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The Journal of Neuroscience, March 15, 1999, 19(6):2326-2336
Early Visual Experience Shapes the Representation of Auditory Space in the Forebrain Gaze Fields of the Barn Owl
Greg L. Miller and Eric I. Knudsen Department of Neurobiology, Stanford University, Stanford, California 94305
ABSTRACT
Top
Abstract
Introduction
Auditory spatial information is processed in parallel forebrain and midbrain pathways. Sensory experience early in life has been shown to exert a powerful influence on the representation of auditory space in the midbrain space-processing pathway. The goal of this study was to determine whether early experience also shapes the representation of auditory space in the forebrain.
Owls were raised wearing prismatic spectacles that shifted the visual field in the horizontal plane. This manipulation altered the relationship between interaural time differences (ITDs), the principal cue used for azimuthal localization, and locations of auditory stimuli in the visual field. Extracellular recordings were used to characterize ITD tuning in the auditory archistriatum (AAr), a subdivision of the forebrain gaze fields, in normal and prism-reared owls.
Prism rearing altered the representation of ITD in the AAr. In prism-reared owls, unit tuning for ITD was shifted in the adaptive direction, according to the direction of the optical displacement imposed by the spectacles. Changes in ITD tuning involved the acquisition of unit responses to adaptive ITD values and, to a lesser extent, the elimination of responses to nonadaptive (previously normal) ITD values. Shifts in ITD tuning in the AAr were similar to shifts in ITD tuning observed in the optic tectum of the same owls.
This experience-based adjustment of binaural tuning in the AAr helps to maintain mutual registry between the forebrain and midbrain representations of auditory space and may help to ensure consistent behavioral responses to auditory stimuli.
Key words: sound localization; experience-dependent plasticity; archistriatum; forebrain; gaze control; barn owl
INTRODUCTION
The forebrain plays an essential role in directing complex sound localization behaviors (Ravizza and Diamond, 1974
; Heffner and Masterton, 1975
In barn owls, an output structure of the forebrain auditory space-processing pathway is the archistriatal gaze fields (AGFs) (Knudsen et al., 1995
The representation of auditory space that underlies the contribution of the AGF to localization behavior is contained in a subdivision of the AGF, the auditory archistriatum (AAr) (Cohen and Knudsen, 1995
To assess the influence of experience on the representation of auditory space in the AAr, we characterized unit tuning for ITD and ILD in the AAr of owls raised wearing prismatic spectacles that displaced the visual field in the horizontal plane. Because the owl's eyes are essentially stationary in the head, the spectacles altered the relationships between ITD values and locations in the visual field. Prism rearing caused adjustments in ITD tuning that tended to realign the representation of auditory space in the AAr with the optically displaced visual field. This experience-based adjustment of binaural tuning in the AAr helps to maintain mutual registry between the forebrain and midbrain representations of auditory space.
MATERIALS AND METHODS Visual experience. Visual experience was altered by raising owls with prismatic spectacles that shifted the visual field 23° to the left (L23 spectacles) or 23° to the right (R23 spectacles). Wearing prismatic spectacles did not alter the range of ITD or ILD values experienced by the owl (Knudsen and Knudsen, 1989
Adjustments in ITD tuning that tended to realign the auditory representation of space with the optically displaced visual field were considered "adaptive." Thus, for owls raised with right-shifting spectacles (R23 owls), shifts toward left-ear leading values were adaptive, and for owls raised with left-shifting spectacles (L23 owls), shifts toward right-ear leading values were adaptive.
Electrophysiology. Owls were prepared for multiple experiments. Before electrophysiological recordings, an owl was anesthetized with halothane and nitrous oxide, and a headpiece was mounted to the skull. At the same time, a craniotomy was made over the optic tectum and AAr. Chloramphenical antibiotic (0.5%) was applied to the exposed brain surface, and the craniotomy was sealed with dental acrylic. All skin wounds were infused with Xylocaine (2%), and the owl was allowed to recover fully from the anesthetic before being returned to the aviary.
On the day of an experiment, the owl was anesthetized with halothane and nitrous oxide. The owl was then wrapped in a leather harness, suspended in a prone position inside a sound-attenuating chamber (AD2000, Eckel Industries), and secured to a stereotaxic device by its headpiece. The head was positioned using retinal landmarks so that the visual axes were in the horizontal plane, and the dental acrylic was removed from the craniotomy. Light anesthesia was maintained throughout the experiment with the nitrous oxide/oxygen mixture or, occasionally, with nitrous oxide and halothane.
