Department of Neurobiology, Stanford University, Stanford, California 94305-5125
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ABSTRACT |
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Gold, Joshua I. and Eric I. Knudsen. Adaptive Adjustment of Connectivity in the Inferior Colliculus Revealed by Focal Pharmacological Inactivation. J. Neurophysiol. 85: 1575-1584, 2001. In the midbrain sound localization pathway of the barn owl, a map of auditory space is synthesized in the external nucleus of the inferior colliculus (ICX) and transmitted to the optic tectum. Early auditory experience shapes these maps of auditory space in part by modifying the tuning of the constituent neurons for interaural time difference (ITD), a primary cue for sound-source azimuth. Here we show that these adaptive modifications in ITD tuning correspond to changes in the pattern of connectivity within the inferior colliculus. We raised owls with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. As reported previously, device rearing shifted the representation of ITD in the ICX and tectum but not in the primary source of input to the ICX, the central nucleus of the inferior colliculus (ICC). We applied the local anesthetic lidocaine (QX-314) iontophoretically in the ICC to inactivate small populations of neurons that represented particular values of frequency and ITD. We measured the effect of this inactivation in the optic tecta of a normal owl and owls raised with the device. In the normal owl, inactivation at a critical site in the ICC eliminated responses in the tectum to the frequency-specific ITD value represented at the site of inactivation in the ICC. The location of this site was consistent with the known pattern of ICC-ICX-tectum connectivity. In the device-reared owls, adaptive changes in the representation of ITD in the tectum corresponded to dramatic and predictable changes in the locations of the critical sites of inactivation in the ICC. Given that the abnormal representation of ITD in the tectum depended on frequency and was likely conveyed directly from the ICX, these results suggest that experience causes large-scale, frequency-specific adjustments in the pattern of connectivity between the ICC and the ICX.
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INTRODUCTION |
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Early experience can have a
profound influence on the representation of sensory information in the
brain. This influence is thought to involve plasticity in the
connectivity between neurons, which can shape their stimulus
selectivity and other complex response properties (Buonomano and
Merzenich 1998). A prerequisite for understanding the
mechanisms responsible for this kind of plasticity is the
identification of sites in the nervous system where experience-induced changes in connectivity take place. Here we use the technique of
reversible, focal inactivation of neurons with the anesthetic lidocaine
(QX-314) to identify auditory experience-induced changes in functional
connectivity in the midbrain auditory localization pathway of the barn owl.
The midbrain of birds and mammals contains a map of auditory space that
is based on the tuning of neurons for sound localization cues, such as
interaural time differences (ITDs) and interaural level differences
(ILDs) (Carlile and King 1994; Olsen et al. 1989
; Wise and Irvine 1985
). In the barn owl,
this map is created by merging information about cues across frequency
channels to eliminate ambiguities that are inherent to individual cues
(Brainard et al. 1992
). This merging of information
occurs in the projection from the tonotopically organized central
nucleus of the inferior colliculus (ICC) to its space-mapped external
nucleus (ICX).
The map of auditory space in the ICX is shaped by experience. The
shaping influence of experience on the space map is typically assessed
in the optic tectum (also called the superior colliculus), which
receives the map by a topographic projection from the ICX. For example,
raising owls with abnormal auditory experience has been shown to cause
adaptive adjustment of the tectal space map (Gold and Knudsen
1999; Knudsen 1983
, 1985
). This adjustment
corresponds to changes in unit tuning for ITD and ILD in both the ICX
and tectum (Gold and Knudsen 2000a
,b
; Mogdans and
Knudsen 1992
, 1993
).
The same auditory manipulations that alter auditory tuning in the ICX
and tectum have little or no effect on the representations of binaural
cues in the ICC (Gold and Knudsen 2000b; Mogdans
and Knudsen 1994
). Because the ICC projects directly to the
ICX, these data suggest that plasticity occurs in the pattern of
ICC-ICX connectivity (Fig. 1). Indeed,
visual experience-induced adjustment of the space map in the ICX (and
tectum) is associated with systematic changes in the anatomical
projection from the ICC to the ICX (Feldman and Knudsen
1997
).
