Department of Biology, Washington University, St. Louis, Missouri 63130
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ABSTRACT |
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Zhang, Yunfeng and
Nobuo Suga.
Modulation of Responses and Frequency Tuning of Thalamic and
Collicular Neurons by Cortical Activation in Mustached Bats.
J. Neurophysiol. 84: 325-333, 2000.
In the
Jamaican mustached bat, Pteronotus parnellii parnellii,
one of the subdivisions of the primary auditory cortex is
disproportionately large and over-represents sound at ~61 kHz. This
area, called the Doppler-shifted constant frequency (DSCF) processing
area, consists of neurons extremely sharply tuned to a sound at ~61 kHz. We found that a focal activation of the DSCF area evokes highly
specific corticofugal modulation in the inferior colliculus and medial
geniculate body. Namely a focal activation of cortical DSCF neurons
tuned to, say, 61.2 kHz with 0.2-ms-long, 100-nA electric pulses
drastically increases the excitatory responses of thalamic and
collicular neurons tuned to 61.2 kHz without shifting their best
frequencies (BFs). However, it decreases the excitatory responses of
subcortical neurons tuned to frequencies slightly higher or lower than
61.2 kHz and shifts their BFs away from 61.2 kHz. The BF shifts are
symmetrical and centrifugal around 61.2 kHz. These corticofugal effects
are larger on thalamic neurons than on collicular neurons. The cortical
electrical stimulation sharpens the frequency-tuning curves of
subcortical neurons. These corticofugal effects named "egocentric
selection" last 2.5 h after the cessation of a 7-min-long cortical
electrical stimulation. In the mustached bat, corticofugal modulation
serves to increase the contrast in neural representation of sound at
~61 kHz, which is an important component of an echo bearing velocity
information. It is also most likely that the corticofugal system plays
an important role in plasticity of the central auditory system. Another
subdivision of the auditory cortex of the mustached bat is called the
FM-FM area. This area consists of delay-tuned combination-sensitive neurons, called FM-FM neurons, and has the echo-delay axis for the
systematic representation of target distances. A focal electric stimulation of the FM-FM area evokes changes in the responses of
collicular and thalamic FM-FM neurons. These changes are basically the
same as those described in the present paper. Therefore corticofugal modulation takes place for frequency domain analysis in exactly the
same way as it does in time domain analysis.
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INTRODUCTION |
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In the motor (Nudo et al. 1996),
somatosensory (Recanzone et al. 1993
; Spengler
and Dinse 1994
), and auditory cortices (Maldonado and
Gerstein 1996
), an electrical stimulation of a part of the cortex evokes an expansion in the cortical or subcortical
representation of that part. In the big brown bat, Eptesicus
fuscus, a focal electrical stimulation of the auditory cortex
evokes asymmetrical and centripetal shifts in best frequencies (BFs)
accompanied with the shifts of frequency-tuning curves (hereafter,
"BF shifts" for simplicity) of neurons in the inferior colliculus
(Yan and Suga 1998
) and the auditory cortex
(Chowdhury and Suga 2000
). That is, the BF shifts
predominantly occur for the BFs slightly higher than the BF of
electrically stimulated cortical neurons (hereafter, cortical BF), and
the direction of the shifts is downward toward the cortical BF.
Basically the same BF shifts can also be evoked in the inferior
colliculus (Gao and Suga 1998
) and the auditory cortex
(Gao and Suga 2000
) by an acoustic stimulus alone or
paired with an electric leg-stimulation as in a conditioning paradigm.
The auditory cortex and the somatosensory cortex both are necessary for
the BF shifts in the inferior colliculus evoked by auditory
conditioning (Gao and Suga 1998
). The data obtained from
the big brown bat strongly suggest that the corticofugal system plays
an important role in the plasticity of the central auditory system.
