Department of Neurobiology, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272-0095
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ABSTRACT |
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Portfors, Christine V. and
Jeffrey J. Wenstrup.
Delay-Tuned Neurons in the Inferior Colliculus of the Mustached
Bat: Implications for Analyses of Target Distance.
J. Neurophysiol. 82: 1326-1338, 1999.
We examined response properties of delay-tuned neurons in the
central nucleus of the inferior colliculus (ICC) of the mustached bat.
In the mustached bat, delay-tuned neurons respond best to the
combination of the first-harmonic, frequency-modulated (FM1) sweep in
the emitted pulse and a higher harmonic frequency-modulated (FM2, FM3
or FM4) component in returning echoes and are referred to as FM-FM
neurons. We also examined H1-CF2 neurons. H1-CF2 neurons responded to
simultaneous presentation of the first harmonic (H1) in the emitted
pulse and the second constant frequency (CF2) component in returning
echoes. These neurons served as a comparison as they are thought to
encode different features of sonar targets than FM-FM neurons. Only 7%
of our neurons (14/198) displayed a single excitatory tuning curve. The
rest of the neurons (184) displayed complex responses to sounds in two
separate frequency bands. The majority (51%, 101) of neurons were
facilitated by the combination of specific components in the mustached
bat's vocalizations. Twenty-five percent showed purely inhibitory
interactions. The remaining neurons responded to two separate
frequencies, without any facilitation or inhibition. FM-FM neurons (69)
were facilitated by the FM1 component in the simulated pulse and a
higher harmonic FM component in simulated echoes, provided the
high-frequency signal was delayed the appropriate amount. The delay
producing maximal facilitation ("best delay") among FM-FM neurons
ranged between 0 and 20 ms, corresponding to target distances 3.4 m.
Sharpness of delay tuning varied among FM-FM neurons with 50% delay
widths between 2 and 13 ms. On average, the facilitated responses of
FM-FM neurons were 104% greater than the sum of the responses to the
two signals alone. In comparing response properties of delay-tuned,
FM-FM neurons in the ICC with those in the medial geniculate body (MGB) from other studies, we find that the range of best delays, sharpness of
delay tuning and strength of facilitation are similar in the ICC and
MGB. This suggests that by the level of the IC, the basic response
properties of FM-FM neurons are established, and they do not undergo
extensive transformations with ascending auditory processing.
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INTRODUCTION |
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Analyzing the distance to a target is an important
task for many animals. Echolocating bats use the time interval (delay) between their emitted sonar vocalization and a returning echo to obtain
target distance information (Simmons 1971, 1973
;
Simmons et al. 1979
). The echolocation calls of most
bats contain a brief, frequency-modulated (FM) sweep that is well
suited for determining target distance information (Simmons and
Stein 1980
; Simmons et al. 1979
). This
information is encoded by neurons tuned to the delay between the FM
sweep in the emitted call and the returning FM sweep in an echo
(delay-tuned neurons). These delay-tuned neurons occur in the central
auditory systems of several species of bats (Myotis
lucifugus, Sullivan 1982a
,b
; Eptesicus
fuscus, Dear et al. 1993
; Feng et al.
1978
; Rhinolophus rouxi, Schuller et al. 1988
, 1991
; Pteronotus parnellii, O'Neill
and Suga 1979
; Suga et al. 1979
). In this study,
we examine the basic response properties of delay-tuned neurons in the
central nucleus of the inferior colliculus in the mustached bat to
understand the mechanisms underlying their delay tuning.
Delay-tuned neurons in the mustached bat, P. parnellii,
differ in one major respect from those in most other bat species
studied. In bats like E. fuscus, delay-tuned neurons respond
to the same FM harmonic in the simulated pulse and echo (Dear et
al. 1993; Feng et al. 1978
). However, in the
mustached bat, delay-tuned neurons respond to different FM harmonics in
the simulated pulse and echo, integrating information from different
frequency bands (O'Neill and Suga 1979
, 1982
;
Suga and O'Neill 1979
; Suga et al. 1979
,
1983
). Specifically, they respond well to the combination of
frequencies within the first-harmonic FM (FM1) sweep from the emitted
sound and frequencies within a higher harmonic FM (FM2, FM3, or FM4)
component of the echoes (O'Neill and Suga 1979
, 1982
; Suga and O'Neill 1979
; Suga et al. 1979
,
1983
). These delay-tuned neurons are called FM-FM due to their
responsiveness to the combination of FM sweeps in the sonar call. FM-FM
neurons in the mustached bat are an example of a broader class of
neurons also found in other vertebrates, called combination- sensitive,
that respond to combinations of different frequencies in vocalizations
(frogs, Fuzessery and Feng 1983
; birds,
Margoliash and Fortune 1992
; bats, Ohlemiller et
al. 1996
; Schuller et al. 1988
, 1991
;
Suga 1988
; Suga et al. 1979
, 1983
;
monkeys, Olsen 1994
).