Insulated tungsten microelectrodes (1-3 M
at 1.0 kHz) were positioned stereotaxically and advanced through the brain with a microdrive. A level discriminator was used to isolate units, and the timing of action potentials elicited by auditory stimuli was stored on a computer. To calibrate the position of the electrode in the brain, the electrode was first advanced into the optic tectum. Because the visual map in the optic tectum is precise and well characterized, the position of the electrode within the tectum can be determined from the location of the visual receptive field (VRF) of the recorded units. The AAr is a small structure, ~1 mm3, located approximately 2.0 mm rostral, 0.5 mm lateral, and 3.0 mm dorsal to the representation of 0° azimuth and 0° elevation in the superficial layers of the optic tectum (Cohen and Knudsen, 1995
Throughout an experiment, chloramphenical antibiotic was applied to the exposed brain surface. At the conclusion of an experiment, the craniotomy was resealed with dental acrylic, and an intramuscular injection (2-3 cc) of 2.5% dextrose saline solution was administered. Owls were allowed to recover from the anesthetic before being returned to the aviary.
Auditory stimuli and assessment of binaural tuning. Auditory stimuli were generated digitally and delivered dichotically via earphones (Knowles earphones, model 1914, coupled to damping assemblies BF-1743) placed in the external ear canals. Each earphone was aligned parallel to the long axis of the ear canal and centered within the canal ~5 mm from the tympanic membrane. The timing and level of sound presented at the two ears was under computer control.
Noise-burst (50 msec duration, bandpass 3-12 kHz) stimuli with various ITDs were presented at an average binaural level (the sum of the sound level, in decibels, presented at the two ears divided by two) of 20 dB above threshold. A series of binaural stimuli consisted of noise bursts with different ITD values presented in random order. For each tuning curve, at least 10 series of stimuli were presented. Net response to a noise burst was quantified by subtracting the baseline discharge rate during the 100 msec interval before stimulus presentation from the number of spikes occurring during the 100 msec after stimulus onset. The "best ITD" of a site was defined as the midpoint of the range of ITD values that elicited at least 50% of the maximal response of the site. The range of ITD values that elicited at least 50% of the maximal response defined the "ITD tuning width" of the site (see Fig. 1). The left-ear leading endpoint of this range defined the "left 50% cutoff" of the site, and the right-ear leading endpoint defined the "right 50% cutoff." Tuning for ILD was determined and quantified in an analogous manner. ITD tuning was assessed with ILD held constant at the best ILD value of the site, and vice versa.
Optic tectum sampling. Assessments of experience-dependent shifts in ITD tuning in the optic tectum were made according to a method reported previously (Brainard and Knudsen, 1993
AAr sampling. Unit tuning for ITD and ILD was sampled in five left and seven right AArs in eight owls raised with normal visual experience, in two left and two right AArs in two owls raised with L23 spectacles, and in four left and five right AArs in five owls raised with R23 spectacles.
In contrast to the topographic maps of ITD and ILD found in the midbrain space-processing pathway (Moiseff and Konishi, 1981
Therefore, to assess the effect of prism rearing on the representation of ITD in the AAr, it was necessary to compare ITD tuning across populations of sites in the AAr of prism-reared and normal owls. The technique used for sampling ITD tuning in the AAr was identical for prism-reared and normal owls and was designed to obtain a sample of sites that was representative of the entire population. In each owl, a coarse grid of electrode penetrations was made to determine the extent of the AAr. These grids consisted of series of penetrations separated by 500 µm along the rostrocaudal or mediolateral axis. In some cases, additional penetrations were made at locations between the penetrations of the initial grid. All penetrations were separated by at least 250 µm along the rostrocaudal or mediolateral axis. Within a dorsoventral penetration through the AAr, ITD tuning was assessed at 150-250 µm increments. This method typically produced a sample of 10-30 AAr sites (median, 17).
