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Previous Article | Next Article
The Journal of Neuroscience, January 15, 2000, 20(2):862-877
Abnormal Auditory Experience Induces Frequency-Specific Adjustments in Unit Tuning for Binaural Localization Cues in the Optic Tectum of Juvenile Owls
Joshua I. Gold and Eric I. Knudsen Department of Neurobiology, Stanford University, Stanford, California 94305-5125
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Early auditory experience shapes the auditory spatial tuning of neurons in the barn owl's optic tectum in a frequency-dependent manner. We examined the basis for this adaptive plasticity in terms of changes in tuning for frequency-specific interaural time differences (ITDs) and level differences (ILDs), the dominant sound localization cues. We characterized broadband and narrowband ITD and ILD tuning in normal owls and in owls raised with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. In normal owls, units were tuned to frequency-specific ITD and ILD values that matched those produced by sound sources located in their visual receptive fields. In contrast, in device-reared owls, ITD tuning at most sites was shifted from normal by ~55 µsec toward open-ear leading for 4 kHz stimuli and 15 µsec toward the opposite-ear leading for 8 kHz stimuli, reflecting the acoustic effects of the device. ILD tuning was shifted in the adaptive direction by ~3 dB for 4 kHz stimuli and 8 dB for 8 kHz stimuli, but these shifts were substantially smaller than expected based on the acoustic effects of the device. Most sites also exhibited conspicuously abnormal frequency-response functions, including a strong dependence on stimulus ITD and a reduction of normally robust responses to 6 kHz stimuli. The results demonstrate that the response properties of high-order auditory neurons in the optic tectum are adjusted during development to reflect the influence of frequency-specific features of the binaural localization cues experienced by the individual.
Key words: sound localization; hearing impairment; development; auditory plasticity; superior colliculus; Tyto alba
INTRODUCTION
The response properties of sensory neurons in the CNS can be extremely complex and, in some cases, reflect the experience of the individual. For example, visual neurons in the primate temporal cortex that respond preferentially to faces (Rolls et al., 1989
; Perrett et al., 1992
Sound localization cues arise from interactions between incident sound waves and the animal's head and external ears. In barn owls, these cues include frequency-specific interaural time differences (ITDs), which vary primarily with sound source azimuth, and level differences (ILDs), which vary primarily with sound source azimuth for frequencies below ~4 kHz but with elevation for higher frequencies (attributable to an asymmetry in the owl's external ears). Previous work has demonstrated that adaptive modification of tectal unit auditory receptive fields (RFs) corresponds to changes in their tuning for broadband ITD and ILD. For example, either monaural occlusion with a dense foam plug or removal of the sound collecting structures of the external ears alters sound timing and level and leads to adaptive changes in the values of broadband ITD and ILD to which tectal units are tuned (Mogdans and Knudsen, 1992
We investigated the extent to which the binaural tuning properties of tectal neurons accurately reflect frequency-specific features of the individual's auditory experience. In a previous study, we caused frequency-dependent changes in the auditory localization cues experienced by young owls by raising them with an acoustic filtering device in one ear. We found frequency-specific changes in the auditory RFs of tectal units that compensated for the acoustic effects of the device (Gold and Knudsen, 1999
MATERIALS AND METHODS
We collected data from eight normal barn owls (Tyto alba) and eight barn owls raised with an acoustic filtering device in one ear. Four of the device-reared owls and two of the normal owls were also used in a previous study (Gold and Knudsen, 1999
Auditory experience. The acoustic filtering device used to alter auditory experience was a custom-designed chamber made from acetal delrin (Plastics SRT) that was sutured into the owl's right ear canal, just behind the preaural flap and in front of the sound-collecting surface formed by the facial ruff feathers (the owl's ear canals are asymmetrically positioned on its head, and the left ear canal opens at an angle relative to the facial ruff feathers that makes it difficult to place the device on the left side). We designed the device to increase the path length of sounds reaching the affected ear and to change the resonance properties of the ear canal while still providing a low impedance pathway to the tympanic membrane. The device is described in more detail in a previous study (Gold and Knudsen, 1999
Owls raised with an acoustic filtering device were first binaurally occluded from 25-35 d of age with dense foam rubber plugs (E.A.R. Cabot Corporation) to disrupt early auditory experience while the ear canals were open but too narrow to hold the device. The plugs were sutured into the ear canals while the animal was anesthetized with halothane (1%) in a mixture of oxygen and nitrous oxide (5:4). At ~35 d of age, the owl was again anesthetized, the binaural foam plugs were removed, and the filtering device was sutured into the right ear canal.
All owls were raised initially in brooding boxes with their siblings. After device insertion, owls were removed from the brooding box and were placed into a small cage located next to a large flight cage that housed adult owls, to ensure a rich auditory and visual environment. When the owls could fly (normally at ~60 d of age), they were transferred to the flight cage, where they were housed for the duration of the experiment.
