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Department of Anatomy, University of Connecticut Health Center, Farmington, Connecticut 06030-3405
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Batra, Ranjan, Shigeyuki Kuwada, and Douglas C. Fitzpatrick. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J. Neurophysiol. 78: 1222-1236, 1997. Interaural temporal disparities (ITDs) are a cue for localization of sounds along the azimuth. Listeners can detect ITDs in the fine structure of low-frequency sounds and also in the envelopes of high-frequency sounds. Sensitivity to ITDs originates in the main nuclei of the superior olivary complex (SOC), the medial and lateral superior olives (MSO and LSO, respectively). This sensitivity is believed to arise from bilateral excitation converging on neurons of the MSO and ipsilateral excitation converging with contralateral inhibition on neurons of the LSO. Here we investigate whether the sensitivity of neurons in the SOC to ITDs can be adequately explained by one of these two mechanisms. Single and multiple units (n = 124) were studied extracellularly in the SOC of unanesthetized rabbits. We found units that were sensitive to ITDs in the fine structure of low-frequency (<2 kHz) tones and also units that were sensitive to ITDs in the envelopes of sinusoidally amplitude-modulated high-frequency tones. For both categories there were "peak-type" units that discharged maximally at a particular ITD across frequencies or modulation frequencies. These units were consistent with an MSO-type mechanism. There were also "trough-type" units that discharged minimally at a particular ITD. These units were consistent with an LSO-type mechanism. There was a general trend for peak-type units to be located in the vicinity of the MSO and for trough-type units to be located in the vicinity of the LSO. Units of both types appeared to encode ITDs within the estimated free-field range of the rabbit (±300 µs). Many units had varying degrees of irregularities in their responses, which manifested themselves in one of two ways. First, for some units there was no ITD at which the response was consistently maximal or minimal across frequencies. Instead there was an ITD at which the unit consistently responded at some intermediate level. Second, a unit could display considerable jitter from frequency to frequency in the ITD at which it responded maximally or minimally. Units with irregular responses had properties that were continuous with those of other units. They therefore appeared to be variants of peak- and trough-type units. The irregular responses could be modeled by assuming additional phase-locked inputs to a neuron in the MSO or LSO. The function of irregularities may be to shift the ITD sensitivity of a neuron without requiring changes in the anatomic delays of its inputs.
Ongoing interaural temporal disparities (ITDs) are a major cue for localization of sounds along the azimuth (Wightman and Kistler 1997 Surgery and recording
Eight female Dutch-belted rabbits (~2 kg) with clean external ears were used in these experiments. Surgical and recording procedures were the same as previously described (Batra et al. 1993 Acoustic stimulation
The sensitivity of units to ITDs of pure low-frequency tones was tested with a "binaural-beat" stimulus (Kuwada et al. 1979 Localization of recording sites
For each electrode penetration, the position of the electrode was set relative to a reference mark on the skull. The depth at which each unit was studied was recorded. During the last recording session, electrolytic lesions were made at selected sites (10 µA for 10-20 s). In some cases the animal was killed and the brain was fixed by immersion, whereas in other cases the animal was deeply anesthetized and then perfused with a 10% solution of formol saline. The brain was sectioned and stained with cresyl violet or thionin (Kuwada et al. 1987 Analysis
ASSESSMENT OF BINAURAL RESPONSE TYPE.
The ipsilateral and contralateral input to a unit was evaluated with the use of one of two techniques. The first technique was used with low-frequency units and some high-frequency units. In this technique, the response of the unit to monaural tone bursts was visually assessed and also quantitatively analyzed to determine whether it responded to the tone and whether the response during the stimulus interval was excitatory or inhibitory. The quantitative analysis was performed to objectively demarcate weak excitation or inhibition from the absence of a response. We restricted this analysis to records for which the stimulus duty cycle was
PHASE PLOTS.
For each unit, a phase plot of the mean interaural phase of the response at different frequencies (or modulation frequencies, for SAM tones) was constructed. The mean interaural phase is the circular mean of the interaural phases (or modulation phases) at which action potentials occur (Kuwada et al. 1987 We recorded from 124 single neurons and multiunit clusters that were sensitive to ITDs. Of these, 100 were sensitive to ITDs in the fine structure of low-frequency tones (43 neurons, 57 multiple units) and 25 were sensitive to ITDs in the envelopes of SAM tones with high-frequency carriers (21 neurons, 4 multiple units). The responses of one neuron to both types of ITDs were studied; that neuron is therefore included twice in statistics and plots that combine high-frequency and low-frequency responses. At the time each neuron or multiunit cluster was studied, we visually assessed whether or not the recording was contaminated with the neurophonic that is present in the SOC. No unit for which recordings were contaminated with neurophonic are included here. All illustrated responses are those of single neurons; multiunit responses are included only in histograms and scatter plots. We saw no clear differences between responses of neurons and multiple units.
Peak-type and trough-type units: general characteristics
Both peak-type and trough-type neurons were present in the SOC. Responses of four neurons sensitive to ITDs of low-frequency tones are illustrated in Fig. 1.