Composite response curves. Composite response curves were constructed as a graphic representation of population ITD or ILD tuning in the AAr. Composite ITD response curves were constructed by calculating the percentage of sampled sites that responded at or above 50% of their maximal response for each of 21 ITD values that spanned the physiological range of ITDs (200 µsec left-ear leading to 200 µsec right-ear leading) in 20 µsec increments. Composite ITD response curves were constructed for each AAr in which a sample of more than 10 sites was obtained (three left and four right AArs in normal owls; two left and two right AArs in L23 owls; two left and four right AArs in R23 owls). Grand composite ITD response curves were calculated in the same manner and included data from all owls in each condition (i.e., left and right sides of the brain in normal, R23, and L23 owls). Grand composite ILD response curves were constructed by calculating the percentage of sampled sites that responded at or above 50% of their maximal response for each of 13 ILD values that spanned the physiological range of ILDs (30 dB left-ear greater to 30 dB right-ear greater) in 5 dB increments. The weighted averages of composite response curves were calculated and used as an indicator of population ITD (or ILD) tuning.
RESULTS Representation of ITD in the optic tectum
Recordings were made first in the optic tectum of prism-reared owls to verify that prism rearing had altered the representation of ITD in the midbrain space-processing pathway of each owl. Shifts in ITD tuning for single tecta ranged from 14 to 51 µsec (median shift, 28 µsec) and were always in the adaptive direction.
Representation of ITD in the AAr of owls raised with normal visual experience
As reported previously (Cohen and Knudsen, 1995
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Figure 1. ITD tuning curve collected at a single site in the AAr of an owl raised with normal visual experience. The black line indicates the range of ITD values that elicited at least 50% of the maximal response for this site (the "ITD tuning width" of the site). The endpoints of this range defined the "left 50% cutoff" and "right 50% cutoff" for this site.
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Figure 2. Representation of ITD in the AAr of owls raised with normal visual experience. A, B, Horizontal lines indicate the ranges of ITD values that elicited at least 50% of the maximal response for sites in the left (n = 61) and right (n = 76) AAr. The endpoints of each line indicate the left and right 50% cutoffs. Gray bars indicate the range of ITDs that elicited 50% of the maximal response for
Representation of ITD in the AAr of prism-reared owls
The representation of ITD in the left and right AAr of an owl raised wearing R23 spectacles is shown in Figure 3. On both sides of the brain, an increased percentage of sites responded strongly to left-ear leading ITD values. For example, the percentage of sites that responded at or above 50% of their maximal response to 60 µsec left-ear leading ITD was increased relative to normal (52 vs 11% in the left AAr; 59 vs 32% in the right AAr). In contrast, the percentage of sites that responded at or above 50% of their maximal response to 0 µsec ITD was smaller in both AArs (31 vs 64% in the left AAr; 24 vs 58% in the right AAr). The weighted averages of the composite ITD response curves for the left and right AAr in this owl were shifted toward left-ear leading by 54 and 18 µsec, respectively, relative to the weighted averages of the corresponding normal grand composite response curves. The direction of this shift was adaptive for R23 spectacles.
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Figure 3. Representation of ITD in the left and right AAr of an owl raised with R23 spectacles. A, B, Horizontal lines indicate the ranges of ITD values that elicited at least 50% of the maximal response for sites in the left (n = 29) and right (n = 17) AAr. Dark circles indicate the 50% cutoff values on the adaptive flank of the ITD tuning curve (the left 50% cutoffs) for each site, and open circles indicate the 50% cutoff values on the nonadaptive flank (the right 50% cutoffs). Gray bars indicate the range of ITDs that elicited
The representation of ITD in the left and right AAr of an owl raised wearing L23 spectacles is shown in Figure 4. Relative to normal, a greater percentage of sites responded strongly to right-ear leading ITD values in this owl. In the left AAr, 89% of sites responded at or above 50% of their maximal response to 60 µsec right-ear leading ITD, compared with only 31% in normal owls. In the right AAr, 36% of sites responded at or above 50% of their maximal response to 60 µsec right-ear leading ITD, compared with only 3% in normal owls. The percentage of sites that responded at or above 50% of their maximal response to 0 µsec ITD was smaller in both AArs (35 vs 64% in the left AAr; 43 vs 58% in the right AAr). The weighted averages of the composite ITD response curves for the left and right AArs were shifted toward right-ear leading by 42 and 37 µsec, respectively, relative to the weighted averages of the corresponding normal grand composite response curves. The direction of this shift was adaptive for L23 spectacles.