The acoustic device was removed only during experiments, at which time the canal, eardrum, and device were inspected for damage and cleaned of earwax. The device was sutured back into place immediately after each experiment.
The owls were provided for in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and the guidelines of the Stanford University Institutional Animal Care and Use Committee.
Electrophysiology. Electrophysiological recordings were performed on owls that were at least 95-d-old. Each owl was prepared for recordings in a single surgical session, at which time the owl was anesthetized with halothane and nitrous oxide, and a small, stainless steel plate was cemented to the base of the skull. In addition, small craniotomies were made above the left and right optic tecta. These openings were covered with dental acrylic, which was removed and replaced for each recording session. At the end of the procedure, lidocaine was infused into any incised tissue, and all incisions were treated with betadine and sutured closed.
At the beginning of each recording session, the owl was anesthetized with halothane and nitrous oxide, given an intramuscular injection of 2.5% dextrose in 0.45% sterile saline, and wrapped in a soft leather jacket. The owl was then suspended in a prone position in a stereotaxic apparatus that was centered in a sound attenuating chamber (Industrial Acoustics Company 404A) lined with acoustic foam to suppress echoes. The owl's head was bolted to the stereotaxic apparatus via the surgically implanted steel plate and aligned using retinal landmarks (a barn owl's eyes are essentially fixed in its head). A tungsten microelectrode was positioned and then advanced through the telencephalon to the tectum using a mechanical microdrive. A characteristic bursting pattern of unit activity indicated when the electrode tip entered the superficial layers of the optic tectum (Knudsen, 1982
Other than the initial 20 min of set-up, the owl typically remained unanesthetized and was calm and motionless during the course of the experiment. Occasionally, however, an owl became restless, in which case recording was suspended temporarily and brief doses of halothane and nitrous oxide or nitrous oxide alone were administered.
After each experiment, the owl recovered under a heat lamp overnight before being returned to the flight cage.
Auditory measurements. Dichotic stimuli consisted of computer-generated broadband, narrowband, or tonal bursts lasting 50 msec. The stimuli were presented through matched Knowles subminiature earphones (ED-1914) coupled to damping assemblies (BF-1743) placed in each ear ~5 mm from the tympanic membrane. The amplitude and phase spectra of the earphones were equalized to within ±2 dB and ±2 µsec from 1 to 12 kHz by computer adjustments. Sound levels were calibrated using A-weighted signals from a Bruel and Kjær 1/2 inch condenser microphone positioned 1 cm from the earphone. Broadband noise bursts had rise-fall times of 0 msec and had a passband of 3-12 kHz, the lower bound set to minimize propagation through the interaural canal (Moiseff and Konishi, 1981
A level discriminator was used to isolate action potentials ("spikes") generated by a small number of tectal neurons. Spike times relative to the onset of a given sound presentation were stored on a computer. The response to a sound presentation was defined as the number of spikes counted in the 100 msec immediately after stimulus onset (poststimulus response) minus the number of spikes counted in the 100 msec immediately preceding stimulus onset (baseline activity).
At each site, we characterized response thresholds, frequency responses, and ITD and ILD tuning using broadband and narrowband stimuli. Response threshold was defined as the lowest average binaural level at which responses to a given stimulus were at least 25% of the maximum responses produced by that stimulus for any average level up to 70 dB SPL. Frequency, ITD, and ILD tuning curves were characterized by calculating the widths and best values of tuning curve peaks. For each tuning curve, the maximum response was determined, and the width of the peak was defined as the uninterrupted range over which responses were >50% of the maximum. The midpoint of that range was defined as the best value for that peak. For some tuning curves, responses to values outside of the peak containing the maximum response exceeded 50% of the maximum response. The widths and best values from all such peaks were determined separately.
Frequency-response functions were measured using tonal and 1 kHz bandwidth stimuli. Tone bursts were presented using the best ITD and best ILD measured for the broadband stimulus and at ~20 dB above the threshold measured for the lowest frequency above 3 kHz that elicited a response. Stimuli of 1 kHz bandwidth were presented using the best ITD and best ILD and at 20-30 dB above the threshold measured for the given stimulus.
ITD tuning was measured at 10-20 µsec intervals over a 100-300 µsec range of values (positive and negative values indicate right- and left-ear leading, respectively). Each ITD value was presented at the estimated best ILD and at 20-30 dB above the threshold measured for the given stimulus.
ILD tuning was measured at 2-4 dB intervals over a 15-40 dB range of values (positive and negative values indicate right- and left-ear greater, respectively). Each ILD value was presented at the best ITD and at a constant average binaural level 20-30 dB above the threshold measured for the given stimulus. For sites with ITD tuning curves with multiple peaks for a broadband stimulus, ILD tuning was measured using the best ITD for each peak.
