1Zoological Institute, Munich University, D-80333 Munich; 2Max-Planck-Institute of Neurobiology, D-82152 Martinsried, Germany; and 3Department of Psychology, University of Washington, Seattle, Washington 98195
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Grothe, Benedikt, Ellen Covey, and John H. Casseday. Medial Superior Olive of the Big Brown Bat: Neuronal Responses to Pure Tones, Amplitude Modulations, and Pulse Trains. J. Neurophysiol. 86: 2219-2230, 2001. The structure and function of the medial superior olive (MSO) is highly variable among mammals. In species with large heads and low-frequency hearing, MSO is adapted for processing interaural time differences. In some species with small heads and high-frequency hearing, the MSO is greatly reduced in size; in others, including those echolocating bats that have been examined, the MSO is large. Moreover, the MSO of bats appears to have undergone different functional specializations depending on the type of echolocation call used. The echolocation call of the mustached bat contains a prominent CF component, and its MSO is predominantly monaural; the free-tailed bat uses pure frequency-modulated calls, and its MSO is predominantly binaural. To further explore the relation of call structure to MSO properties, we recorded extracellularly from 97 single neurons in the MSO of the big brown bat, Eptesicus fuscus, a species whose echolocation call is intermediate between that of the mustached bat and the free-tailed bat. The best frequencies of MSO neurons in the big brown bat ranged from 11 to 79 kHz, spanning most of the audible range. Half of the neurons were monaural, excited by sound at the contralateral ear, while the other half showed evidence of binaural interactions, supporting the idea that the binaural characteristics of MSO neurons in the big brown bat are midway between those of the mustached bat and the free-tailed bat. Within the population of binaural neurons, the majority were excited by sound at the contralateral ear and inhibited by sound at the ipsilateral ear; only 21% were excited by sound at either ear. Discharge patterns were characterized as transient ON (37%), primary-like (33%), or transient OFF (23%). When presented with sinusoidally amplitude modulated tones, most neurons had low-pass filter characteristics with cutoffs between 100 and 300 Hz modulation frequency. For comparison with the sinusoidally modulated sounds, we presented trains of tone pips in which the pulse duration and interstimulus interval were varied. The results of these experiments indicated that it is not the modulation frequency but rather the interstimulus interval that determines the low-pass filter characteristics of MSO neurons.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The superior olivary complex is the first stage of the mammalian ascending auditory system at which binaural processing takes place. In the traditional view, the two principal nuclei of the superior olive are thought to function exclusively in the context of azimuthal sound localization. According to this scheme, the lateral superior olive (LSO) processes interaural level differences (ILDs) of high-frequency sounds while the medial superior olive (MSO) processes interaural time differences (ITDs).
The LSO appears to be anatomically and physiologically similar in all
mammals that have been investigated (see Covey and Casseday 1995; Irvine 1992
; Schwartz 1992
for reviews). In contrast, both the structure and the function of the
MSO are highly variable across mammals. In mammals with good
low-frequency hearing and sufficient interaural distance to generate
significant ITDs, the MSO is large, the low frequency representation is
greatly expanded, and most neurons are responsive to sound at either
ear, with the maximal response occurring when both ears are stimulated
with a specific ITD (dogs: Goldberg and Brown 1969
;
cats: Galambos et al. 1959
; Yin and Chan
1990
; gerbils: Spitzer and Semple 1995
; rabbits:
Batra et al. 1997
). In some small mammals with
high-frequency hearing, such as mice, the MSO is very small. However,
despite the fact that echolocating bats are some of the smallest
mammals and have the highest frequency hearing range of any terrestrial mammals, the MSO of many bat species (e.g., mustached bats) is well
differentiated. Moreover, its relative size exceeds that of the MSO in
cats or dogs. Apparently, this increase in size is due to an increase
in the number of cells receiving monaural inputs only (for review, see
Grothe 2000
; Grothe and Park 2000
).