Distribution of CP and linearity of the phase plots
To assess how well ITD-sensitive units in the SOC could be divided into peak-type and trough-type categories, we examined the distribution of the CP. The CP is well defined only when the phase plot for the unit is linear. Most low-frequency units (91 of 100) and all high-frequency units (25 of 25) met the linearity criterion of Yin and Kuwada (1983b)
Contralateral and ipsilateral influences
The influences of contralateral and ipsilateral stimulation on the responses of each unit were classified (see METHODS) as excitatory (E), inhibitory (I), absent (0), or complex (C). The complex category consisted of transient excitation followed by sustained inhibition. The response of each unit was represented by a contralateral-ipsilateral pair, e.g., IE.
The encoded ITD
Neurons in the SOC presumably encode ITDs that are then transmitted to higher levels. The encoded ITD for a given neuron may be reflected in its composite delay curve or in its CD. The composite delay curve of a unit is obtained by averaging its response as a function of ITD across frequencies (Kuwada et al. 1987
Location of peak-type and trough-type units
Our method for locating individual units was subject to considerable error. First, recordings were made over months, and then locations of all recording sites were reconstructed relative to one or a few lesions made at the end of this period (see METHODS). Second, the distance between the entry point and the SOC was large (~15 mm), so any deviation in the straightness of the electrode or in the hypodermic guide would lead to error in placement. For example, a mere 2° deviation in straightness could lead to a ~500-µm error, roughly the width of the MSO in the rabbit.
We have shown that, as in the IC, there are peak-type and trough-type neurons in the SOC. However, we have also shown that many neurons have irregular responses. We discuss the possible reason for the presence of cells with these irregular responses, followed by discussions of low- and high-frequency peak-type and trough-type units in the SOC and the relationship between ITD sensitivity in the SOC and in the IC.
Irregular responses
We defined units as having irregular responses if they had phase plots that deviated systematically from linearity or had intercepts (CPs) far from 0 or 0.5 cycles. It is conceivable that irregular responses were caused by erroneous acoustic calibrations resulting from day-to-day variations in the position of the ear molds. This seems unlikely, at least for low-frequency units. Repeated measurements of the calibrations indicated that any existing pattern of irregularities in the interaural phase differences at these frequencies was maintained after the ear molds were removed and reinserted. Furthermore, irregular responses were observed in the same animals as units that were not irregular, and different units from a particular animal could have different patterns of irregularities. At high frequencies, however, the variability in the interaural phase calibrations was greater. This variability precluded phase corrections, and it is possible that the small, systematic deviations from linearity that were observed in high-frequency units reflected irregularities in the acoustic calibrations.
Low-frequency peak-type units
Most low-frequency peak-type units in the rabbit were localized to the vicinity of the MSO. This location is consistent with other reports that units near or in MSO have CPs near 0 cycles (Spitzer and Semple 1995 Low-frequency trough-type units
Most of our low-frequency trough-type units were localized to the vicinity of the lateral limb of the LSO. Reports of such neurons are few. There are doubtless many reasons for this. Jeffress' (1948) early model for generating a sensitivity to ITDs produced peak-type units and required bilateral excitatory input, which matched the anatomy of the MSO (Jeffress 1958 High-frequency peak-type units
Most of the few high-frequency peak-type neurons were located near or in the ventral portion of the MSO, as was the one neuron encountered by Yin and Chan (1990) High-frequency trough-type units
High-frequency trough-type units were located in the vicinity of the medial (high-frequency) limb of LSO. Neurons with similar properties have also been reported in the LSO of the cat (Joris 1996 Comparisons with the IC
There were many similarities between the sensitivity to ITDs of neurons in the SOC and in the IC. In both structures, low- and high-frequency peak- and trough-type neurons were present, as were neurons that had responses that were irregular to varying degrees. In what follows we compare the irregular responses in the two centers, the proportions of different neurons, and the ITDs encoded.
IRREGULAR RESPONSES.
In both the SOC and the IC, there were units with nonlinear phase plots and units with CPs that were far from 0 and 0.5 cycles (Batra et al. 1993 PROPORTIONS OF DIFFERENT NEURONS.
Low- and high-frequency peak- and trough-type neurons are found in the IC, but their proportions appear to differ from those in the SOC. In the IC (Kuwada et al. 1987 THE ENCODED ITDS.
Most neurons in both the SOC and the IC encoded ITDs within the free-field range of the rabbit (Batra et al. 1993
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). In the inferior colliculus (IC) there are neurons sensitive to ITDs in low-frequency sounds (;lr2 kHz) (e.g., Kuwada et al. 1979, 1987; Rose et al. 1966; Roth et al. 1978; Stillman 1971) and neurons sensitive to ITDs in envelopes of high-frequency sounds (e.g., Batra et al. 1989; Crow et al. 1980; Yin et al. 1984). Some of the neurons sensitive to ITDs in low-frequency sounds appear to encode a particular ITD by discharging maximally at this ITD at all frequencies to which they are sensitive. We refer to such neurons as "peak-type" neurons. Other neurons encode a particular ITD by discharging minimally. We refer to such neurons as "trough-type" neurons. However, the responses of many peak- and trough-type neurons in the IC are irregular in that the ITD at which delay curves at different frequencies align does not lie precisely at the peak or the trough or in that there is considerable jitter in the ITD that evokes maximal or minimal discharge (Kuwada et al. 1987). Similarly, neurons in the IC that are sensitive to ITDs in envelopes of high-frequency sounds can be of the peak type or the trough type, and neurons of both types can exhibit irregularities (Batra et al. 1993).
