous noise was produced by a noise generator (Tucker-Davis, WG1) and through a graphic equalizer (Rane, Model GE27) was fed into a second attenuator (Tucker-Davis, Type PA4) and finally into the second channel of the power amplifier.

Sound field. Sound stimuli were delivered from two small mid-range tweeters (Realistic soft dome, Type 40-1289A) mounted on the cage walls (30 cm apart) and facing each other in line with the bird's head as it faced the response keys. Stimulus calibration was performed with a precision sound-level meter with octave band filters (General Radio, Type 1982), a V2-in. microphone with a 3-m extension cable, and a fast Fourier transform spectrum analyzer (Stanford Research Systems, Type SR760). Tone and white-noise intensities were measured by placing the microphone in front of the keys in the position normally occupied by the bird's head during testing and pointed upwards (at an angle of 90°). The overall noise level in the test booth was below the lowest level of

592 DENT, LARSEN, AND DOOLING

sensitivity of the sound level meter on the A scale (30 dB sound pressure level, SPL).

The octave band levels of the noise masker at 1.0, 2.0, and 4.0 kHz were 52, 61, and 63 dB SPL, respectively, for the one-speaker condition and 54, 67, and 69 dB SPL for the two-speaker condition. To obtain a measure of the spectrum level of the noise immediately surrounding each test tone frequency, we calculated the spectrum level for the octave band, one-half octave band, and one-third octave band surrounding each test frequency (1.0, 2.0, 2.86, and 4.0 kHz). The spectrum levels were 21.8, 29.5, 30.4, and 29.3 dB SPL, respectively, for the one-speaker condition and 28.3, 35.5, 36.5, and 35.5 dB SPL for the two-speaker condition. The spectrum levels calculated from each bandwidth were similar, except at 1 kHz. The noise-spectrum levels were low at 1.0 kHz because of the roll-off at low frequencies of the mid-range tweeter used in this experiment. These spectrum levels were used to compute the amount of masking at each test frequency. The harmonic distortion measured for the four test tones used in these experiments showed that in all cases the second harmonic was down at least 60 dB from the fundamental and below audibility for the birds.

Training and testing procedures. The training and testing procedures have been described in detail previously by Okanoya and Dooling (1991). Briefly, a microcomputer controlled all experimental events, including stimulus delivery and reinforcement contingencies. The bird was trained by a standard operant auto-shaping program to peck at two microswitch keys for food reinforcement. During the testing phase, a peck on the observation key initiated a random interval of 1-6 s. Following this interval, the next peck on the observation key initiated a trial (defined as an alternation of the target stimulus with the background stimulus). A peck to the right microswitch key (report key) within 2 s following the alternating sounds was considered a hit. A hit was reinforced with a 2-s access to food on a schedule of 80-100%. If the bird failed to respond (miss), a response latency of 2 s was recorded, and a new trial sequence began with the observation interval for the next trial. Approximately 30% of the trials were sham trials in which the target stimulus was the same as the background stimulus. A response on the report key during a sham trial or during the waiting interval was punished with a variable blackout period during which the lights in the chamber were extinguished while the repeating background continued. The blackout time ranged from 5 to 20 s depending on the bird's recent history for false responding.

Once the bird learned the task, testing began by randomly varying tone intensity on successive trials according to the method of constant stimuli. Sessions with a false-alarm rate of 16% or higher were discarded. An average of 10% of all test sessions were discarded for this reason.

The experiment proceeded in several phases. In the first phase, masked thresholds were measured for a pure tone presented from the right speaker in the presence of correlated broadband noise from both the left and right speakers (bilateral-masking condition). Once threshold was roughly determined for each bird, final test sessions were run with the tone presented at seven different intensity levels in 5-dB steps surrounding the animal's threshold, such that only the lowest one or two levels of the tone were clearly below threshold.

In all, masked thresholds were obtained at four frequencies: 1.0, 2.0, 2.86, and 4.0 kHz. Each bird was tested for a minimum of 200 trials at each frequency, or until the birds' thresholds varied by less than 3 dB across successive sessions. In the second phase of testing, the test tone and the noise masker were both presented from the right speaker only (unilateral-masking condition), and masked thresholds were again obtained for all four test frequencies using the same procedure as above.