In the Jamaican mustached bat, Pteronotus
parnellii parnellii, the auditory cortex consists of several
subdivisions which are physiologically distinct from each other
(Suga 1990). The FM-FM area consists of delay-tuned
combination-sensitive neurons, called FM-FM neurons, and has the
echo-delay axis for the systematic representation of target distances
(O'Neill and Suga 1979
, 1982
; Suga and O'Neill
1979
; Suga et al. 1978
; 1983
). A focal
inactivation of cortical FM-FM neurons tuned to, say, a 5-ms echo-delay
with a local anesthetic drastically reduces the facilitative responses of thalamic and collicular FM-FM neurons tuned to a 5- ms echo-delay without shifting their best (echo) delays for facilitative responses. However, subcortical FM-FM neurons tuned to echo delays other than 5-ms
increase their facilitative responses and shift their best delays
toward 5 ms. A focal activation of the FM-FM area with electric pulses
evokes changes in subcortical FM-FM neurons that are opposite to those
evoked by focal inactivation. These data clearly indicate that cortical
FM-FM neurons mediate, via corticofugal projection, a highly focused
positive feedback to subcortical neurons "matched" in tuning to a
particular echo delay, and a widespread lateral inhibition to
"unmatched" subcortical neurons (Suga et al. 1995
;
Yan and Suga 1996
). The corticofugal system modulates
the subcortical delay maps, augments auditory responses, and sharpens
neuronal tuning curves so as to enhance the neural representation of
frequently occurring signals in the central auditory system. In other
words, the corticofugal functions, named "egocentric selection,"
adjust and improve the cortical neurons' own input and, consequently,
cortical signal processing, perhaps according to auditory experience
(Yan and Suga 1996
).
The Doppler-shifted constant frequency (DSCF) area of the primary
auditory cortex of the mustached bat is large and consists of neurons
extremely sharply tuned to ~61 kHz. The disproportionally large DSCF
area and the sharp tuning of DSCF neurons can be easily correlated with
fine frequency analysis of the DSCF component of an echo for processing
velocity information (Suga and Jen 1976). A focal
inactivation of cortical DSCF neurons tuned to, say, 61.2 kHz with a
local anesthetic drastically reduces the excitatory responses of
thalamic and collicular DSCF neurons tuned to 61.2 kHz ("matched"
subcortical neurons) without shifting their BFs. However, subcortical
neurons tuned to frequencies slightly higher or lower than 61.2 kHz
("unmatched" subcortical neurons) increase their excitatory
responses and shift their BFs toward 61.2 kHz. These corticofugal
effects are almost two times larger on thalamic neurons than on
collicular neurons (Zhang et al. 1997
). Therefore egocentric selection works for the adjustment and improvement of
auditory signal processing not only in the time domain but also in the
frequency domain. A focal activation of the cortical DSCF area with
electric pulses is expected to produce the changes in subcortical DSCF
neurons that are opposite to those evoked by the focal inactivation of
the cortical DSCF area. The aim of the present paper is to report our
findings resulting from cortical activation experiments that are
complementary to the cortical inactivation experiments.
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METHODS |
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Materials, surgery, recording of neural activity, and acoustic
stimulation were basically the same as those described in Suga et al. (1983). Cortical electrical stimulation, data
acquisition, and data processing were basically the same as those
described in Yan and Suga (1996)
. The essential portions
of the methods are summarized in the following text.
Nine adult mustached bats were used for the present experiments. The
"resting" frequency of the second harmonic CF component (CF2) of biosonar signals emitted by each bat was
measured before surgery. The CF2 resting
frequency was used to normalize the BFs of individual neurons to those
in the mustached bat, which emitted biosonar pulses at a 61.00 kHz
CF2 resting frequency (Suga and Tsuzuki
1985). Under neuroleptanalgesia (Innovar 4.08 mg/kg body wt),
the dorsal surface of the bat's skull was exposed and a 1.8 cm-long
metal post was glued onto the skull. Four days after the surgery, the
unanesthetized bat was placed in a styrofoam restraint suspended by an
elastic band at the center of a soundproof, echo-attenuated room
maintained at 30-32°C. The head was immobilized by fixing the post
on the skull to a metal rod with set-screws and adjusted to face
directly at a condenser loudspeaker located 74 cm away. DSCF neurons of
the bat emitting biosonar pulses of a 61.00 kHz CF2 resting frequency are tuned to 60.6-62.3 kHz
sounds (Suga et al. 1987
) and are clustered in the DSCF
area of the auditory cortex (AC), the ventral division of the
medial geniculate body (MGB), and the dorsoposterior division of the
inferior colliculus (IC). To record their auditory responses, a
tungsten-wire microelectrode was inserted into one of these structures
through holes of ~50 µm in diameter made in the skull. DSCF neurons
were identified by their BFs and locations in the AC, MGB, and IC. A
BAK amplitude window discriminator was used to isolate action
potentials of single neurons.
Electrical stimulation
The best frequencies of cortical neurons were first measured at
four to five loci in the DSCF area representing 60.47-62.30 kHz, as in
our previous experiments (Zhang et al. 1997). To
activate one of these cortical loci, a tungsten wire electrode
(negative pole) was placed at a depth of ~700 µm from the cortical
surface and another (positive pole) was placed at a depth of ~150
µm. (The AC of the mustached bat is ~900-µm thick.) A 100-nA,
0.2-ms electrical pulse was delivered to the cortical locus at a rate of 5/s for 7 min through these electrodes. Each electric pulse was
synchronized with the onset of each acoustic stimulus.
