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Departments of Biomedical Engineering and Neurobiology and Anatomy and the Center for Navigation and Communication Sciences, University of Rochester, Rochester, New York
Submitted 20 April 2007; accepted in final form 21 July 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Glendenning et al. 1981; Shneiderman et al. 1988; Vater et al. 1995; Yang et al. 1996). It also receives a heavy input from the contralateral DNLL by the commissure of Probst (Glendenning et al. 1981; Iwahori 1986; Oliver and Shneiderman 1989; Shneiderman et al. 1988). Some of the inputs to the DNLL are excitatory, whereas others are inhibitory (Fu et al. 1997; Wu 1999; Wu and Kelly 1995, 1996; Yang and Pollak 1994a,b). The DNLL, in turn, projects to the contralateral DNLL and to the IC bilaterally (Adams 1979; Bajo et al. 1999; Brunso-Bechtold et al. 1981; Iwahori 1986; Ross et al. 1988; Shneiderman et al. 1988; Tanaka et al. 1985; Zook and Casseday 1982).
Most DNLL neurons are immunoreactive for antibodies against 
-aminobutyric acid (GABA) or glutamic acid decarboxylase (Adams and Mugnaini 1984; Gonzalez-Hernandez et al. 1996; Moore and Moore 1987; Roberts and Ribak 1987; Saint-Marie et al. 1997; Shneiderman et al. 1993; Thompson et al. 1985; Vater et al. 1992b; Winer et al. 1995), indicating that the DNLL is primarily a source of inhibitory projections. Consistent with this idea, the projections to the contralateral DNLL and IC are characterized by terminals with pleomorphic vesicles and symmetrical synaptic contacts (Oliver and Shneiderman 1989; Shneiderman and Oliver 1989). Moreover, reversible inactivation of the DNLL has been shown to weaken the strength of tonic, monaural, and binaural inhibition recorded from neurons in the IC (Faingold et al. 1993; Kelly and Li 1997; Kidd and Kelly 1996; Li and Kelly 1992; Thornton and Rees 1997). Behavioral studies have shown that lesions of the DNLL or transection of its crossed efferent projections in the commissure of Probst degrade the ability of animals to localize sounds in the horizontal plane (Ito et al. 1996; Kelly et al. 1996).
The physiological response properties of DNLL neurons have been described in a variety of species including cat (Aitkin et al. 1970; Brugge et al. 1970), horseshoe bat (Metzner and Radtke-Schuller 1987), big brown bat (Covey 1993), mustache bat (Markovitz and Pollak 1993, 1994; Yang and Pollak 1994a,b, 1998; Yang et al. 1996), rat (Bajo et al. 1998; Kelly et al. 1998), Mexican free-tailed bat (Bauer et al. 2002; Xie et al. 2005), gerbil (Siveke et al. 2006), and rabbit (Kuwada et al. 2006). There is good agreement among these studies that most units in the DNLL show V-shaped excitatory tuning curves for contralateral stimulation and that most units are binaural. The majority of binaural units are excited by stimulation of the contralateral ear and inhibited by simultaneous stimulation of the ipsilateral ear, whereas fewer units are excited by sound in both ears. So far, there are only few data on the extent to which inhibition shapes the contralateral and ipsilateral frequency selectivity of DNLL neurons because most prior studies were conducted in anesthetized preparations or awake bats that lack the spontaneous activity necessary for direct observation of inhibition.
The goal of the present study was to characterize the monaural and binaural response properties of single units in the DNLL of unanesthetized decerebrate cat. The results show that DNLL units can be grouped into three types based on the patterns of excitation and inhibition observed in monaural frequency response maps. These types have been named types v, i, and o (lower- vs. uppercase letters) following the convention first used by Ramachandran et al. (1999) to identify response map types in the IC of decerebrate cat. The contralateral response maps of type v units show a broad V-shaped excitatory area and little or no inhibition. These units are excited by ipsilateral stimulation and show binaural facilitation. The maps of type i units show a more level tolerant I-shaped excitatory area that is flanked by inhibition and type o maps display an O-shaped island of excitation at low stimulus levels that is bounded by inhibition at higher levels. Both type i and type o units show ipsilateral inhibition and exhibit binaural inhibition. Other basics differences among these unit types include their distribution of best frequencies (BFs), thresholds to tones, shapes of BF tone rate-level functions, and relative responsiveness to tones versus broadband noise. The results suggest that the DNLL contains a heterogeneous population of units that can exert strong, differential effects in the IC.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Experiments were performed on 10 adult male cats (3–4 kg) with infection-free ears and clear tympanic membranes. All procedures were carried out under guidelines approved by the University Committee on Animal Resources at the University of Rochester. Before surgery, cats were anesthetized with a combination of ketamine [40 mg/kg, administered intramuscularly (im)] and xylazine (0.5 mg/kg im), and given single doses of atropine sulfate (0.05 mg/kg im) to minimize mucous secretions and dexamethasone (2 mg/kg, im) to reduce cerebral edema. Thereafter, body temperature was maintained at 39 ± 0.5°C using a regulated heating blanket. Breath and heart rates were monitored. The cephalic vein was cannulated to allow intravenous infusions of fluids, including supplemental doses of ketamine (15 mg/kg) and xylazine (0.1 mg/kg) as needed to maintain areflexia. A tracheotomy was performed to facilitate quiet breathing.
