Medical Research Council Institute of Hearing Research, University of Nottingham, Nottingham NG7 2RD, United Kingdom
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ABSTRACT |
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McAlpine, David, Dan Jiang, Trevor M. Shackleton, and Alan R. Palmer. Responses of Neurons in the Inferior Colliculus to Dynamic Interaural Phase Cues: Evidence for a Mechanism of Binaural Adaptation. J. Neurophysiol. 83: 1356-1365, 2000. Responses to sound stimuli that humans perceive as moving were obtained for 89 neurons in the inferior colliculus (IC) of urethan-anesthetized guinea pigs. Triangular and sinusoidal interaural phase modulation (IPM), which produced dynamically varying interaural phase disparities (IPDs), was used to present stimuli with different depths, directions, centers, and rates of apparent motion. Many neurons appeared sensitive to dynamic IPDs, with responses at any given IPD depending strongly on the IPDs the stimulus had just passed through. However, it was the temporal pattern of the response, rather than the motion cues in the IPM, that determined sensitivity to features such as motion depth, direction, and center locus. IPM restricted only to the center of the IPD responsive area, evoked lower discharge rates than when the stimulus either moved through the IPD responsive area from outside, or up and down its flanks. When the stimulus was moved through the response area first in one direction and then back in the other, and the same IPDs evoked different responses, the response to the motion away from the center of the IPD responsive area was always lower than the response to the motion toward the center. When the IPD was closer at which the direction of motion reversed was to the center, the response to the following motion was lower. In no case did we find any evidence for neurons that under all conditions preferred one direction of motion to the other. We conclude that responses of IC neurons to IPM stimuli depend not on the history of stimulation, per se, but on the history of their response to stimulation, irrespective of the specific motion cues that evoke those responses. These data are consistent with the involvement of an adaptation mechanism that resides at or above the level of binaural integration. We conclude that our data provide no evidence for specialized motion detection involving dynamic IPD cues in the auditory midbrain of the mammal.
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INTRODUCTION |
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It is well established that the azimuthal position
of low-frequency (<1,500 Hz) sounds is determined by humans using
microsecond differences in the timing of the signals at the two ears
(Rayleigh 1907; Stevens and Newman 1936
).
A widely accepted model to account for this remarkable binaural
sensitivity is the coincidence detection model (Jeffress
1948
). In this model, an array of neurons receives inputs from
the two ears such that a neuron fires maximally when the difference in
arrival time at the two ears, due to the location of a sound source,
offsets the difference in neural conduction time to that neuron. A
central tenet of this model is that the coincidence detectors signal
the instantaneous value of the interaural delay. In other
words, a neuron's probability of discharge is related solely to the
relative time of arrival of the inputs from each ear, providing the
auditory system with a representation of static azimuthal position.
Recordings from single neurons in the medial superior olive (MSO)
(Goldberg and Brown 1969
; Spitzer and Semple
1995
; Yin and Chan 1990
) indicate that many
neurons do act as coincidence detectors, firing maximally at a
particular interaural delay of the stimulus, and at delays equivalent
to multiple periods of the stimulating waveform. No evidence of
sensitivity to motion was obtained in studies of the MSO.
More detailed analyses of the processing of interaural time delays
comes from the inferior colliculus (IC), the major target of the MSO.
Yin and his colleagues demonstrated that IC neurons responded to the
dynamic interaural phase disparities (IPDs) of binaural beats like they
responded to the static interaural delay of tonal stimuli (Yin
and Kuwada 1983a). The vast majority of IC neurons were
insensitive to the rate or direction of the apparent motion generated
by binaural beats (Yin and Kuwada 1983b
). These findings
suggested that processing of interaural delay in the IC reflects the
simple coincidence detection observed in the MSO. However,
Spitzer and Semple (1993)
, using interaural phase
modulation (IPM), which they described as a more "physiologically
realistic" apparent-motion stimulus than binaural beats, found that
the vast majority of IC neurons in gerbil and cat were responsive to
IPD cues in a manner more reflective of the change of IPD
than of the absolute IPDs over which the changes occurred. In
particular, they observed that the neuronal discharge rates at any
particular IPD were dependent on the direction in which the interaural
phase was changed, the depth of the change, and the IPD around which the phase changes were centered. They concluded that the instantaneous probability of discharge of IC neurons reflects not only current stimulus conditions but also the recent history of stimulation. More
recently, these same authors (Spitzer and Semple 1998
)
demonstrated that neurons in the MSO, the primary site of binaural
interaction, respond only to the instantaneous IPD. This suggests a
hierarchy of binaural responses, with the sensitivity to motion cues
increasing from the level of the brain stem to the midbrain.