Acoustic stimulation
The acoustic stimuli were 23-ms-long tone bursts with a 0.5-ms rise-decay time. These were generated by a voltage-controlled oscillator and an electronic switch, and were delivered at a rate of 5/s. The frequency of a tone burst was varied manually or by a computer.
Collicular, thalamic and cortical DSCF neurons were tuned to particular frequencies (BFs), and particular amplitudes (best amplitudes). To obtain a "frequency-response" curve of a single neuron, the amplitudes of the tone bursts of a computer-controlled frequency scan were set at the best amplitude of a given neuron, which was usually ~30 dB above minimum threshold. When the best amplitude of a neuron could not be determined because of a monotonic or plateau amplitude-response curve, the amplitudes of the tone bursts were set at 30 dB above minimum threshold of the neuron. The frequency scan consisted of 21 time blocks. In the first 20 blocks, frequency was changed in 0.10-kHz steps, and in the 21st (last) block, no stimulus was presented to count background discharges. The duration of each block was 200 ms so that the duration of the frequency scan was 4,200 ms. An identical frequency scan was repeated 50 times, and the responses of a single neuron to them were displayed as an array of peri-stimulus time (PST) histograms or PST cumulative (PSTC) histograms (Figs. 1 and 2).
To obtain a "frequency-tuning" curve of a single neuron, both the frequency and amplitude of a tone burst were computer controlled. In this frequency-amplitude scan, an identical frequency scan consisting of 33 time blocks was delivered five times. Every five scans, the amplitude of the tone bursts was changed in a 5-dB step from 0 to 100 dB SPL. Action potentials discharged by a single neuron were displayed as a raster (Fig. 6A) or the arrays of PST or PSTC histograms. A frequency-tuning curve was obtained with a criterion of threshold at 20% increase in background discharges.
Data acquisition and processing
To study the effects of cortical activation on the auditory responses of neurons in the MGB and the IC (hereafter, subcortical neurons), the responses of single subcortical neurons to tone bursts in the frequency or frequency-amplitude scan were recorded with a computer before, during, and after the focal cortical activation with electric pulses. The waveform of an action potential was stored on a digital storage oscilloscope at the beginning of the data acquisition. This waveform was used to compare with incoming action potentials. Action potentials were continuously monitored on the screen of the digital storage oscilloscope before, during, and after the cortical activation. Data acquisition was continued as far as incoming action potentials visually matched the template. Data were stored on a computer hard drive and were used for off-line analysis.
Off-line data processing included plotting PST or PSTC histograms displaying responses to 50 identical acoustic stimuli and frequency-response curves based on frequency scans or frequency-tuning curves based on frequency-amplitude scans obtained before, during, and after cortical activation. The magnitude of auditory responses was expressed by a number of impulses per 50 identical stimuli after subtracting background discharges counted in the last block of the frequency or frequency-amplitude scan. A t-test was used to test the difference between the auditory responses obtained before and after the focal cortical stimulation and to test the difference between the responses of thalamic and collicular neurons.
The following criteria were used for a shift in the frequency-response
or -tuning curve (or BF) of a subcortical neuron evoked by a focal
cortical activation. If a shifted frequency-response or -tuning curve
did not recover by 50%, the data were excluded from the analysis. In
stable, long recording conditions, all curves shifted by the cortical
activation 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 responses to five consecutive frequency
scans (Blaisdell 1993). 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 obtained for control and stimulus
conditions were significantly different for P < 0.05. The criterion for an increase or decrease in response magnitude (number
of impulses per stimulus) was a change of 20% from a control value.
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RESULTS |
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All neurons studied and reported in the present paper were sharply tuned to a sound between 60.47 and 62.30 kHz. For simplicity, they are called DSCF neurons. The number of DSCF neurons studied was 62 in the AC, 32 in the MGB, and 30 in the IC. The cortical neurons were first recorded to measure their BFs and then electrically stimulated. On the other hand, the subcortical neurons were recorded and were studied to examine the effects of the electrical stimulation of the cortical neurons on their responses.