A midline incision was made over the skull and the temporalis muscles reflected to visualize the top of the skull and the ear canals. A craniotomy was performed over parietal cortex, and the cat made decerebrate by aspirating under visual guidance the underlying cortex and brain stem between the thalamus and superior colliculus. Anesthesia was then discontinued. The ear canals were transected near the tympanic membrane to accept hollow ear bars for delivering closed-field acoustic stimuli. The cat's head was secured in a stereotaxic frame in a standard horizontal orientation. A second craniotomy was performed over occipital cortex and the tissue overlying the IC was aspirated. Part of the tentorium was removed to allow complete access to the IC. The DNLL was accessed by advancing recording electrodes dorsoventrally through the IC.
Cats were killed with an overdose of sodium pentobarbital (100 mg/kg, administered intravenously) at the end of recording sessions. Animals were perfused intracardially with 0.9% saline followed by fixative (3% paraformaldehyde and 0.1% glutaraldehyde in 0.1 M phosphate buffer; pH 7.4) and two sucrose solutions (10 and 30%). The brains were removed from the skull and immersed in a 30% sucrose solution until they sank. Parasagittal sections (40 µm thick) of frozen brains were cut on a sliding microtome and stained with cresyl violet. The locations of electrode tracks and recording sites were verified from patterns of gliosis and electrolytic lesions. Images of sections were acquired using a MicroFire digital camera mounted on an Olympus AX70 microscope and Image-Pro software.
Stimulus generation and delivery
All experiments were carried out in a double-walled sound-attenuating chamber (IAC). Acoustic stimuli were delivered bilaterally by electrostatic speakers (TDT) that were coupled to hollow ear bars. At the start of each experiment, the frequency response of both systems was measured with a probe tube microphone (Brüel & Kjær) that inserted into the ear bars near the tympanic membrane. The calibration function of each closed acoustic system decreased relatively monotonically from 120 dB SPL at 40 Hz to 90 dB SPL at 40 kHz. Interaural cross talk was 
30 dB (and typically >50 dB) down in the ear opposite to the sound source (Davis 2005a), which is well below the maximum interaural level difference (ILD) used during binaural testing.
Pure tones and white noise were digitally created using TDT System 3 hardware. Noise stimuli were synthesized in the frequency domain and converted to time-domain waveforms by taking the inverse Fourier transform of the noise spectrum. The magnitude spectrum of the noise was corrected to compensate for the nonflat calibration curves. Analog signals were created by playing the waveforms through a 16-bit D/A converter at a sampling rate of 100 kHz. Most stimuli were 200 ms in duration and presented at a rate of one burst/s; detailed frequency response maps were constructed from responses to tone bursts that were 50 ms long and presented at a rate of four bursts/s. All stimuli were gated on and off with 10-ms rise/fall times. Tones were attenuated relative to the acoustic ceiling at each frequency to achieve a desired input sound pressure level in dB SPL. Noise stimuli were attenuated relative to the maximum spectrum level achievable without any attenuation (
45 dB SL).
Data collection and analysis
Single-unit activity was recorded with platinum–iridium microelectrodes. Electrodes were advanced using a motor-controlled multielectrode positioning system (EPS; Alpha-Omega). The signal from the electrode was amplified (x10,000–30,000) and filtered from 0.3 to 6 kHz (MCP; Alpha-Omega). Action potentials were detected using template-matching software (MSD; Alpha-Omega). Spike times relative to stimulus onset were stored for on- and off-line analyses.
Recording electrodes were advanced dorsoventrally through the IC and into the DNLL, while 50-ms search tones or noise bursts were presented to the contralateral ear. Electrode entry into the DNLL was signaled by an abrupt change in the best frequency of background activity from high frequencies (30–40 kHz) to low frequencies (<1 kHz) (Aitkin et al. 1970) at a depth of about 5–6 mm. When a single DNLL unit was isolated, its BF and threshold were determined using audiovisual feedback and the following characterization protocol was initiated. Detailed frequency response maps for contralateral and ipsilateral monaural tones were created from responses to tone bursts presented over 31–36 levels (a 60- to 70-dB range in 2-dB steps) and 31 frequencies (a 3-octave range centered on the unit's contralateral BF in 0.1-octave steps). The stimuli were presented in ascending intensity at BF, and then at frequencies alternately above and below BF. Rate-level functions were obtained for BF tones and broadband noise presented to the contralateral ear by sweeping the level of stimulus over a 100-dB range. For binaural testing, the same pure tone was presented to both ears but a 40-dB range of ILDs was created by varying the level of the ipsilateral tone relative to a fixed-level contralateral tone. The intensity of the contralateral BF tone was fixed at 10 dB re threshold. Two electrolytic lesions (10 µA; 30 s), spaced 0.5–1 mm apart, were made with the metal recording electrode at the end of unit-rich electrode tracks to mark the location of recording sites.