In the present study, we examined the possible mechanism/s that might
be contributing to the apparent sensitivity of IC neurons to
virtual-motion cues. We recorded responses of IC neurons to a wide
range of IPM stimuli that produced apparent motion with different
angular extents, directions, centers, and rates. Our data suggest that
the responses of IC neurons to the apparent-motion cues of IPM are
consistent with adaptation-of-excitation occurring subsequent to
coincidence detection. Thus, whereas our results are consistent with
those of Spitzer and Semple (1993) in that the
instantaneous probability of discharge of IC neurons reflects the
recent history, the effects may be nonspecific in that they are related
to the history of the response, and not the history of the
dynamic IPD cues per se.
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METHODS |
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Many of the detailed methods have been described previously
(McAlpine et al. 1996; Palmer et al.
1990
) and are recounted only briefly here, but methods
specific to the present study are described in detail.
Preparation and recording
Recordings were made from the central nucleus of the right IC of
300-400 g guinea pigs anesthetized with urethan (1.5 g/kg in 20%
solution) with additional analgesia obtained using phenoperidine (1 mg/kg). A premedication of atropine sulfate (0.06 mg/kg) was administered to reduce bronchial secretions. Supplementary doses of
urethan (1/2 to of the induction dose) or phenoperidine were administered when required. All animals were tracheotomized, and core temperature was maintained at 37°C with a
heating blanket and rectal probe. Most animals respired spontaneously, but a few were artificially respired with 95%
O2-5% CO2 and end-tidal CO2 was monitored.
The animals were placed in a stereotaxic frame with hollow earbars into which fitted 12.7 mm Brüel and Kjær condenser earphones and 1-mm probe tubes fitted to 12.7-mm Brüel and Kjær microphones. In every experiment the probe tube microphone was used to calibrate the sound system in dB re 20 µPa a few millimeters from the tympanic membrane. The sound systems for each ear were flat ±5 dB from 100 to 10,000 Hz and were matched to within ±2 dB.
A silver wire electrode was placed on the round window of one side via a hole in the posterior aspect of the bulla, and the threshold of the cochlear action potential (CAP) evoked by short tone pips was examined as a function of frequency (from 500 to 30,000 Hz) throughout the experiment to monitor the condition of the cochlea. A thin (0.5-mm diam) polythene tube was sealed into the bulla of both sides, to provide pressure equalization while maintaining closed-field recording conditions.
Single-unit action potentials were measured using tungsten-in-glass
microelectrodes (Bullock et al. 1988; Merrill and
Ainsworth 1972
).
Stimulus production and presentation
Stimuli were delivered to separate left and right signal mixers and presented to each ear via attenuators to the separate closed-field sound systems. Search stimuli consisted of 50-ms bursts of white noise presented binaurally. When a single unit was isolated, its best frequency (BF) and threshold to binaural tones at zero interaural delay were determined audiovisually.
IPM stimuli were produced by fixing the phase at the left
(contralateral) ear and sinusoidally or triangularly modulating the
phase at the right (ipsilateral) ear. Thus the stimulus at the left ear
was a simple sine wave
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When the interaural phase was modulated triangularly, the instantaneous
amplitude of the sine wave at the right ear was
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RESULTS |
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A total of 89 IC neurons was examined with IPM stimuli. For 39 the interaural phase was sinusoidally modulated, and for 50 the interaural phase was triangularly modulated. BFs ranged from 98 Hz to 1.16 kHz. Of the 89 neurons, 85 were examined at BF, and only 4 below BF. In these four cases, IPM using BF signals only poorly modulated the response, and a lower signal frequency was used.
Responses to partially overlapping IPMs
Figures 2 and
3 illustrate the range of responses that
we observed in this study. Figure 2 shows responses of an IC neuron that was insensitive to the apparent-motion cues of IPM. Responses to
the partially overlapping IPMs modulated around various center IPDs
(60, 0, +60, +120, 180 and
90°) at a rate of 2 Hz and at ±45°
depth, in both the counterclockwise (Fig. 2A) and clockwise (Fig. 2B) directions, evoked similar responses at each IPD.
Responses to the two directions of motion were virtually identical.
Neurons insensitive to the motion cues were relatively rare in our
study, as also reported by Spitzer and Semple (1993)
.