The in-phase addition of two acoustic signals results in an increase of about 6 dB SPL at each frequency. Thus, for comparison of masked thresholds for the unilateral condition and bilateral condition, critical ratios (signal-to-noise ratios at masked threshold) were used for data analysis. The critical ratios at each test frequency were calculated by subtracting the spectrum level of the noise at the one-third octave bandwidth surrounding that tone's frequency.

In the third phase of testing, changes were made in the binaural input to the ears. The birds' left (contralateral) ears were plugged with cotton and sealed with Nexaband S/C liquid, and both the bilateral and the unilateral conditions were tested again. Another set of masked thresholds was taken after removing the earplugs to ensure that there were no residual effects of the plugs. Finally, one of the birds was tested with plugs in both ears to determine the overall effective attenuation of the cotton-Nexaband plugs.

Another set of critical ratio measurements was taken from the birds in another control condition. In this condition, the noise was emitted from an overhead speaker and the tone was presented from the right speaker. This provided bilateral noise input to the ears and provided a check as to whether the correlated noise presented binaurally in the bilateral testing condition actually was a correlated binaural input. If it was, then critical ratios for this control condition should match critical ratios in the binaural-bilateral testing condition.

At the conclusion of testing, thresholds defined in several ways were examined, including the level of the tone that the bird detected 50% of the time (uncorrected threshold), the level of the tone detected 50% of the time adjusted by the false-alarm rate (corrected threshold; Hienz, Sinnott, & Sachs, 1977; Sinnott, Sachs, & Hienz, 1980), and the level of the tone resulting in a constant d' of 1.5 (Dooling & Okanoya, 1995; Green & Swets, 1966; Penner, 1995).

Data analysis. The data were analyzed with a three-way (Test Frequency × Earplug × Noise Source) analysis of variance (ANOVA) to compare masked thresholds across all of the conditions. In addition, planned comparisons were used to analyze the effects of noise source for binaural and monaural conditions and the effects of earplugging conditions within each noise-source condition.

Results

There was little difference be tween corrected, uncorrected, and d ' threshold values, so corrected thresholds were used for all subsequent data analysis. The main effects o f noise source, earplug, and f requency were all significant: F(1 , 3) = 141.42, p < .01; F(1, 3) = 33.07, p < .01; F(3, 9) = 57.69, p < .01, respectively. The interact ion o f noise source by earplug was also significant, F(1, 3) = 74.53, p < .01, and planned compar isons y ie lded significant results within those condit ions.

The effect o f noise source on the binaural l is tening condi t ion was significant, F(1 , 3) = 526.67, p < .01, but not in the monaura l condit ion, F(1 , 3) = 10.06, p > .05. In other words, adding a second source o f correlated noise to the opposi te ear caused a release f rom masking in the binaural l istening condit ion, but not in the monaura l l istening condi- t ion (left ear plugged). The average amount o f masking release when the tone was presented f rom the f ight speaker and noise was presented f rom ei ther the f ight speaker (unilateral) or both left and right speakers (bilateral) is shown in Figure 1. There is a considerable amount of masking release at all test frequencies. The amount of masking when correlated noise was presented f rom both


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Figure 1. Mean critical ratios for 4 birds at four frequencies. Open squares show thresholds of a tone masked by a unilateral noise source, and solid squares the bilateral sound source. Error bars indicate SEM.

speakers was, on average, about 7.5 dB less than when noise was presented from only one speaker.

Plugging the left ear during the unilateral speaker condition resulted in masked thresholds that were not significantly different from the binaural, unilateral noise presentation, F(1, 3) = 0.17, p > .05. However, plugging the left ear during the bilateral noise presentation resulted in significantly higher thresholds than the binaural listening condition, F(1, 3) = 53.94, p < .01, at all frequencies. These results show that plugging the contralateral ear increases the signal-to-noise ratio when noise is presented bilaterally, but not unilaterally. In other words, there is an unmasking effect due to binaural processing (Figure 2). To ensure that plugging itself caused no difficulties, the birds were retested with the plugs removed, and thresholds returned to previous levels. Finally, one bird was tested with both ears plugged and showed an increase in the critical ratio of approximately 30 dB, which is about the limit of effectiveness of removable earplugs with the overhead speaker at 2.86 kHz.