Sound-driven activity was analyzed in terms of average discharge rates over the final 80% of the stimulus-on interval to reflect steady-state responses. Spontaneous rates were computed over the last 40% of the stimulus-off interval. All data were smoothed with a triangularly weighted moving-average filter to reduce noise. Excitatory (inhibitory) responses were defined as those for which the stimulus-evoked rate was at least 1 SD above (below) the spontaneous discharge rate. Informal analyses suggest that response magnitudes, and not the general patterns of excitatory and inhibitory responses, were affected by changes in the duration of the response window.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Merzenich and Reid 1974). The dorsal edge of the DNLL was reached when the BF changed abruptly from high frequencies (30 kHz) to low frequencies (<1 kHz) at a depth of 4.5 mm (Aitkin et al. 1970; Brugge et al. 1970). Within the DNLL, the BF of neurons jumped progressively from low to high frequencies with increasing depth (numerical labels). That is, in this penetration, as in all others, the DNLL in cat showed a clear tonotopic organization along its dorsoventral extent that was marked by a strong tendency for the BF to change rapidly over short distances (e.g., from 1.49 to 16.1 kHz in 400 µm). Lesions were found throughout the DNLL, suggesting that the full extent of the DNLL was sampled.
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Units were divided into three groups based on the patterns of excitation and inhibition observed in their contralateral and ipsilateral monaural frequency response maps. Representative data for each unit type are shown in Fig. 2; contralateral response maps are shown in the left column and ipsilateral response maps are shown in the right column. In these plots, stimulus-driven rates (vertical bars) are plotted at the frequency and level coordinates of the tones that elicited the responses, where the length of a bar is proportional to the maximum spike rate evoked in that unit by stimulation of the contralateral ear. The contralateral and ipsilateral response maps of type v units (Fig. 2, top row) exhibit V-shaped excitatory areas that widen about unit BF with increasing sound levels. These units show few, if any, inhibitory responses to monaural pure tones. The contralateral maps of type i units (Fig. 2, middle row) generally exhibit an I-shaped (i.e., narrow V-shaped) excitatory area that is flanked on both sides by inhibition. Some (predominantly low-BF) type i units show less pronounced inhibitory effects at lower frequencies and thus exhibit more broadly tuned V-shaped excitatory areas; nonetheless, these units are easily distinguishable from type v units based on the presence of strong high-side inhibition and the fact that the ipsilateral maps of type i units show V-shaped inhibition. The contralateral maps of type o units (Fig. 2, bottom row) have a clearly circumscribed O-shaped excitatory response area at low stimulus levels that is bounded by inhibition at higher stimulus levels. These units are strictly inhibited by ipsilateral tones. Type i units were the most abundant unit type in our sample (46/62); type v (10/62) and type o units (6/62) were less prevalent (Table 1).
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; Miller et al. 1997). Threshold was identified as the lowest stimulus level at a given frequency that elicited a response 1 SD above or below the average spontaneous rate of the unit, and BF was identified as the frequency with the lowest threshold. BFs of the units were evenly distributed between 0.6 and 37 kHz, which corresponds to most of the cat's audible range. However, the unit types were not distributed uniformly as a function of BF (Fig. 3B). Type v units (black) always had low BFs (<2.5 kHz), whereas most type i (white) and type o units (hatched) had high BFs. Given that BFs increased as a function of depth along the dorsoventral axis of the DNLL, type v units were found at the start of electrode tracks and type i and type o units were found more ventrally.
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The sharpness of contralateral excitatory frequency tuning was quantified using Qn values (defined as BF divided by the bandwidth of excitation "n" dB above threshold). At 10 dB above threshold (Fig. 4 A), Q10 values increase monotonically with BF up to about 10 kHz, after which they remain relatively constant. Most values are within the range exhibited by ANFs (solid lines; Calhoun et al. 1997; Miller et al. 1997), suggesting that the low-level tuning of DNLL units is determined by peripheral processes. At 40 dB above threshold (Fig. 4B), the tuning of type v units continues to match that of ANFs (Liberman 1978). In contrast, type i units show much sharper tuning than ANFs (symbols above the upper solid line) and type o units show no excitation at all (i.e., nonexistent Q40 values). These results suggest that the high-level tuning of type i and type o units is sculpted by central inhibitory mechanisms. Analysis of the shapes of type i and type v unit excitatory tuning curves (Hernández et al. 2005; Sutter 2000) indicated that type i units differ from type v units only along the low-frequency border, where the average slope for a type i unit was much steeper than that of a type v unit (–0.2 octaves per 40 dB vs. –1.2 octaves per 40 dB). This sixfold difference in slope is statistically significant (P < 0.01, Student's t-test), suggesting that it is the effects of inhibition on the low-frequency side of type i units that maintains the sharp tuning of type i units at high stimulus levels.