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In this study, we used focal pharmacological inactivation in the ICC to
test whether changes in the midbrain space map that are induced by
abnormal auditory experience are accompanied by changes in ICC-ICX
connectivity. We found that auditory experience-induced changes in unit
tuning for ITD in the tectum (and equivalent changes in the ICX)
(Gold and Knudsen 2000b) corresponded to changes in the
locations of the ICC units that drove the tectal responses. The results
indicate that changes in functional connectivity within the inferior
colliculus can account for the adaptive adjustment of the midbrain
auditory space maps.
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METHODS |
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Auditory experience
We raised four barn owls (Tyto alba), three with an
acoustic filtering device implanted chronically in the right ear to
alter auditory experience and one without a device. The device was a custom-designed plastic chamber that was sutured in the right ear canal
and rested just behind the preaural flap and in front of the facial
ruff feathers. A more detailed description of the device, including
cochlear microphonic measurements of its frequency-specific effects on
sound timing and level, can be found in Gold and Knudsen (1999). All four owls were used in previous studies
(Gold and Knudsen 1999
, 2000a
,b
).
The owls were initially raised in brooding boxes with their siblings.
At ~25 days of age, the owls were anesthetized with halothane (1%)
in a mixture of oxygen and nitrous oxide (5:4) and dense-foam-rubber
earplugs (E.A.R. Cabot) were sutured into both ear canals. The
earplugs, which attenuate frequencies between 2 and 8 kHz by ~20-40
dB (Knudsen et al. 1984), were used to limit auditory
experience while the owls' ear canals were open but not yet large
enough to accommodate the acoustic device. At ~35 days of age, the
owls were re-anesthetized, the binaural foam plugs were removed, and
the acoustic device was sutured into the right ear canal. Each owl was
then placed in an individual cage located next to a large flight cage
that housed many adult owls, providing a rich visual and auditory
environment. When the owls could fly, at ~60 days of age, they were
placed in the large flight cage.
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
Owls were prepared for electrophysiological measurements as
described in detail elsewhere (Gold and Knudsen 2000b).
Briefly, each owl was anesthetized with halothane (1%) in a mixture of oxygen and nitrous oxide (5:4), a stainless steel plate was cemented to
the base of the skull, and small craniotomies were made. All incised
tissues were infused with lidocaine, treated with betadine, and sutured
back together. To begin each recording session, the owl was
anesthetized with halothane and nitrous oxide, wrapped in a soft
leather jacket, and given an intramuscular injection of 2.5% dextrose
in sterile saline. The acoustic device was removed, and the eardrum and
ear canal were inspected for damage and cleaned of earwax. The owl was
suspended in a prone position in a stereotaxic apparatus located in a
sound-attenuated chamber. The owl's head was held in place with the
surgically implanted steel plate and positioned using retinal landmarks.
Unit activity was recorded extracellularly with tungsten
microelectrodes (1-2 M at 1 kHz). A level discriminator was used to
isolate action potentials ("spikes") generated by a small number of
nearby neurons. For each sound presentation, the response was calculated as the number of spikes in the 100 ms immediately following stimulus onset minus the number of spikes in the 100 ms immediately preceding stimulus onset.
Nitrous oxide was normally administered continuously through the course of the experiment. At the end of a session, the craniotomy was bathed in chloramphenicol (0.5%) and re-sealed with dental acrylic, and the device was sutured back into place. The owl was placed under a heat lamp and monitored until fully recovered (~1-2 h).
Dichotic stimulation
Dichotic stimuli consisted of digitally filtered broadband (3-12 kHz passband) and narrowband (1-kHz bandwidth centered on the given frequency) noise bursts, 50 ms in duration, with 0- and 5-ms rise/fall times, respectively. Sounds were presented via matched Knowles earphones (ED-1914) coupled to damping assemblies (BF-1743), placed ~5 mm from each tympanic membrane. The frequency response of each earphone was flat to within ±2 dB from 3 to 10 kHz. For a given ITD, ILD, or frequency tuning curve, the peak width was defined as the range of stimulus values that elicited a response >50% of the maximum response. The best value was defined as the center of this range. Positive and negative ITD values refer to right- and left-ear leading, respectively.