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Figure 3 shows responses of an IC neuron to IPM, with many
similarities to those reported by Spitzer and Semple
(1993). Responses to partially overlapping IPMs for motion in
both the counterclockwise (Fig. 3A) and clockwise directions
(Fig. 3B) around center IPDs of IPDs of 0, +90, 180, and
90° (1 Hz IPM rate and ±90° depth) are clearly discontiguous,
with very different discharges evoked by the same IPD. The discharge
rate depends on the center IPD around which the phase was modulated,
and not simply the absolute IPD.
Responses to IPMs with different centers
The effect of altering center IPD on the responses to IPM is
illustrated in Fig. 2, C-F, and Fig. 3, C-F.
Changing the IPD around which the interaural phase is modulated changes
the position or "locus" of the apparent motion. In both cases the
IPM was modulated over ±180°. In each case, the center IPDs were
0° (Figs. 2C and 3C), +90° (Fig.
2D), 180° (Fig. 2E) and 90° (Fig.
2F). In Fig. 2, C-F, altering the center IPD had
no effect on the neuron's response, and responses to counterclockwise
(black lines) and clockwise motion (gray lines) were identical. In Fig.
3, C-F, the responses to the two directions of motion
differed greatly at each center IPD. The neuron appears to be sensitive
to the motion direction, with greatly differing response profiles
depending on the center IPD. Of particular note is that this neuron was more responsive to clockwise motion when centered at 180° (Fig. 3E), whereas it was more responsive to counterclockwise
motion for the other three centers (Fig. 3, C, D,
and F).
Responses to different depths of IPM
The effect of reducing the depth of IPM was examined for 52 neurons: 28 neurons using triangular IPM and 24 neurons using sinusoidal IPM. For triangular IPM, the two paradigms of Fig. 1, C and D, were used. First, IPM rate was kept constant as depth was reduced, so that the velocity was also reduced. Second, as depth was reduced, the IPM rate was increased to maintain equal velocity of motion. Generally, the effects observed were similar for equal rate and equal velocity stimuli, and this is illustrated in Fig. 2, G-J, and Fig. 3, G-J.
In Fig. 2, G and H, reducing the depth of IPM from ±135° to ±30 for a fixed IPM rate of 1 Hz had little effect on the discharge rate evoked at favorable IPDs by either counterclockwise (Fig. 2G) or clockwise (Fig. 2H) excursions. Similarly, when the IPM rate was increased to maintain equal velocity (Fig. 2, I and J), peak discharge rates were unaltered when the depth of IPM was reduced. For the other example in Fig. 3, G and H, reducing the depth of IPM for a fixed IPM rate of 1 Hz reduced maximum discharge rates at favorable IPDs. Similarly, reducing the depth of IPM while increasing the IPM rate to maintain a constant velocity (Fig. 3, I and J) also had the effect of reducing maximum discharge rates at favorable IPDs.
The only differences that were observed between equal IPM rate and
equal velocity responses arose because as the IPM rate was increased,
the neuronal latencies constituted an increasing proportion of each
cycle of IPM. As IPM rate increases, responses are plotted further into
the IPM cycle. This was manifested as a slight shift in the response in
the direction of the motion. This was commonly observed for all neurons
for which responses to equal IPM rate and equal velocity stimuli were
obtained and has been well described previously (e.g., Spitzer
and Semple 1998).
Temporal order of the response underlies apparent sensitivity to IPM direction
We suggest that it is response history that determines
sensitivity to IPM. Evidence for this hypothesis is provided in Fig. 4. Figure 4, A-D,
shows peristimulus time histograms (PSTHs) of the response to 1-Hz IPM
centered at 0° (Fig. 4A), 90° (Fig. 4B), 180° (Fig. 4C), and 90° (Fig. 4D). In each
case, the PSTH shows the response to the complete 3 s of the IPM
stimulus, modulated over ±180°. There were 5 complete excursions of
motion (i.e., a full 360° in one direction or the other) over the
3 s of the stimulus as in Fig. 1A. The complete
unidirectional motion excursions are labeled 1-5 in Fig. 4,
A-D. Odd numbers (black) indicate counterclockwise excursions, whereas even numbers (gray) indicate clockwise excursions. The dotted vertical lines indicate the point at which the direction of
motion reversed. It is evident from Fig. 4A that, for IPM
centered at 0°, the response evoked by the clockwise excursion was
preceded by a slightly shorter period during which no response was
elicited than was the response evoked by the counterclockwise
excursion. This is an inevitable consequence of the fact that IPD
functions are asymmetrically placed around zero IPD, the center IPD
used in Fig. 4A. The panel to the right of the
PSTH in Fig. 4A plots the average discharge rate over each
of the five complete cycles of motion. The average discharge rate
varied systematically from cycle to cycle, interleaving relatively
higher and relatively lower average discharge rates, with
counterclockwise excursions always evoking higher discharge rates than
clockwise excursions. The situation was reversed when the stimulus was
centered at +90° (Fig. 4B). Here, the period of time
preceding the response to each cycle of clockwise excursions (gray) was
greater than that preceding the response to counterclockwise excursions
(black). Accordingly, the interleaving of relatively higher and lower
discharge rates from counterclockwise to clockwise excursions was
opposite to that when the IPM stimulus was centered at 0° IPD. For
IPM centered at 180° (Fig. 4C) and
90° (Fig.