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). Figure 4C plots the so-called Q40 of inhibition for type i and type o units; for comparison, the range of excitatory Q40 values for auditory nerve fibers is shown. In general, Q40 values of inhibition are about one third those of excitation. This broad bandwidth suggests a convergence of multiple inhibitory inputs at, or below, the level of the DNLL. A comparison of the contralateral and ipsilateral monaural frequency response maps in Fig. 2 suggests that there is substantial overlap of the response areas. Figure 5 A plots the most sensitive frequency of the ipsilateral versus the contralateral ear for all the units in this study. Note that many of the symbols lie on the equity (solid) line, indicating equal BFs in both ears. Overall, the contralateral and ipsilateral BFs differed by less than ±0.2 octaves in 60/62 cases.
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Figure 5C plots the Q40 value of each unit's ipsilateral tuning curve (where available) versus the Q40 value of its contralateral tuning curve. This comparison of sharpness of tuning is between the widest extent of the respective receptive fields; that is, for type v units, this comparison is between excitatory tuning curves, whereas for type i and type o units it is between inhibitory tuning curves. Note that the data points cluster about the equity line, indicating that a unit's ipsilateral and contralateral frequency response areas are well matched in bandwidth.
Responses to contralateral BF tones and noise
The narrowband and wideband responses of DNLL units were characterized by obtaining rate-level functions for contralateral BF tone and broadband noise bursts. Figure 6 A shows representative BF-tone rate-level data for each unit type. Type v and type i units all show monotonic (or nearly monotonic) functions; that is, the discharge rate increases rapidly as a function of level and then saturates or shows only a slight decrease over a wide range of intensities. In contrast, the responses of type o units are highly nonmonotonic. They first increase and then decrease sharply with level and become and remain inhibited. To quantify the monotonicity of these functions, a straight-line (least-squares) fit was applied to the portion of the curve between the maximum (the first sharp change in slope) and the next inflection point or the end of the data (e.g., the dotted line on the rate-level function for the type i unit). This estimate of slope was normalized by dividing through by the maximum rate (Young and Voigt 1982). Figure 6B shows the distribution of normalized slopes for each unit type. The typical saturating monotonicity of type v and type i units is indicated by the clustering of values near 0. Type o units, on the other hand, exhibit strictly negative normalized slopes and thus exclusively nonmonotonic rate-level functions.
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All DNLL units responded to broadband noise and, for most unit types, the response functions were similar in shape to those evoked by BF tones. Figure 8 A shows representative noise rate-level functions for each unit type. As for BF tones, the responses of type v and type i units climb to a maximum and then maintain a steady discharge rate. On the other hand, type o units, which show highly nonmonotonic responses to BF tones, exhibit monotonic rate-level functions to noise. The monotonicity of each unit's noise and tone-driven responses is compared in Fig. 8B, which plots the normalized slopes of noise rate-level functions against the values obtained in response to BF tones. Each symbol represents an individual unit and the diagonal line represents equal slopes for both stimuli. Note that all of the data points for type v and type i units are clustered about the origin, indicating that the responses to both noise and tones are monotonic and saturating. In contrast, the data points for most type o units (5/6) lie well above the equity line, indicating that type o units usually show very different degrees of monotonicity for tones and noise. In particular, the tone response is strongly nonmonotonic, whereas the noise response is monotonic.
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Figure 8D plots each unit's maximum discharge rate to noise against its maximum BF tone-driven rate. Type i units showed significantly lower discharge rates to noise than to tones (the data points lie below the equity line; P < 0.01, sign test). This is likely due to noise-evoked activation of the extensive inhibitory sidebands of these units. Type v units, whose lateral inhibitory effects are presumed to be weak or nonexistent, tended to have comparable responses to tone and noise. Interestingly, the maximum noise-driven rates of type o units, whose frequency response maps are dominated by inhibition, were approximately equal to or greater than their maximum tone-driven rates, suggesting nonlinear integration properties.
Sensitivity to interaural level differences
The effects of ipsilateral inputs to DNLL units were assessed by recording responses to changes in interaural level differences (ILDs). ILD functions for representative type V, type i, and type o units are shown in Fig. 9. In these plots, the stimuli were dichotic tones at the contralateral BF. The contralateral excitatory stimulus was fixed at a level 10 dB above threshold, whereas the ipsilateral intensity was increased in 1-dB steps from 20 dB below to 20 dB above this fixed level [the excitatory monaural intensity (EMI) constant method]. By convention, positive ILDs indicate stronger sounds in the contralateral ear. For the type v unit (solid line), firing rates remained relatively constant at low levels of ipsilateral stimulation (positive ILDs) because the binaural responses were dominated by the response to the fixed contralateral tone. As the intensity of the ipsilateral tone increased (negative ILDs), the firing rates increased to a maximum and saturated. By contrast, the discharge rates of the type i (dotted line) and type o units (dashed line) decreased when the balance of inputs shifted toward inhibition at increased levels of ipsilateral stimulation (negative ILDs).