Figure 3 summarizes the amount of unmasking that occurs at all four frequencies when a second, correlated noise is presented from the left speaker. The unmasking in the normal condition ranged from 5 dB at 2.86 kHz to 11 dB at 4.0 kHz. The addition of a second noise source in the monaural listening conditions, however, produced little or no unmasking at all of the four frequencies.

When the noise was presented from an overhead speaker and the tone was presented from the right speaker, critical ratios were very similar (see Table 1) to those from the bilateral testing conditions. This means that the condition in which identical noise was presented from both speakers produced correlated noise to the ears.

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Figure 2. Mean critical ratios for 4 birds before, during, and after plugging of the contralateral ear. Error bars indicate SEM.

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'i!t Figure 3. Summary of the effect of adding a second noise source in the binaural and monaural test conditions at four frequencies. The binaural condition is represented by open bars and the monaural condition is represented by solid bars. Negative values indicate improvement in detection (masking release) when chang- ing noise sources from unilateral to bilateral.


Table 1 Critical Ratios in Budgerigars (n = 4) for Several Speaker Conditions

Frequency 1.0 kHz 2.0 kHz 2.86 kHz 4.0 kHz

lpsilateral noise and tone speaker, contralateral noise speaker (binaural listening) a 10 15 17 21

Overhead noise speaker, lateral tone speaker (binaural listening) a 11 16 19 21

One unilateral noise and tone speaker (binaural listening) a 15 25 22 32

One unilateral noise and tone speaker (monaural listening) a 18 23 24 27

Ipsilateral noise and tone speaker, contralateral noise speaker (monaural listening) a 21 20 20 24

One overhead noise and tone speaker (binaural listening) b 26 22 20 22

aCritical ratios were measured in Experiment 1. bOverhead speaker critical ratios were measured by Farabaugh et al. (in press).

Discussion

This experiment tested whether budgerigars experience BMLD as mammals do. We found that the amount of unmasking for budgerigars at the lowest (1.0 kHz) and highest (4.0 kHz) frequencies tested was surprisingly similar to that found at 500 Hz by Hine et al. (1994) in ferrets. The ferrets, with much larger heads (average interaural distance = 24.2 ram; S. Carlile, personal communication, Feb- ruary 6, 1996) than the budgerigars (average interaural distance = 14 ram), had an average of 11 dB of unmasking at 500 Hz in the bilateral speaker condition before and after plugging. Second, the greatest amount of unmasking (the difference between the binaural and monaural bars on Figure 3) was about 8 dB for budgerigars at the lowest test frequency of 1.0 kHz and the highest test frequency of 4.0 kHz.

Interestingly, we also found that critical ratios obtained with the laterally placed signal speakers were significantly different from critical ratios collected with both signal and noise presented from an overhead speaker (Dooling & Saunders, 1975; Okanoya & Dooling, 1987). Critical ratios from an overhead speaker are available from the same birds used in these experiments (Farabaugh et al., in press) and are presented in Table 1 along with the present data. There are little or no differences in critical ratios between the overhead speaker and the bilaterally placed speakers at 2.0 kHz and 2.86 kHz, although there are large differences at 1.0 kHz and 4.0 kHz. At 1.0 kHz, critical ratios (both monaural and binaural conditions) are much smaller than those obtained with the speaker overhead, which may be a result of speaker

roll-off. At 4.0 kHz, on the other hand, the critical ratios obtained with noise presented from a unilateral speaker are larger than when noise and signal are presented from an overhead speaker (except for the binaural condition with bilateral noise source). This strongly suggests that the masking release obtained at 4.0 kHz is related to the location of the signal speaker.

Since presenting tone and noise from a single overhead speaker presumably results in the same signal and the same noise being presented to both ears, we could consider the difference between the overhead speaker condition in previous experiments and the bilateral speaker condition in the present experiment (signal to one ear, correlated noise to both ears), as a kind of masking release. Considered in this way, there is large masking release at 1.0 kHz decreasing to no masking release at 4.0 kHz, consistent with expected results.