In the mustached bat, combination-sensitive neurons are found in the
auditory cortex (Fitzpatrick et al. 1993;
O'Neill and Suga 1979
; Suga and O'Neill
1979
; Suga et al. 1979
, 1983
), the medial
geniculate body (MGB) (Olsen and Suga 1991a
,b
; Wenstrup, 1999
) and the ICC (Mittmann and Wenstrup 1995
;
O'Neill 1985
). We address the question of whether
response properties are modified within the ascending auditory pathway.
The major focus here is transformations in delay-tuning properties
between the ICC and MGB, the main synaptic relay between the auditory
midbrain and the auditory cortex. There is some evidence that FM-FM
neurons in the MGB have sharper delay tuning and stronger facilitation than FM-FM neurons in the ICC (Yan and Suga 1996
). In
this paper, we compare the response properties of a large population of
FM-FM neurons in the ICC with response properties of MGB neurons
documented in other studies (Olsen and Suga 1991b
;
Yan and Suga 1996
; Wenstrup 1999
). We find that most
basic response properties of FM-FM neurons related to delay sensitivity
are similar in the ICC and MGB.
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METHODS |
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Surgical procedure
We examined responses of single neurons in the ICC to pure tones in nine mustached bats (P. parnellii parnellii) from Jamaica, West Indies. Bats were anesthetized with methoxyflurane (Metofane, Mallinckrodt Veterinary, Mundelein, IL) in combination with sodium pentobarbital (5 mg/kg ip; Nembutal, Abbott Laboratories, North Chicago, IL) and acepromazine (2 mg/kg ip; Med-Tech, Buffalo, NY). The dorsal surface of the inferior colliculus was exposed by reflecting the skin and musculature overlying the skull. A tungsten reference electrode was implanted into the right cerebral cortex and cemented in place. A metal pin was cemented to the skull to secure the bat's head during physiological recordings. A small hole was cut in the skull (usually <0.5 mm) over the appropriate region of the inferior colliculus. We applied a local anesthetic (lidocaine, Elkins-Sinns, Cherry Hill, NJ) and a topical antibiotic to the edges of the cut tissue and allowed the bat to recover from surgery for 2-3 days before electrophysiological recording. These procedures were approved by the Northeastern Ohio Universities College of Medicine Animal Care and Use Committee.
Acoustic stimulation and recording procedures
During physiological recording sessions, the awake bat was placed in a Plexiglas restraining apparatus contained in a heated and humidified acoustic chamber. The acoustic chamber was covered inside with anechoic foam to reduce echoes. Acoustic stimuli were delivered through a speaker (Technics leaf tweeter) placed 10 cm away from the bat and 25° into the sound field contralateral to the inferior colliculus under investigation. A computer running custom-made applications within the Labview environment (National Instruments) controlled the acoustic stimulation and data acquisition. Two arbitrary waveform generators (Wavetek, model 395) produced two different tone burst or frequency modulated sweep stimuli (3- to 30-ms duration, 0.5-ms rise/fall time, 3-4/s). The two sinusoids from the signal generators were shaped with switches (Tucker-Davis Technologies, model SW2), attenuated (Tucker-Davis Technologies, model PA4), added (Tucker-Davis Technologies, model SM3), fed to a power amplifier (Parasound, model HCA-800 II), and then fed to the speaker in the recording chamber.
We recorded single neurons using micropipette electrodes (5-20 M
resistance) filled with one of several tracers (dextran-conjugated rhodamine, dextran rhodamine green, biotin dextran amine (Molecular Probes, Eugene, OR) or Fluoro-Gold (Fluorochrome, Engleweed, CO) in 1 M
NaCl (or 0.9% physiological saline when using Fluoro-Gold). The action
potentials were amplified, filtered (band-pass, 500-6,000 Hz) and fed
to a window discriminator (Frederick Haer, model 74-60-3), loudspeaker, and oscilloscope. The pulse output of the window discriminator was digitized at 10 kHz (National Instruments, model NB-MIO-16X) for quantitative data analysis including
peristimulus (PST) histograms, raster displays, and
statistics on the neural responses.
The electrodes were advanced through the hole in the skull into the inferior colliculus by a hydraulic micropositioner (David Kopf Instruments, model 650). We directed the electrode penetrations to record single neurons in tonotopic regions of the ICC representing the higher frequencies of the mustached bat's audible range (55-120 kHz). For the majority of recording sessions, we set the electrode penetration angle at 15-20° directed lateral to medial.