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Figure 4. Representation of ITD in the left and right AAr of an owl raised with L23 spectacles. A, B, Horizontal lines indicate the ranges of ITD values that elicited at least 50% of the maximal response for sites in the left (n = 26) and right (n = 14) AAr. Dark circles indicate the 50% cutoff values on the adaptive flank of the ITD tuning curve (the right 50% cutoffs) for each site, and open circles indicate the 50% cutoff values on the nonadaptive flank (the left 50% cutoffs). The gray bar indicates the range of ITDs that elicited
Although the weighted averages of all composite ITD response curves for prism-reared owls were shifted in the adaptive direction relative to the weighted averages of the corresponding normal grand composite response curve, we observed considerable variability in the composite response curves obtained from different owls (Fig. 5). The shapes of the curves varied from owl to owl, as did the magnitude of ITD shifts in prism-reared owls. To determine whether shifts in ITD tuning had occurred in the AAr of individual prism-reared owls, we compared distributions of left and right 50% ITD cutoff values from the AAr of each prism-reared owl to the corresponding distributions of 50% ITD cutoff values for all normal owls. For all four AArs sampled in L23 owls, the distributions of left and right 50% cutoffs were shifted in the adaptive direction relative to normal (Mann-Whitney U test, p < 0.05). For four of the six AArs sampled in R23 owls, the distributions of left and right 50% ITD cutoffs were shifted in the adaptive direction relative to normal (Mann-Whitney U test, p < 0.05). Thus, of the 20 distributions of 50% ITD cutoff values obtained in prism-reared owls (left and right cutoffs for 10 AArs), 16 were shifted in the adaptive direction. The same analysis was also applied to normal owls. Distributions of 50% ITD cutoff values for each normal owl were compared with the corresponding distributions of 50% ITD cutoff values for all other normal owls. Of the 14 distributions of 50% ITD cutoff values obtained in normal owls (left and right cutoffs for seven AArs), only two differed significantly from the distributions of cutoff values for the other normal owls.
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Figure 5. Individual variability of ITD representation in the AAr. Composite ITD response curves for each AAr in which a sample of more than 10 sites was obtained. A,D, Normal owls (3 left AArs, 4 right AArs). B,E, L23 owls (2 left AArs, 2 right AArs). C,F, R23 owls (2 left AArs, 4 right AArs). The gray curve in each panel is the normal grand composite ITD response curve for the corresponding side of the brain (from Fig. 2C,D).
Grand composite ITD response curves were constructed using data from all sites recorded in the AAr of all prism-reared owls (Fig. 6). In prism-reared owls, weighted averages for the grand composite response curves were shifted in the adaptive direction for the optical displacement imposed by the spectacles. In the left AAr (Fig. 6A), the weighted average of the grand composite curve for L23 owls was shifted toward right-ear leading (54 µsec right-ear leading vs 16 µsec right-ear leading for normal owls), and the weighted average for R23 owls was shifted toward left-ear leading (1 µsec left-ear leading vs 16 µsec right-ear leading). Similarly, in the right AAr (Fig. 6B), the weighted average of the grand composite curve for L23 owls was shifted toward right-ear leading (17 µsec right-ear leading vs 27 µsec left-ear leading for normal owls), and the weighted average for R23 owls was shifted toward left-ear leading (58 µsec left-ear leading vs 27 µsec left-ear leading).
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Figure 6. Summary of ITD representation by condition. Grand composite response curves constructed with data from all sites recorded in prism-reared owls. Gray curves are the grand composite ITD response curves for all normal owls for the corresponding sides of the brain (from Fig. 2C,D). A, Left AAr (normal owls, 61 sites from 5 AArs; L23 owls, 46 sites from 2 AArs; and R23 owls, 91 sites from 4 AArs). B, Right AAr (normal owls, 76 sites from 7 AArs; L23 owls, 25 sites from 2 AArs; and R23 owls, 84 sites from 5 AArs).
Shifts of the adaptive and nonadaptive flanks of ITD tuning curves
The observed shifts in the composite response curves of prism-reared owls could result from the acquisition of responses to adaptive ITD values, the elimination of responses to nonadaptive (previously normal) ITD values, or both. Inspection of composite response curves from individual owls (Figs. 3-5) and from all owls combined (Fig. 6) suggests that both processes were involved, although to different degrees. In nearly all cases, the shift appeared to be greater for the adaptive flank (the right-ear leading flank for owls raised with L23 spectacles; the left-ear leading flank for owls raised with R23 spectacles).