Iontophoresis protocol
Iontophoresis electrodes were made by pulling a five-barrel
glass capillary (WPI) that had a 7-µm carbon fiber (Amoco Performance Products, Alpharetta, GA) inserted into the central barrel
(Armstrong-James and Millar 1979). The tips of the
electrode were cut so that the inner diameter of each outer barrel was
1-3 µm and the tips were flush with the carbon fiber. The central
barrel was filled with 1 M NaCl to make contact with the carbon fiber
for recording. A chloride-coated silver wire made contact with the
solution in each barrel. QX-314 (Research Biochemicals), a quaternary
lidocaine derivative, was used to block fast,
Na+-dependent action potentials (Connors
and Prince 1982
) in the ICC. Two of the four outer barrels of
the iontophoresis electrode were filled with 2% QX-314 solution in
dH2O (58 mM), with HCl, NaOH, or both added to
achieve a pH of 6.5. The lidocaine solution was applied by
iontophoresis (NeuroData IPX-5), typically using 90-nA injection
currents through each of two barrels. Before and after injections, a
10-nA retaining current was applied to the lidocaine-filled barrels.
Experimental protocol
ITD is represented systematically along the rostrocaudal axes of
the ICC, ICX, and tectum as described in Fig.
2A. We recently demonstrated
that device rearing causes adaptive shifts in the representation of ITD
in both the optic tectum and the ICX (Gold and Knudsen
2000a,b
). In contrast, device rearing does not affect the
representation of ITD in the ICC. As shown in Fig. 2B,
changes in the pattern of ICC-ICX connectivity could, in principle,
account for these device-induced shifts. According to this model, the ICX-tectum connections remain unchanged, and the adaptive response properties created in the ICX are conveyed along normal projections to
the optic tectum.
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We tested this model by recording from neurons in the tectum while simultaneously inactivating local regions of the ICC in both normal and device-reared owls. The idea was to test whether device rearing changed the locations of the ICC units that drove the tectal responses. We measured the effects of ipsilateral ICC inactivation on responses in the tectum and not the ICX because it was easier to place electrodes simultaneously in the ICC and tectum than in the ICC and ICX.
The optic tectum was targeted stereotaxically and was recognized by
characteristic bursting activity and spatially restricted auditory and
visual receptive fields (RFs) (Knudsen 1982). Electrode position within the tectum was determined on the basis of visual RF
location, which was used to determine predicted normal ITD values
(Olsen et al. 1989
). The inferior colliculus was
targeted stereotaxically by positioning the electrode relative to the
tectal representation of frontal space. Within the inferior colliculus, the lateral shell of the ICC was recognized using a number of criteria,
including stereotaxic position, response latencies, sensitivity for
interaural level difference (ILD), width of frequency tuning, and
progression of best frequency with dorsoventral depth (Gold and
Knudsen 2000b
).
With the injection electrode positioned in the lateral shell, a tungsten electrode was positioned in the ipsilateral tectum. In most cases, we targeted tectal sites with a best ITD and best ILD that matched the best values at the ICC site, using a narrowband stimulus with a center frequency that matched the best frequency at the ICC site (typically ~4 kHz). We also measured ITD tuning at the tectal recording site using a narrowband stimulus with a center frequency that did not match the best frequency at the ICC site (typically ~8 kHz). During drug injection, responses at the ICC injection site to a broadband stimulus, using the site's best ITD and best ILD, were measured every 3-6 s until they were <35% of preinjection levels (~5-15 min). A series of ITD tuning curves of 10-20 repetitions each and alternately using the 4- or 8-kHz stimulus was then measured at the tectal recording site. Finally, a retaining current was turned on or the injection electrode was removed, and more ITD tuning curves were measured at the tectal recording site as the ICC recovered from the lidocaine injection.
