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Department of Biology, Washington University, St. Louis, Missouri 63130
Submitted 25 March 2004; accepted in final form 10 July 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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and Suga et al. 2002 for reviews). The reorganization is attributed to the shifts of best frequencies (BFs), together with frequency–tuning curves of neurons. Focal electric stimulation of the AC evokes 2 types of BF shifts of cortical and subcortical auditory neurons: centripetal and centrifugal. Centripetal BF shifts are the shifts toward the BF of electrically stimulated cortical neurons, whereas centrifugal BF shifts are the shifts away from the stimulated cortical BF. Suga et al. (2000) hypothesized that strong and widespread facilitation evoked by focal electric stimulation of the AC creates centripetal BF shifts, whereas strong and widespread inhibition creates centrifugal BF shifts.
In the auditory (He 1997; Yan and Suga 1996; Zhang et al. 1997), visual (Tsumoto et al. 1978), and somatosensory (Canedo and Aguilar 2000; Malmierca and Nunez 1998) systems of different species of animals, focal cortical electric stimulation evokes facilitation of "matched" subcortical sensory neurons and inhibition of "unmatched" subcortical sensory neurons. Therefore corticofugal positive feedback associated with negative feedback (lateral inhibition) is apparently shared by the different sensory systems of different species of animals. Therefore the hypothesis proposed by Suga et al. (2000) predicts that focal electric stimulation of the sensory cortex evokes "center-surround" reorganization of sensory maps: centripetal shifts of tuning curves (or receptive fields) at the center and centrifugal shifts at the surround. Thus far, however, center-surround reorganization has been found only in the Mongolian gerbil (Sakai and Suga 2002). This is probably because the centrifugal shifts are small and short lasting, making the surround difficult to find. A small number of neurons showing a centrifugal BF shift were found at the edge of the area for centripetal BF shifts in the AC of the big brown bat (Chowdhury and Suga 2000; Ma and Suga 2001, 2003) and in the posterior division of the primary auditory cortex of the mustached bat (Sakai and Suga 2001). It has been reported that the role of the corticofugal pathway in reorganization may be different between the big brown bat and the rat (Nwabueze-Ogbo et al. 2002). We report here that the big brown bat indeed shows center-surround reorganization, and that the big brown bat and gerbil show the identical reorganization of the AC for cortical electric stimulation.
It is reasonable to assume that specialized auditory behaviors are based on specialized auditory mechanisms, and that the specialized auditory mechanisms have evolved from common mechanisms shared by many species of mammals. The auditory system of the mustached bat clearly shows both specialized and nonspecialized neural mechanisms. In the mustached bat, the Doppler-shifted constant-frequency (DSCF) area of the AC and subcortical DSCF regions are highly specialized for the processing of biosonar information in the frequency domain (for review, see Suga 1984, 1994). Electric stimulation of cortical DSCF neurons evokes the centrifugal BF shifts of collicular, thalamic (Zhang et al. 1997), and cortical (Xiao and Suga 2002) DSCF neurons in a large area surrounding the stimulated cortical DSCF neurons or surrounding the collicular and thalamic neurons matched in BF with the stimulated cortical neurons. In the DSCF area, centripetal BF shifts have only been rarely observed (Xiao and Suga 2002). In this highly specialized DSCF area, an antagonist (bicuculline) of inhibitory synaptic transmitter receptors (GABA-A receptors) applied to the stimulation site changes centrifugal BF shifts into centripetal BF shifts (Xiao and Suga 2002). However, it is not yet known whether centrifugal BF shifts found in nonspecialized auditory cortices are also changed into centripetal BF shifts by decreasing inhibition or that centripetal BF shifts are changed into centrifugal BF shifts by increasing inhibition. Here, we show that centrifugal BF shifts at the surround in the AC of the big brown bat are also changed into centripetal BF shifts by bicuculline, and that centripetal BF shifts at the center are changed into centrifugal BF shifts by an agonist (muscimol) of GABA-A receptors. Our present study indicates that nonspecialized and specialized cortical areas share basically an identical mechanism for reorganization, although the specialized area, because of strong lateral inhibition, shows a different type of reorganization of a frequency map from that found in nonspecialized areas.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Surgery, acoustic and electric stimulation, and recording of neural activity were the same as those described in Ma and Suga (2003). Drug applications to the AC were the same as those described in Xiao and Suga (2002). The animal studies committee of Washington University in St. Louis approved the protocol for this research.