Examination of the MSO in different bat species has revealed pronounced
species-specific differences. The MSO, more than any other part of the
brain except the ventral nucleus of the lateral lemniscus, varies in
both structure and function from one species of bat to another. It is
therefore reasonable to suppose that the variations in the MSO of
different species of bats have come about as an adaptation for
processing the different patterns of auditory information that are
commonly used by each species. For example, in the mustached bat,
Pteronotus parnellii, the MSO is a large
homogeneous-appearing structure that receives mainly contralateral input. Most MSO neurons in this species are monaural, responding to
sound at the contralateral ear (Covey et al. 1991;
Grothe 1994
). In the mustached bat, MSO neurons receive
both excitatory and inhibitory input from neurons driven by sound at
the contralateral ear. The excitatory and inhibitory inputs are both
sustained for the sound's duration and slightly offset in time
relative to one another. In neurons in which the excitatory input
arrives first, inhibition cancels the latter part of the excitation,
leaving only a transient onset response. In neurons in which the
inhibitory input arrives first, the inhibition cancels the early part
of the excitation, leaving only a transient offset response
(Grothe 1994
; Grothe et al. 1992
). In
addition to creating ON and OFF responses, this
pattern of time-delayed excitatory and inhibitory inputs produces
low-pass filtering for periodic stimuli, including amplitude
modulations (AM). The mustached bat's MSO appears to be specialized in
that it contains predominantly neurons that process temporal information.
A different functional arrangement is found in the MSO of the
free-tailed bat, Tadarida brasiliensis. This bat's MSO is
also large and well developed. However, in addition to monaural cells with ON or OFF discharge patterns like those in
the mustached bat, it has a considerable population of binaural cells.
These cells also show filter properties for the temporal structure of sounds but are heavily influenced by spatial cues including IIDs (Grothe et al. 1997).
It seems likely that the differences between the MSOs of these two
species of bats are related in some way to the different environments
in which they feed and the different echolocation strategies that they
employ. The mustached bat's echolocation call consists of a relatively
long (20-30 ms) constant frequency (CF) component followed by a short
(1-3 ms) downward frequency modulated (FM) component. This type of
call, commonly referred to as a "CF-FM" call, is useful for
detecting fluttering targets within the clutter of foliage in which
these bats forage for insects. A fluttering insect would impose a
characteristic pattern of periodic AM on the CF component of the echo,
generally within the range of modulation frequencies to which MSO cells
in the mustached bat are sensitive. The free-tailed bat is considered a
pure "FM" bat because it emits a short downward FM sweep that can
be varied in shape and duration depending on the bat's hunting
strategy. These calls are not well suited for the detection of flutter
(for review, see Neuweiler 1990). Its MSO shows low-pass
properties for modulation rate, but the filter cutoffs in most neurons
depend on the binaural context (Grothe et al. 1997
).
Thus the MSO of the free-tailed bat has considerably fewer neurons with
stable filter cutoffs independent of other stimulus parameters than
does the mustached bat's MSO.
The big brown bat, Eptesicus fuscus, employs an echolocation
strategy that incorporates elements of the calls used by both the
mustached bat and the free-tailed bat. When searching for prey, the big
brown bat emits a long (20 ms) "quasi-CF" call that is in the
range between 23 and 28 kHz (Simmons and Stein 1980
).
When pursuing prey, it uses a short (<1-10 ms) FM call, the main
harmonic of which sweeps from ~50 to ~20 kHz. Given that the big
brown bat must sometimes process information similar to that generated
by the CF component of the mustached bat's echolocation call, it would
be reasonable to hypothesize that its MSO should contain a significant
population of monaural neurons that act as low-pass filters for
sinusoidal AM (SAM) sounds. Because the big brown bat also processes FM
information similar to that used by the free-tailed bat, it might be
supposed that its MSO would contain a large number of binaural neurons.
The aim of this study was to test these hypotheses by recording
responses of MSO neurons in the big brown bat to monaurally and
binaurally presented SAM sounds.