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; Wenstrup et al. 1988) and is defined to be the ILD at which the excitatory response to contralateral sound is suppressed by 50% (i.e., the half-maximal ILD). In this report, the excitatory threshold for facilitated units indicates the binaural condition that elicits a response 50% greater than the contralateral response. The distributions of excitatory and inhibitory thresholds for the three DNLL unit types are shown in Fig. 11 A; the thresholds for one type v unit excited <50%, and seven type i units inhibited <50%, could not be measured. The excitatory thresholds for type v units were tightly clustered between +10 and 0 dB. By contrast, the inhibitory thresholds of type i units were distributed in a roughly normal fashion from +20 to –20 dB, covering most of the range of ILDs generated by the head and pinna of the cat (Irvine 1987). The dependence of the transition threshold on ipsilateral sensitivity is illustrated in Fig. 11B by plotting the excitatory or inhibitory threshold for each unit against the unit's difference in ipsilateral and contralateral thresholds for BF tones. Note that the data points cluster about the equity line, indicating that transition thresholds are correlated positively with ipsilateral sensitivity. In particular, a unit's transition threshold usually occurs within 10 dB of ipsilateral threshold (the data points lie below the equity line; P < 0.01, sign test).
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; Wenstrup et al. 1988) of <15 dB. Roughly 60% of type i (23/38) and type o units (3/5) also exhibited steep ILD functions. The remainder of units had functions with shallow slopes and dynamic ranges of 
30 dB.
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= 0.67, P < 0.001; Kendall rank-correlation test) and between the inhibitory threshold and slope of the function ( = 0.57, P < 0.001). Units with lower (more positive) inhibitory thresholds generally displayed greater maximum inhibition and steeper slopes than units with higher inhibitory thresholds. In particular, nearly all of the units with inhibitory thresholds between +20 and 0 dB (i.e., the range of ILDs representing the contralateral hemifield) exhibited maximum inhibitions >90% and slopes >4%/dB (dynamic ranges <15 dB).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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The monaural and binaural properties of DNLL neurons in the decerebrate cat are similar in many respects to those seen in the DNLL of anesthetized cat (Aitkin et al. 1970; Brugge et al. 1970) and other species (rat: Bajo et al. 1998; Kelly et al. 1998; big brown bat: Covey 1993; mustache bat: Markovitz and Pollak 1993, 1994; Mexican free-tailed bat: Bauer et al. 2002; Xie et al. 2005). First, in all of these prior studies, the vast majority of DNLL units displayed V-shaped excitatory tuning in response to stimulation of the contralateral ear. Although these studies did not quantify the sharpness of the tuning curves at higher stimulus levels (e.g., using Q40 values), it appears that both broad and narrow types of curves were observed. In the present study, 90% of units including type v and type i units showed open tuning curves; the remainder showed upper thresholds or closed tuning curves (type o units). Covey (1993) also found that a small minority of units (4%) in the big brown bat showed closed tuning curves. Second, most DNLL neurons showed either monotonic or weakly nonmonotonic BF-tone rate-level functions. In the decerebrate cat, the functions of all type v and type i units were more or less monotonic. Third, most DNLL neurons were binaural, with the large majority being excited by contralateral stimulation and inhibited by simultaneous ipsilateral stimulation and the minority being excited by monaural stimulation of both ears. Here, where the nature of ipsilateral inputs could be evaluated directly, 84% of the population of units including type i and type o units received ipsilateral inhibition and exhibited binaural excitatory–inhibitory interactions, and the remainder (type v units) received ipsilateral excitation and exhibited binaural facilitation.
One marked difference between this and prior studies, however, is the prevalence of inhibition observed in contralateral monaural frequency response maps. In decerebrate cat, the response maps of 84% of DNLL units including type i and type o units exhibited inhibitory areas. By contrast, the percentage of units showing inhibitory responses was <3% in anesthetized cat (Aitkin et al. 1970), rat (Kelly et al. 1998), and three species of echolocating bats (big brown bat: Covey 1993; mustache bat: Markovitz and Pollak 1993; Mexican free-tailed bat: Bauer et al. 2002; Xie et al. 2005). One possible explanation for this discrepancy is that the decerebration procedure alters the balance of excitation and inhibition in the DNLL by disrupting descending inputs from the auditory cortex to the IC (Anderson et al. 1980; Bajo and Moore 2005; Doucet et al. 2003; Winer et al. 1998), which in turn projects to the DNLL (Caicedo and Herbert 1993; Malmierca et al. 1996). The good agreement of results obtained from the IC in decerebrate cats (Ramachandran et al. 1999) and intact, awake preparations (cat: Bock and Webster 1974; Bock et al. 1972; rhesus monkey: Ryan and Miller 1978) suggests, however, that deefferentiation does not introduce fundamental changes in IC (thus DNLL) discharge patterns. The more likely explanation for the difference between the present study and that of Aitkin et al. (1970), and perhaps that of Kelly et al. (1998), is the effect of anesthesia. It is well known that barbiturate anesthesia can reduce or even abolish the amount of inhibition in the response maps of cochlear nucleus units (Evans and Nelson 1973; Young and Brownell 1976), which are the precursors directly or indirectly of all response types in the DNLL. The recordings in bats, however, were made in awake animals without anesthesia; thus the difference between decerebrate cat and echolocating bats may reflect a species-specific variation.