When cortical DSCF neurons were electrically stimulated, subcortical
neurons showed either augmentation of the auditory responses at their
BFs and no BF shift (i.e., no shift in frequency-tuning curve) or
suppression of the auditory responses at their BFs and BF shift (i.e.,
shift in frequency-tuning curve). Subcortical neurons that showed no BF
shift had a BF within ±0.2 kHz of the BF of electrically stimulated
cortical neurons (hereafter, cortical BF), while those that showed BF
shift had a BF different by more than 0.2 kHz from the cortical BF.
These two groups of neurons are called "matched" and
"unmatched" neurons, respectively. The effects of focal cortical
activation on subcortical neurons were opposite to those of focal
cortical inactivation on them reported by Zhang et al.
(1997).
In our sample, eight thalamic and six collicular neurons were matched
in BF to electrically stimulated cortical neurons. Figure 1A shows the PST histograms
displaying the responses to tone bursts (a) and the arrays
of PSTC histograms displaying frequency-response curves (b)
of a thalamic neuron which was tuned to 61.40 kHz (Fig. 1Ab1; ). When cortical neurons tuned to 61.50 kHz
(b2,
) were electrically stimulated, the responses to
tone bursts of 61.3-61.5 kHz increased, but the BF stayed the same,
61.4 kHz (x in b2). The increase in response was 75.9% of
the control at 61.40 kHz. This increase was due to an overall increase
in response and was not due to an increase in the later portion of the
response, nor to an addition of a long latency response
(a2). Therefore the envelope of the PST histogram of the
augmented response (a2) was the same as that in the control
condition (a1). The increase in response was not accompanied
by an increase in background discharges (the last PSTC histogram in
b2). This was also true in 11 neurons of the 14. The
augmented response reduced toward the response in the control condition
(hereafter, recovered) by 71.6% 39 min after the cessation of the
cortical electrical stimulation (b3). Complete recovery was
observed 69 min after the electrical stimulation.
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Figure 1B shows the responses to tone bursts (a)
and frequency-response curves (b) of a collicular neuron
which was tuned to 60.91 kHz (b1, ). When cortical
neurons tuned to 61.00 kHz (b2,
) were electrically
stimulated, the responses to tone bursts of 60.3-61.5 kHz increased
but the BF stayed the same, 60.9 kHz (b2, x). The increase
in response was 53.9% of the control at 60.9 kHz. This was due to an
overall increase in response (a2), which was not accompanied
by an increase in background discharges (the last PSTC histogram in
b2). The augmented response recovered by 84.6% 42 min after
the cessation of the cortical electrical stimulation (b3).
Complete recovery was observed 108 min after the electrical stimulation.
In our sample, 24 thalamic and 24 collicular neurons were unmatched in
BF to electrically stimulated cortical neurons. Figure 2A shows the PST histograms
displaying responses to tone bursts (a) and the arrays of
PSTC histograms displaying frequency-response curves (b) of
a thalamic neuron tuned to 60.70 kHz. When cortical neurons tuned to
61.50 kHz were electrically stimulated (b2, ), all the
responses to tone bursts shown in b1 reduced. The amount of
the reduction was 80.8% at 60.7 kHz. Percent reduction was smaller at
frequencies <60.7 and was only 42.4% at 60.5 kHz. As a result of
these frequency-dependent percent reductions, the BF shifted from 60.7 kHz to 60.5 kHz (b2, x), together with the frequency-response curve (b2). That is, the BF and the
frequency-response curve shifted away from the cortical BF. The
decrease in response was due to an overall decrease in response
(a2), including a decrease in background discharges (the
last PSTC histogram in b2). This was also true in 19 neurons
out of the 48. The suppressed responses recovered by 89.4% 35 min
after the cessation of the cortical electric stimulation
(b3).
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Figure 2B shows the responses to tone bursts (a)
and the frequency-response curves (b) of a collicular neuron
tuned to 61.22 kHz (b1, ). Electrical stimulation of the
cortical neurons tuned to 60.70 kHz (b2,
) reduced all
the responses of the collicular neuron to tone bursts from 60.9 to 61.8 kHz (b2). Percent reduction was large for 61.2 kHz (77.6%)
and frequencies below it, but was small for frequencies higher than
61.2 kHz (e.g., 27.4% at 61.3 kHz). As a result of these
frequency-dependent reductions, the BF shifted from 61.2 to 61.3 kHz
(b2, x) together with the frequency-response curve. That is,
it shifted away from the cortical BF. The reduction in response was due
to an overall decrease in response. However, the long-latency component
of the response (a1, right of
) was more reduced
than the short latency component (a2). The decrease in
response was not accompanied by a decrease in background discharges (the last PSTC histogram in b2). This was also observed in
29 neurons of the 48. The responses and the frequency-response curve of
the neuron recovered to those in the control condition ~26 min after
the cessation of the cortical electrical stimulation.