Parts of this study have been presented in abstract form (Grothe et al. 2001).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Surgery and stereotaxic setup
We recorded from the MSO of three North American big brown bats,
E. fuscus. Two days before recording began, each bat was anesthetized with methoxyflurane (Metofane, Pittman-Moore) and a
subcutaneous injection (1 ml per 100 g body wt) of the
neuroleptanalgetic, Thalamonal (Janssen; 0.05 mg Fentanyl plus 2.5 mg
Droperidol per ml). After deflecting the skin and muscles overlying the
dorsal part of the skull, a small hollow metal post was mounted on the surface of the skull using cyanoacrylate adhesive and dental cement. The post was used to fix the head in a standard position in a custom-made stereotaxic apparatus during multiple recording sessions. To determine the stereotaxic coordinates and angle of electrode penetration, we used a procedure described in detail by Schuller et al. (1986). Briefly, the sagittal profile of the skull was reconstructed in 50-µm steps along the midline and 100 µm lateral to the midline on both sides. Additionally, the transverse profile of
the skull was reconstructed in 50-µm steps at two different rostrocaudal positions. The reconstructed profiles were compared with a
standard profile for the big brown bat's skull and brain derived from
earlier studies. The alignment of the experimental bat's skull profile
with the standard profile allowed us to calculate the stereotaxic
coordinates of the MSO relative to a fixed reference point on the
stereotaxic apparatus with an error of ±100 µm or less. The
histological analysis performed at the end of the experiments allowed
us to confirm that our recordings were from MSO and to reconstruct the
recording sites.
On the first day of recording, a small opening, <1 mm diam, was made in the skull overlying the inferior colliculus (IC) for insertion of the recording electrode. Recording sessions were conducted in a sound-attenuating chamber, heated to ~28°C. Prior to each recording session, the bat was tranquilized with 0.15-0.2 ml Thalamonal injected subcutaneously. Incisions and pressure points were treated with a local anesthetic (Xylocaine). Each recording session lasted four hours or less. Drinking water was offered at periodic intervals during the recording session. The recording session was terminated if the bat showed signs of restlessness.
Stimuli
Sounds were generated digitally using instrumentation from
Tucker-Davis Technologies and delivered using custom-made
earphones (Schlegel 1977) fitted to the ears with tubes
5 mm in diameter. The earphone system was calibrated using a 1/8-in
Brüel and Kjaer microphone and a Brüel and Kjaer measuring
amplifier (type 2606). The variability in the output of the system was
less than ±4 dB over the frequency range used (10-80 kHz).
Acoustic isolation between the ears was 40 dB for all frequencies
presented. The output levels of the two loudspeakers differed from one
another by less than ±3 dB.
Stimuli were single pure tone bursts, trains of pure tone bursts, and sinusoidally amplitude modulated tones (SAM). SAM tones were modulated at frequencies (Fmod) from 20 Hz up to 1 kHz with 100% modulation depth. The duration of SAM stimuli was 100 ms. Pure tone durations ranged from 3 to 100 ms. Stimuli were presented at repetition rates ranging from 1 to 4/s and had rise-fall times of 0.5 ms.
Recording and analysis
Each stimulus was presented 20 times unless otherwise stated in
the text or figure legends. Action potentials were recorded extracellularly using glass micropipettes filled with 2 M NaCl. The
resistance of the recording electrodes ranged from 5 to 15 M. The
electrodes were advanced by a hydraulic motorized microdrive (Wells)
operated by remote control from outside the recording chamber. Action
potentials from single neurons with a constant, biphasic waveform and
stable amplitude were fed into a PC via a recording amplifier, a
band-pass filter (0.3-5 kHz), and a window discriminator.
To quantify the degree to which neuronal discharges evoked by SAM
stimuli were correlated with the phase of
Fmod, the vector strength (VS) was
calculated as described by Goldberg and Brown (1969).
For the analysis of modulation transfer functions based on spike count
or VS, the response to the first cycle was excluded. If the first cycle
was <10 ms, the first 10 ms of the response were excluded. Only
statistically significant VS values that fulfilled the
P < 0.001 criterion in the Rayleigh test following
Batchelet (1991)
are presented in this paper or used for
population statistics.
At the end of each experiment, horseradish peroxidase (HRP) was
iontophoretically injected from the recording electrode to mark
recording sites. Methods for iontophoretic HRP injection, perfusion,
and histochemistry have been described in detail by Feng and
Vater (1985).
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We recorded from 97 neurons in the medial regions of the superior olivary complex in three animals (Ept01: n = 24; Ept02: n = 48; Ept03: n = 25). In two animals (Ept01 and Ept02), the stereotaxic coordinates, visible electrode penetrations and HRP injections together confirmed that the recording sites were within the MSO. In the third animal (Ept03), no HRP histology was available, so we cannot rule out the possibility that in this animal some recording sites may have been in areas adjacent to MSO such as the superior paraolivary nucleus. However, visible electrode tracks indicated that the recording sites were within the MSO, and the response properties of all neurons were consistent with their being in the MSO.