4D), the asymmetry was greater than observed for centers of
0° and +90°. For IPM centered at 180° (Figs. 4C),
there was no time at all between the response to counterclockwise
excursions and the response to clockwise excursions; the motion
reversed direction immediately after passing through the neuron's most
favorable range of IPDs. Here, the cycle-by-cycle variation in
discharge rate was considerable. The situation was reversed again for
IPM centerd at
90° (Fig. 4D). Now, counterclockwise excursions were preceded by a longer period of time during which the
neuron was not responding, whereas clockwise excursions were followed
immediately after the response to counterclockwise excursions. The
cycle-by-cycle variation in discharge rate was therefore opposite to
that when IPM was centered at 180°. When the PSTHs are "folded" and displayed as IPD functions at different center IPDs (Fig. 4E, and Figs. 2 and 3), the effect is to produce
discontiguous responses to partially overlapping IPMs: i.e., very
different discharge rates for the same IPD values. However, we would
argue that this folded display can be misleading because it obscures the response history evident in the full PSTH.
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We calculated a "recovery time" as the time between the peak
response evoked by counterclockwise motion to the peak response evoked
by the clockwise excursion (i.e., from peak response in cycle
2 to peak response in cycle 3, and from peak response
in cycle 4 to peak response in cycle 5, in each
panel of Fig. 4A). We then plotted the ratio of the
clockwise average discharge rate to the counterclockwise average
discharge rate as a function of the recovery time. The dependence of
the average discharge rate on recovery time is illustrated in Fig.
5. Figure 5A plots the relationship between the recovery time and the ratio of average discharge rates for four representative neurons. Figure 5A, top left, shows data from the neuron in Fig. 4. When the recovery time
preceding the main response peak of clockwise responses was relatively
long (Fig. 4, B and C), the ratio of the
discharge rates was relatively high; i.e., more activity was evoked
during clockwise excursions. However, when the recovery time preceding clockwise motion was relatively short (Fig. 4, A and
D), the ratio of discharge rates was relatively low; i.e.,
more activity was evoked during counterclockwise excursions. The
dependence of this neuron's response on the preceding recovery time is
indicated by the steepness of the regression line fitted to the data
points in Fig. 5A, top left, which is a measure of the
magnitude of the adaptation in the neuron. Figure 5A, bottom
right, comes from the neuron in Fig. 2, which appeared insensitive
to the motion cues of IPM. Other neurons showed different slopes of
their discharge ratio versus recovery time functions (e.g., remaining
panels in Fig. 5A). Figure 5B plots the
distribution of slopes of discharge ratio versus recovery times for the
37 neurons for which this analysis was performed. Apart from the few
cells that show slopes >1,000 ms, the slopes are centered around a
peak of 200-300 ms1.
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If response adaptation is causing the asymmetry of responses, then equal recovery time between the responses to the two directions should give equal average discharge rates. In each of the panels in Fig. 5A, the intercept of the vertical and horizontal dotted lines indicates a ratio of 1.0 and an equal recovery time of 500 ms. In each case, the regression line fitted to the data points crossed the horizontal dotted line at a ratio very close to 1.0. The distribution of ratios of discharge rates at equal recovery time is plotted in Fig. 5C. For the 37 neurons for which this analysis was performed, the mean ratio at 500 ms was 0.98 ± 0.05 (mean ± SE), indicating that equal recovery times between counterclockwise and clockwise excursions produces equal average discharge rates for the two directions of motion. This argues for a nonspecific adaptation rather than a direction-related motion mechanism. There was no difference between neurons examined using trapezoidal IPM (0.99 ± 0.06, n = 15) and sinusoidal IPM (0.97 ± 0.03, n = 22).