There was no significant masking release at 2.86 kHz. This was somewhat surprising since most of the energy in budgerigar communication signals occurs in the frequency region of 2-4 kHz and one would expect, from ecological considerations, the best performance in this frequency region. For this reason, we designed a second experiment to address masking release using an arrangement of signal and noise sources that might more closely approximate those found under more natural conditions.

Exper imen t 2

Results from Experiment 1 show that binaural masking release occurs at the greatest separation between tone and noise source. Experiment 2 was designed to examine the amount of unmasking as a function of other azimuthal angular separations between a 2.86-kHz signal and the masking noise. This experimental setup has more ecological relevance for the bird in the biotope since a bird in the wild does not usually encounter either symmetrically bilateral or only unilateral sound sources. Sounds have varying phase relationships between a signal and a masker. These variable phase relationships determine if masking release will occur, and if so, how much will occur. Varying the azimuthal angular separations of a signal and a masker is one way to change the phase relationships of sounds. In this experiment, we measured the amount of masking release at many different angular separations of signal and noise, similar to a study by Saberi et al. (1991) in humans.

Method

Subjects. Three adult male budgerigars were used as subjects. Two of the birds had absolute thresholds within the normal range, and one had slightly elevated thresholds. The birds were bred and housed in a vivarium at the University of Maryland at 90% of their free-feeding body weights and kept on a normal photoperiod that varied with the season.

Behavioral apparatus. Subjects were tested in a 2.8 × 2.5 X 2.0 m single-walled sound-attenuating chamber (Internal Acoustics Company, New York, NY), which was carpeted and lined on the walls with wedge foam (5.1 cm, Sonex Illbruck, Inc., Minneapolis, MN) to reduce echoes. Overall background-noise level was 27


dB(A) SPL. A wire test cage (14 × 18 × 14 cm) was placed in the center of the chamber on a stand about 90 cm tall lined with two layers of the wedge foam. The floor of the test cage concealing the automatic feeder (hopper) was lined with flat foam (1 cm Sound Coat, Deer Park, NY) to reduce echoes. The cage contained a wooden perch 1 cm in diameter and two vertical-lever response keys (observation and report keys) 7 cm long. Each key consisted of an LED 8 mm in diameter mounted on the end of a thin microswitch arm. During a session, the test cage was illuminated by a 12-V light mounted on top of the cage while the rest of the room was dark. The custom-built food hopper delivered food through a funnel-shaped opening 1 cm in diameter located beneath the response keys. A small light illuminated the food when the hopper was activated.

The pure-tone stimuli and the continuous masking noise were generated as described in Experiment 1. Sound was delivered by two midrange tweeters (Realistic soft dome, Type 40-1281A) mounted on moveable stands 100 cm from the position normally occupied by the bird's head in front of the observation key. The noise-generating speaker (masking speaker) remained at 0 ° directly in front of the bird. The tone-generating speaker (target speaker) could be placed in any of 12 predetermined azimuth positions separated by 30 ° increments. The precision in placing the speakers was 1 cm in distance and 1 ° in azimuth. For azimuth 0 °, the target speaker was mounted on top of the masking speaker (elevation angle 10°). The sound pressure level in the test cage was measured with precision sound-level meters (General Radio, Type 1982, and a 1-cm microphone, or Bruel & Kjaer, Type 2231, with a ¼-in. microphone, Type 4135, both with 3-m extension cables). Har- monic distortion of the tone probes was measured with a spectrum analyzer. At all test frequencies, energy at harmonic frequencies was more than 52 dB down relative to the fundamentals. The noise spectrum was flattened (---3 dB, 0.6-11.8 kHz) with a graphic equalizer, and the overall level of masking noise at the bird's head was 52 dB(A). In the 2-kHz octave band, the noise level was 40.5 dB, corresponding to a spectrum level of 9 dB/Hz.

It was impossible to create a totally homogeneous sound field in the experimental cage. For a given angle of sound incidence, the sound field at the position normally occupied by the bird's head varied less than 1 dB when the 1A-in. microphone was moved 1 cm in all directions, but up to 3 dB in worst cases when it was moved by 3 cm. The sound pressure level at the position normally occupied by the bird's head varied with the azimuth position of the target speaker by ---2 dB, but in a smooth manner and symmetrically relative to the direction of the masking speaker. To correct for this variation, absolute thresholds as a function of azimuth were calculated using the sound pressure level measured at each azimuth angle.