Alternatively, the lack of inhibition in prior studies could be explained by the fact that most neurons in these preparations had little or no spontaneous activity, making it difficult to detect the presence of monaural inhibition. For example, Covey (1993) reported that 64% of DNLL units in the big brown bat exhibited no spontaneous activity, whereas Markovitz and Pollak (1993) found that 42% of units in the mustache bat were either silent or displayed very low spontaneous rates. Yang and Pollak (1994a,b) later reported that 94% of DNLL units in the mustache bat exhibited no spontaneous activity. To test for the presence of inhibition in the Mexican free-tailed bat, Xie et al. (2005) measured excitatory tuning curves before and after local iontophoretic application of strychnine or bicuculline to block glycinergic or GABAergic receptors, respectively, and before and after application of glutamate to produce a carpet of background activity. Their results indicated that the excitatory tuning curves of DNLL neurons are largely unchanged after inhibitory blockade and that tones outside the excitatory tuning curve do not suppress glutamate-evoked background activity. Taken together, these results suggest that the inhibitory inputs to DNLL neurons act primarily within the excitatory tuning curve of the neuron to regulate response magnitude. However, these tests cannot rule out the possibility that DNLL neurons inherit inhibitory response areas; that is, DNLL neurons are inhibited by tones outside of their excitatory tuning curve by virtue of receiving a lack of excitation at those frequencies from their lower-order sources. Thus the generality of a role for inhibition in shaping at some level the excitatory tuning curves of DNLL neurons remains an open question.
Origins of the unit types
Principal cells in the medial superior olive (MSO), the lateral superior olive (LSO), and the cochlear nuclei have unique response patterns and are primary sources of ascending inputs to the DNLL (Casseday et al. 1988; Glendenning et al. 1981; Shneiderman et al. 1988; Vater et al. 1995; Yang et al. 1996). Shneiderman et al. (1988) showed that the afferent axons from these sources to the DNLL are distributed in horizontal bands and have a tonotopic organization. In general, projections from low-frequency areas in the brain stem nuclei terminated in the dorsal part of the DNLL, whereas high-frequency areas projected to the ventral DNLL. It was found, however, that not all parts of the DNLL share the same set of inputs. The dorsal DNLL received all of the ascending inputs, whereas the ventral DNLL lacked inputs from the MSO and ipsilateral anteroventral cochlear nucleus. Given that most DNLL neurons have horizontal dendritic fields that are oriented along the path of the incoming afferents (Iwahori 1986; Kane and Barone 1980), the responses of DNLL neurons may be expected to reflect different mixtures of the physiological properties of the ascending inputs to the DNLL.
Several lines of experimental evidence lead to the conjecture that type v response patterns are strongly shaped by inputs from the MSO. Type v units show purely excitatory responses when stimulated with tones in either ear (Fig. 2). Only one source of direct DNLL projections, the MSO, exhibits similar response properties (Goldberg and Brown 1969; Guinan et al. 1972), although bilateral projections from stellate cells in the anteroventral cochlear nucleus cannot be discounted as additional sources (Adams 1979; Oliver 1987; Shneiderman et al. 1988; Shofner and Young 1985). In addition, only type v and MSO units are more sensitive to variations in the average intensity of binaural stimuli than they are to comparable monaural variations (i.e., they show binaural facilitation) (Fig. 9; Goldberg and Brown 1969). Type v units have low BFs and >50% of the cat MSO is devoted to the processing of low frequencies. Injections of anterograde tracers in the dorsal part of the MSO (i.e., the low-frequency half of the nucleus) produce tonotopically organized labeling in dorsal DNLL (Henkel and Spangler 1983; Shneiderman et al. 1988); in this study, type v units were recorded at the start of dorsoventrally oriented electrode tracks. Consistent with these observations, many excitatory–excitatory neurons in the low-frequency part of the DNLL are sensitive to interaural time differences (Brugge et al. 1970; Siveke et al. 2006) in a manner resembling that of the MSO (Batra et al. 1997).