With the exception of tonotopy, there did not appear to be any topographic distribution of response properties within MSO. For example, neurons that were excited by sound at the ipsilateral ear and unaffected by sound at the contralateral ear (EO) were intermingled with those excited by sound at either ear (EE) and those excited by sound at the contralateral ear and unaffected by sound at the ipsilateral ear (OE). Similarly, ON, OFF, and primary-like discharge patterns were intermingled throughout the MSO of all three animals.
General response characteristics
FREQUENCY TUNING.
The best frequencies (BFs) of the 97 neurons from which we recorded
were distributed throughout most of the audible range of the big brown
bat (Koay et al. 1997). The lowest BF encountered was 11 kHz and the highest 79 kHz. The distribution of BFs (Fig. 1A) shows that the majority of
neurons were tuned to frequencies between 20 and 40 kHz. This expanded
frequency representation, particularly between 20 and 30 kHz, matches
the BF distribution seen in other brain stem nuclei in the big brown
bat (IC: Casseday and Covey 1992
; Jen et al.
1989
; Poon et al. 1990
; nuclei of the lateral
lemniscus: Covey and Casseday 1991
; cochlear nucleus: Haplea et al. 1994
). The expanded frequency range
corresponds to the range of frequencies within the first and most
intense harmonic of the big brown bat's echolocation call
(Simmons 1979
). In single-electrode penetrations, BFs
tended to increase with depth, indicating that in the big brown bat, as
in other mammals, the MSO has a tonotopic arrangement in which neurons
with low BFs are located dorsally and those with high BFs are located
ventrally (e.g., Irvine 1992
). This tonotopic
arrangement of the MSO has been seen in all bats so far studied
(Molossus ater: Harnischfeger et al.
1985
; mustached bat: Covey et al. 1991
;
Grothe 1994
; free-tailed bat: Grothe et al. 1994
,
1997
; for review, see Grothe and Park 2000
).
|
DISCHARGE PATTERNS. For 93 neurons we obtained discharge patterns from PSTHs that were recorded using test tones at BF, 20 dB above threshold (Fig. 1B). Primary-like responses were seen in 33% of the neurons (Fig. 2), transient ON in 37% (Fig. 2), and transient OFF in 23% (Fig. 3). About half of the ON responders had a weak sustained component. Four neurons responded with a chopper-type discharge that lasted only a few milliseconds regardless of the stimulus duration, and two neurons responded with pauser-build-up response patterns. We tested 70 MSO neurons with pure tones at BF at different sound pressure levels. Of these, 81% had monotonic rate-level functions. Their discharge patterns remained consistent across all stimulus levels tested.
|
|
|
|
|
Binaural response types
To obtain the simplest and most general assessment of binaural response characteristics, we presented pure tones and varied the ILD for 87 neurons. The resulting distribution of binaural characteristics is shown in Fig. 7. About half (54%) of the neurons were driven by pure tones presented to the contralateral ear and showed no signs of ipsilateral excitation, inhibition, facilitation, or suppression. Following the terminology of earlier studies in the bat MSO, we designated these neurons as OE. Another 21% of the neurons could be driven by sound presented to either ear alone and/or showed facilitatory effects indicating that both contralateral and ipsilateral inputs were excitatory. We defined these neurons as EE. Seventeen percent of the neurons were excited by sound at the contralateral ear and inhibited by sound at the ipsilateral ear (IE), whereas 5% of the neurons were excited by a sound at the ipsilateral ear and inhibited by one at the contralateral ear (EI). Only 3% of the neurons were excited by a sound at the ipsilateral ear and unaffected by one at the contralateral ear (EO).
|
Responses to SAM tones
We tested 64 cells with SAM tones in which the carrier frequency was the cell's BF, and the modulation depth was 100%. Of these neurons, three cells did not respond at all to SAM stimuli with any modulation frequency tested. Of the 61 cells that did respond to SAM stimuli, 46 (75%) responded in a phase-locked pattern to at least some Fmod. Fifteen neurons (25% of the 61 cells) responded to at least some SAM stimuli but did not phaselock to any Fmod (VS <0.3 or not significant). Six of these latter cells responded only to the onset of sound, and nine responded to SAM with an irregular, sustained primary-like discharge in which spike times were uncorrelated with the stimulus envelope.