Most tests were conducted with tone burst stimuli (3- to 30-ms duration, 0.5-ms rise/fall time). When a single neuron was isolated, we obtained its best frequency, threshold and tuning curve audiovisually. We defined best frequency (BF) as the frequency requiring the lowest intensity to elicit stimulus-locked spikes and threshold as the lowest intensity required to elicit one or more spikes from each of five consecutive stimuli. For neurons that were responsive to two frequency bands, we refer to a best high-frequency response and a best low-frequency response.
We then tested the neuron for sensitivity to a combination of two frequencies by presenting both a low- and a high-frequency signal. Sensitivity to delay between the low- and high-frequency signals was assessed by varying the delay in steps of 1 or 2 ms and collecting neural responses to 32 presentations of the stimuli at each delay. The range of delays tested included conditions with the low-frequency signal presented first and the high-frequency signal delayed and also with the high-frequency signal presented first and the low-frequency signal delayed. All delay tests were performed using 3-ms tone bursts with 0.5-ms rise/fall times (total duration of 4 ms). The delay between the low- and high-frequency signals that elicited the greatest response (or the least response in the case of an inhibited combination-sensitive effect) was defined as the neuron's best delay. By plotting the neural response at each delay, we quantified sharpness of delay tuning by measuring the width of the delay response curve at 50% of the maximal facilitated (or inhibited) response. We then tuned the facilitated or inhibited response. For facilitated neurons, we tuned both the low- and high-frequency sounds. To assess the low frequencies that elicited a facilitated response, the high-frequency signal was held constant, and the low frequencies eliciting a facilitated response at various intensities were recorded. Then the low-frequency signal was held constant, and the responses to the high frequencies were tuned across intensities. For inhibited neurons, we determined the range of low frequencies that inhibited the high-frequency response while the high-frequency sound was held constant. For both facilitated and inhibited responses, the sound held constant was typically presented at 10 dB above threshold.
The strength of combination-sensitive facilitation or inhibition was
quantified in two ways: as a percent change compared with the sum of
the individual responses to the high- and low-frequency signals and as
an interaction index that was defined as (Rc Rl
Rh)/(Rc + Rl + Rh) where Rc, Rl and Rh are, respectively, the neuron's
responses to the combination of the high- and low-frequency signals,
low-frequency signal alone, and high-frequency signal alone
(Dear and Suga 1995
). A positive interaction value is
referred to as a facilitation index and a negative value an inhibition index. A neuron was classified as facilitated if the facilitation index
was
0.09, corresponding to an increase in response of 20% above the
summed responses to the low- and high-frequency sounds. A neuron was
inhibited if the inhibition index was
0.11, corresponding to at
least a 20% decrease in response from the summed responses to the low-
and high-frequency signals. A facilitation index of 1.0 indicates the
strongest possible facilitation, whereas an inhibition index of
1.0
indicates the strongest inhibition.
At the end of penetrations where we recorded several single neurons, we deposited the tracer that was in the recording electrode. Ionotophoretic deposits using positive current (+5 µA, 5-10 min, 50% duty cycle) usually were made where we documented a delay-tuned neuron and were always in the ICC.
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RESULTS |
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In dorsolateral to ventromedial electrode penetrations through the ICC, we recorded 198 single neurons having best high frequencies between 54.0 and 110.0 kHz. Most neurons were from the tonotopic representations of two frequency bands, 60-63 and 72-89 kHz. Neurons in the tonotopic representation of the 72- to 89-kHz frequency band respond to sounds within the frequency range of the third-harmonic, frequency-modulated (FM3) sweep of the sonar signal (Fig. 1). A major goal of this study was to characterize neurons responding to this frequency band, and thus the majority of neurons recorded had best frequencies between 72 and 89 kHz. The 60- to 63-kHz representation in the ICC comprises the dorsoposterior division, and its neurons respond to frequencies in the range of the second-harmonic, constant-frequency (CF2) component of the mustached bat sonar signal (Fig. 1). Neurons responsive to CF2 signals serve as a comparison to neurons responding to FM3 signals because the two types of neurons are thought to encode different features of sonar targets.