While the birds were able to freely move about in the sound field, the behavioral procedure required that the bird had to peck the observation key repeatedly to initiate a trial. This served to constrain the position of the bird's head and its movement within the test cage during tone presentation. Thus, a reasonable estimate of the signal and noise level at the bird's head during a trial could be obtained by placing a microphone in the position occupied by the bird's head as it stood in front of the observation key. To obtain a measure of the variability of the bird's head position during a trial (i.e., during the 2-s presentation of 400-ms tones when head scanning might be used), the bird's behavior was recorded by a video camera (Panasonic, Type WV3230) permanently suspended directly overhead at a distance of 70 cm. Analysis of these tapes revealed no scanning movements, and the center of the head remained in front of the observation key with variation of about 1 cm. However, the direction of the bird's head when hearing the tone was slightly biased towards the right side (report key). The bias did

not vary between birds or between target-speaker positions. On average, it was 7.9 ° -+ 10.6 ° (N = 608 observations). (Note that for all measurements reported in this experiment, the azimuth angle is given in the clockwise direction, where 0 ° is directly in front of the bird.) This means that on average the masking speaker was at about - 8 ° azimuth relative to the bird's head.

Procedure. The training, testing, and threshold-determination procedures were the same as those used in Experiment 1. Masked thresholds (i.e., thresholds in the noise) were determined for a 2.86-kHz pure tone at the 12 azimuthal angles in 30 ° steps from 0 ° to 360 ° in random order. The birds were tested in 100-trial sessions daily, and each threshold is based on a minimum of 200 trials at each azimuth position when thresholds from successive sessions varied by less than 3 dB. Once masked thresholds were obtained, the same procedure was repeated for measurement of absolute thresholds (thresholds in quiet). One of the birds began to behave erratically during these tests and consequently was tested only on masked thresholds. The data were analyzed with a one-way repeated measures ANOVA to compare masked thresholds across all of the positions.

Results

Absolute thresholds (ATs) averaged about 9 dB across all azimuthal positions, with a range of 7 to 10 dB. These thresholds in the quiet are in general agreement with those reported from a number of earlier studies using various techniques, but with a speaker mounted overhead (e.g., Dooling & Saunders, 1975; Okanoya & Dooling, 1987; Saunders, Rintelmann, & Bock, 1979). For all birds at all angles and test frequencies, ATs were well below masked absolute thresholds (MATs).

Figure 4 shows the mean masking release for all three birds at 2.86 kHz set relative to 0 °. Masked thresholds are the highest when the target speaker is between - 3 0 ° and +30 °. Masking release increased significantly, F ( l l , 22) = 3.08, p < .01, by almost 10 dB when the target speaker was moved to more posterior positions on either side. Toward a location of 180 ° (i.e., directly behind the birds) there was a slight but consistent decrease in masking release.

Discussion

When the target and masking speakers were spatially coincident at azimuth angles 0 °, the masked absolute threshold at 2.86 kHz was about 30 dB SPL. This represents an increase in absolute threshold of almost 20 dB due to the introduction of a broadband noise masker. The level of the tone at masked threshold minus the spectrum level of the noise corresponds to a critical ratio of 21 dB, which is close to that typically reported for this species (Dooling & Saunders, 1975; Okanoya & Dooling, 1987).

Genera l D i scuss ion

Taken together, results from these experiments show that budgerigars exhibit the phenomenon of binaural release from masking in the free field. Because the birds were able to move their heads in these experiments (as they presumably do in nature), these results have particular ecological validity. For budgerigars, there was about 8 dB of masking


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o ~ 150 ° 180 °

Figure 4. Average masked thresholds for three birds when noise source is directly ahead and tone is moved around in 30 ° increments. The center of the plot is 0 dB and each dashed ring represents an increase of 5 dB. At 0 ° azimuth when noise and tone are coincident, masked threshold is 30 dB. Masked thresholds less than 30 dB represent release from masking.

release when a second noise source was added in Experi- ment 1, and MATs at 2.86 kHz improved up to 9 dB as the tonal source was spatially separated by more than 30 ° from the broadband masker in Experiment 2. Biologically important sound signals for the bird in the biotope (such as contact calls) that fall in this frequency range and are emitted close to a broadband masking sound source (such as running water), may only be detected at close range. However, if a calling budgerigar and environmental masker were spatially separated by more than 30 ° azimuth, another budgerigar could detect calls from the sender at a greater distance than when the noise and signal are coincident.