RELATION TO TEMPORAL RESPONSE PATTERNS. Of the 46 neurons that phaselocked to SAM tones, the average VS in response to a 100-Hz SAM stimulus was 0.61 ± 0.18 (mean ± SD). However, the precision of phaselocking varied considerably across neurons and was correlated with the neuron's pattern of discharge to unmodulated pure tones. There was a difference in phase locking between neurons that had a transient response and those that had a sustained response to unmodulated pure tones. Neurons that responded with a transient discharge pattern (18 with an ON and 8 with an OFF discharge) had a mean VS of 0.71. Neurons that responded to unmodulated tones with a sustained discharge had a mean VS of 0.52. The difference between the two means was statistically significant (P < 0.05; Mann-Whitney test). Interestingly, the highest precision was reached by the neurons responding with an OFF discharge (VS = 0.95 in 1 neuron; average VS = 0.79 ± 1.6, n = 8). Only one of nine OFF neurons failed to phaselock to SAM stimuli.
RESPONSE TO DIFFERENT MODULATION FREQUENCIES. We tested 55 neurons with SAM stimuli at different Fmods. For these tests we used the binaural stimulation conditions that evoked the highest discharge rate. As would be expected, the responses of MSO neurons to SAM varied as a function of Fmod.
Figure 8 shows representative responses of a neuron to SAM tones with different Fmods. This neuron responded to pure tones with a precise ON response (not shown). At modulation rates of 50 and 100 Hz, it responded to each modulation cycle with one or more spikes that were correlated in time with the stimulus envelope. At Fmods >100 Hz (e.g., 500 Hz in Fig. 8), the neuron responded mainly or exclusively to the onset of the sound.
|
|
|
BINAURAL STIMULATION. We tested five EE neurons to see whether there was any difference in SAM sensitivity when stimuli were presented contralaterally, ipsilaterally, or binaurally. For all of these neurons, the 50% cutoffs changed by >25 Hz across different binaural conditions, but there was no consistent pattern. Two neurons were tested under all three binaural conditions (ipsi, contra, and binaural). One of them had the highest cutoff under binaural stimulation, whereas the other one had the lowest cutoff under binaural stimulation. This indicates that one cannot conclude from monaural stimulation what the cutoff for binaural stimulation might be.
Responses to trains of unmodulated pure tone bursts
Our observation that neurons with low-pass filter characteristics
tended to have transient ON or OFF discharge
patterns is consistent with data from other bats. For the mustached
bat, it has been shown that the transient ON and
OFF discharge patterns of MSO neurons are created through
the interaction of excitation and inhibition slightly offset in time
(Grothe 1994; Grothe et al. 1992
). When
the Fmod of SAM tones is varied, the time each cycle is above the neuron's threshold, the interstimulus interval (IPI; time each cycle is below the neuron's threshold), and the rise
time all vary interactively, so there is no way to evaluate the
relative importance of these variables in determining the neuron's
filter characteristics. For this reason, we used trains of unmodulated
pure tones to independently vary duty cycle and repetition rate,
keeping rise time constant. We tested seven neurons with transient
ON responses to pure tones and low-pass characteristics for
SAM stimuli with trains of pure tone pulses, systematically varying
pulse duration and IPI. The results for all seven neurons were similar.
A representative example of one neuron's responses to trains of tone
pulses is shown in Fig. 11. This neuron
responded to a single unmodulated tone with a transient ON
response. When the IPI was 2.5 ms, the neuron's response to the first
pulse of the train was equal to or only slightly larger than the
responses to subsequent pulses in the train (top row of
PSTHs). The slight reduction in the magnitude of responses to pulses
after the initial one was virtually identical regardless of pulse
duration. At an IPI of 1.5 ms (middle row of PSTHs), the
responses to all but the first pulse were clearly reduced. When the IPI
was 0.5 ms (bottom row of PSTHs), the responses to all but
the first one or two pulses were almost completely suppressed for all
three pulse durations. The bottom diagrams show the analysis
of the responses to the different stimulus durations as functions of IPI, duty cycle, and repetition rate (which would correspond to Fmod of a SAM stimulus). The response
to the first pulse was excluded from the analysis. When plotted as a
function of IPI, the response functions for the three different
durations are virtually identical. In contrast, when plotted as a
function of duty cycle or repetition rate, the functions are widely
divergent. These observations indicate that the IPI is the main factor
that contributes to establishing low-pass cutoffs for AM.