; Stanford et al. 1992). Thus irregularities in the responses of these neurons may be due to the convergence of inputs from lower centers. The superior olivary complex (SOC) is the main site in the brain stem where neural signals from the two ears are compared to generate a sensitivity to ITDs. Both principal binaural nuclei of the SOC, the medial and lateral superior olives (MSO and LSO, respectively) receive binaural input and contain neurons sensitive to ITDs (Caird and Klinke 1983; Finlayson and Caspary 1991; Goldberg and Brown 1969; Joris and Yin 1995; Langford 1984; Spitzer and Semple 1995; Yin and Chan 1990). However, the MSO and LSO receive different types of inputs and so are likely to encode ITDs in different ways. Most neurons of the MSO are excited by acoustic stimulation of either ear (Caird and Klinke 1983; Goldberg and Brown 1968; Guinan et al. 1972a,b; Langford 1984; Yin and Chan 1990). These neurons are believed to encode ITDs by firing maximally at the ITD for which the temporal pattern of the discharge arriving from both sides is in coincidence (Goldberg and Brown 1969; Jeffress 1948), resulting in a peak-type response. In contrast, most neurons of the LSO are excited by ipsilateral stimulation but inhibited by contralateral stimulation (Boudreau and Tsuchitani 1968; Caird and Klinke 1983; Covey et al. 1991; Finlayson and Caspary 1989; Guinan et al. 1972a,b; Harnischfeger et al. 1985; Moore and Caspary 1983; Sanes 1990; Tsuchitani 1977; Wu and Kelly 1991). These neurons should encode ITD by being maximally suppressed at the ITD at which coincidence occurs (Kuwada et al. 1987; Yin and Kuwada 1983b), resulting in a trough-type response.
; Spitzer and Semple 1995; Yin and Chan 1990) have reported neurons in the vicinity of the MSO with peak-type responses to ITDs both in the fine structure of low-frequency sounds and in the envelopes of high-frequency sounds. Trough-type neurons sensitive to ITDs in the envelopes of high-frequency sounds have been reported in the LSO (Joris 1996). However, no population of trough-type neurons in the SOC sensitive to ITDs in the fine structure has yet been reported, despite a search for such neurons by Spitzer and Semple (1995).
) we demonstrate that all types of units in the SOC act as coincidence detectors.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
; Kuwada et al. 1987). Each rabbit was surgically prepared for recording in three steps. During each step the rabbit was anesthetized with a mixture of ketamine and xylazine (35 and 5 mg/kg im, respectively). In the first step, the dorsal surface of the skull was surgically exposed with the use of aseptic techniques. A short brass rod of square stock was mounted on the left side, parallel to the sagittal suture, with screws and dental cement. The right side of the skull was left exposed between lambda and bregma to allow electrodes to be lowered to the right SOC. In one case, the bone over the left SOC was also left exposed. The rabbit was then allowed several days to recover. In the second step, custom ear molds were made of Audalin (Esschem, Essington, PA), an ear-impression compound. Each ear mold was penetrated by a tube through which sound could be delivered. The tubes for the two ears were matched in length.
). In this paradigm, tones that differed in frequency by 1 Hz were delivered to the two ears, with the frequency to the contralateral ear usually higher. This stimulus produced a 1-Hz cyclic variation in the ongoing ITD. Units sensitive to ITDs in the fine structure were typically tested only below 2 kHz. The "best binaural-beat frequency" was taken to be the frequency at which the response to the binaural-beat stimulus was maximal. The sensitivity of units to ITDs in high-frequency sounds (>2 kHz) was tested in a similar manner with the use of sinusoidally amplitude-modulated (SAM) tones. In this case, the tones at the two ears were set to the same carrier frequency, usually at or near the best frequency of the unit, or at an effective frequency if they were broadly tuned. The best frequency of these units was assessed with the use of monaural (usually ipsilateral) tones at a fixed suprathreshold intensity presented over a wide range of frequencies. The modulation frequencies at the two ears differed by 1 Hz (Batra et al. 1989; Yin et al. 1984), again with the frequency to the contralateral ear usually higher. This stimulus produced a 1-Hz cyclic variation in the ITD of the envelope, but no variation in the ITD of the carrier. The ITD of the carrier was zero relative to the standard calibration (see below). All tones and tone bursts had linear rise/fall times of 4 ms. For the sake of brevity, we often refer to "low-frequency units" or "high-frequency units," depending on whether sensitivity of the unit to fine-structure or envelope ITDs was tested. This should cause no confusion, because only one unit was tested with both kinds of stimuli.
; Yin and Kuwada 1983b). The period histograms had 10 bins.
). The acoustic delay for signals to reach the tympanum was 216 ± 12 (SD) µs (n = 16, estimated from the slope of the phase-vs.-frequency plot). The average difference between the ears was 5.0 ± 9.6 µs, with the delay for the right ear nominally longer. Calibration corrections for the phases of responses to SAM tones were not performed; however, the intensities quoted in the figure legends were corrected to reflect the true levels in dB SPL.
).
50%, because it was difficult to distinguish weak excitation or inhibition when the off-time was brief. From each record, a "repetition-interval synchronization coefficient" and a "repetition-interval phase" were calculated by treating the repetition interval of the tone as the period of a cyclic stimulus. A repetition-interval synchronization coefficient that was significant (Rayleigh test of uniformity, P < 0.001) (Mardia 1972) denoted a response that followed the stimulus. Excitation was distinguished from inhibition by examining the repetition-interval phase. A phase less than the duty cycle implied excitation, whereas a phase greater than the duty cycle implied inhibition. An exception to this rule was responses with repetition-interval phases that exceeded 0.85 cycles or that corresponded to times that were shorter than the latency of the unit (e.g., Fig. 6 A and B, left). Such responses invariably consisted of transient excitation followed by sustained inhibition and were classified as complex.