Eleven adult big brown bats (Eptesicus fuscus) from Illinois and Missouri were used. Under neuroleptanalgesia (Innovar 4.08 mg/kg b.w.), a 1.5-cm-long metal post was glued onto the dorsal surface of the bat's skull. A local anesthetic (lidocaine HCI) and antibiotic ointment (Furacin) were applied to the surgical wound. Three days after surgery, the awake animal was placed in a polyethylene-foam body mold that was hung with an elastic band at the center of a 31°C soundproof room. The metal post glued onto the skull was attached to a metal rod with set screws to immobilize the animal's head. The head was adjusted to face directly at the loudspeaker located 74 cm away. A few holes (50–100 µm diameter) were made in the skull covering the AC. A pair of tungsten-wire electrodes (tip diameter 
7 µm; 20–35 µm apart, one proximal to the other) was inserted to a 500- to 700-µm depth in the AC through one of the holes. The responses (action potentials) of neurons to tone bursts were recorded and the best frequency (BF) to excite the neurons was measured. Then, this electrode pair was used to electrically stimulate the neurons. A single tungsten-wire electrode (tip diameter 7 µm) was also inserted into the AC through another hole to record the responses of a single neuron to tone bursts and to examine the effect of electric stimulation on the responses. In addition to the electric stimulation, bicuculline methiodide (BMI; an antagonist of inhibitory GABA-A receptors) or muscimol (an agonist of GABA-A receptors) was also applied to the stimulation site, and its effect on the responses of the neuron was examined.
Acoustic stimulation
Acoustic stimuli were 20-ms-long tone bursts with a 0.5-ms rise–decay time. They were generated by a voltage-controlled oscillator and an electronic switch and were delivered at a rate of 5/s with a leaf tweeter. The frequency and amplitude of the tone bursts were varied manually or computer-controlled. When computer-controlled, the frequency of a tone burst in the frequency scan was randomly varied with a stimulus-control and recording software (Tucker-Davis Technologies). The amplitude was calibrated with a Brüel & Kj ær microphone and was expressed in dB SPL.
The frequency–tuning curve of a single cortical neuron was first manually measured. Then the amplitude of a tone burst was fixed at 10 dB above minimum threshold of the neuron, and a computer-controlled frequency scan was delivered. The frequency scan consisted of 21 time blocks 200 ms in length. In the first 20 blocks, frequency was changed in 0.3- or 0.5-kHz steps, and in the 21st (last) block, no stimulus was presented to count background discharges. An identical frequency scan was repeated 50 or 20 times.
Electric stimulation
Electric stimulation was a 6.2-ms-long train of 4 monophasic electric pulses (100 nA, 0.2-ms duration, 2.0-ms interval). The train of electric stimuli was delivered at a rate of 10/s for 30 min to the AC. Such stimulation was estimated to stimulate neurons within a 60-µm radius around the electrode tip (Yan and Suga 1996). The bat showed no behavioral response at all to such weak electric stimulation.
Applications of bicuculline methiodide (BMI) or muscimol
A glass micropipette (tip diameter 10 µm) filled with 5.0 mM BMI or muscimol in saline was placed at the site where the BF of electrically stimulated cortical neurons was measured. Then, 1.0 nl of 5.0 mM BMI or 0.2 µg muscimol was applied to the site with a Picospritzer II (General Valve, Fairfield, NJ). The Picospritzer pulse for a drug application was set at a pressure of 0.67 bar and duration of 30 ms.
Data acquisition
Action potentials of a single cortical neuron tuned to a particular frequency were selected with a time-amplitude window-discriminator software (Tucker-Davis Technologies). At the beginning of data acquisition, the waveform of an action potential was stored and displayed on the monitor screen. This action potential (i.e., template) was compared with action potentials during data acquisition. The responses of the neuron to a frequency scan delivered 50 times, unless otherwise stated, were recorded before and after electric stimulation without or with BMI or muscimol, and were displayed as an array of peristimulus time (PST) histograms or PST-cumulative (PSTC) histograms. The data were stored in the computer hard drive and were used for off-line analysis. In a one-day experiment, only one neuron was studied for the effect of and recovery from electric stimulation and/or BMI or muscimol application.