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Our results show that the MSO of the big brown bat, like other
brain stem nuclei (review see: Covey and Casseday 1995),
has a full representation of this animal's hearing range, with a bias for BFs corresponding to the dominant frequency range of the
echolocation call. About half of the neurons studied appeared to be
monaural, while the other half showed clear indications of binaural
interactions among multiple excitatory inputs or excitatory and
inhibitory inputs. The cells that had binaural excitatory inputs (EE)
made up 20% of the total.
The majority of MSO cells exhibited transient discharge patterns correlated with either the beginning or the end of the stimulus. Most MSO neurons responded with a phaselocked discharge to the envelope of SAM sounds, but only at Fmods <300 Hz. Tests with trains of pulses showed that it is not modulation rate per se that is responsible for low-pass filtering but rather the IPI.
As we will point out in the following text, these characteristics place the MSO of the big brown bat midway between that of the free-tailed bat and that of the mustached bat, adding evidence to the notion that the structure and function of the MSO in bats is correlated with the characteristics of each species' echolocation signal.
Comparisons with MSO in other bats
The MSO of the big brown bat, like that of the mustached bat and
the free-tailed bat, differs somewhat from the MSO of cats or dogs with
respect to morphology, connections, discharge patterns, binaural
characteristics, and the representation of BFs. In dogs (Goldberg and Brown 1968) and cats (Guinan et al.
1972
), the tonotopic representation in MSO encompasses the
animal's entire frequency range but is clearly biased to low
frequencies. As in mustached bats (Covey et al. 1991
;
Grothe 1994
) and free-tailed bats (Grothe et al.
1997
), the BFs in the MSO of the big brown bat encompass the
entire hearing range with a bias to the main harmonics of the
echolocation call.
While all three species of bats have a large number of neurons with
binaural properties other than EE, and dogs and cats have some, the
distribution of the different binaural types varies among species.
Figure 12 compares the binaural types
found in the MSO of the dog and rat with those in the three species of
bats. The predominant binaural type in the dog (1st bar, top
graph) (Goldberg and Brown 1968) as well as in the
free-tailed bat (third bar top graph) is EE, with only a
small proportion of IE or OE cells (middle and bottom
graphs). In the rat, there are approximately equal numbers of EE
and IE cells and no OE (Inbody and Feng 1981
). The
predominant type in the MSO of the mustached bat is OE, with a very
small proportion of IE or EE cells (right bars in Fig. 12).
As evident from these graphs, the MSO in the big brown bat is
intermediate between the two other bat species, consistent with its
use, under some conditions, of a quasi-CF signal resembling that of the
mustached bat and its use of a purely FM signal resembling that of the
free-tailed bat under other conditions (Simmons and Stein
1980
) (see following text).
|
Comparison of bat MSO neurons' discharge patterns with those in animals that have low-frequency hearing, such as the dog, cat, and gerbil, is difficult because published data from these latter species were obtained almost exclusively from low-frequency neurons that phaselock to pure tones.
Comparing discharge patterns among bat species, however (Fig.
13), the MSO of the big brown bat and
the free-tailed bat contain nearly 40% sustained responders whereas in
the mustached bat these make up <20% of the total. In this respect,
the MSO of the big brown bat resembles that of the free tailed bat.
However, transient OFF responders are virtually absent in
the free-tailed bat (Grothe et al. 1997) but are rather
common in the big brown bat and mustached bat MSO (Covey et al.
1991
; Grothe 1994
). Therefore the big brown bat
again occupies an intermediate position between the mustached bat and
the free-tailed bat.
|
Possible function of MSO in bats
From this and other studies (Grothe 2000;
Grothe and Park 1998
), it becomes clear that the bat MSO
did not evolve into a processor of ITDs as did that of mammals with
well-developed low-frequency hearing such as dogs (Goldberg and
Brown 1969
), cats (Yin and Chan 1990
), gerbils
(Spitzer and Semple 1995
), and rabbits (Batra et
al. 1997
). Even though there is evidence for ITD sensitivity and coincidence detection in bat MSO neurons similar to ITD processing in other mammals (Grothe and Park 1998
), the behavioral
relevance of this ITD sensitivity for sound localization is obscure.