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RESULTS |
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We used focal pharmacological inactivation to test whether changes in the pattern of connectivity in the inferior colliculus were responsible for auditory experience-induced changes in the midbrain ITD map. Below, we first show that injection of lidocaine in the ICC reversibly blocked auditory-evoked activity at the injection site. Next, we demonstrate that, consistent with the pattern of connectivity in normal owls, inactivation at a critical site in the ICC blocked ITD tuning at a site in the tectum in a frequency-dependent manner. Finally, we show that the locations of these critical, frequency-specific ICC sites were altered by auditory experience.
Local effect of lidocaine in the ICC
Lidocaine reversibly blocked auditory-evoked responses at the ICC
injection site. Figure 3 illustrates this
effect at a site in the lateral shell of the ICC of a device-reared
owl. Before lidocaine application, units at this site were tuned to 3.9 kHz (data not shown) and 82 µs ITD (Fig. 3, B and
C). Ten minutes of lidocaine injection eliminated auditory
responses at this site (Fig. 3, B and D). One
hundred thirty minutes after drug injection ceased, unit responses
returned to preinjection levels (Fig. 3, B and
E). These results were typical of the effect of lidocaine on
responses at the ICC injection site in both normal and device-reared owls: 5-15 min of lidocaine injection caused auditory responses to a
broadband stimulus at the site's best ITD to be reduced by
70%
relative to the baseline level (Fig. 4).
For all 12 sites tested, responses returned to
90% of baseline
levels within 150 min of termination of drug injection.
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Effect on tectal responses in normal owls
Units in the optic tectum are tuned for ITD but, unlike units in the ICC, are broadly tuned for frequency. Thus we used narrowband stimuli that matched the frequency tuning at the ICC injection sites to test the effects of ICC inactivation on frequency-specific ITD representations in the tectum.
Figure 5 illustrates responses to binaural stimuli at a tectal site before, during, and after recovery from lidocaine injection in the ICC. The injection site was located at the rostral end of the lateral shell in the ICC (Fig. 5A). The units at this site were tuned to 5.1 kHz and 5 µs ITD. The recording site was located at the rostral end of the optic tectum. Prior to the injection of lidocaine in the ICC, the units at this site responded robustly to a narrowband stimulus centered on 5.1 kHz, with a best ITD of 9 µs (Fig. 5, B and C). This stimulus and ITD tuning matched the frequency and ITD tuning, respectively, at the ICC injection site. After 9 min of lidocaine injection, responses at the ICC injection site were blocked (data not shown). Responses at the tectal recording site to the 5.1-kHz stimulus were blocked, as well (Fig. 5, B and D). The tectal responses returned to baseline levels 45 min after termination of the drug injection (Fig. 5, B and E). Similar results were obtained in two other experiments in which the best ITD at the ICC injection site was within 11 µs of the frequency-matched best ITD at the tectal recording site.
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In contrast, responses at the same tectal site to a narrowband stimulus centered on 7.5 kHz, instead of 5.1 kHz, were not affected by injection of lidocaine at the same ICC site (Fig. 6). This stimulus did not match the frequency tuning at the injection site. Prior to the injection of lidocaine in the ICC, the tectal units responded to the 7.5-kHz stimulus with a best ITD of 11 µs. After 23 min of lidocaine injection in the ICC, responses at the tectal recording site were unchanged relative to baseline levels.
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Unit responses in the tectum were also unaffected by injection of
lidocaine into the ICC when the ITD tuning of units at the ICC
injection site did not match that of the units at the tectal recording
site. For the experiment illustrated in Fig.
7, the injection site was located at the
rostral end of the lateral shell in the ICC. The units at this site
were tuned to 4.8 kHz and 15 µs ITD. The recording site was located
at the caudal end of the optic tectum. Prior to the injection of
lidocaine in the ICC, the units at this site responded to a narrowband
stimulus centered on 4.8 kHz with a best ITD of
66 µs. After 25 min
of lidocaine injection, responses at the ICC injection site were
blocked (data not shown), but there was no effect on the responses at
the tectal recording site to the 4.8-kHz stimulus at any ITD. Similar
results were obtained in one other experiment in which the
frequency-matched best ITDs at the ICC injection site and the tectal
recording site differed by 36 µs.
