Full text of DOI:10.1007/BF02900434

NOTES
tatory frequency tuning curves (EFTCs) of IC neurons can
be changed by corticofugal innervation[7—10]. AC stimula-
tion narrowed the EFTCs and asymmetrically expanded
the lateral inhibitory frequency tuning curves (IFTCs) of
corticofugally inhibited IC neurons, the opposite results
were observed in corticofugally facilitated IC neurons[8].
In spite of these studies, little is known about the mecha-
nism of improvement of excitatory frequency tuning dur-
ing corticofugal modulation.
Corticofugal modulation of
frequency tuning of inferior
collicular neurons in big
brown bat, Eptesicus fuscus
ZHANG Jiping1, SUN Xinde1 & Philip H.-S. Jen2
In this study, we examined the change of sharpness,
frequency-intensity response area and MT of EFTCs and
IFTCs of IC neurons with and without activation of audi-
tory cortex. Possible mechanism has been discussed.
1. Department of Biology, East China Normal University, Shanghai
200062, China;
2. Division of Biological Sciences, University of Missouri-Columbia,
MO 65211, USA
Correspondence should be addressed to Zhang Jiping (e-mail: jiping
zhang@yahoo.com)
1
Materials and methods
(ν) Materials. Surgical procedures and the ex-
Abstract
In order to explore the possible mechanism of
perimental setup were basically the same as in the previ-
ous studies[8]. Briefly, one or two days before the re-
cording session, each of 10 big brown bats, Eptesicus
fuscus (b.w. 17.0—28.5 g), was anesthetized with nembu-
tal (45—50 mg/kg b.w.) for surgery. The flat head of a 1.8
cm nail was attached to the anterior portion of the exposed
skull of each bat with acrylic glue and dental cement for
later fixation of the head. During recording, the bat was
corticofugal modulation of excitatory frequency tuning
curves (EFTCs) of midbrain neurons, we examined the
change of sharpness, frequency-intensity response area,
minimum threshold of both EFTCs and inhibitory frequency
tuning curves (IFTCs) of inferior collicular neurons during
corticofugal modulation using two-tone inhibition paradigm
and micro-electrical stimulation technique. Our data showed
that corticofugal inhibition increased sharpness, minimum
threshold, and decreased the frequency-intensity response
area of EFTCs, at the same time it decreased the sharpness,
minimum threshold but increased the frequency-intensity
response area of IFTCs. The opposite results were observed
for EFTCs and IFTCs of corticofugally facilitated inferior
collicular neurons. During corticofugal inhibition, the per-
cent change of frequency-intensity response area of EFTCs
had significant correlation with the percent change of that of
IFTCs. These data suggest that cortical neurons are likely to
improve frequency information processing of inferior col-
licular neurons by modulation of IFTCs.
tied to an aluminum plate inside
a double-wall
sound-proof room. After fixing the head, small holes were
bored in the skull above the primary AC and the IC for
insertion of electrodes.
(ξ) Sound stimulation. Continuous sine waves
from an oscillator (KH-1400) were formed into 3 ms
pulses (0.5 ms rise-decay times) by a tone burst generator
driven by a stimulator. The sound pulses were amplified
after passing through a decade attenuator before being fed
into a small condenser loudspeaker placed 27 cm away
from the bat. The loudspeaker was calibrated with a Brüel
& Kjaer 1/4 inch (4135) microphone placed at the bat’s
head. The output was expressed in dB SPL in reference to
20 PPa.
(ο) Electrical stimulation. A custom-made two
tungsten-in-glass electrodes (tip: <10ꢀPm, inter-tip dis-
tance: 30—50 Pm) was inserted into the AC at depths of
600—700 Pm corresponding to the 5th layer of the AC
where corticofugal fibers originate[11]. AC stimulation was
4 ms train stimulus consisting of 4 monophasic pulses of
0.1 ms at 2 trains/s and the electrical current was 4—55
PA.
Keywords: bat, auditory cortex, inferior colliculus, frequency tuning,
modulation.
During sensory information coding, the sensory in-
formation is not only edited and integrated by ascending
sensory pathway but also modulated by descending sen-
sory pathway. The inferior colliculus (IC), a very impor-
tant relay station in the ascending auditory pathway, re-
ceives almost all the inputs from the auditory nuclei below
the IC. The auditory cortex (AC), a principal target of the
ascending auditory pathway, may modulate the processing
of ascending information via descending projection to the
medial geniculate body and the IC[1—6]. Thus, the cor-
tico-collicular pathway is a very good model to study the
physiological significance of the role of descending audi-
tory system in sensory coding. As frequency discrimina-
tion is one of the most important factors during auditory
signal processing, we are particularly interested in corti-
cofugal effects on the frequency tuning of IC neurons.