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FIG. 6.
Responses of high-frequency peak-type and trough-type neurons to monaural stimulation. A and B: same 2 peak-type neurons as in Fig. 2, A and B. C and D: same 2 trough-type neurons as in Fig. 2, C and D. In D, left, contralateral stimulation ( 
) is superimposed on an ongoing ipsilateral stimulus. Insets in A and B: same responses plotted with a coarser binwidth to demonstrate sustained inhibition. Insets in C and D: 1st 20 ms of response. Each plot illustrates a full repetition interval. Stimulus durations (ms) and number of repetitions (contralateral/ipsilateral): 50, 50/50 (A); 75, 100/150 (B); 50, 75/75 (C); 50 (contra) + 150 (ipsi)/50, 20/100 (D). Intensities and frequencies as in Fig. 2. Binwidth: 5 ms (A and B, insets), 500 µs (D, contralateral), and 200 µs elsewhere.
have suggested that the facilitation observed in some neurons of the LSO is a consequence of rebound excitation. Conversely, Colburn et al. (1990) have argued that the suppression observed in neurons of the MSO can be adequately modeled without resorting to inhibitory inputs.
; Yin and Kuwada 1983a). The phase plots were fit with a straight line with the use of a least-squares procedure (Kuwada et al. 1987). Each phase value was weighted by the product of the interaural synchronization coefficient and the mean rate to reduce the effect of responses at frequencies for which sensitivity to ITDs was weak.
compares the mean square error (MSE) of deviations about the fit with that obtained from a random simulation. If the MSE is less than that obtained from the simulation for a particular significance level (P < 0.005), then the phase plot is considered significantly linear. The 
2 test used by Kuwada et al. (1987)1 compares the MSE with the average variability of the measurements of the mean phases. If the MSE is significantly greater (P < 0.005) than the average variability, then the phase plot is considered to deviate significantly from linearity. We also used a one-sample runs test (Siegel 1956) to examine systematic patterns of deviations about the fit. This procedure examines the number of runs of values in a sequence that are greater or less than some criterion. It then tests whether the number of runs is more or fewer than statistically expected (P < 0.05). We applied this runs test to ascertain whether there was a systematic pattern of deviations about the fit, i.e., whether a phase plot contained a statistically low number of runs. Our usage differs from that intended in two regards. First, the test is intended to be applied to a situation in which the point from which positive and negative deviations are measured is independent of the data. Our use of the fitted line as the zero point is not in accord with this condition. In our situation, at least three runs of deviations had to occur, because the fit has two parameters (intercept and slope). Consequently, the likelihood of a low number of runs in our situation is even lower than for the test as described. Second, phase plots for which the number of runs were greater than expected were not considered significant, because this was the more conservative approach. These two factors imply that our significance level is more strict than P < 0.05. The runs test requires a large number of measurements, so this analysis was restricted to units for which the response was measured at 
11 frequencies.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 1.
Sensitivity of 4 neurons in the superior olivary complex (SOC) to interaural temporal disparities (ITDs) of low frequencies. Left: response as a function of ITD at selected frequencies. Functions were generated from the responses to binaural-beat stimuli (Kuwada et al. 1987 ; Yin and Kuwada 1983b). The neurons of A and B exhibited peak-type sensitivity to ITDs in that the maximal response occurred at about the same ITD at all frequencies. The neurons of C and D exhibited trough-type sensitivity to ITDs in that the response was minimal at about the same ITD at all frequencies. Right: peak- or trough-type sensitivity of these neurons was confirmed by their phase plots, which show the mean interaural phase of the response at different frequencies. The mean interaural phase is the circular mean of the interaural phases at which action potentials occurred (Kuwada et al. 1987; Yin and Kuwada 1983a). The line is a weighted least-squares fit. In A and B, the fit indicates that the characteristic phase (CP), given by the intercept, is near 0 cycles, confirming that the neuron responded maximally at about the same ITD across frequencies. In C and D, the CP is near 0.5 cycles, confirming that the response of the neuron was minimal at about the same ITD across frequency. Because the CP is an angular measurement, its value can be quoted only over 1 complete cycle of phase change. Here we take the CP to lie between 
0.25 and 0.75 cycles. The characteristic delay (CD), equal to the slope of the phase plot, lies near the common peaks (A and B) or troughs (C and D) of the delay curves (left, arrowheads). Best binaural-beat frequencies and average contralateral (re: site of recording)/ipsilateral intensity levels (dB SPL): 850 Hz, 64/64 (A); 700 Hz, 52/53 (B); 400 Hz, 64/65 (C); 350 Hz, 64/65 (D).
). A CP near 0 cycles (Fig. 1, A and B) indicated that the neuron was of the peak type, whereas a CP of 0.5 cycles (Fig. 1, C and D) indicated that it was of the trough type. The slope of the linear fit yielded a quantitative measure of the neuron's "characteristic delay" (CD, arrowheads in Fig. 1, left) (Rose et al. 1966; Yin and Kuwada 1983b), which is a measure of the ITD at which the signals from the two sides arrive in coincidence.
