Department of Biology, Washington University, St. Louis, Missouri 63130
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ABSTRACT |
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Chowdhury, Syed A. and Nobuo Suga. Reorganization of the Frequency Map of the Auditory Cortex Evoked by Cortical Electrical Stimulation in the Big Brown Bat. J. Neurophysiol. 83: 1856-1863, 2000. In a search phase of echolocation, big brown bats, Eptesicus fuscus, emit biosonar pulses at a rate of 10/s and listen to echoes. When a short acoustic stimulus was repetitively delivered at this rate, the reorganization of the frequency map of the primary auditory cortex took place at and around the neurons tuned to the frequency of the acoustic stimulus. Such reorganization became larger when the acoustic stimulus was paired with electrical stimulation of the cortical neurons tuned to the frequency of the acoustic stimulus. This reorganization was mainly due to the decrease in the best frequencies of the neurons that had best frequencies slightly higher than those of the electrically stimulated cortical neurons or the frequency of the acoustic stimulus. Neurons with best frequencies slightly lower than those of the acoustically and/or electrically stimulated neurons slightly increased their best frequencies. These changes resulted in the over-representation of repetitively delivered acoustic stimulus. Because the over-representation resulted in under-representation of other frequencies, the changes increased the contrast of the neural representation of the acoustic stimulus. Best frequency shifts for over-representation were associated with sharpening of frequency-tuning curves of 25% of the neurons studied. Because of the increases in both the contrast of neural representation and the sharpness of tuning, the over-representation of the acoustic stimulus is accompanied with an improvement of analysis of the acoustic stimulus.
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INTRODUCTION |
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The auditory, visual, and somatosensory systems,
respectively, have cochleotopic, retinotopic, and somatosensory maps in
their central neural pathways. These sensory epithelial maps are
modified by deprivation, injury, and experience in young (Hubel
et al. 1977) and adult animals (Clark et al.
1988
; Irvine and Rajan 1996
; Jenkins et
al. 1990
; Kaas et al. 1990
; Merzenich et
al. 1984
; Pettet and Gilbert 1992
;
Recanzone et al. 1993
; Snyder et al. 1990
, 1991
; Weinberger et al.
1993
). Such plasticity has been explained by changes in
divergent and convergent projections of neurons in the ascending
sensory system. However, recent findings, briefly reviewed below,
indicate that the cerebral cortex and the descending (corticofugal)
system play an important role in modifying these maps.
In the motor (Nudo et al. 1996), somatosensory
(Recanzone et al. 1993
; Spengler and Dinse
1994
), and auditory cortices (Maldonado and Gerstein
1996
; Yan and Suga 1998
), electrical stimulation of particular parts of the cortex evokes an expansion in the cortical or subcortical representation of those parts. In the big brown bat, an
acoustic stimulus paired with electric leg-stimulation as in a
classical conditioning paradigm evokes an expansion in the
representation of the acoustic stimulus in the inferior colliculus. The
auditory cortex is necessary for this expansion (Gao and Suga 1998
).
In the mustached bat (Pteronotus parnellii), cortical
auditory neurons mediate, via corticofugal projection, a highly focused positive feedback to subcortical neurons "matched" in tuning to a
particular acoustic parameter in the frequency or time domain, and a
widespread lateral inhibition to "unmatched" subcortical neurons.
This cortical feedback changes subcortical maps, augments excitatory
neural responses, and sharpens neural tuning curves so as to enhance
the neural representation of frequently occurring signals in the
central auditory system. This function, named "egocentric selection," adjusts and improves the cortical neurons' own input, and, consequently, cortical signal processing (Yan and Suga
1996; Zhang et al. 1997
). In the big brown bat
(Eptesicus fuscus), egocentric selection shifts the best
frequencies (BFs) of collicular neurons not only toward the BF of
electrically stimulated cortical neurons but also toward the frequency
of a repetitively delivered acoustic stimulus (tone burst), resulting
in local reorganization of the frequency map in the inferior colliculus
(Yan and Suga 1998
). Egocentric selection also evokes BF
shifts according to auditory experience based on associative learning
(Gao and Suga 1998
).
