Abnormal auditory experience induces frequency-specific adjustments in unit tuning for binaural localization cues in the optic tectum of juvenile owls

Abstract

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 approximately 55 microsec toward open-ear leading for 4 kHz stimuli and 15 microsec 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 approximately 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.

Fig. 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 = −0.04x + 7.0;r² = 0.38; ANOVA,p < 0.001). B, Response threshold as a function of the center frequency of the narrowband (1 kHz bandwidth) stimulus. Responses were measured using the best ITD–ILD pair for the given stimulus at 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 barsindicate medians, quartiles, and 10^th–90^th percentiles, respectively, of binned data. C, Strength of response as a function of the center frequency of the narrowband (1 kHz bandwidth) stimulus, normalized to the maximum response elicited by any 1-kHz-wide stimulus at the same recording site. Responses were measured as inB at sites with visual RFs between L25° and R25° az.Thick lines, boxes, and bars as inB. D, Data measured as inC, but at sites with visual RFs more peripheral than 25° az. The solid line is a linear fit to the data (y = −13.5x + 136.9;r² = 0.65; ANOVA,p < 0.001).

Fig. 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 inbold.

Fig. 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 = −72 μsec, ILD = +3 dB. B, Maximum response = 0.8 spikes per stimulus at ITD = +50 μsec, ILD = +6 dB (presented at 30 dB above the threshold measured with the 4 kHz stimulus).C, Maximum response = 6.2 spikes per stimulus at ITD = −106 μsec, ILD = +3 dB.

Fig. 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 10^th–90^th 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= −10.0x + 111.5; r² = 0.34; ANOVA, p < 0.001).

Fig. 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. Thesolid 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.

Fig. 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

Fig. 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 −10° and + 15° el. A, Best ITD as a function of center stimulus frequency. Each line connects points representing measurements taken at a single recording site (n = 32). B, Best ITDs for low-frequency (3, 5 kHz), and high-frequency (7, 9 kHz) stimuli as functions of visual RF azimuth. Linear least-squares fits are shown for the low- (solid line; y = 2.3x − 1.7; r² = 0.93) and high- (dashed line; y = 2.1x − 0.9;r² = 0.89) frequency data, both of which were highly significant (ANOVA, p < 0.001). C, Best ITD relative to the acoustic ITD produced by a source located at the visual RF of the site as a function of the center stimulus frequency; the two were not correlated (ANOVA,p = 0.85). the center frequency of the given range (e.g., offset by integer multiples of 143 μsec for a 7 kHz tone). 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. 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 for sound sources located in the center of this visual RF of the site (circles).

Fig. 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.

Fig. 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). At 38 sites, ITD tuning curves had multiple peaks, which are shown inbold. ITD tuning fell into three categories that roughly corresponded to regions representing space to the far left (visual RF az, ≥L25°; panels B, E, and H), directly ahead (visual RF az between L25° and R25°; panelsC, F, and I), and to the far right (visual RF az, ≥R25°; panels D, G, andJ). B–D, Examples of ITD tuning curves from device-reared (solid) and normal (dashed) owls. In each panel, curves were measured at sites with matching visual RF locations (visual RF azimuths were L40°, L2° and R41°, respectively). Distributions of the differences between best ITDs and the normal regression (E–G) and of ITD tuning widths (H–J) are shown for each region: far left, mean ± SD difference = −77 ± 18 μsec (E), mean ± SD width = 60 ± 23 μsec (H). Middle, Difference = −42 ± 45 μsec (F), width = 46 ± 22 μsec (I).Far right, Difference = 2 ± 16 μsec (G), width = 53 ± 11 μsec (J). The dashed lines in E–Jrepresent mean ± SD values in normal owls. pvalues from unpaired t tests comparing the given distribution of data with comparable data from normal owls are shown inE–J.

Fig. 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 −17° and +27° el.A, Best ITD as a function of center stimulus frequency. Each line connects points representing measurements taken at a single recording site. The open circlesrepresent frequencies that did not elicit strong enough responses to measure ITD tuning at the given sites. B, Best ITDs for low-frequency (3, 5 kHz) or high-frequency (7, 9 kHz) stimuli as functions of visual RF azimuth. Linear fits are shown for the low- (solid line; y = 2.9x − 55.2;r² = 0.91) and high- (dashed line; y = 3.0x − 8.0;r² = 0.54) frequency data, both of which were highly significant (ANOVA, p < 0.001). C, Best ITD relative to the acoustic ITD produced by a source located at the visual RF of the site as a function of the center frequency of the narrowband stimulus. Data are from sites with visual RFs between L25° and R25° az. For ITD tuning curves with two peaks within the range of ITDs tested, both peaks are shown inbold. Dashed lines and shaded regionsrepresent the median values and the ranges, respectively, of phase-equivalent shifts in the timing of sound reaching the right eardrum caused by insertion of the acoustic filtering device (cochlear microphonic measurements from five owls; Gold and Knudsen, 1999).

Fig. 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 (−47 ± 19 μsec; mean ± SD) and right (−58 ± 14 μsec) tecta differed significantly (unpaired t test,p < 0.001). B, ITD shifts for 6 kHz stimuli did not significantly regress as a function of visual RF azimuth (r² = 0.09; ANOVA,p = 0.08). C, The solid lines are linear least-squares fits to the two distributions (y = −0.5x + 22.5;r² = 0.20 above andy = −0.6x − 100.8;r² = 0.20 below; ANOVA,p < 0.001 in both cases). Trianglesindicate best values from tuning curves with a single peak within the range of ITDs tested.

Fig. 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.

Fig. 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).

Fig. 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.

Fig. 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). The solid line is a linear fit to the data from device-reared owls (y = 0.3x − 3.2; r² = 0.31; ANOVA, p < 0.001). B, Distribution of best ILDs relative to the normal regression; mean ± SD = −6.6 ± 4.4 dB. C, ILD tuning widths for the data in A; mean ± SD = 8.6 ± 3.3 dB. Thedashed line indicates the mean ILD tuning width measured in normal owls. D, Best ILDs relative to the normal regression as a function of visual RF azimuth. The solid line is a linear fit to the data that indicated a weak dependence of best ILD shift on visual RF azimuth (y = 0.06x − 6.8;r² = 0.09; ANOVA,p < 0.001).

Fig. 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. Eachline 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. Thedashed 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).