Off-line data processing
The magnitude of auditory responses of a neuron was expressed by a number of impulses per 50 identical stimuli, unless otherwise stated, and was plotted as the function of frequency to show the frequency–response curve of a neuron. A BF was determined as the frequency to which the neuron showed the largest response. Given that an identical frequency scan was delivered 50 times, there were 50 samples of BFs that could be used to compute a mean and SD of the BFs and to perform statistical analysis: a 2-tailed, paired t-test to determine whether the difference in response magnitude between a BF and adjacent frequencies and between the BFs obtained before and after the electric stimulation and/or drug application was significantly different for P < 0.05. BF shifts and the recovery of the BF shifts observed in all neurons studied were significant (P < 0.05), respectively. Therefore these BF shifts were highly significant (P < 0.0025). In other words, the BF shift evoked by cortical electric stimulation with or without BMI or muscimol was highly significant as it shifted back (i.e., recovered) to the BF in the control condition. The sharpness of the frequency–response curve was measured by the width at a 50% maximum response.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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All neurons recorded or electrically stimulated were within the primary auditory cortex (Fig. 1). Focal electric stimulation of the AC evoked 3 types of changes in the auditory responses of nearby cortical neurons: facilitation without a BF shift (6 neurons with a BF between 21 and 31.5 kHz), centripetal BF shift (34 neurons with a BF between 24 and 48 kHz), and centrifugal BF shift (38 neurons with a BF between 21 and 42 kHz). The BFs of electrically stimulated neurons ranged from 16 to 58 kHz (n = 46).
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). The center-surround reorganization is presumably related to excitatory and inhibitory connections in the auditory cortex (see DISCUSSION).
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). Therefore the frequency axis based on BFs measured in our current study is placed along the distance axis (Fig. 3C). BF shifts occurred within a range between 20 kHz higher and 7 kHz lower than the BF of stimulated neurons. The amount of BF shifts changed with a difference in BF between recorded and stimulated cortical neurons along the frequency axis as shown in Fig. 3C. The largest BF shift occurred at neurons with the BF about 5 kHz higher than that of the stimulated ones. To show the change in the amount of a BF shift as a function of distance from the stimulated neurons along an iso-BF line, the distribution of the amounts of BF shifts along the iso-BF line crossing the BF of the stimulated neurons is plotted for the caudal portion (Fig. 3D) and for the rostral portion (Fig. 3E), separately. As expected from Fig. 3C, the amount of BF shifts was larger at the rostral portion than at the caudal portion. The largest centripetal BF shift was found along the frequency axis crossing the stimulated neurons. BF shifts became smaller with an increase in distance from the stimulated neurons along the iso-BF line. This decrease in BF shift was symmetrical on the dorsal and ventral sides of the stimulated neurons (Fig. 3, D and E). When a recorded neuron was the same in BF as stimulated neurons, the neuron showed no BF shift even if they were separated from each other by certain distances (Figs. 2A, 3D and E). Therefore BF shifts depended on both the distance of a recorded neuron from the stimulated cortical neurons and the difference in BF between the recorded and stimulated neurons.
As described above, the amount of BF shifts evoked by the electric stimulation was asymmetrical along the frequency axis: large on the high-frequency (rostral) side of the stimulated neurons and small on the low-frequency (caudal) side. This asymmetry was related to the nonlinear frequency axis: small BF shifts in the area where the frequency representation was expanded and large BF shifts in the area where the frequency representation was not expanded (Fig. 3C).
The role of inhibition in center-surround reorganization
Out of the 38 neurons that showed a centrifugal BF shift for cortical electric stimulation, 33 neurons were studied to examine the effect of a GABA-A receptor antagonist [bicuculline methiodide (BMI)] on centrifugal BF shifts. In all these neurons, a centrifugal BF shift evoked by electric stimulation was first confirmed. Then, after the recovery of the BF shift, BMI and electric stimulation were applied to the same site. In all these neurons, BMI affected their centrifugal BF shifts: 6 neurons displayed a small reduction in the centrifugal BF shifts, 14 neurons displayed a complete block of their centrifugal BF shifts, and 13 neurons showed a change from a centrifugal to centripetal BF shift and increased their discharges to tone bursts. BMI also increased background discharges in 20 neurons. The neuron in Fig. 4, for example, showed a centrifugal BF shift to electric stimulation (P < 0.05; Fig. 4A), but centripetal BF shift to the electric stimulation accompanied by BMI (P < 0.01; Fig. 4B).