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We tested the neurons for tuning to multiple frequency bands and for sensitivity to combinations of signals with different frequencies. Only 7% (14/198) of the neurons had simple frequency-tuning characteristics showing only a single excitatory, V-shaped tuning curve. The rest of the neurons (n = 184) responded to two separate frequency bands, and of these, 151 showed either facilitated or inhibited combination-sensitive responses (as defined in METHODS). Most combination-sensitive neurons were FM-FM or H1-CF. FM-FM neurons responded to the combination of a low-frequency signal within the FM1 frequency band (29-24 kHz) and a signal in a frequency band associated with one of the higher harmonic FM sweeps (e.g., FM3; 89-72 kHz). H1-CF neurons responded to the combination of signals in the first-harmonic (H1) frequency band (31-24 kHz) and a frequency band associated with one of the higher harmonic CF signals e.g., H1-CF2. We recorded a third type of combination-sensitive response ("other" in Fig. 2) that was neither FM-FM nor H1-CF. These neurons responded to signals within the CF2 frequency band in combination with frequencies below (18-22 kHz) the range of the first sonar harmonic.
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The majority of ICC neurons we recorded (76%, n = 151) were combination-sensitive. For both FM-FM and H1-CF combination-sensitive responses, facilitated responses (70%) were more common than inhibited responses (30%). Figure 2 summarizes the occurrence of all response types, which are described in detail in the following sections. RESULTS describes the frequency tuning, the frequency interactions, and the temporal properties of the facilitated combination-sensitive neurons, then the same for the inhibited combination-sensitive neurons. Finally, we briefly describe the response properties of another 33 neurons that displayed multiple frequency tuning without any combination-sensitive interaction.
Facilitated combination-sensitive responses
FREQUENCY-TUNING PROPERTIES.
Combination-sensitive facilitation was recorded in 69 FM-FM neurons and
32 H1-CF neurons. These two groups were distinguished on the basis of
their high-frequency sensitivity (Fig.
3). Figure 3A shows the
frequency tuning of an FM-FM neuron. This neuron showed an excitatory
tuning curve centered in the FM3 sonar band (BF: 76.0 kHz), and it did
not respond to low-frequency signals within the FM1 band at all
intensities tested (100 dB SPL). However, when a low-frequency signal
was presented in combination with the high-frequency signal at BF, the
response was facilitated. This facilitated response was similarly tuned
in frequency (- - - and
), with a slight decrease in threshold (31 to 26 dB SPL). Among FM-FM neurons, the average threshold for the
high-frequency signal presented individually was 37.8 ± 6.7 (SD) dB SPL. The average threshold for the facilitated
high-frequency response was 32.4 ± 7.8 dB SPL, indicating a
slight, but not significant, decrease in threshold with facilitation.
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DELAY SENSITIVITY. A characteristic feature of FM-FM and H1-CF neurons is their sensitivity to the timing between the high and low frequency signals. In Fig. 4 the responses of a facilitated FM-FM neuron to single sounds and the combination of a low- and high-frequency sound are shown. The neuron did not respond to the presentation of any low-frequency sounds within the FM1 range, even at high intensities (Fig. 4A). A sound within the FM3 frequency band (BF: 82.7 kHz) elicited a weak response (Fig. 4B). Figure 4C, however, shows that the neuron was strongly facilitated by the combination of the two sounds, if the onset of the high-frequency signal was delayed 2 ms from the onset of the low-frequency signal. The facilitation index value for this neuron was 0.73. The magnitude of the facilitation can be seen both from the PST histograms and the facilitation index; this was a strongly facilitated response. The facilitated response was tuned in delay (Fig. 4D), such that there was a maximal response at 2 ms, and the response was reduced at shorter and longer delays. The delay at which the peak facilitation occurred is termed the neuron's "best delay". H1-CF neurons also showed tuned responses to delay. The major difference in the two populations was the distribution of best delays (Fig. 5A). FM-FM neurons had best delays ranging from 0 to 20 ms, with the greatest proportion (84%) <10 ms. In contrast, nearly all (95%) H1-CF neurons had best delays ~0 ms. Thus the range of best delays is a distinguishing feature of FM-FM neurons.
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STRENGTH OF FACILITATION.
The strength of the facilitated response indicates the degree of
selectivity for preferred delays. The strength of facilitation was
measured as the facilitation index (see METHODS) to enable a comparison with previously published data on facilitated, delay-tuned neurons in the ICC and MGB. To be defined as facilitated, the response
to the combination of both tone bursts had to be 20% (FI = 0.09) greater than the sum of the responses to the high-frequency and
the low-frequency signals presented separately. Among the sample of
FM-FM neurons, the mean response rate to tone bursts at best
high-frequency presented 10 dB above thresholds was 0.51 ± 0.45 spikes/stimulus. The mean response rate to tone bursts at best low
frequency was 0.21 ± 0.32 spikes/stimulus, and the mean
facilitated response rate was 1.39 ± 0.65 spikes/stimulus. The
distribution of facilitation index values (Fig.
7) shows that the majority of values were
between 0.1 and 0.5 for FM-FM neurons (average 0.34 ± 0.24),
corresponding to an average response increase of 104%.