The small head of most bats generates ITDs <50 µs, but the actual ITD-sensitivity in the bat MSO is in the range of milliseconds. It
therefore seems likely that ITD sensitivity in bats is a side effect of
processing spatial aspects of acoustic signals other than ITD cues
related to sound location. For instance, naturally occurring interaural
intensity differences influence the temporal processing of binaural MSO
neurons, namely the cutoffs for Fmods (Grothe et al. 1997
). The cutoffs in the MTFs are a
consequence of the sensitivity to the IPI (this study). Therefore one
can assume that the period over which an MSO neuron cannot respond to
the second of two stimuli will also be influenced by the spatial location of the stimuli. This interdependence of spatial and temporal cues in the response of MSO neurons has been interpreted as a neuronal
basis for creating temporal receptive fields that help to segregate
multiple stimuli in a reverberant environment (Grothe and
Neuweiler 2000
). To create such temporal receptive fields might
be one of the original and basic functions of the MSO.
An important clue to the main function of the MSO in bats may be the
predominantly transient ON or OFF nature of the
discharge patterns. Transient response patterns are created within the
MSO by an interaction of excitatory and inhibitory inputs temporally offset from one another (Grothe 1994; Grothe et
al. 1997
). Interactions of excitatory and inhibitory inputs
with different time courses have also been reported to shape response
properties in auditory midbrain neurons (Burger and Pollak
1998
; Covey et al. 1996
; Klug et al.
1999
) and, therefore, seem to represent a fundamental principle in temporal auditory processing. One consequence of this interaction in
the MSO is low-pass filtering for modulated sounds. Low-pass filtering
has been described in the mustached bat, the free-tailed bat and, in
the present study, the big brown bat. Thus temporal processing of the
stimulus envelope seems to be an important function of MSO neurons in
bats. This is most obvious in the mustached bat MSO where the vast
majority of cells are monaural and therefore function independently of
binaural cues. Mustached bats emit echolocation calls that contain a
long CF component. This CF component represents a special adaptation
for hunting in the foliage. Echoes from stationary objects will contain
a more or less unchanged CF component, but wing beats from fluttering
insects will impose sinusoidal amplitude and frequency modulations on
the CF component (Henson et al. 1987
). Thus the temporal
structure of echoes from branches or foliage differs significantly from
that of echoes from fluttering prey, allowing the bat to hunt flying
insects even in cluttered environments. Filtering AM at an early stage
of auditory processing could have been part of the evolutionary process
that led to the bat's ability to utilize nocturnal flying insects as a
food resource. The big brown bat hunts in cluttered spaces as well as
in the open, so it is not surprising that its echolocation signals
incorporate both CF and FM features. In contrast, free-tailed bats do
not hunt in foliage and thus have no special need to recognize insects by their wing beats. For this reason, they almost exclusively use FM
sweeps as echolocation calls.
Another possible function of SAM filtering that has not yet been
mentioned is processing communication calls. The mustached bat uses a
surprisingly wide repertoire of communication calls (Kanwal et
al. 1994), and many of these sounds contain rather complex
temporal patterns of amplitude and frequency modulations. Temporal
filters for repetitive components as well as markers for beginning or
end of certain components of these calls might be important for
processing these sounds and might have their origin in the MSO.
A possible function of MSO neurons in the big brown bat that we have
not mentioned yet is related to the fact that some neurons in the
inferior colliculus are tuned to narrow ranges of sound duration
(Casseday et al. 1994, 2000
; Ehrlich et al.
1997
). It was hypothesized that one essential component of the
synaptic inputs that create duration tuning is excitation at the offset of sound. However, it is unclear whether the offset excitation is
indeed a synaptic input or whether it is due to the intrinsic properties of the duration tuned cell, i.e., rebound from inhibition (Casseday et al. 1994
). Inasmuch as the MSO projects to
the inferior colliculus, the present results indicate a potential
source of offset excitation to duration tuned neurons.
SAM filtering in the medial area of the superior olivary complex
One interesting finding is that neurons with phasic responses to
pure tones show better phase-locking to SAM stimuli than do neurons
with sustained responses to pure tones. Most strikingly, OFF responding neurons phase-lock best to SAM. A similar
difference has been shown previously for sustained and OFF
responding neurons in the medial superior olivary complex of the rabbit
(Kuwada and Batra 1999). In the rabbit, OFF
neurons show low-pass filter characteristics similar to those seen in
the MSO of bats (Grothe 1994
; Grothe et al.