It appears that the cerebral cortex has mechanisms to adjust and improve sensory epithelial (frequency) and computational (echo delay) maps not only in the cortex, but also in subcortical nuclei via corticofugal feedback. In the above experiments on bats, however, changes evoked by acoustic stimuli and/or focal cortical electrical stimulation were studied only in the subcortical auditory nuclei. The aim of our present paper is to report our finding that the changes in the frequency map of the primary auditory cortex are similar to, but slightly larger than, those in the inferior colliculus.
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METHODS |
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Sixteen adult big brown bats, Eptesicus fuscus, were used in the present experiment. Under neuroleptanalgesia (Innovar 4.08 mg/kg body weight), a 1.5-cm-long metal post was glued on the dorsal surface of the bat's skull. The physiological experiment was started 3-4 days after the surgery. The animal was placed in a polyethylene-foam body mold and hung at the center of a soundproof room which was maintained at 31°C. The metal post mounted on the skull was fixed on a metal rod with set screws to immobilize the animal's head and adjusted to face directly at a loudspeaker located 74 cm away. (The protocol of our research was approved by the animal studies committee of Washington University.) To record action potentials of cortical auditory neurons, a tungsten-wire electrode (6-8 µm tip diam) was orthogonally inserted into the auditory cortex (AC), which is tonotopically organized and ~900-µm thick (Fig. 1A). All recordings were made at the depth of 200-800 µm. A BAK window discriminator was used to select action potentials from a single neuron. When the selection was difficult and action potentials originating from 2-3 neurons were recorded, the recording was classified as a multiunit recording. The BF and minimum threshold of a single neuron or multiple neurons were first measured audiovisually. Then, the computer-controlled frequency scan was delivered, which consisted of 22 time blocks, each 200-ms long. A single tone burst was delivered at the beginning of each block. The frequency of the tone burst was shifted from block to block in 0.5-kHz steps across the BF of the neuron(s). The amplitude of tone bursts in the scan was set at 20 dB above the minimum threshold of the neuron or varied every 10 scans in 5 dB steps from 80 to 0 dB sound pressure level. Neural responses to tone bursts were displayed as peristimulus-time (PST) or PST cumulative (PSTC) histograms. (In a PSTC histogram, impulse counts in the bins of a PST histogram are successively added.) The responses to the frequency scans were displayed on a computer monitor as an array or arrays of PST or PSTC histograms, stored on a computer hard drive, and used to construct a frequency-response or frequency-tuning curve. Such a curve was obtained before and after repetitive acoustic stimuli (ASr) or focal cortical electric stimulation (ESa) paired with ASr, delivered at a rate of 10/s for 30 min.
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ASr consisted of 300 tone bursts, each of which was 20-ms long with a 0.5-ms rise-delay time (Fig. 1B). Its amplitude and frequency were set at 50 dB SPL and at a frequency the same as or lower or higher than the BF of a recorded cortical neuron, respectively. ESa was delivered through a pair of tungsten-wire electrodes glued side by side. The tips of these electrodes were 6-8 µm in diameter and were separated by ~150 µm along the electrode shaft. These stimulating electrodes were placed at a 500-700 µm depth of the AC. In the paired acoustic-electrical stimulation (ASr + ESa), the ASr frequency was always the same as the BF of cortical neurons electrically stimulated. ESa was a train of four monophasic electric pulses (100 nA, 0.2-ms duration, 2.0-ms interval). The first pulse of ESa and the onset of each tone burst were in register in time (Fig. 1B). ASr or ASr + ESa was delivered at a rate of 10/s for 30 min.
To measure a BF shift as a function of distance between the recorded and electrically stimulated cortical neurons, the BFs of cortical neurons were first measured at 12-14 locations. These locations were ~100 µm apart and rostral or caudal to the location of ESa along the frequency axis in the AC. Then, ASr + ESa were delivered for 30 min. Within 60 min thereafter, BFs of neurons at these 12-14 locations were remeasured.