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Thus in normal owls, auditory responses in the optic tectum were reversibly eliminated by injection of lidocaine into the ICC only for those responses that corresponded to the frequency-specific ITD tuning at the site of drug injection in the ICC. Tectal responses to other frequencies and ITDs were not affected.
Effect on tectal responses in device-reared owls
Device rearing causes frequency-dependent changes in the
representation of ITD in the optic tectum (Gold and Knudsen
2000a). These changes include shifts in ITD tuning of ~50-80
µs toward open-ear leading for narrowband stimuli near 4 kHz. In
contrast, device rearing does not affect the representation of ITD in
the ICC, with contralateral-ear leading ITD values identically
represented in the lateral shell of the ICC in normal and device-reared
owls (Gold and Knudsen 2000b
). For this study, we
focused on device-induced changes in the 4-kHz ITD tuning of neurons in
the rostral portion of the right tectum. Neurons at this location
typically have a 4-kHz best ITD of ~0 µs in normal owls but may be
tuned to
80 µs in owls raised with the device in the right ear. The
advantage of focusing on this particular aspect of the adaptive change
is that both the normal and learned ITD values are represented in well-characterized regions of the ipsilateral ICC (see Fig. 2) (Brainard and Knudsen 1993
; Gold and Knudsen
2000b
; Wagner et al. 1987
).
Figure 8 illustrates responses to
binaural stimuli at a tectal site before, during, and after lidocaine
injection in the ICC. The injection site was located at the caudal end
of the lateral shell in the ICC (Fig. 8A). The units at this
site were tuned to 3.9 kHz and 98 µs ITD. The recording site was
located at the rostral end of the optic tectum. Prior to the injection
of lidocaine in the ICC, the units at this site responded robustly to a
narrowband stimulus centered on 4.0 kHz with a best ITD of
84 µs,
which is ~80 µs more open-ear leading than normal (Fig. 8,
B and C). This 4.0-kHz stimulus and shifted ITD
tuning matched the frequency and ITD tuning, respectively, at the ICC
injection site. After 25 min of lidocaine injection, responses at the
ICC injection site were blocked (data not shown). After 50 min of
injection, responses at the tectal recording site to the 4.0-kHz
stimulus were significantly reduced as well (Fig. 8, B and
D). The tectal responses returned to baseline levels 30 min
after termination of drug injection (Fig. 8, B and
E).
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In contrast, responses at the same tectal site to a narrowband stimulus
centered on 8.0 kHz, instead of 4.0 kHz, were not blocked by injection
of lidocaine at the same ICC site (Fig.
9). This stimulus did not match the
frequency tuning at the injection site. Before injection of lidocaine,
the units at the tectal site responded to the 8.0-kHz stimulus with a
best ITD of 96 µs. After 28 min of lidocaine injection in the ICC,
responses at the tectal recording site were greater than baseline
levels. These responses returned to baseline levels 50 min after
termination of drug injection.
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Unit responses in the tectum were also unaffected by injection of
lidocaine into the ICC when the ITD tuning of units at the ICC
injection site matched the normal, but not the shifted, ITD tuning of
the units at the tectal recording site. For the experiment illustrated
in Fig. 10, the injection site was
located at the rostral end of the lateral shell in the ICC. The units
at this site were tuned to 4.5 kHz and 0 µs ITD. The recording site
was located at the rostral end of the optic tectum. Prior to the
injection of lidocaine in the ICC, the units at this site, which
normally would have responded to a narrowband stimulus centered on 4.5 kHz with a best ITD of ~0 µs, were instead tuned to 68 µs ITD. After 25 min of lidocaine injection, responses at the ICC injection site were blocked (data not shown), but there was no effect on the
responses at the tectal recording site to the 4.5-kHz stimulus at any
ITD.