The effect of recovery time suggests that a process of adaptation is
occurring when favorable IPDs are presented and the neuron is strongly
activated. One would therefore predict that the longer the neuron
spends within the range of favorable IPDs, the greater will be the
reduction in peak discharge rates at those favorable IPDs, as the
recovery time afforded between periods of strong activation evoked by
IPM in either direction is reduced. This is indeed what was observed.
Figure 6 shows the response of an IC
neuron to counterclockwise and clockwise motion for different depth
IPMs. The motion reversed direction from counterclockwise to clockwise
in the middle of the range of favorable IPDs. As the IPM depth was
reduced (Fig. 6, A-D), the stimulus was
increasingly confined to the range of favorable IPDs. This reduced the
recovery time, and the cycle-by-cycle variation in discharge rate
(panels to right of Fig. 6,
A-D) gradually diminished, so that for
the ±45° IPM (Fig. 6D) it had disappeared completely.
In Fig. 6E, the average discharge rate over IPDs in the
range ±45° (centered at +90°) is plotted for the four modulation
depths examined in Fig. 6, A-D. Similar to the panel to
the right of Fig. 6A, the average discharge rate over
the range ±45° clearly alternated between higher and lower values
when the IPM depth was ±180° (). As the IPM depth was reduced to
+135° (
) and +90° (
), however, the difference between the
average discharge rate for the two directions was reduced until, for
the ±45° IPM (
), the cyclic pattern was no longer evident. Notice
that the effect of reducing IPM depth was mainly to reduce the
discharge rates of the counterclockwise excursions, clockwise
excursions remained low at all depths (cf. Fig. 6,
F and G). The likely reason for this is
that clockwise motion always starts at a favorable IPD. Therefore the
response is already adapted from the counterclockwise response ending
at that favorable IPD.
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Sensitivity to motion direction
The responses to counterclockwise (black) and clockwise (gray)
motion for four representative IC neurons are compared in Fig. 7. In Fig. 7, A-D, responses
are shown for IPM centered at two different IPDs, with the extent of
the motion indicated by the arrows above each plot. For the example in
Fig. 7A, clockwise motion centered at 0° evoked lower
discharge rates than did counterclockwise motion, because
counterclockwise motion was preceded by a period of recovery.
Conversely, for motion centered at +90°, counterclockwise motion
centered at 0° evoked lower discharge rates than did clockwise motion; as for this IPM paradigm clockwise motion was preceded by a
period of recovery. For all neurons we recorded, responses to motion
into the range of favorable IPDs, reversing near the best
IPD, evoked higher peak discharge rates than did the subsequent motion
out of the neuron's range of favorable IPDs, which show the effects of
adaptation. If the reversal, however, occurs at unfavorable IPDs,
adaptation will be equivalent for the two directions, and no effects of
motion direction are observed. This occurred irrespective of the
direction in which the stimulus approached the favorable IPD range and
is consistent with the response history effects that we have described
thus far, and described by Spitzer and Semple (1993).
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Sensitivity to the direction of motion was also manifest in the mean best interaural time differences (ITDs), calculated as the ITD equivalent of the mean best interaural phase at the IPM stimulus frequency, obtained in response to counterclockwise and clockwise motion. Figure 8, A-F, compares responses to counterclockwise and clockwise motion for six IC neurons, all for IPM modulated over ±180° and centered at 0° IPD. As we have shown above, for many neurons, responses to the two motion directions did not overlap completely. This was similarly the case for neurons with peak-type (Fig. 8, A-E) and trough-type (Fig. 8F) neurons. Figure 8G plots mean best ITDs for clockwise motion against those for counterclockwise motion for 55 IC neurons computed from the response to counterclockwise and clockwise motion for ±180° IPMs centered at 0° IPD. Relatively few neurons showed identical mean best ITDs to the two directions of motion, as evidenced from their departure from the line of equality in Fig. 8G. The distribution of mean best ITDs for these 55 neurons is shown in Fig. 8H and are skewed toward the direction from which the stimulus moves. For the counterclockwise motion, the mean of the best ITDs calculated for the 55 neurons was +319 µs, whereas for the clockwise motion, the mean of the best ITDs calculated for the 55 neurons was +448 µs. This cannot be attributed to the effects of latency described earlier, which would tend to shift the functions slightly in the same direction as the motion, i.e., in the opposite direction to that observed. Adaptation effects exceed any latency effects and may be underestimated.