Previous studies have shown that the bandwidth of exci-
(π) Recording. During experiments, the responses
of AC neurons within the 5th layer of AC were isolated by
the tungsten-in-glass electrodes. Then acoustically driven
IC neurons were isolated using 3 mol/L KCl glass micro-
pipette electrodes (impedance 5—10 M:). Recorded ac-
tion potentials were amplified with conventional tech-
niques and sent to a computer for acquisition of PST his-
836
Chinese Science Bulletin Vol. 46 No. 10 May 2001

tograms. The best frequency (BF) and minimum threshold
(MT) of each IC neuron were determined by systemati-
cally changing the frequency and intensity of sound pulses.
The MT was defined as the intensity at which probability
of responding to BF sounds was 50%. The response of IC
neurons to BF sounds (at 10 dB above the MT) was then
examined with AC stimulation. When the neuron’s re-
sponse was affected by AC stimulation, the interval be-
tween electrical and sound stimuli was adjusted to pro-
duce maximal corticofugal effect. At this interstimulus
interval, the electrical current that produced 30%—40%
corticofugal effect was chosen for subsequent experi-
ments.
creased QndB values of IFTCs (two-tailed paired t-test,
P>0.05).
The neuron’s EFTC was plotted by determining the
threshold to each responsive frequency. A two-tone inhibi-
tion paradigm was used to plot IFTC[8,12]. A fixed (excita-
tory) tone was delivered at the BF and 10 dB above the
excitatory MT. Then a test (inhibitory) tone (delivered 3
ms prior to the excitatory tone) was used to determine the
frequency-intensity combinations at which the neuron’s
response to the excitatory tone was reduced by 50%.
(ρ) Data analysis. The sharpness of frequency
tuning curves was expressed with a QndB value that was
obtained by dividing the BF by the bandwidth at n dB
above the MT. The size of frequency intensity response
areas was calculated by first normalizing the frequency
tuning curves with a Cricket program using a Macintosh
computer. The normalized areas in cm2 were then calcu-
lated with a MacDraft program.
Fig. 1. EFTCs and IFTCs of a corticofugally inhibited IC neuron (a)
and a corticofugally facilitated IC neuron (b) under acoustical stimula-
tion only (as) and acoustical stimulation plus electrical stimulation
(as+es) of AC. The IFTCs were depicted as shaded areas. For compari-
son, EFTCs measured before electrical stimulation were replotted (dotted
curves) under “as+es” conditions. The dashed line labeled with in (a)-1
*
indicates the BF axis of EFTCs.
2
Results
Corticofugal inhibition decreased the frequency-
intensity response areas of EFTCs but increased the fre-
quency-intensity response areas of IFTCs, and the oppo-
site effects were observed in corticofugal facilitation (fig.
3). We divided the frequency-intensity response area of
EFTCs into two parts according to its best frequency axis
A total of 48 corticofugally influenced auditory neu-
rons were isolated from the IC. Of these, 40 were inhib-
ited and 8 were facilitated. Electrical stimulation of AC
decreased the number of impulses of corticofugally inhib-
ited and increased the number of impulses of corticofu-
gally facilitated IC neurons. The IFTCs determined by
two-tone inhibition paradigm were lateral or covered the
entire upper portion of the EFTCs. Corticofugal inhibition
narrowed the EFTCs and broadened the IFTCs of IC neu-
rons. The IFTCs expanded into previously excitatory fre-
quency regions (fig. 1(a)-1 vs. fig. 1(a)-2). The opposite
effects were observed in corticofugal facilitation. The
IFTCs narrowed or disappeared during corticofugal fa-
cilitation and the EFTCs expanded into previously inhibi-
tory frequency regions (fig. 1(b)-1 vs. fig. 1(b)-2).
(fig. 1(a)-1, the axis with ), and defined the EFTCs in the
*
low (or high) frequency flank of its best frequency axis as
low (or high) flank EFTCs. It showed that during cortico-
fugal inhibition the percent change of the fre-
quency-intensity response areas of low flank EFTCs was
negatively correlated with that of low flank IFTCs (fig.
4(a)), and the percent change of the frequency-intensity
response area of high flank EFTCs was also negatively
correlated with that of high flank IFTCs (fig. 4(b)).
Table 1 shows the minimum threshold of EFTCs and
IFTCs with and without electrical stimulation of the AC.
During corticofugal inhibition, AC stimulation signifi-
cantly increased the MTs of EFTCs but decreased the MTs
of IFTCs (two-tailed paired t-test, P<0.0001), and corti-
cofugal facilitation produced the opposite effects. As the
sample of corticofugal facilitated IC neurons is small, we
did not perform t-test.