To substantiate the corticofugal modulation of the frequency-response curves of subcortical neurons described in the preceding text, Fig. 3 shows the frequency-response curves of three thalamic (A-C) and three collicular neurons (D-F) measured prior to, during, and after focal electrical stimulation of the AC. The responses of matched subcortical neurons (A and D) were augmented, and their frequency-response curves and BFs were not shifted at all by cortical electric stimulation. On the other hand, the response of the unmatched neurons (B, C, E, and F) were reduced, and their frequency-response curves and BFs were shifted by cortical electric stimulation. The direction of the shifts in the curves and BFs of subcortical neurons depended on the relationship in BF between the stimulated cortical neurons and recorded subcortical neurons studied in a pair. When the cortical BF was higher than the subcortical BF, the shift was toward low frequencies (B and E). When the cortical BF was lower than the subcortical BF, the shift was toward high frequencies (C and F). In other words, the directions of BF shifts and shifts in tuning curves were always away from the BF of electrically stimulated cortical neurons.
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A percent change in response magnitude and a BF shift were measured for
each of the 32 thalamic and the 30 collicular neurons studied (Fig.
4). The percent increase in the responses
of matched neurons at their BFs was 54.2 ± 29.2% (21.6-109%)
for the eight thalamic neurons and 37.3 ± 18.2% (10.1-66.0%)
for the six collicular neurons (Fig. 4, A and C,
). The thalamic increase appeared to be 1.5 times larger than the
collicular increase. However, the difference in percent increase is
statistically insignificant (P = 0.11) due to a large
variation and a small sample. The percent change in the responses of
unmatched neurons at their BFs in the control condition was 54.9 ± 17.8% (25.0-86.3%) for the 24 thalamic neurons and 40.7 ± 17.7% (10.2-68.9%) for the 24 collicular neurons (Fig. 4,
A and C,
). The thalamic decrease was 1.4 times larger than the collicular decrease. This difference in percent
decrease is significant (P < 0.01). The percent
changes in the responses of the unmatched neurons were also calculated
at BFs in the shifted condition by cortical electrical stimulation. The
change was 23.2 ± 16.9% (
10.9-47.7%) for the 24 thalamic
neurons and 7.59 ± 14.5% (
12.9-39.0%) for the 24 collicular
neurons (Fig. 4, A and C,
). The thalamic
decrease was 3.1 times larger than the collicular decrease. This
difference is also significant (P < 0.01). Therefore corticofugal effects on the thalamic neurons are larger than those on
the collicular neurons.
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A change in BF was zero for both the eight matched thalamic and the six
matched collicular neurons (Fig. 4, B and D,
). However, it linearly increased with an increase in BF difference
between recorded subcortical neurons and electrically stimulated
cortical neurons. The direction of BF shifts was centrifugal (Fig. 4,
B and D,
). The slope of a regression line
(a) and the correlation coefficient (r) were,
respectively, 0.30 and 0.89 for the thalamic neurons and 0.20 and 0.82 for the collicular neurons. The slope of the regression line was 1.5 times steeper for the thalamic neurons than for the collicular neurons.
This difference in slope is significant (P < 0.05).
The dashed lines in Fig. 4, B and D, obtained by
Zhang et al. (1997)
, are respectively the regression lines for the BF shifts of thalamic and collicular neurons evoked by
focal inactivation of cortical neurons. The direction of the BF shifts
is centripetal and the slope of the regression line is 0.33 for the
thalamic neurons and 0.18 for the collicular neurons. The effect of
cortical inactivation was 1.8 times larger on the thalamic neurons than
on the collicular neurons. This difference in slope is also significant
(P < 0.05).