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FIG. 2.
Sensitivity of 4 neurons in the SOC to ITDs of high-frequency sinusoidally amplitude-modulated (SAM) tones. Format is the same as for Fig. 1, except that delay curves (left) are at different modulation frequencies and phase plots (right) are a function of modulation frequency. The neurons of A and B exhibited peak-type sensitivity to ITDs, whereas the neurons of C and D exhibited trough-type sensitivity. Neurons in A and B were broadly tuned; those in C and D were tested at their best frequencies. Contralateral/ipsilateral intensities (dB SPL): 51/52 (A); 41/42 (B); 40/19 (C); 32/36 (D). Modulation depth: 80% in all cases. Carrier frequencies as indicated.
. As mentioned, peak-type units should have CPs near 0 cycles, and trough-type units should have CPs near 0.5 cycles, so a strict division into these types should yield a distribution across all units consisting of tight clusters at 0 and 0.5 cycles.
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FIG. 3.
Distribution of the CP. For each neuron, the responses at the stimulus parameters that produced ITD sensitivity over the widest range of frequencies in octaves were used. Filled bars: distribution of CP for units sensitive to ITDs in the fine structure of low-frequency tones (n = 91). Open bars: distribution of CP for units sensitive to ITDs in high-frequency SAM tones (n = 25). Dashed line: CP = 0.25 cycles, midway between the ideal value for peak-type units (0 cycles) and that for trough-type units (0.5 cycles).
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FIG. 4.
Sensitivity to ITDs of 4 neurons with irregular responses. Format as Fig. 1. All neurons were sensitive to ITDs of low-frequency tones. A and B: 2 neurons with delay curves that had the same relative amplitude at a common ITD; but this amplitude was intermediate between the minimum and the maximum. These neurons had CPs that were far from 0 or 0.5 cycles. C and D: 2 neurons with delay curves that did not align well at any relative amplitude. These neurons had nonlinear phase plots. Best binaural-beat frequencies and average intensity levels (dB SPL): 600 Hz, 77/70 (A); 875 Hz, 64/63 (B); 275 Hz, 63/63 (C); 800 Hz, 63/64 (D).
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FIG. 5.
Responses of low-frequency peak-type and trough-type neurons to monaural stimulation. A and B: same 2 peak-type neurons as in Fig. 1, A and B. C and D: same 2 trough-type neurons as in Fig. 1, C and D. Insets: 1st 20 ms of the response, to demonstrate synchrony to the stimulation frequency. Tick marks above insets are at intervals corresponding to the stimulus period. Frequencies (Hz), intensities (dB SPL), and number of repetitions: 850, 66/74, 100 (A); 600, 51/53, 50 (B); 400, 60/63, 50 (C); 350, 60/63, 75 (D). All stimuli were 50 ms long, presented every 125 ms. Binwidth: 200 µs.
; Bourk 1976; Tsuchitani 1982; Young et al. 1988).2 In other neurons there was a brief pause after the first action potential, followed by sustained activity (Fig. 6D, right, inset). This pattern has been referred to as primary-like with notch or OL (e.g., Blackburn and Sachs 1989; Godfrey et al. 1975; Smith et al. 1991). The contralateral inhibitory input was evidenced by suppression of the spontaneous activity (Fig. 6C, left) or by suppression of the discharge elicited by an ongoing ipsilateral tone (Fig. 6D, left).
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FIG. 7.
CPs of units in different binaural categories. Binaural category of a unit was usually determined from the responses at the intensity at which ITD sensitivity was tested. If responses at that intensity were unavailable, then responses at the nearest higher intensity were used. A: low-frequency units (n = 55). An I0, an IE, and an 0I unit were not plotted. The IE unit was a multiunit recording of the trough type. Of the 11 units with CPs nearer 0.5 cycles than 0 cycles that were classified as 0E, 7 had sufficient spontaneous activity to have permitted detection of contralateral inhibition. B: high-frequency units (n = 25). An EI and an II unit were not plotted. 0E units were tested with monaural stimuli. Circles: individual units. Ovals: groups of 4 units with CPs within 0.1 cycles.
). It was surprising that contralateral inhibition was not directly observed in low-frequency trough-type units either as an OFF response or as suppression of the spontaneous activity that was often present. Units with irregular responses (CPs far from 0 and 0.5 cycles) were distributed across the four most common categories. This can be seen by observing that CPs of units in these categories were not tightly clustered around 0 or 0.5 cycles.
; Yin and Kuwada 1983b). For a low-frequency neuron, the composite delay curve has a similar form to the response of the neuron to interaurally delayed noise (Yin and Chan 1990; Yin et al. 1986). For a high-frequency neuron, the composite delay curve is similar to the response to interaural delays of a band of noise centered at the neuron's characteristic frequency (Joris and Yin 1995).
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FIG. 8.
Composite delay curves of selected low-frequency neurons. A-D: the 2 peak-type and 2 trough-type neurons of Fig. 1. E-H: the 4 neurons of Fig. 4 with irregular responses. Composite delay curves were based on delay curves that had 10 bins/cycle. In the ±1.5-ms interval, 300 points were interpolated.
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FIG. 9.