Type i units are excited by BF tones presented to the contralateral ear and inhibited at all frequencies by ipsilateral stimulation (Fig. 2). These response characteristics suggest that the LSO is the primary source of ascending inputs for neurons of these response types (Brownell et al. 1979; Caird and Klinke 1983; Guinan et al. 1972; Tsuchitani and Boudreau 1966). In general, type i units have high BFs and level-tolerant excitatory areas that are flanked by inhibitory areas. The LSO is likewise a predominantly high-frequency nucleus whose principal cells exhibit level-tolerant excitation and strong lateral inhibition (Caird and Klinke 1983; Tsuchitani and Boudreau 1966). In addition, type i units respond to strong binaural stimulation with reduced discharge rates relative to responses elicited by contralateral monaural stimulation (Fig. 9). These response patterns are seen in inhibitory–excitatory (IE) binaural interactions of LSO neurons (Boudreau and Tsuchitani 1968; Caird and Klinke 1983; Guinan et al. 1972; Tsuchitani and Boudreau 1969). Most excitatory LSO projections cross the midline before terminating in the DNLL (Glendenning et al. 1992); thus IE interactions in the LSO would be expected to produce EI properties in the DNLL. This interpretation is supported by pharmacological studies in the mustache bat that suggest that the binaural properties of the vast majority of EI cells are created below the level of the DNLL (Yang and Pollak 1994a).
Type o units show essentially the same binaural input (EI) and inhibitory interaction patterns as those of type i units. However, the contralateral response maps of type o units are dominated by inhibition except for an island of excitation at low stimulus levels (Fig. 2). These properties are similar to those exhibited by so-called type IV units in the dorsal cochlear nucleus (DCN) of decerebrate cats (Davis 2005a; Mast 1970; Spirou and Young 1991; Young and Brownell 1976). A direct projection from the principal cells in the contralateral DCN to the DNLL has been observed in some studies (Adams 1979; Glendenning et al. 1981), but not in others (e.g., Oliver 1984; Shneiderman et al. 1988). Consistent with this sparse-at-best projection, type o units were the least observed unit type in the DNLL. Alternatively, type o unit properties could be created at the level of the DNLL by a suitable convergence of excitatory and inhibitory inputs. For example, the excitatory input could be provided by the LSO (Glendenning et al. 1992) and the inhibitory input could be conveyed by projections from the ipsilateral ventral nucleus of the lateral lemniscus (Glendenning et al. 1981; Saint-Marie et al. 1997; Whitley and Henkel 1984).
Comparison of DNLL and IC units in the cat
The DNLL and IC receive roughly the same set of inputs except that the IC receives ipsilateral DNLL input (Glendenning et al. 1981; Shneiderman et al. 1988); thus it is perhaps not surprising that the monaural properties of DNLL neurons are similar in numerous respects to those of neurons in the IC (Ramachandran et al. 1999). There are, however, some important differences among the two populations. In particular, single units in the DNLL and the IC can be classified into the same set of three distinct types based on the patterns of excitation and inhibition observed in contralateral monaural frequency response maps. The corresponding unit types in both nuclei (v = V; i = I; o = O) have similar BF distributions, shapes of BF tone, and noise rate-level functions, relative responsiveness to tones versus noise, and binaural input patterns. These similarities suggest that the corresponding unit types in the DNLL and the IC have common sources of input. One difference between the two nuclei, however, is the rate of unit incidence. In the DNLL, units with narrow tuning curves predominate, whereas in the IC, units with closed tuning curves are the most prevalent. This difference likely reflects the fact that the LSO, and not the DCN, is a major source of input to the DNLL (e.g., Shneiderman et al. 1988), whereas DCN afferents ramify more widely than LSO afferents in the IC (Oliver et al. 1997). In addition, it is known that the closed tuning curves of some units in the IC are created at the level of the IC by a convergence of excitatory and inhibitory inputs (e.g., Davis 2002; Yang et al. 1992).
The DNLL and IC also differ in the extent to which inhibition sculpts monaural response properties. In both nuclei, units with broad and narrow V-shaped tuning curves are excited by BF tones and noise at all levels. The rate-level functions in the IC are more strongly shaped by inhibition, however, as evidenced by the facts that the tone and noise rate-level functions of narrow units in the IC may become nonmonotonic at high levels. In addition, closed units in the DNLL are usually excited by high level noise, much like their presumed DCN inputs (Young and Brownell 1976), whereas the corresponding unit type in the IC is inhibited by high-level noise. Also noteworthy are several quantitative differences between the corresponding DNLL and IC unit types. In particular, DNLL unit types show higher median spontaneous rates (by a factor of 2), greater maximum BF tone- and noise-driven rates (x1.4), and wider excitatory tuning curves (x1.33, applies to narrow units only). Taken together, these results are consistent with the findings that the DNLL is a source of tonic and monaural inhibition to the IC (Faingold et al. 1993; Kelly and Li 1997; Kidd and Kelly 1996; Li and Kelly 1992; Thornton and Rees 1997).