To quantify the relative shifts of the adaptive and nonadaptive flanks, we examined distributions of 50% ITD cutoff values for normal and prism-reared owls (Fig. 7). In each of the four prism-reared conditions (L23 spectacles, left AAr; L23 spectacles, right AAr; R23 spectacles, left AAr; and R23 spectacles, right AAr), the distribution of 50% cutoff values on the adaptive flank was shifted in the adaptive direction (Fig. 7A; two-tailed t test). For L23 owls, the distribution of right 50% cutoff values was shifted toward right-ear leading relative to normal on both the left (p < 0.0001) and right (p < 0.0001) sides of the brain (Fig. 7A, striped bars). On the left side of the brain, the mean right 50% cutoff value was 94 µsec right-ear leading (SD = 47 µsec; n = 46 sites) compared with 45 µsec right-ear leading (SD = 41 µsec; n = 61 sites) in normal owls; on the right side of the brain, the mean right 50% cutoff value was 57 µsec right-ear leading (SD = 61 µsec; n = 25 sites) compared with 5 µsec right-ear leading (SD = 33 µsec; n = 76 sites) in normal owls. For R23 owls, the distribution of left 50% cutoff values was shifted toward left-ear leading relative to normal on the left (p = 0.006) and right (p < 0.0001) sides of the brain (Fig. 7A, cross-hatched bars). On the left side of the brain, the mean left 50% cutoff value was 40 µsec left-ear leading (SD = 60 µsec; n = 91 sites) compared with 16 µsec left-ear leading (SD = 38 µsec; n = 61 sites) in normal owls; on the right side of the brain, the mean left 50% cutoff value was 92 µsec left-ear leading (SD = 46 µsec; n = 84 sites) compared with 50 µsec left-ear leading (SD = 39 µsec; n = 76 sites) in normal owls. Averaged across all prism-reared conditions, the mean 50% cutoff value on the adaptive side was shifted 42 µsec in the adaptive direction.
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Figure 7. Shifts of adaptive and nonadaptive flanks of ITD tuning curves. Bars indicate the mean 50% cutoff values of all ITD tuning curves recorded in the AAr of normal (gray bars), L23 (striped bars), and R23 owls (cross-hatched bars). A, The adaptive flank is the side of the ITD tuning curve in the adaptive direction (the left-ear leading flank for owls raised wearing R23 spectacles and the right-ear leading flank for owls raised wearing L23 spectacles). B, The nonadaptive flank is the side of the ITD tuning curve opposite to the adaptive direction (the right-ear leading flank for owls raised with L23 spectacles and the left-ear leading flank for owls raised with R23 spectacles). Error bars indicate SEM. Asterisks indicate conditions for which flanks in prism-reared owls were significantly different from normal.
For three of the four prism-reared conditions, the distribution of 50% cutoff values on the nonadaptive side of the tuning curve was also shifted in the adaptive direction (Fig. 7B; two-tailed t test). For L23 owls, the distribution of left 50% cutoff values was shifted toward right-ear leading relative to normal on the left (p = 0.0003) and right (p = 0.0002) sides of the brain (Fig. 7B, striped bars). On the left side of the brain, the mean left 50% cutoff value was 13 µsec right-ear leading (SD = 43 µsec; n = 46 sites) compared with 16 µsec left-ear leading (SD = 38 µsec; n = 61 sites) in normal owls; on the right side of the brain, the mean left 50% cutoff value was 8 µsec left-ear leading (SD = 70 µsec; n = 25 sites) compared with 50 µsec left-ear leading (SD = 39 µsec; n = 76 sites) in normal owls. For R23 owls, the distribution of right 50% cutoff values was shifted toward left-ear leading relative to normal on the right side of the brain (Fig. 7B, cross-hatched bars; p = 0.0003). On the right side of the brain, the mean right 50% cutoff value was 17 µsec left-ear leading (SD = 41 µsec; n = 84 sites), compared with 5 µsec right-ear leading (SD = 33 µsec; n = 76 sites) in normal owls. On the left side of the brain, the distribution of 50% cutoff values was not significantly shifted relative to normal (p = 0.13). The mean right 50% cutoff value was 31 µsec right-ear leading (SD = 62 µsec; n = 91 sites) compared with 45 µsec right-ear leading (SD = 41 µsec; n = 61 sites) in normal owls. Averaged across all prism-reared conditions, the mean 50% cutoff value on the nonadaptive side was shifted 27 µsec in the adaptive direction.