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). A mean centrifugal BF shift at the end of electric stimulation was 0.38 ± 0.06 kHz (n = 38) and its recovery time was 115 ± 12 min (n = 33) (Fig. 5A). For the electric stimulation accompanied by BMI, the mean centrifugal BF shift of the 6 neurons at the end of electric stimulation was 0.31 ± 0.09 kHz, and its recovery time was 90 ± 8 min (Fig. 5B, filled circles). The centrifugal BF shifts of these 6 neurons apparently reduced by BMI (P < 0.05). The mean centripetal BF shift of the 13 neurons at the end of electric stimulation was –0.33 ± 0.11 kHz, and its recovery time was 71 ± 14 min (Fig. 5B, open circles). There is no significant difference in recovery time between BF shifts evoked by electric stimulation with and without BMI (P > 0.05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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In our previous studies (Ma and Suga 2001, 2003), the frequency–response (or frequency–tuning) curves in the control and test conditions were both measured with the identical frequency scans in which the frequency of a tone burst systematically increased. Therefore one might consider that the asymmetrical BF shifts reported in the previous papers depended on the direction of a frequency scan. In our current studies, we used the randomized frequency scan to measure BF shifts. The newly obtained BF shifts (Fig. 3C) also showed the asymmetrical distribution. Therefore the asymmetrical BF shifts reported previously were not attributed to the direction of a frequency scan. Anyway, it is hardly possible that the asymmetrical BF shifts depended on the direction of the frequency scan. As shown in Fig. 3, BF shifts depended on the differences in distance and BF between recorded and electrically stimulated cortical neurons, and the asymmetry is related to the nonlinear frequency (tonotopic) axis. The asymmetry in BF shift has also been found in the Mongolian gerbil (Sakai and Suga 2001, 2002). In the gerbil, the amount of BF shifts was expressed in distance (mm), as well as in frequency (kHz), along the frequency axis, because the frequency axis in millimeters is directly related to best frequencies in kilohertz. Then, it was found that BF shifts in millimeters did not show asymmetry (Sakai and Suga 2002).
Expanded and compressed reorganizations
Centripetal BF shifts result in an increase in the number of neurons responding to frequencies near or equal to the BF of stimulated cortical neurons or the frequency of a repetitively delivered stimulus tone (Gao and Suga 1998, 2000; Ma and Suga 2001; Yan and Suga 1998). Such reorganization is designated "expanded" reorganization. In contrast, centrifugal BF shifts result in a reduced representation that is associated with the augmentation of responses and sharpening of tuning curves of "matched" neurons whose BF is the same as the BF of the stimulated cortical neurons (Zhang et al. 1997). Therefore such reorganization is designated "compressed" reorganization instead of reduced reorganization (Suga et al. 2002). Compressed reorganization is presumably more suited for the improvement of discrimination of acoustic signals than expanded reorganization. In center-surround reorganization in the ACs of the big brown bat and Mongolian gerbil, centripetal BF shifts at the center is larger and longer-lasting than centrifugal BF shifts, so that the major change is expanded reorganization.
Centripetal BF shifts evoked by electric stimulation of cortical neurons have been observed in the cortex (AC) and/or midbrain (IC) of the big brown bat (Chowdhury and Suga 2000; Ma and Suga 2001, 2003; Yan and Suga 1998) mustached bat (Sakai and Suga 2001), Mongolian gerbil (Sakai and Suga 2002), and house mouse (Yan and Ehret 2002). Centripetal BF shifts can also be evoked in the AC by tone bursts paired with electric stimulation of the basal forebrain (guinea pig: Bakin and Weinberger 1996; rat: Kilgard and Merzenich 1998; big brown bat: Ma and Suga 2003) and by auditory fear conditioning (guinea pig: Weinberger and Bakin 1998; big brown bat: Gao and Suga 2000; Ji et al. 2001). The shifts in the receptive fields of neurons in the somatosensory cortex are centripetal in different species of mammals (Buonomano and Merzenich 1998; Rasmusson 2000 for review). The shifts in the orientation selectivity of neurons in the cat visual cortex are also centripetal (Godde et al. 2002). Therefore expanded reorganization is widely shared between mammalian sensory systems. In contrast, compressed reorganization has been reported only in the highly specialized auditory pathways of the mustached bat (Xiao and Suga 2002; Yan and Suga 1996; Zhang et al. 1997).
Change in the direction of BF shifts evoked by drugs
It was hypothesized that a BF shift is evoked by an uneven distribution of excitation or inhibition across the AC and that the direction of a BF shift depends on which is stronger and wider-spread, facilitation or inhibition (Suga et al. 2000). Xiao and Suga (2002) demonstrated that BMI focally applied to the DSCF area of the AC of the mustached bat changes centrifugal BF shifts to centripetal BF shifts and that BMI delivered together with focal electric stimulation of the DSCF area evokes a change slightly larger than that evoked by BMI alone. Therefore our current BMI data may be interpreted that a reduction of inhibition in the AC caused by an antagonist (BMI) of GABA-A receptors evoked a focal increase in excitation of the AC and that such excitation evoked the change from centrifugal BF shifts to centripetal BF shifts.