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LATENCY AND DELAY-TUNED FACILITATION.
Delay-tuned FM-FM neurons showed strong facilitation with a broad range
of best delays. A possible mechanism for creating these response
properties involves the coincidence of excitatory responses to the low-
and high-frequency signals (Suga et al. 1990). This
coincidence hypothesis requires that the response to the low-frequency
component (simulated pulse) be neurally delayed to coincide with the
response to the acoustically delayed higher frequency signal (simulated
echo). The timing of the responses to the low- and high-frequency
signals is likely reflected in the latencies of response to these
signals presented individually. We therefore examined the latencies of
FM-FM neurons in response to their best low and high frequencies. The
response latencies to best high frequencies ranged from 4 to 12 ms,
with a clustering ~7 ms (average latency: 6.6 ± 1.6 ms).
Because not all FM-FM neurons showed an excitatory response to
low-frequency signals presented alone, we could measure response
latencies in only 19 (28%) of the delay-tuned neurons. Among these,
latency to low-frequency sounds ranged from 6 to 30 ms (average
latency: 12.8 ± 6.3 ms).
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Inhibited combination-sensitive responses
A second type of combination-sensitive interaction recorded in the ICC was inhibitory. In inhibited FM-FM neurons, the excitatory response to a high-frequency signal was inhibited by simultaneous presentation of a low-frequency signal. Twenty-eight FM-FM neurons and 15 H1-CF2 neurons displayed inhibited combination-sensitive responses (Fig. 2).
FREQUENCY-TUNING PROPERTIES. Inhibited combination-sensitive neurons displayed typical excitatory tuning curves in response to high-frequency stimulation. Figure 10A shows an FM-FM neuron for which the excitatory response was tuned to 79.8 kHz. There was no excitatory response to signals within the FM1 frequency range presented alone. However, the neuron's excitatory response to the high-frequency signal was strongly inhibited by simultaneous presentation of signals within the FM1 frequency band. The shaded tuning curve in Fig. 10A shows the frequencies and intensities that produced detectable inhibition of the high-frequency response. The best frequency of inhibition was 27.0 kHz, within the FM1 frequency band. For most inhibited combination-sensitive neurons, the low-frequency inhibition was tuned within the frequency range of the first sonar harmonic. However, seven units with best high frequencies in the CF2 frequency range were inhibited by a second signal in the 18- to 23-kHz frequency range, below the first sonar harmonic.
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SENSITIVITY TO DELAY. As with facilitated neurons, inhibited FM-FM and H1-CF neurons were sensitive to the timing of the two signals. The characteristic feature of these neurons, however, is that the strongest inhibition occurred at simultaneous presentation of the two signals. The delay curve in Fig. 10B shows that the neuron's response to the high-frequency signal was strongly inhibited by simultaneous presentation of a low-frequency signal. Thus the best delay of inhibition was 0 ms. The inhibited neurons had a narrow distribution of best delays of inhibition, with most (84%) at 0 ms. The sharpness of delay tuning (50% delay width) among inhibited FM-FM neurons varied between 2 and 10 ms with an average 50% delay width of 5.9 ± 1.8 ms.
STRENGTH OF INHIBITION. The neuron in Fig. 10B illustrates a strongly inhibited combination-sensitive response. At simultaneous presentation of the low- and high-frequency signals, the response of the neuron was suppressed by 85%. For the population of inhibited FM-FM neurons, there was a broad distribution of inhibition strengths (Fig. 7). The average response rate to the best high-frequency signal presented 10 dB above threshold was 1.23 ± 0.67 spikes/stimulus. The mean inhibited response rate was 0.52 ± 0.53 spikes/stimulus. Corresponding values for H1-CF neurons were 1.7 ± 0.84 and 1.04 ± 1.02 spikes/stimulus, respectively.
Multiply tuned complex interactions
Eighteen neurons in the FM3 representation and 15 neurons in CF2 representation of the ICC showed complex response properties without any facilitated or inhibited response. These neurons displayed two separate excitatory tuning curves with best frequencies separated by an octave or more. The responses to low-frequency signals were clearly separate from the high-frequency responses and were not the flanks of the high-frequency excitatory tuning curves. Seven of the CF2 multiply tuned neurons had best low frequencies of 18-23 kHz, below the range of the first sonar harmonic.
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DISCUSSION |
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This study describes the physiological response properties of
combination-sensitive neurons in the mustached bat's ICC with the main
objective of understanding the mechanisms underlying delay tuning. A
variety of combination-sensitive responses occur in the mustached
bat's ICC, and we found that these responses are abundant in the
tonotopic regions representing the frequencies in the higher harmonics
of the sonar signal. In contrast, Leroy and Wenstrup
(1996) did not find combination-sensitive responses in the
tontopic regions representing the first harmonic of the sonar signal.