The following criteria were used for a shift in the frequency-response or -tuning curve (or BF) of a neuron by ASr or ASr + ESa: if a shifted frequency-response or -tuning curve did not shift back by more than 50%, the data were excluded from the analysis. In stable, long recording conditions, all curves shifted by the stimulation recovered by more than 50%. This recovery itself helped prove that the shift was significant. When a BF shift was small and its significance was not obvious, a weighted average frequency (i.e., BF) was calculated for the summed response to five consecutive frequency scans. Then the mean and standard deviation of these weighted averages were computed, and a two-tailed paired t-test was used to determine whether or not the weighted-average frequencies (BFs) obtained for control and stimulus conditions were significantly different for P < 0.01.
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RESULTS |
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Shifts in best frequencies
In the AC of the big brown bat, the low-to-high-frequency axis was
parallel to the caudorostral axis of the brain, as previously reported
(Fig. 1A; Dear et al. 1993; Jen et al.
1989
). We recorded 71 single and 45 multiple neurons in the AC
and found shifts in BFs that were the same as those found in the
inferior colliculus (Yan and Suga 1998
). That is,
ASr or ESa paired with
the ASr mainly evoked downward shifts in the BFs of cortical neurons which had a BF slightly higher than the frequency of the ASr. These cortical neurons were located
within ~600 µm rostral to the neurons activated with the
ESa. The BF shifts were larger and
longer-lasting for the ASr + ESa than for the ASr alone.
In Fig. 2, the frequency-response curves of two single cortical neurons (A and B) are shown by the arrays of PSTC histograms displaying their responses to tone bursts obtained before, immediately after, and 90 min after ASr (Aa) or ASr + ESa (Ba). The amplitude of the tone bursts was 10 dB above the minimum threshold of a given neuron. In Aa, the neuron was tuned to 43.5 kHz in the control condition. When ASr at 41.0 kHz was delivered for 30 min, its BF shifted down to 43.0 kHz. The BF returned to 43.5 kHz 90 min after the ASr. In Ba, the neuron was tuned to 58.5 kHz in the control condition. When ASr at 53.0 kHz was paired with ESa to stimulate 53.0 kHz tuned cortical neurons, the 58.5-kHz BF shifted down to 55.5 kHz. The BF returned to 58.5 kHz 90 min after ASr + ESa. These shifts in the BFs were due to a decrease in the response at the BF in the control condition and an increase in the response at the shifted BF. Neither decrease nor increase in response was associated with a change in response pattern, as shown by the PST histograms in Fig. 2.
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The time course of a BF shift evoked by ASr alone or ASr + ESa was measured in 19 and 42 neurons, respectively. The BF shift was always largest and stayed nearly the same in a period of 30-60 min after the cessation of ASr or ASr + ESa. Then, BFs gradually returned to those in the control condition over 2-3 h after the cessation (Fig. 3). A 75% recovery occurred at 55.0 ± 21.2 min (n = 19) after ASr or at 100.2 ± 28.3 min (n = 42) after ASr + ESa.
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The data obtained from 154 neurons indicate that the amount of the
maximum BF shift of each neuron was different depending on the
difference between its BF and the frequency of
ASr (Figs. 4,
A and B, and
5). (Note that in
ASr + ESa the BF of
neurons electrically stimulated was the same as the frequency of
ASr.) We considered that the higher the ASr and/or the BF of cortical neurons
electrically stimulated, the larger the range of BFs affected by the
ASr and/or ESa. That is,
we considered that if the ASr was one octave
higher, the amount of a BF shift was one octave larger. The
ASr frequency in ASr + ESa was between 22.6 and 54.0 kHz (34.6 ± 11.2 kHz; n = 83). The maximum BF shift and the largest
BF difference between recorded and stimulated cortical neurons for a
just-noticeable BF shift were, respectively, 2.6 and 11 kHz for
23-27 kHz ASr frequencies (n = 9), and
2.4 and 14 kHz for 46-54 kHz ASr
frequencies (n = 7). The maximum BF shift and the
largest BF difference for a just-noticeable BF shift did not differ
between the above two ranges of ASr frequencies.
Therefore in the following text, the BF shifts and the differences
between BF and ASr are expressed in kilohertz,
not in octave.