Composite delay curves of selected high-frequency neurons. The 2 peak-type and two trough-type neurons of Fig. 2 are illustrated. Composite delay curves were based on delay curves that had 10 bins/cycle. In the ±6-ms interval, 300 points were interpolated.
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FIG. 10.
Distributions of CD and composite peak and trough delay. Filled bars: low-frequency units. Open bars: high-frequency units. A: distribution of CD for peak-type units (low-frequency, n = 52; high-frequency, n = 6). B: distribution of CD for trough-type units (low-frequency, n = 39; high-frequency, n = 19). C: distribution of composite peak delay for peak-type units. D: distribution of composite trough delay for trough-type units. Number of units in C and D is the same as in A and B. Composite peak and trough delays were calculated from composite delay curves constructed over a ±4-ms interval by fitting a parabola to the upper 30% of the peak of the composite delay curve (Kuwada et al. 1987 ) and the lower 30% of the trough of the composite delay curve. Number of units outside plotted range (low-frequency, high-frequency): 1, 1 (A); 1, 3 (B); 5, 1 (C); 1, 1 (D).
). However, the two types of units had CDs associated with sounds arising in different hemifields. Almost all peak-type units (42 of 52, 81%) had CDs corresponding to the contralateral hemifield (ipsilateral delays). In contrast, the CDs of low-frequency trough-type units were biased (24 of 39, 62%) toward the ipsilateral hemifield (contralateral delays).
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FIG. 11.
Location of recording sites. A: locations of lesions in a case for which units studied in the vicinity of the lesion were of the peak type. The middle of 3 lesions is just medial to the medial superior olive (MSO). In this animal, recordings were made from both sides. Medial limb of the lateral superior olive (LSO) on side opposite lesions is obscured by electrode tracks. LTB, lateral nucleus of trapezoid body; MTB, medial nucleus of trapezoid body; VTB, nucleus of ventral trapezoid body; Pyr, pyramid; Tz, trapezoid body. B: locations of lesions in a case for which most units studied were of the trough type. In this case, ITD sensitivity was encountered ~700 µm dorsal to the most ventral of 3 closely spaced lesions, in the region of the lateral limb of LSO. Note that the LSO of the rabbit has 4 limbs and is M shaped. C: reconstruction of recording sites for peak-type units. One animal (88S09) was excluded because of a large scatter in the reconstructed sites, perhaps because of the loss of a needed reference mark on the skull. 
, low-frequency units (n = 43); 
, high-frequency units (n = 5). D: similar reconstruction for trough-type units (low-frequency, n = 36; high-frequency, n = 17).
and ) tended to lie in the vicinity of the MSO, with a smaller grouping near the medial limbs of LSO. In contrast, low-frequency trough-type units (Fig. 11D, ) tended to lie laterally and dorsally, in the vicinity of the lateral limb, or low-frequency region, of the LSO. High-frequency trough-type units () were located in or near the medial, high-frequency part of LSO.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Third, units with irregular responses did not differ from other units in the distribution of their CDs or in the positions of their composite peaks or troughs. Finally, they did not appear to lie in locations distinct from those of other units.
found that ITD-sensitive neurons were present in a dorsal-rostral-medial region of the SOC of the gerbil. These neurons typically did not phase lock, and they were monaurally unresponsive, i.e., they did not respond to stimulation of one or both ears individually (E0, 0E, and 00 units). However, in the present study there was no clear association between monaurally unresponsive units and units with irregular responses, suggesting that irregularities were not specific to neurons in periolivary nuclei. Further evidence that irregular responses were not specifically associated withperiolivary neurons is provided in the companion paper (Batra et al. 1997), in which the phase locking of neurons in the SOC is examined. For these reasons we consider units with irregular responses to be variants of peak- and trough-type units rather than a distinct population. Thus it seems likely that the MSO and LSO both contain neurons with irregular responses.
reported a neuron in the kangaroo rat with delay curves at different frequencies that did not coincide "...either at the peak, valley or at any other point." This description is consistent with the nonlinear phase plots associated with some irregular responses. Two other studies of the MSO reported irregular responses (Spitzer and Semple 1995; Yin and Chan 1990), although they did not draw specific attention to them. The phase plot shown by Yin and Chan (1990), and one of the two shown by Spitzer and Semple (1995), show oscillations. In addition, the distributions of CP in both studies were not tightly clustered about 0 cycles. The spread of the CP distribution in the gerbil (Spitzer and Semple 1995) was wider than that in the cat (Yin and Chan 1990) and about as wide as we observed for peak-type units in the rabbit.
e and i). An external interaural phase difference could also be imposed (
). The response amplitude of the binaural cell was the amplitude of the summed inputs. By varying the external interaural phase difference, we could calculate the mean interaural phase of the response.
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FIG. 12.
A possible model for irregular responses. A: schematic of the model. Binaural cell ( ) receives 3 inputs: an ipsilateral excitatory input (Ei), a contralateral excitatory input (Ec), and a contralateral inhibitory input (Ic). Model represents either a neuron in the MSO with an additional contralateral inhibitory input or a neuron in the LSO with an additional contralateral excitatory input. Inputs were modeled by sine waves at the stimulus frequency (f) with individual amplitudes. The contralateral inputs were delayed (e, i) or advanced relative to the ipsilateral input. An external interaural phase difference () could be introduced. Response amplitude |R| was equal to the amplitude of the summed inputs. B-D: model was used to generate phase plots such as those in Fig. 4. Ai dropped out of the final equations for these plots. Values of the 3 free parameters Aci/Ace, e, and i (ms): 0.8, 0.3, 0.3 (B); 2.0, 1.9, 1.9 (C); 1.4, 0.9, 0.2 (D).