The binaural properties of DNLL units are also largely similar to those of IC units (Davis et al. 1999). One common feature of the DNLL and the IC is that EE/f and EI/I units are found in both nuclei. In each nucleus, units with broad V-shaped excitatory tuning curves for contralateral tones are excited by ipsilateral tones and exhibit binaural facilitation, whereas units with narrow or closed tuning curves are inhibited by ipsilateral stimulation and exhibit binaural inhibition. Another common feature of DNLL and IC binaural neurons is the distribution of excitatory and inhibitory thresholds of their ILD functions. In particular, the 50% points of the ILD functions of EI/I neurons in both nuclei range from +20 to –20 dB, which covers the majority of the range of behaviorally relevant ILDs in the cat (Irvine 1987). The maximum strength of inhibition and slope of the ILD functions for EI neurons also appear to be similar in both nuclei (Davis, unpublished data). One difference between the DNLL and the IC is the absence/presence of EI neurons with complex ILD functions. Some 25% of EI neurons in the IC had complex ILD functions, called EI/f after Park and Pollak (1993), which showed facilitation at low levels of ipsilateral stimulation and inhibition at higher levels. No EI/f units were found in the DNLL of the cat. A comparison of DNLL and IC units in the mustache bat also found a lower proportion of EI units showing EI/f properties in the DNLL (10 vs. 30%: Markovitz and Pollak 1994; Park and Pollak 1993). These results are consistent with the idea that some binaural facilitation is created within the IC (Park and Pollak 1993).
On the roles of the DNLL in processing acoustic information
The DNLL is predominantly an inhibitory binaural nucleus and has been shown to play an important role in the processing of binaural sound localization cues. Pharmacological blockade of the excitatory activity in the DNLL reduces the strength of inhibition in the contralateral IC and thereby alters in numerous ways the sensitivity of neurons in the IC to interaural differences in time and intensity (Burger and Pollak 2001; Faingold et al. 1993; Kelly and Kidd 2000; Kelly and Li 1997; Kidd and Kelly 1996; Li and Kelly 1992). A similar range of effects, including the transformation of strongly inhibited EI units into monaural units, is observed when GABAergic inhibition is blocked in the IC of the cat (Davis et al. 1999) and other mammals (Faingold et al. 1989; Klug et al. 1995; Park and Pollak 1993; Vater et al. 1992a). Stimulus-evoked inhibition of the DNLL also weakens the strength of inhibition in the contralateral IC; however, the effect is unusually long-lasting and prevents DNLL neurons from responding to excitatory signals for tens of milliseconds after the inhibitory signal has ended (Burger and Pollak 2001; Kelly et al. 1998; Yang and Pollak 1994c, 1998). This persistent inhibition allows IC neurons to respond to trailing binaural signals that are inhibitory when presented alone. The effects of persistent inhibition of the DNLL should be especially important for the processing of ILDs that change over time, such as the ILDs generated by moving sound sources or by multiple sounds that emanate from different regions of space (Burger and Pollak 2001; Pollak 1997; Yang and Pollak 1994c). Behavioral studies to date have shown that lesions of the DNLL or transection of its crossed efferent projections in the commissure of Probst degrade the ability of animals to localize sounds in the horizontal plane and increase the minimum audible angle for spatial discrimination (Ito et al. 1996; Kelly et al. 1996).
The DNLL may also play a variety of roles in the monaural processing of acoustic information. One known role of the DNLL is to shape the tuning curve properties of IC neurons. In particular, Thornton and Rees (2001) showed that reversible inactivation of the ipsilateral DNLL caused both expansion and contraction of narrow units and expansion of one closed unit in the IC of the anesthetized guinea pig. Consistent with these results, the tuning curves of many such units in the IC of cats (Davis 2002, 2005b) and other mammals (Fuzessery and Hall 1996; LeBeau et al. 1995; Palombi and Caspary 1996; Pollak and Park 1993; Vater et al. 1992a; Yang et al. 1992) expand when GABAergic inhibition is blocked within the IC. A second role of the DNLL is to transmit a rate-based tonotopic representation of spectral shape to the IC (Bauer et al. 2002). It was found that the processing of complex sounds in the DNLL can be largely explained by a linear integration of excitation, suggesting that inhibition plays little role in shaping the responses of DNLL neurons. The results of the current study showing that most DNLL units have inhibitory areas in their monaural response maps do not necessarily contradict this finding; the responses of units with sideband inhibition in the ventral cochlear nucleus are also dominated by the processing of excitatory spectral energy around BF (Young et al. 2005; Yu and Young 2000). Additional roles of the DNLL may be to endow IC neurons with a selectivity for species-specific calls (Klug et al. 2002; Xie et al. 2005) or with a selectivity for monaural sound localization cues (Davis et al. 2003). In both cases, this specificity is lost when GABAergic inhibition is blocked, suggesting a potential role for the DNLL; in the latter case, the inhibitor further needs to be narrowly tuned and have a high BF, like type i units. The exact roles of the DNLL and at a more refined level its three distinct response types in these and other information processing streams remain to be revealed in future studies.
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Address for reprint requests and other correspondence: K. Davis, Department of Neurobiology and Anatomy, University of Rochester, 601 Elmwood Ave., Box 603, Rochester, NY 14642 (E-mail: Kevin_Davis{at}urmc.rochester.edu)
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