Visual receptive field measurements. Visual RFs were measured by projecting bars and spots of light onto a translucent hemisphere placed in front of the owl. Visual RF location is reported as the geometric center of the RF in a double-pole coordinate system (Knudsen, 1982
) the visual (horizontal) plane.
Comparison with expected values of ITD and ILD. Best ITDs and best ILDs were compared to the values predicted for sites with matching visual RF locations in normal owls. For broadband stimuli, predicted normal best ITD and best ILD values were determined from previously published linear regressions that describe the predictable relationships between best values and visual RF location in the optic tecta of normal owls (ITD, Brainard and Knudsen, 1993
RESULTS
We examined the extent to which early experience with the chronically implanted acoustic device altered the binaural tuning properties of tectal neurons by comparing the frequency responses and the narrowband and broadband ITD and ILD tuning of tectal neurons in normal and device-reared owls. The effects of the device on the timing and level of sound reaching the right eardrum were measured in a previous study using cochlear microphonics (Gold and Knudsen, 1999
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Table 1. Acoustic properties of the devicea Frequency-response functions in normal owls
Frequency-response functions, when measured using dichotic stimuli with constant ITD and ILD values, reflect both the spectral sensitivity of a unit and its tuning for binaural cues. The effect of binaural tuning on dichotically measured frequency-response functions is eliminated when the binaural tuning of a unit is independent of frequency. Therefore, to minimize the effect of binaural tuning on frequency-response functions measured using constant ITD and ILD values in normal owls, we sampled frequency responses primarily from the rostral tectum, which represents frontal space where sounds produce nearly constant values of ITD and ILD across frequency (Knudsen et al., 1991
Figure 1A depicts frequency-response functions of tectal neurons measured dichotically, using tonal stimuli with the best ITD and best ILD values measured with a broadband stimulus for the given site. These frequency-response functions were consistently broad (width = 3.1 ± 1.1 kHz, mean ± SD), a characteristic known to play a key role in resolving the spatial ambiguities that are inherent to sound localization cues (Brainard et al., 1992
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Figure 1. Frequency tuning in normal owls. A, Best frequency as a function of visual RF azimuth. Responses were measured using tonal stimuli and the broadband best ITD-ILD pair for the given site. The solid line is a linear fit to the data (y =
To account for possible effects of stimulus ITD and ILD on frequency-response functions, we also assessed frequency responses using the best ITD and best ILD measured for each stimulus. Because responses to tones were often weak, we measured these frequency responses using stimuli with a bandwidth of 1 kHz, which typically elicited much stronger responses. For frontal sites, with visual RF azimuths between L25° and R25°, responses to these stimuli were typically strong for all frequencies between 3 and 9 kHz. Responses were strongest and thresholds were lowest, however, for stimuli near 6 kHz (Fig. 1B,C). In contrast, for sites with more peripherally located visual RFs, the strongest responses were elicited by lower frequencies (Fig. 1D).
Frequency-response functions in device-reared owls
Because the acoustic device altered ITD and ILD differently for different frequencies, an adaptive adjustment to the effects of the device would require the ITD and ILD tuning even of frontal units to vary commensurately with stimulus frequency. This type of adjustment would cause the frequency tuning of these units, measured with dichotic stimuli, to vary dramatically depending on the values of ITD and ILD that were chosen for the stimulus. Indeed, such ITD- and ILD-dependent frequency-response functions were observed routinely among frontal units in device-reared owls (Fig. 2).
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Figure 2. Frequency tuning in device-reared owls. Responses were measured using tonal stimuli. A, Two frequency-response curves from a tectal site with a visual RF at L2° az, +10° el in a device-reared owl. The two curves were measured under identical conditions except for the stimulus ITD used, as indicated. B, Best frequency as a function of the stimulus ITD relative to the predicted normal broadband best ITD. The predicted normal broadband best ITD was determined from the visual RF azimuth (see Materials and Methods). The stimulus ITD used was the broadband best ITD at the given site; for sites with multiple best ITDs, frequency tuning was measured using each best ITD separately. Best values from all peaks of all curves measured at sites with visual RFs between L25° and R25° az are shown. C, Best frequency as a function of visual RF azimuth. The dashed line is a linear fit to the data from normal owls (Fig. 1A). For frequency tuning curves with more than one peak, best values from both peaks are shown in bold.
In the example shown in Figure 2A, the frequency-response curve for a tectal site with a visual RF at L2° azimuth (az), +10° elevation (el) in a device-reared owl had a best value of 4.0 kHz when measured with an ITD of
The frequency-response functions measured in device-reared owls using the broadband best ITD and best ILD values for the given site were abnormal (Fig. 2C). As in normal owls, best frequency varied with visual RF azimuth such that, on average, best frequencies were higher for sites with frontally located visual RFs. In contrast to the normal distribution of best frequencies found for sites representing frontal space in normal owls (Fig. 1A), however, the distribution of best frequencies for comparable sites in device-reared owls was bimodal, with most best frequencies clustered near 4 and 7.5 kHz and few between 5 and 6 kHz. Indeed, many of the frequency-response curves measured at sites with frontally located visual RFs were themselves bimodal, with strong responses near 4 and 8 kHz and weak responses near 6 kHz.