, 1994; Smith 1995) in addition to bilateral excitatory input. Ipsilateral inhibitory input is likely to come via the lateral nucleus of the trapezoid body (Cant and Hyson 1992; Kuwabara and Zook 1992) and contralateral inhibitory input via the medial nucleus of the trapezoid body (Banks and Smith 1992; Cant and Hyson 1992; Covey et al. 1991; Kiss and Majorossy 1983; Kuwabara and Zook 1992; Spangler et al. 1985). The inhibitory input from both these nuclei is likely to be phase locked because they receive input from globular bushy cells of the anteroventral cochlear nucleus (Kuwabara et al. 1991; Smith et al. 1991; Tolbert et al. 1982; Warr 1972, 1982), which synchronize strongly to tones (Smith et al. 1991). Parts of the MSO may also receive multiple excitatory inputs from the contralateral side with differing delays (Oliver and Beckius 1996), which could contribute to the presence of irregular responses as well.
; Goldberg and Brown 1968; Kil et al. 1995; Warr 1982), although its extent varies among species. There are also other ipsilateral inputs from the lateral nucleus of the trapezoid body (Kuwabara and Zook 1992) and from a region of the cochlear nucleus that does not contain spherical bushy cells (Cant and Casseday 1986).
). Nonlinearities in the interaural phase plots of neurons in the SOC could result if the nonlinearities of the inputs from the two sides (or even 2 inputs from the same side) were mismatched, as might occur if the best frequencies of the two inputs differed slightly. It is unlikely that the "peak splitting" observed in auditory nerve fibers (e.g., Ruggero and Rich 1989) contributes to the nonlinearities, because this effect occurs only at high intensities not employed here.
; Yin and Chan 1990). Other peak-type units were localized to the vicinity of the LSO. This may be an error in localization. However, neurons with peak-type characteristics have been reported in the hilus of the LSO of the gerbil (Spitzer and Semple 1995). It is also possible that some of these units may have been high-frequency units that were studied in the tails of their tuning curves.
; Yin and Chan 1990) and with the main excitatory afferents to MSO.
; gerbil: Spitzer and Semple 1995). Other studies have used the ITD at which maximal discharge occurs as a measure of the encoded ITD. Crow et al. (1978) found a nearly even distribution of the best delay between the sound fields in the MSO of the kangaroo rat, with a slight bias toward ipsilateral delays. The preference for ipsilateral delays presumably reflects a shorter path length from the ipsilateral side compared with the contralateral side. Langford (1984), by contrast, found that most neurons in the MSO of the chinchilla preferred contralateral delays.
; chinchilla: Langford 1984; gerbil: Spitzer and Semple 1995; cat: Yin and Chan 1990). This is a consistent feature despite the fact that some of these species have small heads, which should limit the ITDs available. For example, the ITD available to a gerbil in the free field should be <100 µs. Palmer et al. (1990) made a similar observation for the ITDs encoded in the ICs of different species.
), neurons with large CDs were not necessarily of low best frequency as measured with the use of the binaural-beat stimulus.
). Many investigators may therefore have focused their attention on the MSO. The mechanism for trough-type sensitivity to ITDs was not explored until much later (Batra et al. 1993; Joris 1996; Kuwada et al. 1987; Rose et al. 1966; Yin and Kuwada 1983b).
; Finlayson and Caspary 1991; Joris and Yin 1995; Spitzer and Semple 1995). Caird and Klinke (1983) and Joris and Yin (1995) each reported the responses of one neuron tested at one frequency. These responses were IE, and therefore consistent with a trough-type mechanism. Finlayson and Caspary (1991) demonstrated ITD sensitivity in a large sample of neurons in the lateral limb that were also IE. In contrast to the present results, Finlayson and Caspary found that these neurons discharged more strongly at zero ITD than at the large ITDs produced by 180°-out-of-phase stimulation. The reason for this difference is unclear.
found no trough-type neurons in the LSO, despite a specific search for them. They found only a few neurons near the medial edge of the lateral limb that were ITD sensitive. In contrast to our results, the responses of these neurons were more consistent with a peak-type mechanism. Spitzer and Semple attributed the presence of peak-type sensitivity in the LSO to a direct input from the contralateral cochlear nucleus that is probably excitatory (Kil et al. 1995). Although this input appears to be present in a number of species, it is exceptionally large in the gerbil.
).
.
).
). We have already suggested that high-frequency trough-type neurons in the IC may sharpen the azimuthal receptive fields of peak-type neurons via lateral inhibition (Batra et al. 1993). Low-frequency trough-type neurons in the SOC could sharpen the receptive fields of peak-type neurons in the IC by feedforward inhibition (Kuwada et al. 1997). Some neurons of the LSO are presumed to be inhibitory, and these project directly to the ipsilateral IC (Glendenning et al. 1992; Saint Marie and Baker 1990; Saint Marie et al. 1989). Others are presumed to be excitatory, and feedforward inhibition could arise indirectly from these via the dorsal nucleus of the lateral lemniscus.
in the cat. This is the part of the MSO that is believed to be sensitive to high frequencies (Goldberg and Brown 1968; Guinan et al. 1972b).
in the MSO of the cat had similar properties.