All the frequency-response curves in the present paper were measured with tone bursts fixed at the best amplitude or 30 dB above minimum threshold of a given neuron. The shifts in a frequency-response curve and BF were always associated with an overall shift in a frequency-tuning curve along the frequency axis. Figure 5 shows the frequency-tuning curves of matched (A and C) and unmatched subcortical neurons (B and D) to electrically stimulated cortical neurons. The thalamic neuron in A tuned to 61.61 kHz showed augmented responses to tone bursts and no shift, with slight narrowing of its tuning curve (P < 0.01 for 60 dB SPL) for the electrical stimulation of the cortical neurons also tuned to 61.61 kHz. The shape of the tuning curve returned to that in the control condition 106 min after the electrical stimulation. The collicular neuron in C tuned to 60.80 kHz did not change its tuning curve at all, but increased its responses to tone bursts for the electrical stimulation of the cortical neurons also tuned to 60.80 kHz. Its augmented responses returned to the responses in the control condition 64 min after the cortical electrical stimulation. The thalamic neuron in B was tuned to 60.64 kHz. Its tuning curve shifted to 60.94 kHz for the electrical stimulation of the cortical neurons tuned to 60.04 kHz. The collicular neuron in D was tuned to 61.53 kHz. Its tuning curve shifted down to 61.43 kHz for the electrical stimulation of the cortical neurons tuned to 62.03 kHz. The "shifted" tuning curves in both B and D were slightly narrower than the curves in the control condition (P < 0.01). These curves returned to the curves in the control condition 138 min after the electrical stimulation.
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As described in the preceding text, the frequency-tuning curves of
unmatched collicular neurons tuned to sounds between 60.5 and 62.3 kHz
shifted away from the BF of electrically stimulated cortical neurons.
The amount of the shift could be very small, only 0.1 kHz, but was
significant. To substantiate this further, an additional example of a
shift in frequency-tuning curve is shown in Fig.
6. The rasters in Fig. 6A show
action potentials discharged by a thalamic neuron with a 61.32 kHz BF
during the frequency-amplitude scan (see METHODS). In the
control condition, the neuron responded to a sound between 61.22 and
61.42 kHz. It was very sharply tuned to 61.32 kHz. Its response to the
61.32 kHz tone burst appeared between 22 and 72 dB SPL, which were the minimum and upper thresholds of the neuron, respectively
(A1). When 61.03 kHz tuned cortical neurons () were
electrically stimulated, the response of this thalamic neuron decreased
to 61.32 kHz, dramatically increased to 61.42 kHz and appeared for
61.52 kHz. As a result, the frequency-tuning curve of the neuron
shifted higher by 0.1 kHz (A2) (P < 0.01).
The shifted frequency-tuning curve returned to that in the control
condition 110 min after the cortical electrical stimulation
(A3). In Fig. 6B, all action potentials
discharged over 12-72 dB SPL shown in Fig. 6A are summed up
as a function of the frequency scan. It is clear that the peak response
at 61.32 kHz shifted to 61.42 kHz for the cortical electrical
stimulation and then returned to 61.32 kHz 110 min after the cortical
stimulation (P < 0.01). Background discharges of this
collicular neuron were not affected by the cortical electrical
stimulation.
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As shown in Fig. 5, A, B, and D, frequency-tuning curves of some subcortical neurons became narrower when cortical neurons are electrically stimulated. A width of a tuning curve was measured at 10, 30, 50, and 70 dB above the minimum threshold of each of the 32 thalamic and 30 collicular neurons studied with cortical electrical stimulation. A change in width due to cortical electric stimulation is plotted as a function of the difference between the BFs of recorded subcortical and stimulated cortical neurons (Fig. 7). Ten thalamic and 8 collicular neurons showed changes larger than 0.1 kHz at 50 dB above minimum threshold. However, neither thalamic nor collicular neurons, except one thalamic neuron, showed a change larger than 0.1 kHz at 10 dB above minimum threshold.
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DISCUSSION |
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Corticofugal modulation of matched and unmatched subcortical neurons
As shown in our present paper, focal cortical activation with
electric pulses evoked the changes in subcortical neurons that were
opposite to those evoked by cortical inactivation. Namely matched
subcortical neurons, with BFs within ±0.2 kHz of the BF of the
activated cortical neurons, were augmented, without shifting their BFs,
by a focal cortical activation. Unmatched subcortical neurons, with BFs
different by more than ±0.2 kHz from the BF of the activated cortical
neurons, were inhibited at their BFs and were shifted in BF by a
focal cortical activation. The BF shifts, always accompanied with the
shifts in frequency-tuning curves, were based on
frequency-dependent inhibition and facilitation. The frequency-tuning
curves of most matched and unmatched subcortical neurons were sharpened
by a focal cortical activation. [It has been known that the width of a
frequency-tuning curve sharpened by lateral inhibition generally does
not change at 10 dB above minimum threshold but changes noticeably at
higher stimulus levels (e.g., Suga et al. 1997). This is
also true for our data shown in Fig. 7.] These corticofugal functions,
called "egocentric selection," were first found in an auditory
subsystem specialized for processing echo delays, bearing
target-distance information (Suga et al. 1995
;
Yan and Suga 1996
). Our present and previous experiments (Zhang et al. 1997
) indicate that exactly the same
mechanisms operate for the processing of auditory information not only
in the time domain but also in the frequency domain and that the subcortical frequency map and response properties of subcortical neurons are adjusted and improved by the corticofugal system according to cortical excitation.