The dependence of best frequency on stimulus ITD in device-reared owls implies frequency-dependent changes in ITD tuning. Thus, the abnormal frequency-response functions using constant ITD and ILD values likely reflected the effects of nonoptimal binaural cue values at particular frequencies. However, as shown in Figures 3 and 4, frequency-response functions measured using the best ITD and best ILD for each narrowband (1-kHz-wide) stimulus revealed that the device did, in addition, induce abnormal spectral sensitivity. In particular, tectal units representing frontal space in device-reared owls exhibited a substantial reduction in responses to stimuli near 6 kHz. These changes match those measured using free field stimulation, as reported in a previous study (Gold and Knudsen, 1999
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Figure 3. Responses to narrowband (1-kHz-wide) stimuli centered on 4 (A), 6 (B), or 8 (C) kHz for a tectal site in a device-reared owl with a visual RF at 0° az, +3° el. A, Maximum response = 3.2 spikes per stimulus at ITD =
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Figure 4. Summary of responses to narrowband (1-kHz-wide) stimuli in device-reared owls. All responses were measured using the best ITD-ILD pair for the given stimulus. A, Response threshold as a function of the center frequency of the stimulus for sites with visual RFs between L25° and R25° az. "70+" indicates that no reliable responses could be elicited using the given stimulus presented at sound levels up to 70 dB SPL. Thick lines, boxes, and bars indicate medians, quartiles, and 10th-90th percentiles, respectively, of binned data. B, Strength of response as a function of the center frequency, normalized to the maximum response elicited by any such narrowband stimulus at the same recording site, for sites with visual RFs between L25° and R25° az. Thick lines, boxes, and bars as in A. C, Data measured as in B, but at sites with visual RFs more peripheral than 25° az. The solid line is a linear fit to the data (y =
Figure 3 illustrates responses for a single site (visual RF at 0° az, +3° el) in a device-reared owl for narrowband stimuli centered on 4, 6, and 8 kHz. For this site, the best ITD-ILD pair for the 8 kHz stimulus elicited the strongest responses, which were nearly twice as strong as those elicited by the best ITD-ILD pair for the 4 kHz stimulus. In contrast, no ITD-ILD pair for the 6 kHz stimulus elicited robust responses. Similar results were found for sites with visual RF azimuths between L25° and R25°. For these sites, response thresholds were relatively normal for stimuli near 4 and 8 kHz but not for stimuli near 6 kHz, which in some cases did not elicit any responses for sound levels up to 70 dB SPL (Fig. 4A). Responses to 4 and 8 kHz stimuli were strong, but responses to stimuli near 6 and 7 kHz were typically <40% of the maximum response elicited by any narrowband stimulus at a given site, which was significantly weaker than normal (Mann-Whitney U test, p < 0.01; Fig. 4B). For sites with more peripherally located visual RFs, frequency responses were relatively normal, however, with the strongest responses to stimuli near 3 and 4 kHz and weaker responses to higher frequencies (Fig. 4C).
Bandwidth for testing narrowband tuning
We used primarily stimuli with a bandwidth of 1 kHz to characterize the frequency-dependent effects of device rearing on the ITD and ILD tuning of tectal neurons. Stimuli with this bandwidth elicited stronger responses than did pure tones and provided adequate specificity to characterize differences in binaural tuning for different stimulus frequencies (Fig. 3). However, nontonal stimuli can trigger inhibitory interactions across frequency channels (Takahashi and Konishi, 1986
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Figure 5. Effect of stimulus bandwidth on ITD tuning curves in the optic tectum of a device-reared owl. A, ITD tuning curves measured using stimuli centered on 7.4 kHz (the best frequency of the site) with a variety of bandwidths (see key for the ranges of stimulus frequencies used). B, The interval between adjacent peaks for all narrowband ITD tuning curves from both normal and device-reared owls that had multiple peaks. The data are plotted as a function of the center frequency of the stimulus. The solid line indicates the interval (in microseconds) that represents an interaural phase offset of 360°. C, ITD tuning curves from A measured using either a 7.2-7.6 kHz (solid line) or a 6.0-8.8 kHz (shaded line) narrowband stimulus. Best ITD (downward arrow in each curve) was computed as the midpoint of the response peak closest to the predicted normal value (asterisk), which was based on the visual RF location.