The difference in the degree of shift observed for the adaptive and nonadaptive flanks of ITD tuning curves predicts that ITD-tuning widths in prism-reared owls were increased relative to normal. Indeed, tuning widths were significantly broader in prism-reared owls (Fig. 8; Mann-Whitney U test, p < 0.0001). The median ITD tuning width in normal owls was 52 µsec (n = 137), and the median ITD tuning width in prism-reared owls was 71 µsec (n = 246).
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Figure 8. Distributions of ITD tuning widths in normal (A) and prism-reared (B) owls.
The representation of ILD in the AAr of prism-reared owls
For frequencies <4 kHz, ILD, like ITD, varies with sound source azimuth. For frequencies >4 kHz, however, ILDs vary primarily with sound source elevation (because of the asymmetrical orientation of the owl's ears) and are the principal cues for elevational localization. Because the majority of sites in the AAr are tuned to frequencies >4 kHz (Cohen and Knudsen, 1995
Grand composite ILD response curves for the left and right AAr in normal and prism-reared owls are shown in Figure 9. For owls raised wearing R23 spectacles, the grand composite ILD response curves on both sides of the brain were shifted toward left-ear greater ILDs relative to normal by 3 and 5 dB, respectively. No shift in ILD tuning was apparent in L23 owls.
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Figure 9. Summary of ILD representation by condition. Grand composite response curves constructed with data from all sites recorded in prism-reared owls. Gray curves are the grand composite ILD response curves for all normal owls for the corresponding sides of the brain. A, Left AAr (normal owls, 41 sites from 4 AArs; L23 owls, 42 sites from 2 AArs; and R23 owls, 96 sites from 4 AArs). B, Right AAr (normal owls, 63 sites from 7 AArs; L23 owls, 26 sites from 2 AArs; and R23 owls, 85 sites from 5 AArs).
Analysis of the 50% cutoffs for ILD tuning curves was consistent with this trend (Fig. 10). For R23 owls, the distribution of left 50% cutoff values was significantly shifted toward left-ear greater on the right side of the brain (Fig. 10A, cross-hatched bars; two-tailed t test, p = 0.001; n = 85 sites from R23 owls; n = 63 sites from normal owls). No shift was observed on the left side of the brain (p = 0.13; n = 96 sites from R23 owls; n = 41 sites from normal owls). Distributions of right 50% cutoff values for R23 owls were significantly shifted toward left-ear greater on both the left (p = 0.0015; n = 85 sites from R23 owls; n = 63 sites from normal owls) and the right (p < 0.0001; n = 96 sites from R23 owls; n = 41 sites from normal owls) sides of the brain (Fig. 10B, cross-hatched bars). For L23 owls, there was no significant difference in the distributions of 50% cutoffs on either side of the brain (Fig. 10 A,B, striped bars; left cutoff, left side of the brain: p = 0.89, n = 42 sites from L23 owls, n = 41 sites from normal owls; left cutoff, right side of the brain: p = 0.68, n = 26 sites from L23 owls, n = 63 sites from normal owls; right cutoff, left side of the brain: p = 0.34, n = 42 sites from L23 owls, n = 41 sites from normal owls; and right cutoff, right side of the brain: p = 0.42, n = 26 sites from L23 owls, n = 63 sites from normal owls).
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Figure 10. Effect of prism rearing on the flanks of ILD tuning curves. Bars indicate the mean 50% cutoff values of all ILD tuning curves recorded in the AAr of normal (gray bars), L23 (striped bars), and R23 (cross-hatched bars) owls. A, Left-ear greater flanks. B, Right-ear greater flanks. Error bars indicate SEM. Asterisks indicate conditions for which flanks in the prism-reared owls were significantly different from those in normal owls.
DISCUSSION These results demonstrate that the representation of auditory space in the barn owl forebrain is shaped by visual experience during early life. Raising owls with prismatic spectacles that displaced the visual field in the horizontal plane altered the ITD tuning of units in the AAr, an output structure of the forebrain space-processing pathway. Shifts in ITD tuning were dependent on the direction of optical displacement imposed by the spectacles and were in the direction appropriate to align the representation of auditory space with the owls' optically displaced visual fields (Figs. 3-7).