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Figures 11 and 12 summarize data from seven experiments in device-reared owls. In each experiment, the injection site was located in the ~4 kHz frequency lamina at the caudal end of the ICC. The recording site was located at the rostral end of the optic tectum and was tuned to a shifted, ~4-kHz ITD that matched the ITD tuning at the ICC injection site. As shown in Fig. 11, 15-90 min of lidocaine injection in the ICC in all cases caused a significant reduction of responses in the optic tectum for a stimulus that matched the frequency and ITD tuning at the ICC injection site (unpaired t-test, P < 0.05). In all but one case (Fig. 11E), responses during lidocaine injection were also significantly less than responses after termination of the injection. As shown in Fig. 12A, these effects were confined to stimulus ITDs that matched the best ITD at the ICC injection site to within 10 µs. In contrast, responses to an ~8-kHz stimulus that did not match the frequency tuning at the ICC injection site were not substantially affected by lidocaine injection at any ITD (Figs. 11 and 12B).
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Figure 13 summarizes the effect of lidocaine injection in the ICC on auditory responses in the optic tectum of normal and device-reared owls. In general, responses in the tectum were substantially reduced following injection of the anesthetic in the ICC only when the frequency and ITD tuning at the ICC injection site matched the frequency-specific ITD tuning at the tectal recording site (Fig. 13A). Thus to block tectal responses, the injection electrode had to be placed at different sites in the ICC in device-reared versus normal owls (Fig. 13B).
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DISCUSSION |
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This study demonstrates that abnormal auditory experience can cause plasticity in the functional connectivity between neurons in the barn owl's inferior colliculus. This plasticity can account for shaping the midbrain map of auditory space to reflect the experience of the individual. In the sections that follow, we first review the pattern of connectivity in the inferior colliculus and optic tectum of normal owls, focusing on how this pattern contributes to the representation of ITD in these nuclei. We then discuss the present results that indicate experience-induced plasticity in this pattern of connectivity. Finally, we consider the implications of this type of plasticity for the connectivity within the inferior colliculus.
Connectivity in normal owls
In normal owls, the representation of ITD in the inferior
colliculus and optic tectum is maintained along systematic connections within and between these nuclei (see Figs. 1 and 2A). The
inferior colliculus receives timing information from the nucleus
laminaris, where interaural phase differences are first measured
(Carr and Konishi 1988, 1990
; Sullivan and
Konishi 1986
). This information is received by the core
subdivision of the ICC (Takahashi and Konishi 1988
),
which projects, in turn, to the contralateral ICC lateral shell
(Takahashi et al. 1989
). ITD information from the lateral shell converges across frequency channels in the projection from the ICC to the ICX. Thus ICX neurons are broadly tuned for frequency and are tuned for ITD. These neurons are organized with respect to their tuning to sound localization cues, including ITD and
ILD, to form a physiological map of auditory space (Mogdans and
Knudsen 1993
; Moiseff and Konishi 1981
). The ICX
space map, including the systematic ITD representation along its
rostrocaudal dimension, is conveyed via point-to-point projections to
the optic tectum (Knudsen and Knudsen 1983
).
This pattern of connectivity in the inferior colliculus and optic tectum predicts that the representation of a certain frequency-specific ITD is conveyed from a particular site in the lateral shell to a site in the ICX and, from there, to a site in the tectum. Accordingly, the present results demonstrate that, in a normal owl, elimination of neuronal activity at a critical site in the ICC that is tuned for a certain combination of frequency and ITD causes the selective elimination of responses in the tectum to that same combination of frequency and ITD (Figs. 5-7). This result supports the idea that the pattern of ICC-ICX-tectum connectivity is responsible for the representation of ITD in the ICX and tectum.
Experience-induced changes in connectivity
In device-reared owls, as in normal owls, elimination of neuronal
activity at a critical site in the ICC tuned to a certain combination
of frequency and ITD blocked auditory responses of neurons in the
tectum only for that frequency and ITD (Figs. 8-13). However, the
critical site of injection in the ICC was at vastly different locations
in device-reared versus normal owls (Fig. 13B) because
device rearing dramatically altered the representation of ITD in the
tectum but not in the ICC (Gold and Knudsen 2000a,b
). These results indicate that adaptive adjustment to the device corresponded to a change in the pattern of connectivity between the ICC
and tectum.