ITD tuning in normal owls
We measured ITD tuning at tectal sites with visual RFs between L30° and R41° azimuth and
Figure 6 shows ITD tuning for broadband and narrowband stimuli for a tectal site with a visual RF at L2° az, +10° el. For this site, broadband ITD tuning was narrow and had a best value of
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Figure 6. ITD tuning at a tectal site in a normal owl. The visual RF at this site was centered at L2° az, +10° el. A, ITD tuning curves obtained using broadband (3-12 kHz, top curve) or narrowband (the range of stimulus frequencies used is shown for each curve) stimuli. In some cases a second, smaller peak appeared when using a narrowband stimulus (e.g., stimulus = 6.5-7.5 kHz). In each case, the location of the second peak matched the expected location of an interaural phase equivalent peak for
In agreement with previously published reports (Olsen et al., 1989
For individual sites, the narrowband ITD tuning curves each had a peak that was aligned with the peak in the broadband ITD tuning curve. For 30 of 32 sites, the broadband best ITD matched to within 10 µsec at least one narrowband best ITD. Moreover, 102 of the 113 narrowband ITD tuning curves that we measured had a peak with a best value that was within the 50% cutoff limits of the broadband ITD peak.
Narrowband best ITDs in normal owls matched the acoustic ITDs produced by sources located at the visual RF of the site. For all 32 sites, narrowband best ITDs were relatively constant across the range of frequencies tested (Figs. 6, 7A). Across sites, narrowband best ITDs varied systematically with visual RF azimuth. As shown in Figure 7B, for example, best ITDs for narrowband stimuli centered on 4 and 8 kHz progressed from left-ear leading to right-ear leading as visual RF azimuth moved from left to right. Linear fits to these data had slopes of slightly >2 µsec/° and intercepts of close to 0 µsec at 0° azimuth. For all sites and stimulus frequencies tested, the measured best ITD matched to within 30 µsec the value predicted from the visual RF azimuth (Fig. 7C).
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Figure 7. Summary of narrowband ITD tuning of tectal neurons in normal owls. Data are from 32 sites with visual RFs between L30° and R37° az and
ITD tuning in device-reared owls
We measured ITD tuning at sites with visual RFs between L81° and R60° az and
Figure 8 shows ITD tuning for broadband and narrowband stimuli for a site with a visual RF at 0° az, +8° el in a device-reared owl. The broadband ITD tuning curve was broad and had a best value of
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Figure 8. ITD tuning at a tectal site in a device-reared owl. The visual RF at this site was centered at 0° az, +8° el. A, ITD tuning curves obtained using broadband (3-12 kHz, top curve) or narrowband (the range of stimulus frequencies used is shown for each curve) stimuli. Broadband responses were normalized relative to the maximum response elicited with the broadband stimulus. Tuning curves for all narrowband stimuli were normalized relative to the maximum response elicited with any narrowband stimulus. In some cases, a second, smaller peak appeared when using a narrowband stimulus (e.g., stimulus = 7.5-8.5 kHz). In each case, the location of the second peak matched the expected location of an interaural phase equivalent peak for the center frequency of the given range. B, Best values from the tuning curves in A for narrowband stimuli plotted as a function of the center frequency (squares), along with the frequency-specific, average acoustic ITDs experienced by normal owls (circles) and by owls wearing the acoustic device (triangles) for sound sources located in the center of the visual RF of this site.
The effects of device rearing on broadband ITD tuning are summarized in Figure 9. Figure 9A shows broadband best ITD as a function of visual RF azimuth for all sites tested in device-reared owls, whereas Figure 9B-J highlights the device-induced changes in ITD tuning that were evident in different regions of the tectal space map. For sites representing space to the far left (visual RF az,
L25°), broadband ITD tuning curves had similar shapes (Fig. 9B) as those found at corresponding sites in normal owls, but had best ITDs that were shifted from normal by 79 ± 19 µsec toward left-ear leading (mean ± SD; Fig. 9E) and were broader than normal (Fig. 9H). For sites representing frontal space (visual RF az between L25° and R25°), broadband tuning curves were often irregular in shape and typically contained multiple peaks (Fig. 9C, solid line) with normal widths (Fig. 9I), some of which aligned with those found in normal owls and others of which were shifted from normal by as much as 150 µsec toward left-ear leading (Fig. 9F). For sites representing space to the far right (visual RF az,
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Figure 9. Summary of broadband ITD tuning of tectal neurons in device-reared owls. A, Best ITD as a function of visual RF azimuth from 219 sites in eight device-reared owls. The linear fit from previously published normal data are plotted for comparison (dashed line; Brainard and Knudsen, 1993
To determine the frequency-specific adjustments that were responsible for these changes in broadband ITD tuning, we compared narrowband and broadband ITD tuning curves for 98 tectal sites in device-reared owls. Using narrowband stimuli with center frequencies of between 3.0 and 9.0 kHz, 201 of 261 ITD tuning curves had peaks with best values that were within the 50% cutoff limits of a site-matched broadband ITD peak. Of the narrowband best ITDs that did not fall within these limits, most (39 of 60) were for stimuli with center frequencies of
5 kHz, suggesting that responses to these lower frequencies could be suppressed by cross-frequency inhibition. However, those that did fall within the limits of a broadband peak were for stimuli that covered the entire range of frequencies tested (although relatively fewer were with stimuli near 6 kHz because, at many sites, responses to those stimuli were too weak to determine tuning) and indicated shifts from normal values, the magnitude of which varied with stimulus frequency (Fig. 10). The correspondence between broadband and narrowband best ITDs indicates that in device-reared owls, these shifts in narrowband best ITDs could account for the shifts in broadband ITD tuning.