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The relationship between a BF shift and a difference between the BF of
a recorded neuron and a ASr frequency or a BF
difference between recorded and stimulated cortical neurons is shown in
Fig. 4. Figure 4A shows that ASr
alone evoked the downward shifts of the BFs of neurons which had a BF
within 8 kHz above the ASr frequency. The
maximum BF shift observed was 1.0 kHz, which occurred at ~3 kHz above
the ASr frequency. Figure 4B shows
that ASr + ESa evoked the
downward shifts of the BFs of neurons which had a BF within 12 kHz
above the BFs of electrically stimulated cortical neurons. The maximum BF shift observed was 3.0 kHz, which occurred at 5 kHz above the BFs of
electrically stimulated neurons. Small but significant BF shifts were
also noticed for neurons in which BFs were more than 12 kHz higher or
lower than the BFs of neurons electrically stimulated. Therefore the BF
shifts between 1.0 and +0.5 kHz shown in Fig. 4B are
replotted on the expanded ordinate in Fig. 4C. The following
are indicated by Fig. 4C. 1)
ASr + ESa also evoked the
decrease in the BFs of some neurons with a BF within a range of 6-8
kHz lower (4 open circles on the left) or ~19 kHz higher
(3 triangles on the far right) than the BF of electrically
stimulated neurons. 2) It also evoked an increase in the BFs
of some neurons with a BF within a range of 1-6 kHz lower (7 triangles
on the left) or 12-15 kHz higher (7 open circles on the
right) than the BF of electrically stimulated neurons. 3) BF shifts between
3 and +8 kHz (triangle) tended to
evoke over-representation of the ASr frequency
or the BF of electrically stimulated cortical neurons, but those
between
3 and
8 kHz and between +8 and +15 kHz (open circles)
tended to evoke under-representation of these frequencies. In other
words, the BF shifts occurred to increase the contrast of neural
representation of ASr or the BF of electrically
stimulated cortical neurons.
As shown in Fig. 4, the most noticeable BF shifts were downward toward
the BF of electrically stimulated cortical neurons and occurred on the
high-frequency side of the BF of electrically stimulated cortical
neurons or the frequency of ASr. Therefore the
BF shifts (i.e., frequency map adjustment) is asymmetrical and
centripetal. The comparison of the present cortical data with the
collicular data obtained by Yan and Suga (1998) indicate
that BF shifts evoked by ASr + ESa were slightly larger for cortical neurons
than for collicular neurons (P < 0.005 at 6 and 9 kHz
above the BF of cortical neurons electrically stimulated) (Fig.
4D).
The BF shifts at a given BF difference between recorded and stimulated
cortical neurons are different from neuron to neuron. For example, a BF
shift occurred in some neurons, but did not occur in some others at the
BF difference of 5 kHz. If a shift did occur, the direction of BF
shift could be different between neurons. Such variation might be due
to pooling the data obtained for ASr + ESa in which ESa was
delivered to different locations of cortical iso-BF lines tuned to a
frequency between 22.6 and 54.0 kHz (34.9 ± 11.2 kHz,
n = 83). Therefore a pair of electrodes for
ESa was implanted at a 500-700 µm depth at a
30.2 ± 0.6 kHz tuned location and single or multiple neurons were
recorded from different locations rostral or caudal to the stimulation
electrodes along the frequency axis of the AC. The data obtained from
three animals (Fig. 5) indicate that cortical neurons located rostrally
<600 µm (corresponding to ~47 kHz) to the stimulation electrodes
decreased their best frequencies and that those located caudally <400
µm (corresponding to ~22 kHz) to the stimulation electrodes
increased their best frequencies. The decrease in BF was much larger
than the increase in BF. The BF shifts were thus asymmetrical and
centripetal. The largest downward BF shift observed was 1.8 kHz, which
occurred at 0.2 mm rostral (corresponding to ~35 kHz) to the
electrically stimulated neurons. The largest upward BF shift was 0.4 kHz, which occurred at 0.1 mm caudal (corresponding to ~24 kHz) to
the electrically stimulated neurons. The BF shifts toward the BF of the
electrically stimulated neurons tended to evoke an over-representation
of the BF of the electrically stimulated neurons. The
over-representation is, however, associated with the
under-representation of BFs at 0.2-0.6 mm rostral and
0.1 to
0.4
mm caudal portions to the electrically stimulated neurons, because the
amount of BF shift became less at the portion more rostral to the 0.2 mm rostral place or more caudal to the 0.1 mm caudal place to the
electrically stimulated neurons.