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Sensitivity to motion center correlates with sensitivity to motion depth
Those neurons that were most sensitive to changes in IPM depth
were also those neurons that were most sensitive to changes in the
center IPD around which the interaural phase was modulated. This is
quantified in Fig. 9A, which
plots the modulation depth index as a function of the
modulation center index for 27 neurons. The modulation depth
index is a measure of how sensitive IC neurons were to changing the
depth of IPM (the extent of apparent motion). It was calculated as the
ratio of the peak discharge rate for ±45° motion to the peak
discharge rate for ±180° motion at the center IPD closest to the
neuron's most favorable IPDs. Neurons were included in this analysis
only if the ±45° IPM moved through the range of favorable IPDs. The
modulation center index is a measure of how sensitive IC neurons were
to changing the center IPD. It was calculated as the ratio of the
lowest peak discharge to the highest peak discharge rate evoked
±180° IPM measured at each of the four center IPDs, 0, +90, 180, and
90°.
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The 27 neurons each contribute 2 data points to Fig. 9A, one
for counterclockwise motion () and one for clockwise motion (
).
It is clear from Fig. 9A that those neurons most sensitive to motion depth were also those neurons that were most sensitive to
motion center. The regressions fitted to the counterclockwise and
clockwise data had coefficients of 0.80 and 0.73, respectively.
It is possible that adaptation below the level of binaural integration
might have contributed to the effects observed. Such effects, residing
in monaural neurons/fibers only, would not be related to the IPM cycle
but, rather, would be manifest as a reduction in activity over the
entire duration of the IPM stimulus. Spitzer and Semple
(1993) discarded the first few seconds of the responses evoked
by their 10-s long stimulus specifically to avoid the effects of such
"monaural" adaptation. The effects that they observed, which are
qualitatively similar to the effects reported in the present study,
were unlikely to be contaminated with the effects of monaural
adaptation. We only discarded the first and final 0.25 s of our
3-s stimulus, and it is possible that some responses may be subject
also to monaural adaptation effects, but these should be equal for both
motion directions.
However, to assess possible contributions of monaural adaptation, we
compared the adaptation over the duration of the stimulus with the
cycle-by-cycle variation in discharge rate. The discharge rate for the
first full motion excursion was compared with the discharge rate over
the final full motion excursion (i.e., a comparison of cycles
1 and 5 of PSTHs, averaged across the 4 IPM centers of
0, +90, 180, and 90°, such as in Fig. 4). As all responses for
which this analysis was performed were obtained using 1-Hz IPM; this
involved comparing the discharge rate evoked from 250 to 750 ms of the
3,000-ms stimulus with the discharge rate evoked from 2,250 to 2,750 ms
of the 3,000-ms stimulus. This ratio was termed the monaural
adaptation index. The monaural adaptation index is compared with
the modulation depth index in Fig. 9C, and with the
modulation center index in Fig. 9D. Of the 27 neurons for
which this analysis was performed, 2 showed large reductions (>50%)
in discharge rate from cycle 1 to cycle 5 of
motion. Both of these neurons also showed great sensitivity to the
locus and depth of IPM (denoted by arrows in Fig. 9A). When
these data points were removed from the analysis, there was
insignificant correlation between the degree to which neurons showed
adaptation over the duration of the IPM stimulus and the degree to
which they were sensitive to changing the depth or the center of motion
(Fig. 9, E and F, respectively). However, in
the absence of these data points, correlation coefficients for the
variation of modulation depth index with modulation center index were
reduced only slightly to 0.73 and 0.70, respectively, for
counterclockwise and clockwise motion (Fig. 9B). This
suggests that there is no significant relationship between the
cycle-by-cycle variation in the response observed, and any decline in
activity over the 3,000-ms time course of the IPM stimulus that might
be attributed to adaptation mechanisms below the level of binaural integration.
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DISCUSSION |
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The major finding of this study is that the sensitivity of IC
neurons to the apparent-motion cues contained in IPM can be explained
in terms of adaptation-of-excitation. We have replicated, qualitatively
at least, the effects reported by Spitzer and Semple (1993), both for triangular IPM and for sinusoidal IPM. Spitzer and Semple concluded that the responses they observed were a result of
the stimulus history. However, it is clear from our analyses that
presenting data in the form of partially overlapping IPD functions as
Spitzer and Semple did, and as we do in Figs. 2-4, 6, and 7, obscures
the response history at any particular IPD. Responses of IC neurons to
IPM stimuli depend not on the history of stimulation, per se, but on
the history of their response to stimulation, irrespective of the
specific motion cues that evoke those responses. When PSTHs of IC
neurons were examined for a range of different IPM center loci, it was
the temporal pattern of the response to IPM, and not the motion cues
contained in the IPM, that determined sensitivity to features such as
motion depth, direction, and center locus. When any cycle of IPM
contained motion that was restricted to the most favorable IPDs only,
discharge rates were lower than when the stimulus moved through the
responsive area from outside, or moved up and down the flanks of IPD
functions only. This occurred irrespective of the motion configuration
produced by different IPMs. It was always the case that
whenever motion in the two directions over the same IPDs evoked
different responses, the response to the motion moving away from a peak
of activity was lower than the response to the direction moving into
the peak of activity. When the reversal point was closer to the most
favorable IPDs, the response to the opposite direction of motion was
lower. This occurred irrespective of whether the motion through the
favorable IPDs was first counterclockwise or clockwise. Motion that was restricted to the flanks of IPD functions only, or motion that was
restricted to the most favorable IPDs only, showed much less effect of
motion direction and often showed responses that overlapped completely.