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Figure 10. Summary of narrowband ITD tuning of tectal neurons in device-reared owls. Data are from 98 sites with visual RFs between L41° and R51° az and
Narrowband best ITDs in device-reared owls were shifted from normal in a frequency-dependent manner. Figure 10A depicts best ITDs measured with a variety of stimulus frequencies for 98 tectal sites with visual RFs located between L41° and R51° az and
These device-induced changes in narrowband ITD tuning reflected the frequency-specific, acoustic effects of the device on sound timing. Figure 10C depicts the shifts in narrowband best ITDs relative to predicted normal values for sites in the tectum with frontally located visual RFs (between L25° and R25° az and
These device-induced shifts in best ITD relative to predicted normal values varied systematically across the space map. In general, shifts were larger for neurons in the right tectum, representing the left hemifield (i.e., space contralateral to the device), than for those in the left tectum, representing the right hemifield. For narrowband stimuli near 4 kHz (Fig. 11A), the shift was
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Figure 11. Device-induced shifts in frequency-specific ITD tuning as a function of location in the tectal map. In each panel, best ITD relative to the predicted normal value (based on visual RF location) for a narrowband stimulus near 4, 6, or 8 kHz is plotted as a function of visual RF azimuth. Open and closed symbols represent data taken from the left and right tecta, respectively. A, ITD shifts for 6 kHz stimuli did not significantly regress as a function of visual RF azimuth (r2 = 0.17; ANOVA, p = 0.07), although ITD shifts measured in the left (
Device rearing affected not only narrowband best ITDs but, at some sites, the suppression of interaural phase-equivalent peaks, as well. In normal owls, ITD tuning curves for narrowband (1 kHz bandwidth) stimuli near 8 kHz had interaural phase-equivalent peaks at their predicted locations (separated by ~125 µsec). In contrast, some 8 kHz ITD tuning curves in device-reared owls had only a single peak within the same range of ITDs, because of the suppression of one or more of the interaural phase-equivalent peaks by interactions across frequency channels (Takahashi and Konishi, 1986
ILD tuning in normal owls
In normal owls, acoustic ILD varies with both sound source location (Olsen et al., 1989
Tectal units were tuned for broadband and narrowband ILD. Figure 12 shows broadband and narrowband ILD tuning for a site with a visual RF at R5° az, +10° el in a normal owl. For this site, the broadband ILD tuning curve had a peak centered at 5.8 dB with a width of 9.2 dB. Narrowband ILD tuning curves had broader peaks, with best values of 2.4 dB at 4 kHz and ~6-7 dB at higher frequencies. This relationship between best ILD and frequency matched the pattern of acoustic ILDs produced by a source located in the visual RF of the site (Fig. 12B).
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Figure 12. ILD tuning at a tectal site in a normal owl. The visual RF at this site was centered at R5° az, +10° el. A, ILD tuning curves for a broadband stimulus (3-12 kHz, top curve) and for five different narrowband stimuli (the range of stimulus frequencies used is shown for each curve). Broadband responses were normalized relative to the maximum response elicited with the broadband stimulus. Narrowband responses were normalized relative to the maximum response elicited with the given stimulus (dashed curves) or with any narrowband stimulus (solid curves). B, Best values from the curves in A, using narrowband stimuli (squares), along with the average acoustic ILDs experienced by normal owls for a source located in the visual RF of the site (circles), as a function of the center frequency of the narrowband stimulus.
For 23 sites with visual RFs between L20° and R17° az and
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Figure 13. Summary of narrowband ILD tuning of tectal neurons in normal owls. A, Best ILD as a function of center stimulus frequency. Each line connects points representing measurements taken at a single recording site. B, Best ILDs from A relative to the predicted normal best ILDs, plotted as a function of stimulus frequency; the two were not correlated (ANOVA, p = 0.85).