The effect of prism rearing on ILD tuning in the AAr was less consistent. Some evidence of an ILD tuning shift toward left-ear greater values was observed for R23 owls, but no shift was apparent for L23 owls (Figs. 9, 10). We did not expect that the horizontally displacing spectacles used in this study would cause substantial changes in ILD tuning. The majority of sites in the AAr are tuned to frequencies >4 kHz (Cohen and Knudsen, 1995
Limitations of the sampling technique
Because of the clustered organization of auditory space in the AAr, it was not possible to assess changes in binaural tuning caused by prism rearing at individual sites. Therefore, the argument that prism rearing shapes the representation of auditory space in the AAr must be based on changes in binaural tuning across a population of sites.
In principle, the observed differences in ITD tuning could result from a bias in the sampling of sites within the AAr. For several reasons, we believe that this is not likely to be the case. First, the sampling technique was designed to minimize the likelihood that samples of ITD tuning data recorded from individual AAr would be dominated by data from one or two clusters of similarly tuned sites: electrode penetrations were distributed throughout the extent of the AAr, and ITD tuning was assessed at sites that were separated by at least 150 µm along the dorsoventral axis and at least 250 µm along the rostrocaudal and mediolateral axes. Second, the sampling technique used in normal and prism-reared owls was identical. Finally, both leftward and rightward shifts in ITD tuning were observed on both sides of the brain in prism-reared owls, and these shifts were always in the direction that was adaptive for the experienced displacement of the visual field.
In these experiments, it was not possible to determine whether prism rearing affected different regions of the auditory space representation differently. In the optic tectum, spatial tuning is consistently altered only for sites that represent the region of space displaced by the prismatic spectacles (Knudsen et al., 1991
Inferred changes in ITD tuning at individual sites
The observed shifts in ITD tuning could reflect the acquisition of responses to adaptive ITD values, the elimination of responses to nonadaptive ITD values, or both. Our data suggest that both processes are involved, although to different degrees. In prism-reared owls, the adaptive flanks of ITD tuning curves, as indicated by 50% cutoff values, shifted 42 µsec in the adaptive direction on average, whereas the nonadaptive flanks shifted only 27 µsec. For each of the four prism-reared conditions, adaptive flanks shifted more than nonadaptive flanks (Fig. 7). The finding that ITD tuning widths were greater in prism-reared owls (Fig. 8) is consistent with the interpretation that, on average, sites in the AAr of prism-reared owls expanded the range of ITDs to which they responded in the adaptive direction more than they eliminated responses to ITDs in the nonadaptive direction.
Adaptive nature of observed plasticity
Adaptive adjustments of auditory space coding occurred in the presence of essentially normal auditory experience: prism rearing changed the relationships between specific cue values and locations in the visual field, but did not alter the range of cue values experienced. This finding is consistent with the proposed involvement of the AAr in gaze control (Knudsen et al., 1995
Comparison to experience-dependent plasticity in the midbrain
Prism rearing causes adaptive changes in unit tuning for ITD in the midbrain space-processing pathway of the barn owl (Brainard and Knudsen, 1993
Implications for site of plasticity
The representation of auditory space in the AAr is derived independently of input from auditory space maps in the midbrain. Bilateral ablation of the external nucleus of the inferior colliculus (ICX), the structure where the midbrain map of auditory space is first synthesized, does not alter binaural tuning in the AAr (Cohen et al., 1998
Comparison to other models of experience-dependent plasticity in the auditory forebrain
Many previous studies of experience-dependent plasticity in the auditory forebrain have focused on changes in frequency tuning or tonotopic organization in the primary auditory cortex that are induced by deprivation of afferent input or by behavioral training in adult animals (e.g., Bakin and Weinberger, 1990
Another excellent example of developmental, experience-dependent plasticity in the representation of high-order stimulus parameters in the auditory forebrain is the emergence of song-selective neurons in the forebrain of songbirds (Margoliash, 1983
FOOTNOTES Received Oct. 26, 1998; revised Dec. 17, 1998; accepted Jan. 5, 1999.
This work was supported by National Research Service Award MH11238 to G.L.M., by the National Institute on Deafness and Other Communication Disorders, National Institutes of Health Grant R01 DC00155-188, and by a McKnight Senior Investigator Award to E.I.K. We are grateful to Yale E. Cohen and members of the Knudsen laboratory for thoughtful comments on an earlier version of this manuscript.
Correspondence should be addressed to Greg L. Miller, Department of Neurobiology, Fairchild Building, Stanford University School of Medicine, Stanford, CA 94305.
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