Sharpening of frequency tuning curves
A shift in BF of a neuron was always accompanied by a similar shift of the whole frequency-tuning curve. The shift in a tuning curve was mostly parallel to the frequency axis (Fig. 6). For ASr alone, the minimum threshold and the shape of a frequency-tuning curve did not change in all 33 neurons studied, perhaps because a change was too small to be detected in our measurement. However, for ASr + ESa, change in minimum threshold was observed, which was ±5 dB in 61 neurons out of the 83 neurons showing a BF shift and was ±10 dB in the remaining 22 neurons. The overall shape of a tuning curve did not change in 70 neurons out of the 83 (Fig. 6, A, B, and D), but changed in the remaining 13 neurons (Fig. 6C).
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Twenty-one neurons out of the 83 had a BF within a range of 6 and +20
kHz of the ASr frequency and shifted the BF by
3.2 to +1 kHz (Fig. 4B). They showed a decrease in the
width of the tuning curve, i.e., sharpening in the tuning curve.
Sharpening at 30 dB above minimum threshold was small, 0.4-1.0 kHz, in
16 neurons (Fig. 6B), but large, 1.2-1.6 kHz, in the
remaining three neurons (Fig. 6C).
It has been known that the width of a frequency-tuning curve sharpened
by lateral inhibition generally does not change or changes only a
little at 10 dB above the minimum threshold, but changes noticeably at
higher stimulus levels (e.g., Suga et al. 1997).
Therefore a width of a tuning curve was measured at 10, 30, and 50 dB
above the minimum threshold of each of the 83 neurons studied with
ASr + ESa. Sixty-two out
of 83 neurons showed no change at all in the bandwidth of their tuning curves, regardless of stimulus levels because the amount of change was
not more that 0.1 kHz (P > 0.05). However, the
remaining 21 neurons showed changes larger than 0.1 kHz, so that the
changes at different stimulus levels were plotted against the
difference in BF between the recorded and stimulated cortical neurons
(Fig. 7, A-C). Out
of the 21, 19 neurons showed 0.3-1.6 kHz narrower widths of a tuning
curve at 30 dB above minimum threshold than those in the control
condition (Fig. 7B), and 1 neuron showed 1.0 kHz wider width
than that in the control condition. Such changes (sharpening) were
significant at all three stimulus levels: values of P are
0.0330, 0.0002, and 0.0049 for 10, 30, and 50 dB above minimum
threshold, respectively (Fig. 7, A-C).
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There was a tendency that sharpening was somewhat larger for the neurons with BFs within ±2 kHz of the ASr frequency, which was the same as the BF of electrically stimulated cortical neurons (Fig. 7B). However, cross-correlation analysis indicates that there is no correlation between BF shift and change in bandwidth: r = 0.17, 0.24, and 0.10 at 10, 30, and 50 dB above minimum threshold, respectively (Fig. 7, D-F).
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DISCUSSION |
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Adjustment of frequency representation in the AC and inferior colliculus
The adjustment of frequency representation in the AC evoked by
ASr alone or ASr + ESa is similar to that in the inferior
colliculus (Yan and Suga 1998), although the former is
slightly larger than the latter. Classical conditioning with tone
bursts and electric leg-stimulation also evokes the adjustment of
frequency representation in the inferior colliculus which is the same
as that evoked in the inferior colliculus by ASr + ESa. This
adjustment evoked by conditioning does not occur when the AC or the
somatosensory cortex is inactivated during conditioning. These findings
indicate that the corticofugal system plays an important role in the
plasticity of the central auditory system (Gao and Suga
1998
).
Recent studies indicate that the cholinergic basal forebrain plays an
important role in cortical reorganization. Electrical stimulation of
the basal forebrain paired with tone bursts evokes massive cortical
reorganization for the over-representation of the frequency of the tone
bursts (Bakin and Weinberger 1995; Bjordahl et
al. 1998
; Kilgard and Merzenich 1998
).