Difference in egocentric selection between two species of bats
The recent data obtained from the big brown bat (Chowdhury
and Suga 2000; Gao and Suga 1998
; Yan and
Suga 1998
) and the mustached bat (Zhang et al.
1997
; the present paper) indicate that the effects of
egocentric selection on subcortical neurons are different between these
two species of bats. This difference, described in the following text
in detail, indicates that when the ascending auditory system is
specialized for fine frequency analysis, the corticofugal system is
also specialized for fine frequency analysis.
In the big brown bat (Yan and Suga 1998), a focal
cortical activation augments the auditory responses of collicular
neurons whose BFs are within ±0.5 kHz of the BF of the electrically
stimulated cortical neurons (not within ±0.2 kHz as in the mustached
bat). The BFs of these matched collicular neurons are not shifted by the focal cortical activation. The difference in the range of BFs of
matched neurons between the two species appears to be related to the
difference in the sharpness of frequency-tuning curves: wider in the
big brown bat than in the DSCF neurons of the mustached bat. The effect
of the focal cortical activation on unmatched collicular neurons is
inhibitory on the responses at the BFs of collicular neurons in both
the species. However, the direction of BF shifts is centripetal and
asymmetrical in the big brown bat and centrifugal and symmetrical in
the mustached bat. The centripetal BF shifts evoke overrepresentation
of the frequencies adjacent to the frequency to which activated
cortical neurons are tuned, while the centrifugal BF shifts evoke
underrepresentation of frequencies adjacent to the frequency to which
the activated cortical neurons are tuned.
Yan and Suga (1998) speculated that the difference in BF
shift between the big brown bat and the mustached bat is related to the
difference in shape and sharpness of the frequency-tuning curves
between these two species of bats. As in the little brown bat,
Myotis lucifugus (Suga 1964
), guinea pig
(Evans 1975
), cat (Liberman 1978
), and
monkey (Katsuki et al. 1962
), the high-frequency slope
of frequency-tuning curves of peripheral neurons in the big brown bat
is presumably much steeper than the low-frequency slope. Thus a
stimulus tone at a given frequency co-activates many more neurons tuned
to higher frequencies than neurons tuned to lower frequencies. The
corticofugal projection perhaps reflects this, and co-excitation of
subcortical neurons by the corticofugal system is presumably related to
BF shifts toward the BF of neurons optimally excited. On the other
hand, at the auditory periphery of the mustached bat, frequency-tuning
curves tuned to ~61 kHz are extremely sharp and symmetrical in shape
(Suga and Jen 1977
). A stimulation with a ~61-kHz tone
burst excites only neurons tuned to ~61 kHz. In the central auditory
system, such focal excitation is associated with strong lateral
inhibition (Suga 1995
; Suga and Manabe
1982
). The corticofugal projection of the mustached bat perhaps
reflects these and evokes centrifugal BF shifts. The mechanisms for
centripetal and centrifugal BF shifts remain to be explored. However,
it is clear that the auditory system of the mustached bat is highly
specialized for fine frequency analysis not only in its ascending
system but also in its descending (corticofugal) system. Corticofugal
modulation observed in the big brown bat is presumably common among
many mammalian species.
The range of the BFs of unmatched neurons that are affected by focal
cortical activation is also quite different between these two species
of bats: from 5 to 17 kHz (asymmetrical BF shifts) in the big brown
bat (Chowdhury and Suga 2000
; Gao and Suga
1998
; Yan and Suga 1998
) and ±1.6 kHz
(symmetrical BF shifts) in the mustached bat (Zhang et al.
1997
; the present paper). This large difference in the affected
ranges is apparently related to the difference in sharpness of the
frequency-tuning curve: generally wide in the big brown bat
(Haplea et al. 1994
) and very sharp without exception in
the mustached bat at the DSCF area of the cortex (Suga
1995
; Suga and Manabe 1982
) and at the periphery (Suga and Jen 1977
; Suga et al. 1975
).
Possible functions of egocentric selection
Focal cortical inactivation evokes suppression of auditory
responses of matched subcortical neurons, augmentation of the responses of unmatched subcortical neurons, BF shift of the unmatched subcortical neurons toward the BF of inactivated cortical neurons, and broadening of frequency-tuning curves of both matched and unmatched subcortical neurons (Zhang et al. 1997). Focal cortical activation
evokes the phenomena opposite to the preceding ones, as described in our present paper. These observations indicate that the corticofugal system improves and adjusts subcortical auditory signal processing, in
other words, cortical neurons improve and adjust their own input
through the corticofugal system and that auditory signal processing
would become poor without the corticofugal system.