In no case did we find any evidence for neurons that preferred one
direction of motion to the other, or that showed differences in their
response to a wide variety of IPM center loci, depths, rates, or
directions that were not consistent with an adaptation-of-excitation mechanism.
Altered binaural code in the IC?
The degree to which the representation of binaural signals is
altered at subsequent levels of the auditory system remains controversial. Early studies of responses to interaural time delays, both in the IC and in primary auditory cortex, generally indicated that
responses were consistent with the output of the simple coincidence detectors at the superior olivary complex (SOC) (e.g.,
Kuwada et al. 1984; Reale and Brugge
1990
; Rose et al. 1966
; Yin and Kuwada 1983b
; Yin et al. 1986
,
1987
). However, even in these studies there were
indications of further complications in the way that the IC responded
to interaural delays. The simple coincidence detector model predicts
that plots of mean best phase as a function of stimulating frequency
(phase plots) are linear and intersect the frequency origin at zero or
±0.5 cycles of phase (corresponding to the peak or trough of the IPD
function, respectively). Cells in the IC, however, often had phase
plots that were nonlinear and intersected the ordinate at values
between 0 and ±0.5. Evidence for one explanation for this behavior
comes from a recent study by McAlpine et al.
(1998)
, which demonstrated that neurons with intermediate-type and/or nonlinear phase plots were likely the consequence of convergent input from simple coincidence detectors in
the brain stem.
Furthermore, Spitzer and Semple (1993), and the data in
this paper, have convincingly demonstrated that the response to
dynamically varying interaural phase differences in the IC may be quite
different, depending on the context in which the stimulus is presented.
These data are inconsistent with the simple Jeffress model of
coincidence detection and appear to differ from principal cells in the
MSO, which are insensitive to the motion cues of IPM (Spitzer
and Semple 1998
). Although they found a small number of neurons
in the region of the superior olive that were sensitive to motion cues,
they inferred that they were responses from descending neurons and not
MSO or lateral superior olive (LSO) principal neurons. The basis for this was that these neurons did not show monaural
phase-locking, were clustered in regions where known descending inputs
from the IC terminate in rodents, and had long latencies. This suggests that the mechanism responsible for such sensitivity is first
encountered above the level of the brain stem.
Finally, there is the issue of the small number of IC neurons
sensitive to the direction and/or velocity of binaural beats, as
reported by Yin and Kuwada (1983b). Although such
neurons showed a preferred direction and/or rate of binaural beats,
they did so over velocities in the range 360° to 3,600°
s
1, which are undoubtedly at the upper limits and outside
that of physically encountered motion. Nevertheless, the fact that such neurons were found requires explanation, and Yin and Kuwada's inclusion into a coincidence detection model of a presynaptic inhibitory collateral from one side gating the input from the other
side may account for this phenomenon. However, as we discuss below, it
remains the case that for our data, and for our interpretation of
Spitzer and Semple's (1993)
data, a mechanism of
adaptation-of-excitation appears sufficient.
Mechanism of adaptation-of-excitation in the IC?
Spitzer and Semple (1993,
1998
) suggested that one possible explanation for the
effects that they observed was the presence of binaural inhibitory
inputs onto IC neurons, possibly from the dorsal nucleus of lateral
lemniscus, or via local circuits in the IC itself. IC neurons
receive many more binaural and monaural inputs than do SOC neurons,
with a proportion of them characterized as binaural and inhibitory
(Adams and Mugnaini 1984
; Roberts and Ribak
1987
). However, as we have demonstrated above, the
incorporation of inhibitory inputs is not a necessary requirement for
the data we observed, all of which may be explained by the
adaptation-of-excitation hypothesis.