; Joris and Yin 1995).
; Caird and Klinke 1983; Finlayson and Caspary 1989; Guinan et al. 1972a,b; Moore and Caspary 1983; Sanes 1990; Wu and Kelly 1991). In two neurons, both excitatory and inhibitory inputs were observed to ipsilateral stimulation. The PSTs to ipsilateral stimulation were typically of the transient chopper type (3 of 13) or of the primary-like with notch or OL type (6 of 13). Both types are consistent with earlier reports (Boudreau and Tsuchitani 1970; Brownell et al. 1979; Guinan et al. 1972a,b; Tsuchitani 1982), although we encountered a larger fraction of units with primary-like-with notch or OL PSTs. These latter PST types may be more characteristic of the unanesthetized LSO (Brownell et al. 1979).
recently found that high-frequency units in the LSO of the cat had CDs that favored ipsilateral delays. In that study and ours, the sample size was small (~20 units). However, our distribution for high-frequency units is similar to that for our low-frequency trough-type units, for which we have a larger sample.
have convincingly argued that the range of interaural intensity differences that an animal normally encounters in the free field will modulate the response of these neurons more than the range of ITDs. Thus a major function of these neurons is presumably to encode interaural intensity differences. However, in addition, these neurons may also play roles similar to those posited for low-frequency trough-type neurons, encoding information about reverberant environments and sharpening the azimuthal receptive fields of peak-type neurons in the IC.
; Kuwada et al. 1987). In the IC we used a 2 test to assess deviations from linearity of phase plots (see METHODS), whereas in the SOC we assessed systematic deviations with the use of the runs test. To provide comparisons with the IC, we also performed the 2 test on the units in the SOC. With the use of this test, a similar proportion of units in the SOC and the IC had nonlinear phase plots [low-frequency: 67% in the SOC vs. 75% in the IC; high-frequency: 80% in the SOC vs. 77% in the IC, (unpublished observations)]. Thus the nonlinearities in the phase plots of neurons in the IC may be inherited, in part, from the responses of neurons in the SOC.
). In the SOC, nonlinearities did not preferentially occur at lower frequencies, and dual CDs were not evident. Consequently, some of the interactions that produce nonlinear phase plots in the IC probably lie at levels above the SOC. These interactions could occur among the projections to the IC from the MSO, LSO, and dorsal nucleus of the lateral lemniscus (reviewed by Oliver and Huerta 1992), via the intrinsic circuitry of the IC (Oliver et al. 1991), or via descending connections from the cortex (reviewed by Oliver and Huerta 1992).
; Stanford et al. 1992) there are fewer low-frequency trough-type neurons than in the SOC. The greater proportion of trough-type neurons in the SOC may be a consequence of the relative frequency with which we penetrated LSO or MSO. However, there is also another possibility. The trough-type neurons in the LSO may be inhibitory and so not produce trough-type responses in the IC. There is evidence that a proportion of neurons in the LSO that project ipsilaterally is inhibitory (Glendenning et al. 1992; Saint Marie and Baker 1990; Saint Marie et al. 1989). If the rabbit follows the pattern in the cat (Glendenning and Masterton 1983; Saint Marie et al. 1989), where low-frequency LSO projects primarily ipsilaterally, then the proportion of low-frequency trough-type neurons in IC would be small.
). The paucity in the SOC may be due to a sampling bias or may reflect extensive arborization of high-frequency MSO inputs to the IC. Alternatively, the increased number of peak-type neurons in the IC may occur via the complex interaction of multiple sources (Batra et al. 1993). On this point, many high-frequency peak-type neurons in the IC were inhibited by ipsilateral and excited by contralateral stimulation, which is an unexpected combination of inputs for peak-type responses.
; Kuwada et al. 1987; Stanford et al. 1992), a feature that is also preserved at the level of the thalamus (Stanford et al. 1992). Peak-type units in both the SOC and the IC tend to prefer ipsilateral delays. Trough-type units, however, have CDs and composite trough delays biased toward contralateral delays in the SOC, but in the IC show a shift toward ipsilateral delays (low frequency: personal observations; high-frequency: Batra et al. 1993). This shift may be due to the proportion of the projection from LSO that is crossed (reviewed by Oliver and Huerta 1992). Similarly, high-frequency trough-type units in the IC were mostly EI (Batra et al. 1993), whereas in the SOC they were nearly all IE. This reversal in laterality may also reflect the crossed projection from the LSO to the IC.
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ACKNOWLEDGEMENTS |
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We thank T. Trahiotis and D. Kim for comments on the manuscript. We also thank T. Ju and R. F. Manfredi for performing much of the necessary computer programming and L. Seman for histological and technical assistance. T. Stanford participated in some of the early experiments.
This research was supported by National Institute of Deafness and Other Communications Disorders Grant DC-02178. During analysis of the data and preparation of the manuscript, R. Batra was supported by DC-01366.
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FOOTNOTES |
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1
There are two typographical errors in the equations describing our assessment of linearity in Kuwada et al. (1987). In the equations for the weighted MSE s2 and for 2, the entire term in square brackets should be squared, not just 
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, except that a binwidth of 0.2-0.5 ms was used.
Address reprint requests to R. Batra.
Received 9 July 1996; accepted in final form 27 May 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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a disavowal.
J. Acoust. Soc. Am.
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