Weinberger (1995) proposed a model to explain cortical
frequency-tuning plasticity in the learning of a classical conditioning paradigm. An auditory signal (tone burst, conditioning stimulus) is
sent to the AC through the ventral division of the medial geniculate body (MGBv), which is nonplastic, and is also
sent to the magnocellular division of the medial geniculate body
(MGBm), which is plastic, and the posterior
intralaminar complex, both in the thalamus. A somatosensory signal
(electric foot-shock, unconditioned stimulus) is also sent to the
MGBm and posterior intralaminar complex, where
the somatosensory and auditory signals are first associated with each
other for associative learning. The associated signal is sent up to the
AC to strengthen the effect of MGBv neurons,
excited by the conditioning stimulus, on cortical neurons. This
associated signal is also sent to the amygdala, which in turn projects
to the nucleus basalis. Then, the nucleus basalis increases cortical
acetylcholine levels and amplifies the effect of the
MGBm neurons on the cortical neurons which are
excited by the conditioning stimulus.
The MGBv shows "short-term"
frequency-specific plasticity for fear conditioning (Edeline and
Weinberger 1991), although it is assumed to be nonplastic in
the above model. Because the inferior colliculus also shows plastic
changes according to associative learning (Gao and Suga
1998
), as does the AC (Gao and Suga 2000
), the
plastic changes of the MGBm may be at least
partially due to those in the inferior colliculus.
MGBm neurons often have a broad or multipeaked
frequency-tuning curve and habituate after several stimulus
presentations (Aitkin 1973
; Calford
1983
). If so, MGBm may not be suited for
the fine adjustment and improvement of the central auditory system for
signal processing. These must be performed within the auditory system,
where the fine analysis of auditory signals takes place. It has been
demonstrated that egocentric selection mediated by the corticofugal
system evokes subcortical changes which are highly specific to acoustic stimuli (Yan and Suga 1996
, 1998
;
Zhang et al. 1997
). Therefore the corticofugal system is
expected to play an important role in stimulus-specific cortical plasticity.
Gao and Suga (1998) therefore proposed a model which is
somewhat different from Weinberger's model. A train of sounds combined with an electric leg-stimulation excite the AC and the somatosensory cortex, respectively. These sensory cortices send signals to the amygdala through the association cortex (Amaral et al.
1992
; Romanski and LeDoux 1993
). The train of
acoustic stimuli evokes changes in the AC, which are highly specific to
acoustic stimuli, and are based on egocentric selection mediated by the
corticofugal system. When associative learning takes place in the
amygdala, that is, when an animal is conditioned for the train of
acoustic stimuli paired with electric leg stimulation, the cholinergic basal forebrain is excited by these stimuli through the amygdala and
increases the acetylcholine level in the cortex. As a result, the train
of acoustic stimuli-related changes in the AC are augmented in
magnitude and duration. In other words, the processing of behaviorally relevant acoustic stimuli is adjusted and improved. Our present data
favor the hypothesis that the AC has the basic neural circuit which
works together with the corticofugal system for the adjustment and
improvement of auditory signal processing.
In the AC, the duration of plastic changes is 2-3 h for a behaviorally
irrelevant acoustic stimulus or direct cortical electrical stimulation,
but many hours for a behaviorally relevant acoustic stimulus
(Gao and Suga 2000). In the inferior colliculus,
however, it is 2-3 h for both conditions (Gao and Suga
1998
; Yan and Suga 1998
). These data indicate
that Gao and Suga's model is a useful working hypothesis and that
multiple mechanisms are involved in the plastic changes of the auditory system.
Difference in the adjustment of frequency representation between the big brown and mustached bats
The data obtained from the big brown bat (Gao and
Suga 1998; Yan and Suga 1998
) and the mustached
bat (Zhang et al. 1997
; Y. Zhang and N. Suga,
unpublished data) indicate the following. 1) By action of
the corticofugal system, the neural responses of subcortical neurons
tuned to frequencies the same as or close to the BF of activated
cortical neurons (i.e., so-called matched subcortical neurons) are
augmented, but those of unmatched subcortical neurons are suppressed.