It is undoubtedly the case that monaural adaptation-of-excitation was
present in the responses of the neurons reported here. The general
reduction in discharge rate over the 3,000-ms duration of the IPM
stimulus suggests that the responses of auditory nerve fibers and/or
the bushy cell outputs to the binaural neurons in the lower brain stem
adapted to the monaural stimulus presented to each ear. However, such
adaptation cannot account for the cycle-by-cycle variation in discharge
rate observed in the vast majority of IC neurons, because this
cycle-by-cycle variation indicates a change in discharge rate that
depends on binaural stimulation. If this variation is attributable to
an adaptation mechanism, then it must occur at the level of the MSO or
higher, where responses depend on IPD. We have termed this putative
mechanism "binaural adaptation." Our use of this term, however,
should not be confused with the use of the same term by Hafter (e.g.,
Hafter 1997). Hafter describes as binaural
adaptation the reduction in the amount of binaural information derived
from successive portions of a signal with increasing signal duration.
In his studies, this appears to derive from processes occurring in
monaural channels before binaural integration. Conversely, our data,
and the circumstantial evidence of differences between the SOC and IC
described by Spitzer and Semple (1993
,
1998
), suggest that whatever contributes to sensitivity
to the apparent-motion cues of IPM must occur subsequent to primary
binaural integration in the SOC. As such, our use of the term binaural
adaptation appears entirely appropriate.
A recent model of binaural processing in the IC (Cai et al.
1998a,b
) adds weight to our proposal that the mechanism
responsible for sensitivity to the motion cues of IPM is one of
adaptation-of-excitation. In the first of these papers (Cai et
al. 1998a
), the authors were able to simulate many of the
binaural phenomena reported in various physiological studies of the IC.
This included sensitivity to static ITDs (Kuwada and Yin
1983
; Kuwada et al. 1984
; Yin and Kuwada
1983a
,b
), binaural beats (Yin and Kuwada 1983a
),
binaural clicks (Carney and Yin 1989
), and pairs of
binaural clicks (Fitzpatrick et al. 1995
;
Litovsky and Yin 1998a
,b
). However, the model
was unable to simulate the responses to IPM stimulus reported by
Spitzer and Semple (1993)
. Subsequently, in a second
paper (Cai et al. 1998b
), the authors demonstrated that
the addition of an adaptation mechanism, specifically a
calcium-activated, voltage-independent potassium channel responsible
for afterhyperpolarization, enabled their model to simulate sensitivity
to IPM stimuli. They suggested that such a mechanism, which they
modeled with a 500-ms time constant, could account for the results of
Spitzer and Semple (1993)
in the IC. Interestingly, the
presence of strong delay-sensitive inhibition resulted in the modeled
neurons showing less sensitivity to the apparent motion cues of IPM.
Cai et al.'s suggested reason for this was that the reduction in
discharge rate brought about by the inhibition reduced the amount of
adaptation-of-excitation experienced by the neuron and, hence, the
extent to which its response was influenced by apparent-motion cues.
Thus contrary to the conclusion reached by Spitzer and Semple
(1993
, 1998
), the less inhibition, the greater
the sensitivity to the apparent motion cues of IPM. Cai et
al.'s (1998b)
suggestion that the sensitivity to IPM may be
explained by an afterhyperpolarization current residing at the level of
the IC appears to be the simplest explanation for both our data and
those of Spitzer and Semple (1993)
.
Nevertheless, our interpretation does not exclude other, possibly
inhibitory, mechanisms that might contribute to the apparent sensitivity to IPM cues observed by Spitzer and Semple
(1993) and in the present study. Sanes et al.
(1998)
have recently demonstrated, using dynamically varying
interaural level differences, responses of IC neurons that appear to
require long-lasting inhibitory mechanisms to provide an adequate
explanation for their sensitivity to apparent motion stimuli. In
addition, free-field motion studies in the barn owl IC (Wagner
and Takahashi 1992
) appear to indicate some form of sensitivity
to apparent motion, and which may be dependent on binaural inhibition,
although motion-sensitive cells appeared to be confined to external
nucleus of the IC and the tectum. However, whether any of these
observations indicate unequivocally the existence of specialized motion
detectors is open to debate. Further studies are required to resolve
the issue of how moving sound sources are encoded in the auditory system.
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ACKNOWLEDGMENTS |
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Present address and address for reprint requests: D. McAlpine, Dept. of Physiology, University College London, Gower St., London WC1E 6BT, UK.
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FOOTNOTES |
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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 24 June 1999; accepted in final form 9 November 1999.
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REFERENCES |
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