Fig. 2 shows the comparison of QndB values of
EFTCs and IFTCs with and without electrical stimulation
of the AC. Corticofugal inhibition significantly increased
QndB values of EFTCs but decreased QndB values of IFTCs
(two-tailed paired t-test, P<0.05), and corticofugal facili-
tation significantly decreased QndB values of EFTCs
(two-tailed paired t-test, P<0.05) but not significantly in-
Chinese Science Bulletin Vol. 46 No. 10 May 2001
837

NOTES
Fig. 2. Comparison of QndB values of EFTCs and IFTCs of IC neurons determined under different stimulus conditions. The dot-
ted line represents equal values. Ɣ or ż, Corticofugally inhibited or facilitated IC neurons; ni or nf, number of corticofually inhib-
ited or facilitated IC neurons studied.
Fig. 3. Comparisons of frequency intensity response area of EFTCs and IFTCs (h10ꢁ2 cm2) determined under “as” and “as+es”
conditions. The dotted line represents equal values. IFTCl or IFTCh, low or high flank IFTCs.
IFTCs as observed by blocking GABAergic inputs in the
3
Discussion
Previous studies have demonstrated the role of
IC, and that corticofugal facilitation had the opposite ef-
fects. Because AC stimulation always produced closely
related effects on flanking IFTCs and EFTCs, such as the
change of QndB values, MT and frequency-intensity re-
sponse area, we suggest that corticofugal modulation of
EFTCs may be mediated through modulation of IFTCs.
Corticofugal inhibition expanded the inhibitory frequency
regions so as to sharpen the EFTCs, and corticofugal fa-
IFTCs in sharpening the EFTCs. Blocking GABAergic
inputs in the inferior colliculus completely or partially
eliminated the IFTCs, and also resulted an expansion of
EFTCs into frequency regions that were previously in-
hibitory [12]. In the present study, we found that corticofu-
gal facilitation had the similar effects on EFTCs and
838
Chinese Science Bulletin Vol. 46 No. 10 May 2001

Fig. 4. Correlation between percent
change of frequency intensity response
area of EFTCs and IFTCs of corticofu-
gally inhibited IC neurons determined
under “as” and “as+es” conditions.
EFTCl or EFTCh, low or high flank
EFTCs; IFTCl or IFTCh, low or high
flank IFTCs.
Table 1 Average minimum threshold (dB SPL) of EFTCs and IFTCs of inferior collicular neurons
determined under different stimulus conditionsa)
MT(as)
MT(as+es)
P
'MT
Inhibition
EFTC
IFTCl
IFTCh
EFTC
IFTCl
IFTCh
<0.0001
<0.0001
<0.0001
40.35r9.55 (40)
65.33r14.44 (33)
65.82r11.77 (34)
35.25r10.53 (8)
60.13r12.86 (8)
57.00r16.75 (5)
45.57r9.66 (40)
61.34r16.35 (38)
56.32r14.12 (34)
31.88r9.67 (8)
68.0r12.28 (4)
64.60r19.15 (5)
4.82r2.58 (40)
ꢁ7.03r3.98 (33)
ꢁ9.50r5.88 (34)
ꢁ3.58r2.31 (8)
10.25r4.99 (4)
7.60r4.51 (5)
Facilitation
a) as, Acoustical stimulation; es, electrical stimulation; 'MT, MT (as+es)-MT(as); P, two-tailed paired t-test P value. Number of neurons studied
is shown in parentheses.
liculus, J. Neurochem., 1995, 65: 1348.
cilitation blocked some of the inhibitory inputs so that the
EFTCs expanded to the previously inhibitory frequency
regions.
3. Herbert, H., Aschoff, A., Ostwald, J., Topography of projections
from the auditory cortex to the inferior colliculus in the rat, J.
Comp. Neurol., 1991, 304: 103.
One of the functions of corticofugal modulation is to
improve the signal to noise ratio in signal processing. In
our study, we found that corticofugal inhibition increased
the sharpness and MT of EFTCs and corticofugal facilita-
tion decreased the sharpness and MT of EFTCs of IC
neurons, and the opposite effects were observed in IFTCs
of IC neurons. As the big brown bats rely on the echoloca-
tion system to find the target and perceive target feature,
we suggest that bats may also use corticofugal system to
improve signal to noise ratio in target detection and fine
frequency analysis. Bats may utilize corticofugal facilita-
tion to increase the sensitivity to the echoes so as to en-
hance target detection during the early phase of hunting,
and as they are approaching the targets, the echoes be-
come stronger, they may utilize corticofugal inhibition to
increase the MT and sharpness of EFTCs to improve fine
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7. Jen, P. H. S., Chen, Q. C., Sun, X. D., Corticofugal regulation of
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processing in bat auditory system, Nature, 1997, 387: 900.
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Acknowledgements This work was supported by the National Natural
Science Foundation of China (Grant No. 39870246) and the research
fund from the National Science Foundation of USA (Grant No. NSF IBN
9604238).
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