1997
; this study). The only difference is that bat MSO sustained responders also exhibit low-pass filter characteristics to
SAM stimuli whereas those in the medial area of the SOC in the rabbit
do not (Kuwada and Batra 1999
).
The finding that neurons in the medial area of the SOC of rabbits and bats show specific filter characteristics for the temporal structure of sounds indicates that the SOC plays a major role in temporal processing in all mammals.
Role of modulation frequency and interpulse-interval in AM-filtering
In terms of understanding both the function of MSO and the
mechanisms that determine MSO neurons' responses to sound, it is important to stress that our data indicate that the major component that defines the cutoff frequency for modulated stimuli or trains of
tone bursts is not the modulation frequency, the repetition rate, or
the duty cycle, but rather the IPI. The cutoffs for SAM modulation
frequency simply represent a byproduct of filtering for IPI. This
finding is consistent with the model of temporal interactions in MSO
neurons proposed earlier (Grothe 1994) as well as the
model explaining the ITD sensitivity of MSO cells in the free-tailed
bat to the envelope of SAM stimuli (Grothe and Park
1998
). One question that arises is whether the SAM filtering reported for other auditory structures including the auditory midbrain
and cortical areas (review: Langner 1992
) is
Fmod specific or is a byproduct of processing
other temporal aspects of complex sounds. For example, neurons with
band-pass filter properties for sound duration in the auditory midbrain
of various tetrapod species (frog: Gooler and Feng 1992
;
bat: Ehrlich et al. 1997
; guinea pig: Chen
1998
; mouse: Brand et al. 2000
) might respond to
only a small range of SAM frequencies if excitation from MSO provides
the temporal sequence of inputs that yields suprathreshold depolarization. Neuropharmacological studies of neurons in the inferior
colliculus suggest that the low-pass filter characteristics of these
neurons to SAM are not created through the interaction of excitatory
and inhibitory inputs but rather are due either to intrinsic properties
of the neurons or low-pass filter characteristics of an excitatory
input (Burger and Pollak 1998
). Our data suggest that
the source of such an input could be the MSO.
If it is not the modulation frequency per se but rather the IPI that
determines the ability of MSO neurons to follow SAM, does the notion
hold that the large, monaural MSO in mustached bats and big brown bats
is suited for identifying fluttering targets? Echoes coming from
wing-beating insects are modulated in a quasi-sinusoidal fashion so IPI
and modulation frequency are linked, with IPI decreasing as modulation
rate increases. Thus cells in the bat MSO could act as a first stage of
neuronal filtering that helps extract temporal information contained in
echoes from wing beating insects. The fact that the MSO in bats is
large, compared with that of other mammals with high-frequency hearing,
might reflect the behavioral need of these animals to encode signals
that are amplitude modulated in the range of up to a few hundred Hz
(Moss and Schnitzler 1995).
Conclusions
Across mammalian species, whatever the function or set of functions performed by the MSO may be, this function is invariably related to some form of temporal processing. The specific rule of processing that MSO neurons apply to the incoming signal appears to be comparable across species, the rule being that MSO neurons act as coincidence detectors for at least two separate inputs, the temporal relationship of which varies as a function of one or more stimulus parameters. Processing by MSO neurons creates filter characteristics for the temporal structure of a sound, with ITD sensitivity being only one consequence of this rule. In small mammals, temporal filtering by MSO neurons might be more relevant for sound recognition than for sound localization. In dogs, cats, and other large mammals with well-developed low-frequency hearing, the MSO might well be involved in both functions.
![]() |
ACKNOWLEDGMENTS |
---|
We thank the two reviewers and Dr. M. Götz for helpful suggestions.
This research was supported by Max-Planck-Gesellschaft (BG) grants from the Deutsche Forschungsgemeinschaft (FOR 306-1 and GR 1205/11-3) and by grants from the National Institute on Deafness and Other Communication Disorders (DC-00607 and DC-00287).
![]() |
FOOTNOTES |
---|
Address for reprint requests: B. Grothe, Max-Planck-Institute of Neurobiology, Am Klopferspitz 18a, D-82152 Martinsried, Germany (E-mail: bgrothe{at}neuro.mpg.de).
Received 9 April 2001; accepted in final form 31 July 2001.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|