In our sample of neurons, 76% showed a combination-sensitive interaction. Fifty-one percent of the neurons were facilitated and 25%
were inhibited combination-sensitive responses. A smaller percentage
(17%) of neurons were tuned to two separate frequency bands without
any facilitation or inhibition. The smallest proportion (7%) of ICC
neurons we recorded were tuned to a single frequency band. The
abundance of combination-sensitive neurons tuned to frequencies
occurring in vocalizations indicates the importance of
combination-sensitive neurons in processing species-specific vocalizations.
FM-FM neurons show specializations of basic response properties related to selectivity for delay. FM-FM neurons in the ICC show relatively strong facilitation when the low (FM1)- and high-frequency signals are combined at the appropriate delay. In our sample, FM-FM neurons had a range of best delays between 0 and 20 ms. Our data bear on two mechanistic issues for creating combination-sensitive responses. First, the data suggest that coincidence of excitatory responses to the low- and high-frequency signals generates the facilitated response. Second, the range of response latencies to the low-frequency signal creates the range of best delays seen among FM-FM neurons.
Response properties of combination-sensitive neurons
Combination-sensitive responses are common throughout the
tonotopic high-frequency regions of the ICC. Recent evidence suggests that these responses, in particular facilitated responses (Leroy and Wenstrup 1998; Wenstrup et al., 1999
), are created
in the ICC. If this is the case, it is important to understand how
response properties at this early stage of processing compare with
response properties at higher levels. As combination-sensitive neurons are found in the ICC, MGB, and auditory cortex, we examine how the
basic response properties of combination-sensitive neurons are
transformed with ascending processing. The major focus here is a
comparison between response properties of delay-tuned, FM-FM neurons in
the ICC and MGB. There is some evidence that sharpness of delay tuning
and strength of facilitation of FM-FM neurons is greater in the MGB
(Yan and Suga 1996
) than in the ICC. Our data suggest
that basic response properties related to coding delay are similar
between the ICC and MGB.
FACILITATED RESPONSE PROPERTIES.
Basic response properties of FM-FM neurons related to coding delay
include the strength of facilitation, best delay, and the sharpness of
delay tuning. The strength of facilitation provides a measure of how
well the neuron responds to the combination of the two signals,
compared with the responses to each signal separately. Most (95%) of
the neurons in the high-frequency tonotopic representations (FM3 and
FM4) responded to high-frequency tone bursts, whereas only ~25% of
these same neurons responded to low-frequency tone bursts. The average
response rate of neurons to best frequency tone bursts was 0.52 ± 0.45 spikes/stimulus when the best high-frequency signal was presented
10 dB above threshold. However, when both the high- and low-frequency
signals were combined at the appropriate delay, the responses of FM-FM
neurons were facilitated with an average response rate of 1.39 ± 0.65 spikes/stimulus. The average facilitation index was 0.34, equating
to a 104% increase in the facilitated response compared with the sum
of the low- and high-frequency sounds alone. This is relatively strong
facilitation when we consider that our criterion for a facilitated
response is 20% above the summed responses. These results differ
sharply from those of Yan and Suga (1996), who, using
identical tone burst stimuli, reported an average facilitation index of
0.08 for FM-FM neurons in the ICC. In fact, almost two-thirds of their
FM-FM neurons had facilitation indices of
0, i.e., they showed no
facilitation when presented with brief tone bursts. We are unsure why
the results of the two studies differ. One possibility may be the
degree of isolation of single-unit recordings. We report here only
results from well-isolated single units. When we recorded from multiple
units, we found that the combination-sensitive responses were generally
less observable and, when observed, were weaker. This may also explain
why Yan and Suga (1996)
found many fewer facilitated
FM-FM units in the ICC (14% of all recorded neurons vs. 51% in our
study). Interestingly, in the MGB, facilitation is observable in
multiple-unit responses (Wenstrup and Grose 1995
;
Wenstrup 1999
). This may be due to the clustering of similar response
types that occurs in the MGB but not in the ICC (Portfors and
Wenstrup 1998
).
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INHIBITED COMBINATION-SENSITIVE RESPONSE PROPERTIES.