In principle, this plasticity could occur at any point along the
pathway from the ICC to the tectum, which are not directly connected
(see Fig. 1). Nevertheless, several lines of evidence suggest that the
plasticity occurs in the ICC-ICX projection. The first line of evidence
is that device rearing does not affect the representation of ITD in the
ICC but causes similar changes in the two succeeding nuclei in the
ascending pathway, the ICX and optic tectum (Gold and Knudsen
2000a,b
). A straightforward explanation is that plasticity in
the ICC-ICX projection causes the abnormal representation of ITD in the
ICX, which is conveyed directly, along unmodified connections, to the tectum.
The second line of evidence is based on the short latencies of
adaptive responses in the ICX. We reported previously that device-induced changes in the representation of ITD in the ICX are
evident in the earliest responses of ICX units (Gold and Knudsen 2000b). This result demonstrates that the expression of
functional changes in the ICX do not require signals from neurons in
other, more remote parts of the CNS (e.g., the cerebellum or forebrain) (Cohen and Knudsen 1999
) that would take longer to
arrive, implying that this adaptive plasticity involves changes along
the ICC-ICX pathway.
The third line of evidence for plasticity in the ICC-ICX projection is
from experiments in owls raised with abnormal vision. Like device
rearing, raising owls with prismatic spectacles that optically shift
the visual field results in a systematic shift in the representation of
ITD in the ICX and optic tectum but not in the ICC (Brainard and
Knudsen 1993). Recent experiments show that these functional
changes are associated with plasticity occurring within the inferior
colliculus, including the formation of novel anatomical ICC-ICX
connections (DeBello et al. 2001
; Feldman and Knudsen 1997
), changes in the strength of existing connections (Knudsen 1998
), and changes in the balance of excitation
and inhibition (Zheng and Knudsen 1999
). Considering
that these visually driven mechanisms normally function to calibrate
auditory spatial information, all of these mechanisms are ideal
candidates for driving the adaptive, functional changes observed here
in device-reared owls.
Implications for connectivity in the inferior colliculus
The present study focused on changes in the representation of
4-kHz ITDs in the right inferior colliculus and optic tectum because
those representations are well characterized in both normal and
device-reared owls. In principle, other device-induced changes in
auditory tuning could result from a similar form of plasticity. For example, device rearing causes a substantial reduction in normally
robust responses to stimuli near 6 kHz in the ICX and tectum. This
reduction in responses to 6-kHz stimuli, like the loss of responses to
normal ITD values in owls raised with abnormal hearing or vision
(Brainard and Knudsen 1993; Gold and Knudsen 2000a
,b
), could reflect a loss of functional connections from that frequency channel in the ICC. In addition, device rearing shifts
the ICX and tectal representations of ITD at 8 kHz by ~15 µs, in
the direction opposite to the shift in the ITD representations at 4 kHz
(Gold and Knudsen 2000a
,b
). A corresponding change in the representation of ITD at 8 kHz does not occur in the ICC
and therefore probably reflects novel connections from the ICC to the
ICX. These different effects for different frequencies imply that the
connectivity within this pathway can be shaped extensively on a
frequency-by-frequency basis.
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ACKNOWLEDGMENTS |
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We thank M. Shadlen for helpful comments on the manuscript and P. Knudsen for expert technical assistance.
This work was supported by National Institute on Deafness and Other Communication Disorders Grant R01 DC-00155-18.
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FOOTNOTES |
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Present address and address for reprint requests: J. I. Gold, Dept. of Physiology and Biophysics, University of Washington Medical School, Box 357290, Seattle, WA 98195-7290 (E-mail: jig{at}u.washington.edu).
Received 27 September 2000; accepted in final form 22 December 2000.
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REFERENCES |
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