2) The BFs of unmatched neurons are shifted away from the BF
of activated cortical neurons in the mustached bat, but are shifted
toward the BF of activated cortical neurons in the big brown bat.
3) The change in frequency representation due to BF shifts
is symmetrical in the DSCF neurons of the mustached bat, but is
asymmetrical in the big brown bat. 2) and 3) are
also true in the AC of the big brown bat (present study) and are
expected to be true in the AC of the mustached bat. [In the mustached
bat, corticofugal effects on subcortical neurons tuned in echo-delay are the same as those on subcortical DSCF neurons sharply tuned in
frequency. That is, the best delays for the facilitative responses of
unmatched subcortical delay-tuned neurons are symmetrically shifted
away from the best delay of activated cortical delay-tuned neurons
(Yan and Suga 1996
).]
Focused augmentation and widespread lateral inhibition of the auditory responses are respectively evoked for matched and unmatched neurons in both species of bats, but BF shifts are different between these two species. Possible interpretations of this difference are described below.
As in the little brown bat, Myotis lucifugus
(Suga 1964), guinea pig (Evans 1975
), cat
(Liberman 1978
), and monkey (Katsuki et al.
1962
), the frequency-tuning curves of peripheral neurons of the
big brown bat are presumably asymmetrical: their high-frequency slope
is much steeper than their low-frequency slope. Therefore a stimulus
tone at a given frequency activates more neurons tuned to higher
frequencies than neurons tuned to lower frequencies, and the effect of
egocentric selection on auditory neurons is asymmetrical. In the
mustached bat, however, frequency-tuning curves of peripheral neurons
tuned to about 61 kHz are roughly symmetrical (Suga and Jen
1977
), so that the effect of egocentric selection on collicular
neurons is also symmetrical (Zhang et al. 1997
).
In the big brown (Haplea et al. 1994) and little brown
bats (Suga 1964
), frequency-tuning curves of neurons at
the periphery and/or cochlear nucleus are generally much wider
(Q10dB < 20) than those
(Q10dB up to 320) of 61-kHz tuned
neurons of the mustached bat (Suga and Jen 1977
;
Suga et al. 1975
), so that any single tone can excite
many cortical and subcortical neurons tuned to different frequencies in
a much wider range in the big brown bat than in the mustached bat. BF
shifts indicate that each cortical or subcortical neuron has multiple
inputs tuned to different frequencies, and that the BF of an unmatched
neuron shifts toward the BF of the input maximally excited, because the
excitation transmission is augmented for the maximally excited input
and is suppressed for other inputs, including the input for its
original BF (Fig. 2). In the big brown bat, augmentation of cortical
and subcortical responses by corticofugal feedback may be stronger and
more widespread in the frequency domain than the suppression of their
responses. In the mustached bat, however, suppression may be stronger
and more widespread than augmentation. The direction of the BF shifts appears to depend on the interaction of augmentation and suppression.
Because focal cortical electrical stimulation alone evokes the
asymmetric BF shift as repetitive acoustic stimulation does (Yan
and Suga 1998), anatomic differences in the AC and/or
corticofugal projections may exist between the DSCF area of the
mustached bat and the AC of the big brown bat and may be partly
responsible for the differences observed between the two species of
bats. Regardless of this unsolved problem, it is clear that the DSCF area and its corticofugal modulation in the mustached bat are much more
specialized for fine frequency representation than the AC and its
corticofugal modulation in the big brown bat.
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ACKNOWLEDGMENTS |
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We thank Dr. N. M. Weinberger and N. Laleman for comments on the manuscript.
This work was supported by a research grant from the International Brain Research Organization to S. Chowdhury and by National Institute on Deafness and Other Communication Disorders Grant DC-00175 to N. Suga.
Present address of S. A. Chowdhury: University of California at Irvine, Center for Neurobiology of Learning and Memory, Bonney Center, Irvine, CA 92697-3800.
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FOOTNOTES |
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Address for reprint requests: N. Suga, Dept. of Biology, Washington University, One Brookings Dr., St. Louis, MO 63130.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 10 March 1999; accepted in final form 23 December 1999.
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REFERENCES |
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