Since neurons with a BF at ~61 kHz are very sensitive and
sharply tuned to ~61 kHz in the mustached bat, one may consider that
no improvement in their response properties is necessary. We are not in
a position to discuss whether it is necessary or unnecessary but to
describe what is going on in the central auditory system. A nonfocal
inactivation of the cortical DSCF area with muscimol reduces
single-tone responses by 34% in the inferior colliculus and by 60% in
the medial geniculate body (Zhang and Suga 1997).
Therefore subcortical auditory responses to tone bursts would be
noticeably small without the corticofugal system. It is clear that the
corticofugal system plays an important role in subcortical signal processing.
In our present experiments, focal cortical activation was evoked by a
stimulus of 100-nA, 0.2-ms-long electric pulses delivered at a rate of
5/s for 7 min. Each electric pulse perhaps directly excited cortical
neurons within a ~60-µm radius around a stimulating electrode
(Yan and Suga 1996). The mustached bat emits biosonar pulses at a rate of 5-10/s during the search or cruising phase of
echolocation so that its auditory system is self-stimulated at this
rate. The cortical electrical stimulation is of course unnatural but is
somewhat comparable to the self-stimulation by the emitted pulses.
Corticofugal modulation of collicular neurons described in our present
paper occurs in a slow time course. Therefore BF shifts, for example,
do not occur every time when the bat emits a biosonar pulse. Instead
corticofugal modulation (egocentric selection) occurs to maintain the
auditory system in a state appropriate for signal processing in a given
auditory environment. In the big brown bat, Jen et al.
(1998) found short-latency "rapid" modulation of collicular
responses following each cortical electric stimulation with a train of
four electric pulses (1.25-85 µA, 0.1-ms long each). This rapid
modulation was either facilitation of responses accompanied with
broadening of frequency tuning or inhibition of neurons accompanied
with sharpening of frequency tuning. These two types of modulation were
found for both matched and unmatched collicular neurons. Corticofugal
inhibition and facilitation were found for 74 and 26% of collicular
neurons studied, respectively. Therefore they suggested that the
function of corticofugal modulation is to improve the processing of
subsequent biosonar signals for echolocation.
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. It has been demonstrated that cortical
over-representation can be evoked by electrical stimulation of a
particular portion of the cortex (Chowdhury and Suga
2000
; Maldonado and Gerstein 1996
; Nudo
et al. 1996
; Recanzone et al. 1993
;
Spengler and Dinse 1994
; Yan and Suga
1998
). In the big brown bat, Yan and Suga (1998)
studied "short-term" corticofugal modulation, which lasted
180
min. They stimulated the auditory cortex with a train of four electric
pulses (100 nA, 0.2-ms long each) and found facilitation of responses
of matched collicular neurons and suppression of responses at BFs of
unmatched neurons. Gao and Suga (1998
, 2000
) obtained
the data indicating that the short-term corticofugal modulation is
directly involved in long-term plasticity of the auditory cortex evoked
by auditory conditioning. The data we have reported in our present
paper is different from these. The strong augmentation of the responses
of matched subcortical DSCF neurons and the centrifugal BF shifts of
unmatched subcortical DSCF neurons are related to the specialization of
the auditory system of the mustached bat for extremely fine frequency
analysis of the frequency-modulated echoes from flying insects.
Regardless of the difference in corticofugal effect between the
mustached bat and the big brown bat, the corticofugal system of the
mustached bat is most likely to be directly involved in long-term
plasticity of the auditory cortex as that of the big brown bat is.
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ACKNOWLEDGMENTS |
---|
We thank Dr. Jun Yan for help with data processing and N. Laleman for editing the manuscript.
This work was supported by a research grant from the National Institute on Deafness and Other Communication Disorders (DC-00175).
Present address of Y. Zhang: Dept. of Immunology and Molecular Genetics, Mt. Sinai Hospital Research Institute, University of Toronto, 600 University Ave., Toronto, Ontario M5G 1X5, Canada.
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FOOTNOTES |
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Address for reprint requests: N. Suga, Dept. of Biology, Washington University, 1 Brookings Dr., St. Louis, MO 63130 (E-mail: suga{at}biology.wustl.edu).
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 February 2000; accepted in final form 31 March 2000.
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REFERENCES |
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