In our current experiments, a muscimol application to the AC, accompanied with focal electric stimulation of the AC, abolished auditory responses and background discharges within 5 ± 2.3 min. The electric stimulation alone never evoked such strong inhibition. Therefore our data may be interpreted that the change from centripetal BF shifts to centrifugal BF shifts was predominantly, if not totally, caused by the focal inactivation of the AC by muscimol.
Inhibition for centrifugal BF shifts in specialized and nonspecialized cortical areas
The DSCF area of the AC of the mustached bat is large and is highly specialized for fine frequency and amplitude analysis with sharply frequency- and amplitude-tuned neurons and with the frequency-versus-amplitude coordinates (Suga 1977; Suga and Manabe 1982). This area is presumably involved in the fine processing of echoes from flying insects. Lesion of the DSCF area causes a deficit in fine, but not coarse, frequency discrimination (Riquimaroux et al. 1991). Focal electric stimulation of the DSCF area evokes centrifugal BF shifts in the DSCF area surrounding the stimulation site. Centripetal BF shifts are very rare in this area (Xiao and Suga 2002). The AC of the big brown bat is not particularly specialized for fine-frequency analysis and quite different in BF shift from the DSCF area. It shows small centrifugal BF shifts only at the surround (Fig. 3). In spite of such a remarkable difference between 2 species of bats, an antagonist (BMI) of inhibitory synaptic transmitter receptors changes centrifugal BF shifts into centripetal BF shifts in both the DSCF area of the mustached bat (Xiao and Suga 2002) and the AC of the big brown bat (Fig. 4). In the big brown bat, an agonist (muscimol) of inhibitory synaptic transmitter receptors changed centripetal BF shifts into centrifugal BF shifts (Fig. 6).
These data indicate that in the highly specialized area, lateral inhibition is strong compared with the less-specialized area, and that the specialized and nonspecialized areas both share the same inhibitory mechanism for centrifugal BF shifts, although the difference in strengths of facilitation and inhibition causes different types of reorganizations: compressed and expanded. Our current data also indicate that a BF can shift one or the other direction according to the balance between facilitation and inhibition.
Cortical BF shifts and neural net for cortical excitation and inhibition
BF shifts are based on neural interactions. In cats, horizontal arborizations of pyramidal neurons for excitation are classified into short- and long-range projections. The former is 
0.6 mm long and omnidirectional, whereas the latter is several millimeters long and preferentially parallel to iso-BF contour lines (Matsubara and Phillips 1988; Ojima et al. 1991; Reale et al. 1983; Winer 1984). In the small brain of the big brown bat, the short- and long-range projections may be limited: the long-range projection is probably 2.5 mm because iso-BF contour lines are about 2.5 mm long. The center area for centripetal BF shifts is about 0.4 mm in radius. Therefore the short-range horizontal projection of pyramidal neurons may be related to evoking these BF shifts. However, the neural net that may be related to evoking cortical BF shifts is complex. The recurrent fibers of pyramidal neurons form intracortical positive feedback loops. The pyramidal neurons in the deep cortical layers project to the subcortical auditory nuclei, facilitate the auditory responses of subcortical neurons matched in BF, and evoke short-lasting subcortical BF shifts (Ma and Suga 2001, 2003; Yan and Suga 1998; Zhang et al. 1997). Such subcortical BF shifts contribute to evoking long-lasting cortical BF shifts through a feedback loop (Ji et al. 2001). In cats, the recurrent fibers of pyramidal neurons spread over 0.6 to several millimeters within the cortex and form minute connections with inhibitory interneurons. Most inhibitory interneurons (small basket cells) in the auditory cortex radially project 0.2–0.3 mm, forming uniformly dense arbors (Hendry and Jones 1991; Prieto et al. 1994). The surrounding zone for centrifugal BF shifts was 0.5–0.6 mm away from the stimulated cortical neurons and 0.15–0.30 mm wide. Therefore the inhibitory interneurons activated by the recurrent fibers may produce lateral inhibition that evokes centrifugal BF shifts. The neural net and synaptic mechanisms for BF shifts both remain to be further studied.
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: N. Suga (E-mail: suga{at}biology.wustl.edu).
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REFERENCES |
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Y. Zhang and N. Suga Corticofugal Feedback for Collicular Plasticity Evoked by Electric Stimulation of the Inferior Colliculus J Neurophysiol, October 1, 2005; 94(4): 2676 - 2682. [Abstract] [Full Text] [PDF]
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X. Ma and N. Suga Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex PNAS, June 28, 2005; 102(26): 9335 - 9340. [Abstract] [Full Text] [PDF]
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