ILD tuning in device-reared owls
ILD tuning was abnormal in device-reared owls, with broadband and narrowband best ILDs typically shifted from normal values in the adaptive direction. In most cases, however, these shifts in ILD tuning were substantially smaller than expected based on the acoustic effects of the device. Figure 14 shows an example of broadband and narrowband ILD tuning for a site with a visual RF at L11° az, +11° el. For this site, the broadband ILD tuning curve had a best value of 0 dB and a width of 6.9 dB. Narrowband ILD tuning curves were broader and had best values that were close to predicted normal values for low frequencies but were closer to the acoustic values experienced with the device in place for higher frequencies. For example, for the 4 kHz stimulus, the best ILD was
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Figure 14. ILD tuning at a tectal site in a device-reared owl. The visual RF at this site was centered at L11° az, +11° el. A, ILD tuning curves for a broadband stimulus (3-12 kHz, top curve) and for five different narrowband stimuli (the range of stimulus frequencies used is shown for each curve). Broadband responses were normalized relative to the maximum response elicited with the broadband stimulus. Narrowband responses were normalized relative to the maximum response elicited with the given stimulus (dashed curves) or with any narrowband stimulus (solid curves). B, Best values from the curves in A, using narrowband stimuli (squares), along with the average acoustic ILDs experienced by normal owls (circles) and owls wearing the acoustic device (triangles) for a source located in the visual RF of this site, as a function of the center frequency of the narrowband stimulus.
For sites with visual RFs between L25° and R25° az in device-reared owls, broadband ILD tuning curves had slightly but significantly narrower peak widths than comparable curves in normal owls (8.9 ± 3.6 dB vs 12.0 ± 4.3 dB in normal owls; unpaired t test; p < 0.01; Fig. 15C). Like in normal owls, these peaks had best values that varied as a function of visual RF elevation (Fig. 15A). For nearly all sites, however, best ILD was shifted toward left-ear greater values relative to the control regression (shift =
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Figure 15. Summary of broadband ILD tuning of tectal neurons in device-reared owls. A, Best ILDs for broadband stimuli as a function of visual RF elevation from sites with visual RFs between L25° and R25° az. The dashed line is the linear least-squares regression from previously published normal data (Olsen et al., 1989
Narrowband ILD tuning was also abnormal in device-reared owls, although in many cases the device-induced changes did not match the acoustic effects of the device (data from 65 sites are summarized in Fig. 16). For narrowband stimuli with center frequencies in the range of 3-5 kHz, best ILDs were shifted significantly (unpaired t test; p < 0.01) from normal predicted values by
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Figure 16. Summary of narrowband ILD tuning of tectal neurons in device-reared owls. Data are from sites with visual RFs between L25° and R25° az. A, Best ILD as a function of the center frequency of the narrowband stimulus. Each line connects points representing measurements taken at a single recording site. The open circles represent frequencies that did not elicit strong enough responses to measure ILD tuning at the given sites. B, Best ILD relative to the normal acoustic ILD, plotted as a function of stimulus frequency. The dashed line and shaded region represent the median values and the ranges, respectively, of shifts in the level of sound reaching the right eardrum caused by insertion of the acoustic filtering device (cochlear microphonic measurements from four owls; Gold and Knudsen, 1999
DISCUSSION
The present results demonstrate that early experience can alter tectal unit tuning for binaural localization cues in a frequency-dependent manner. In normal owls, such adjustments allow tectal neurons to match their response properties to the cues produced by the acoustic filtering effects of the head and ears (Figs. 6, 12). In animals that experience hearing impairments, this capacity appears to have limits but helps tectal neurons to interpret abnormal cue values correctly to encode the true location of an auditory stimulus. The following sections discuss how these results provide insights into principles of information processing and adaptive plasticity in the auditory localization pathway.
Plasticity of frequency tuning
The broad frequency tuning of tectal neurons enables them to integrate cues across frequency channels, necessary to eliminate spatial ambiguities inherent to individual cues (Brainard et al., 1992
A possible explanation for this effect is that the device caused pathology resulting in sensorineural hearing loss to frequencies near 6 kHz. However, cochlear microphonics measured in device-reared owls with the device removed did not reveal any reduction in the magnitude of responses to 6 kHz stimuli relative to other frequencies. In addition, recordings in the central nucleus of the inferior colliculus of these same owls indicated normal thresholds and frequency responses for all stimuli between 4 and 8 kHz (J. I. Gold and E. I. Knudsen, unpublished observations). Thus, the device altered the frequency tuning of tectal neurons without affecting the sensitivity of the ear to 6 kHz sounds.
The decrease in responses to 6 kHz stimuli might be accounted for by two effects of the acoustic device. First, the device severely altered sound timing and level at 6 kHz, with median shifts of
Second, the effects of the device were most frequency-dependent near 6 kHz, particularly for ITD, which changed by ~50 µsec between 5 and 7 kHz (Fig. 10C). This frequency-dependent variation must have blurred the spatial information around 6 kHz, because even neurons that are narrowly tuned for frequency integrate information across a finite bandwidth. Because of this integration, neurons involved in the binaural comparison of timing and level would derive different values of ITD and ILD, respectively, for a stimulus at the same location in space, depending on the amplitude spectrum near 6 kHz. Thus, the ability of 6 kHz stimuli to drive tectal neurons would be further compromised.