The ICC also contains FM-FM inhibited neurons. Among these neurons, the
low-frequency signal inhibits the excitatory response to the higher
frequency signal, around a best delay of 0 ms. Inhibited FM-FM neurons
are common in the tonotopic regions representing the higher frequencies
of the sonar signal. In this study, they comprised 25% of all
acoustically responding neurons. This percentage is similar to that
reported by Mittmann and Wenstrup (1995). Inhibited FM-FM neurons in the ICC first were reported by O'Neill
(1985)
, but an understanding of their functional significance
is lacking. A comparison between the ICC and MGB may provide an
indication of their significance. The most striking change in
combination-sensitive response properties between the ICC and MGB is
the proportion of inhibited FM-FM neurons; the MGB contains very few
(Olsen and Suga 1991a
,b
; Yan and Suga
1996
; Wenstrup 1999
). Only one report documents the proportion
of inhibited FM-FM neurons in MGB. Wenstrup reported that inhibited
FM-FM neurons comprised 9% of acoustically responsive neurons, whereas
facilitated FM-FM neurons comprised 49%. In contrast, we found that
25% of neurons were inhibited and 51% were facilitated in the ICC.
Neural mechanisms underlying delay tuning
Because recent evidence suggests that most facilitated,
delay-tuned responses are created in the inferior colliculus
(Leroy and Wenstrup 1998; Wenstrup et al. 1999
), the
neural mechanisms underlying delay-tuned facilitation probably occur at
the ICC. One goal of the present study was to examine whether the
response properties of delay-tuned, FM-FM neurons in the ICC provide
evidence in support of particular mechanisms for creating delay sensitivity.
The present results strongly support several aspects of the coincidence
hypothesis proposed by Suga and co-workers (Olsen and Suga
1991b; Suga et al. 1990
). Under this hypothesis,
the delay-tuned response of an FM-FM neuron requires the coincidence of
excitatory postsynaptic responses to both a low- and a high-frequency signal. To create delay-tuned facilitation at nonzero delays, responses
to the low-frequency signal must be neurally delayed to coincide with
the acoustically delayed response to the high-frequency signal. Among
MGB neurons, the coincidence mechanism is supported by the finding that
the difference in the latencies of a neuron's excitatory responses to
the low- and high-frequency signals is highly correlated with the
neuron's best delay (Olsen and Suga 1991b
). Among our
ICC neurons in which this could be tested (27%), there was an even
stronger correlation with a nearly one-to-one relationship between the
latency difference and a neuron's best delay.
A second feature of the coincidence mechanism proposed by Olsen
and Suga (1991b) was that the latency of the low-frequency response was most closely related to a neuron's best delay and, therefore, the mechanisms underlying it. Among MGB neurons, there was a
strong correlation between the latency of the low-frequency response
and the best delay, whereas there was no correlation between the
high-frequency latency and the best delay. This is also true of our ICC
neurons. These ICC data, obtained at the probable site of construction
of delay-tuned neurons, emphasize that understanding the mechanism for
the broad distributions of latencies among low-frequency responses is
fundamental to understanding the mechanism that creates the delay-tuned
response. At present, it is unclear whether the long latency response
to the low frequency is created by delay lines present in the low
frequency input to delay-tuned neurons in the ICC or by the
postsynaptic response of these ICC neurons.
The delay tuning properties of FM-FM neurons in the ICC suggest that
inhibition plays a role in eliciting a facilitated
combination-sensitive response (Fig. 6B). This role may be
different for neurons with shorter and longer best delays. For most
FM-FM neurons with best delays >4-6 ms, whether in the ICC (this
study) or MGB (Olsen and Suga 1991b), there is a
pronounced inhibitory period before the facilitation peak. This
inhibitory period may be related to a mechanism that creates a
postinhibitory rebound excitation at the neuron's best delay. In
contrast, there is not as consistent or strong an inhibitory period
preceding facilitation among neurons with best delays <4-6 ms.
However, inhibition does play a role in short best delay neurons
because the application of the glycine antagonist, strychnine,
eliminates the facilitated response among both long and short
best-delay neurons (Leroy and Wenstrup 1998
). These
several observations suggest that there may be more than one role of
inhibition in creating delay tuning and facilitation.
Functional properties of combination-sensitive neurons
NEURAL ANALYSIS OF TARGET DISTANCE.