Because these data were obtained in the free field, it is difficult to directly compare the results in budgerigars to the data obtained in humans under closed-field conditions (e.g., Durlach & Colburn, 1978; Jeffress et al., 1962). In humans, free-field spatial unmasking is 15-18 dB for click sounds (Saberi et al., 1991) and 11-14 dB for 1-2-kHz tone signals (Gatehouse, 1987). The results for budgerigars are in general accord with these values, despite their much smaller heads.

There are only a few studies that have investigated the physiological basis of the BMLD in mammals. Initial results have been controversial because single-unit responses could not always provide an adequate explanation for the magnitude of the psychophysically observed results (Langford, 1984; Caird, Pillman, & Klinke, 1989; Caird et al., 1991). McAlpine, Jiang, and Palmer (1996) fared much better in their recent work examining BMLD responses in the inferior colliculus of the guinea pig, by showing that when signals are optimized for the frequency, level, and interaural delays

of specific neurons, masking-level differences are of the same magnitude and in the same direction as those typically found with human subjects. This is an important finding since it provides a physiological explanation for BMLD at the level of the mammalian inferior colliculus (McAlpine et al., 1996).

Unfortunately, we know of no similar physiological recordings of BMLDs in birds. Phase locking in auditory nerve fibers of the starling is robust at low frequencies, but nonexistent at frequencies above 3-4 kHz (Gleich & Narins, 1988). In the barn owl, NL neurons acting as coincidence detectors are sensitive to ITDs (see, for example, Carr & Konishi, 1990; Sullivan & Konishi, 1984). Maps of auditory space exist in the barn owl inferior colliculus (Knudsen & Konishi, 1978), and these neurons are more sharply tuned to ITDs than neurons in the lower brainstem.

BMLDs in mammals involve neurons sensitive to interaural delays at the level of the inferior colliculus. It remains unclear whether failure to find a single unit correlate of BMLD of the medial superior olive (equivalent to avian NL) is due to procedural differences or to lack of units sensitive to BMLDs (Langford, 1984). So, we might expect that similar processes in the avian auditory system might be found at levels as low as the NL when signals and maskers are optimized for each unit's delay sensitivity, similar to the inferior colliculus recordings by McAlpine et al. (1996).

The demonstration of masking release in birds with small heads and closely spaced ears raises several interesting questions. Calford and Piddington (1988) proposed a model to predict interaural delay achieved by birds. Actual interaural delays for low-frequency tones exceeded the interaural delay predicted on the basis of the sound transmission time around the head. This model predicts that interaural cues should be more prominent at the lowest frequencies, and masking release, if it exists, should be more pronounced at low frequencies. In zebra finches these low-frequency advantages extended as high as 4 kHz, where ITDs were still 1.5-2 times larger than expected. The results from the present experiment are consistent with this model in that we found a decrease in BMLD as frequency increased from 1 kHz to 2.86 kHz.

The large amount of masking release seen behaviorally in budgerigars at 4 kHz, however, is at variance with this model. This suggests that another mechanism is at work. Experiments using laser vibrometry to measure tympanal frequency response as a function of sound azimuth show large directional effects in several small birds including budgerigars, canaries, zebra finches, and quail. This direction- ality is produced by diffractional effects acting in concert with a substantial interaural transmission, which enhances both interaural intensity differences (IIDs) and ITDs even at 4 kHz (Calford & Piddington, 1988; Larsen & Dooling, 1996; Larsen & Popov, 1995). It is not clear how such a mechanism would provide a basis for binaural-masking release, but physiological studies examining a combination of IIDs and ITDs probably would be a good place to start.


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Received July 9, 1996 Revision received November 25, 1996

Accepted November 26, 1996 •

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Free-field binaural unmasking in budgerigars ( Melopsittacus undulatus )

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