These effects may have resulted in the weak responses and variable shifts in ITD and ILD tuning for 6 kHz stimuli (Figs. 11B, 16B). This interpretation implies that the frequency tuning of tectal neurons is shaped by an activity-dependent process that regulates the strength of responses to particular frequencies according to the degree to which each frequency contributes to postsynaptic discharges. Such a mechanism could be responsible for the normal topographic variation in frequency tuning across the tectum that matches the filtering properties of the external ears (Knudsen, 1984
Plasticity of ITD tuning
Device-induced changes in tectal unit ITD tuning demonstrated that the auditory system interprets and represents ITDs in a frequency-specific and adaptive manner. In regions of the optic tectum representing frontal space in device-reared owls, best ITDs were shifted from normal by averages of 55 µsec toward open-ear leading for 4 kHz stimuli and 15 µsec in the opposite direction for 8 kHz stimuli. These changes were similar to the frequency-specific, acoustic effects of the device on sound timing for frontally located sources (Fig. 10C). In other regions of the space map, changes in ITD tuning varied in magnitude and tended to be smaller in the left tectum (Figs. 9A, 11). A similar, unexplained phenomenon was found in owls raised with one ear occluded, in which adjustments in ITD and ILD tuning were larger and more systematic in the optic tectum ipsilateral to the occluded ear (Mogdans and Knudsen, 1992
The frequency-dependent variation in ITD tuning found in device-reared owls means that tectal sites do not necessarily exhibit a "characteristic delay", which is, by definition, independent of frequency (Rose et al., 1966
Plasticity of ILD tuning
In all species, the head and ears affect sound level in a frequency-dependent manner, producing ILDs that vary markedly with frequency. Therefore, to extract the most information possible from ILD cues, the auditory system must interpret ILD on a frequency-by-frequency basis. Our data suggest only a partial adherence to this principle. In normal owls, best ILDs varied somewhat with stimulus frequency at many sites (differing by ~9 dB for 4 and 8 kHz stimuli, for example). In device-reared owls, best ILDs for frequencies near 4, 6, and 8 kHz were shifted from normal in the adaptive direction by averages of, respectively, 3, 5, and 8 dB (Fig. 16). These changes in ILD tuning were, however, highly variable and, in many cases, did not match the acoustic effects of the device.
The apparent incompleteness of the adaptation of ILD tuning may reflect, in part, the large individual variability in the acoustic effects of the device. For frequencies around 3 and 4 kHz, for example, shifts in best ILD fell short of the median acoustic effects of the device in 70 of 76 measurements. However, they fell within the ranges of those effects in all but two cases (Fig. 16B). In addition, because the acoustic effects of the device were measured at 1 kHz intervals, it is possible that spectral notches or changes in the spatial fine-structure of the ILD cues that were induced by the device were not adequately assessed.
The incomplete adjustments in narrowband best ILDs may have alternative explanations, as well. For example, for frequencies near 6 kHz, the lack of device-induced adjustment in ILD tuning may have resulted from a deprivation effect caused by the device, as described above. For lower frequencies, the lack of adjustment may be explained as follows. Below 4 kHz, ITD and ILD both provide information about the same spatial dimension (azimuth), but the spatial information provided by low-frequency ILD cues is largely redundant with, and less precise than, the information provided by ITD cues (Knudsen et al., 1994
In contrast, best ILDs for higher frequencies were, on average, shifted relative to predicted normal values by larger amounts. Because ILDs at these frequencies indicate the elevation of sound sources in barn owls and are not redundant with the spatial information provided by ITDs, these adjustments were able to improve the accuracy of the representation of auditory space in the tectum, even with full adjustment of ITD tuning. However, in most cases these adjustments still fell substantially short of the acoustic effects of the device and thus may have revealed a limit to the capacity of this pathway to modify frequency-specific ILD tuning.
FOOTNOTES Received June 3, 1999; revised Oct. 8, 1999; accepted Oct. 29, 1999.
This work was supported by the National Institute on Deafness and Other Communication Disorders, National Institutes of Health Grant R01 DC00155-18. We thank Bob Schneeveis for helping to design and construct the acoustic filtering device and Greg Miller, Fred Rieke, Ed Rubel, and Michael Shadlen for helpful comments on this manuscript.
Correspondence should be addressed to Joshua I. Gold, Department of Physiology and Biophysics, University of Washington Medical School, Box 357290, Seattle, WA 98195-7290. E-mail: jig{at}u.washington.edu.
Dr. Gold's present address: Department of Physiology and Biophysics, University of Washington, Seattle, WA 98195-7290.
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