The main difference between the response properties of FM-FM and H1-CF
neurons is the broad distribution of best delays among facilitated
FM-FM neurons. While H1-CF neurons are tuned to delays ~0 ms
(simultaneous presentation of the low- and high-frequency sounds), the
population of FM-FM neurons are tuned to best delays between 0 and 20 ms. This suggests that FM-FM neurons are involved in coding distance
information. That these neurons have best delays between 0 and 20 ms
indicates that target information at distances up to 3.4 ms could be
coded by these neurons. Although best delays among FM-FM neurons in the
mustached bat ranged between 0 and 20 ms, most (84%) neurons were
tuned to delays of <10 ms. These delays correspond to target ranges up
to 170 cm. A similar distribution of best delays is found in the MGB
(Olsen and Suga 1991b; Wenstrup 1999
) and in the FM-FM
area in the auditory cortex of the mustached bat (O'Neill and
Suga 1979
). Neurons tuned to shorter delays also are emphasized
in the auditory cortex of other bat species. In Rhinolophus
rouxi, delays between 2 and 4 ms predominate (Schuller et
al. 1991
), and in Myotis lucifugus, delays <10 ms
are overrepresented (Wong and Shannon 1988
). However, in
the auditory cortex of Eptesicus fuscus, the big brown
bat, there are more neurons with best delays between 10 and 20 ms,
representing target distances between 170 and 340 cm (Dear et
al. 1993
). This is also the case for delay-tuned neurons in the
superior colliculus (Valentine and Moss 1997
) and other
midbrain regions (Dear and Suga 1995
) in the big brown
bat. The greater number of neurons that are delay-tuned to longer
delays in the big brown bat compared with the mustached bat suggests that the former has a longer operating range for echolocation. This
agrees with the range of distances over which big brown bats detect
insect-sized objects (Kick 1982
). There may be a greater emphasis on neurons with short best delays in the mustached bat because
it forages in more cluttered environments and may have a shorter
operational range for echolocation.
MULTIDIMENSIONAL ANALYSIS OF SONAR TARGETS.
On the other hand, delay-tuned neurons may have a function that is
broader than specifically encoding the distance to a target, and the
broad delay tuning of some neurons may play a different role.
Delay-tuned neurons may function as filters to encode aspects of the
target when it is within a particular extent of space, instead of
encoding the specific distance to the target. While a target is at a
particular distance, delay-tuned neurons that are facilitated by that
delay may encode several aspects of the target important for prey
localization and identification, such as horizontal and vertical
location, texture, or wingbeat frequency. In other words, delay-tuned
neurons are involved in multidimensional analyses of targets when the
targets are within a particular extent of space. Evidence from the
auditory cortex of Myotis lucifugus supports the hypothesis
that delay-tuned neurons are involved in multi-dimensional analyses of
targets (Maekawa et al. 1992; Paschal and Wong
1994
; Sullivan 1982a
). As yet, we do not know whether delay-tuned neurons in the ICC of the mustached bat are selective for other stimulus attributes such as interaural intensity differences or amplitude modulations. However, as a large number of ICC
neurons are delay tuned (>50%), and more than one-third of the
neurons in the ICC are sensitive to interaural intensity differences
(IID), encoding horizontal location (Fuzessery and Pollak
1985
; Wenstrup et al. 1986
), it seems likely
that a sizable number of neurons are both delay tuned and IID
sensitive, for example. In the superior colliculus of the big brown
bat, E. fuscus, delay-tuned neurons are directionally
selective, encoding azimuth, elevation, and distance (Valentine
and Moss 1997
). These neurons may represent the convergence of
target spatial information necessary to guide the motor behavior of the
bat. It seems unlikely that the only functional role of delay-tuned
neurons in any bat species is to encode target distance.
INHIBITED COMBINATION-SENSITIVE NEURONS.
Combination-sensitive inhibited responses in the high-frequency
representations of the ICC comprised 25% of acoustically responsive neurons. The key feature of these neurons is that their inhibition prevents a response to certain spectrally complex stimuli that may be
either communication or echolocation sounds. For example, some neurons
that respond to frequencies in the CF2 (~60 kHz) are inhibited by
simultaneous presentation of low frequencies (18-23 kHz) outside the
sonar range. The mustached bat has a rich repertoire of social
communication calls (Kanwal et al. 1994) that contain
frequencies both within and outside the sonar range. The inhibition
evoked by simultaneous presentation of a nonsonar low-frequency signal
and a CF2 signal may inhibit these neurons from responding to
communication calls within these frequency bands, but they still would
respond to CF2 sonar echoes provided the nonsonar signals are not present.
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ACKNOWLEDGMENTS |
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We thank the three anonymous reviewers for helpful comments on the manuscript and C. Grose and F.-M. Chen for technical assistance. We are grateful to the Natural Resources Conservation Authority of Jamaica for permission to collect bats.
This work was supported by research Grant 5 R01 DC-00937 and S15 DC-02544 from the National Institute on Deafness and Other Communication Disorders.
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FOOTNOTES |
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Address for reprint requests: C. V. Portfors, Dept. of Neurobiology, Northeastern Ohio Universities College of Medicine, 4209 State Route 44, P.O. Box 95, Rootstown, OH 44272-0095.
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 30 November 1998; accepted in final form 19 April 1999.
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REFERENCES |
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