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1Auditory Neurophysiology Unit, Laboratory for the Neurobiology of Hearing, The Institute of Neuroscience of Castilla y León and Faculty of Medicine, University of Salamanca, Salamanca, Spain; and 2Department of Psychology, University of Washington, Seattle, Washington
Submitted 14 July 2005; accepted in final form 26 September 2005
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ABSTRACT |
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INTRODUCTION |
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; Potter 1965), bats (Casseday et al. 1994, 2000; Ehrlich et al. 1997; Fuzessery 1994; Mora and Kössl 2004; Pinheiro et al. 1991), cats (He et al. 1997), chinchillas (Chen 1998), and mice (Brand et al. 2000). Duration-selective neurons have only been found at or above the level of the inferior colliculus (IC) or its homolog in any of the species studied, so this form of neural filtering seems to be an emergent property that results from circuitry operating within the midbrain. The IC is innervated by multiple lower brain stem structures with excitatory or inhibitory inputs that vary in latency, temporal pattern, and sensitivity to multiple sound parameters, including frequency and amplitude (e.g., Casseday et al. 2002). Previous studies have suggested that duration selectivity is generated through the interaction of such inputs, in particular, the combination of convergent excitatory and inhibitory inputs with specific temporal relationships (Brand et al. 2000; Casseday et al. 1994, 2002; Ehrlich et al. 1997; Faure et al. 2003).
In certain species with specialized auditory behavior, the ranges of sound durations to which neurons are tuned correspond closely to the range of durations found in behaviorally important sounds. This matching of neural sensitivity to the duration of vocalizations has been described in frogs, where neurons' duration tuning matches the durations of communication calls (Narins and Capranica 1980), and in bats, where neurons' duration tuning matches the durations of echolocation signals (Ehrlich et al. 1997; Faure et al. 2003; Pinheiro et al. 1991). More recently, duration-sensitive neurons have been found in animals that lack obvious auditory specializations. Although the advantages of duration sensitivity in more generalized species have not been thoroughly studied, it potentially serves to identify specific sounds. For example, the IC of mice contains a high proportion of long-pass neurons selective for sounds longer than several tens of milliseconds. The few observed band-pass neurons typically have best durations on the order of tens of milliseconds (Brand et al. 2000). Both of these filtering properties are congruent with the duration of adult and pup ultrasound vocalizations (Liu et al. 2003).
Many calls in rats have highly stereotyped temporal patterns (Kaltwasser 1990), in which call duration could convey important information such as individual identity, social status, or contextual situations. For example, rat ultrasonic vocalizations include long (>300 ms) calls that are emitted during a negative affective state when animals are anticipating punishment or engaging in avoidance behaviors and short (<300 ms) calls that are produced during a positive affective state when they are anticipating a reward or displaying approach behaviors (Knutson et al. 2002). Isolation calls of rat pups range from 
80 to 140 ms, decreasing in duration as a function of the pup's age. They also differ in length between individuals and show greater similarity within than across litters (Brudzynski et al. 1999). Thus duration could be used by receivers to recognize kin and offspring (Brudzynski et al. 1993). Rats have a rich repertoire of sounds that are produced during exploration, agonistic encounters, sexual behavior, and other social interactions for which duration could convey meaning to conspecifics. To date, there have been no studies to determine whether the rat central auditory system contains duration-sensitive neurons and, if so, how these relate to durations of vocal communication signals. The aim of this study was to determine whether there are duration-selective neurons in the midbrain of the rat, one of the most commonly used laboratory animals and, if so, how the range of duration selectivity corresponds to the duration of their known repertoire of vocalizations. Preliminary reports have been presented in abstract form elsewhere (Pérez-González et al. 2004a,b).
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METHODS |
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). A tracheotomy was performed to assure adequate ventilation, and atropine sulfate was administered subcutaneously (0.05 mg/kg) to reduce bronchial secretions. Body temperature was maintained at 38 ± 1°C with a thermostatically controlled electric blanket (Hernández et al. 2005; Malmierca et al. 2003). The rat's head was immobilized by placing it in a stereotaxic frame in which the ear bars had been replaced by hollow specula that accommodated a sound delivery system (Hernández et al. 2005; Rees et al. 1997). A craniotomy was performed to expose the tissue over the recording site, usually over the right IC, and the dura was reflected to allow entry of the electrode. The surface of the brain was irrigated regularly with saline to prevent desiccation.
Acoustic stimulation and electrophysiological recording was performed inside a sound-attenuated booth. A tungsten electrode (Merrill and Ainsworth 1972) was placed over the exposed cortex and moved along the dorsoventral axis using a piezoelectric microdrive (Burleigh 6000) that was advanced by remote control from outside the booth. Once the IC was reached, single neurons were isolated, using white noise and pure tones as search stimuli, and sound-evoked action potentials were recorded extracellularly.
Stimuli were synthesized by a System II workstation (Tucker-Davis Technologies) using custom software and delivered through a closed field delivery system (Rees 1990) through two electrostatic speakers (TDT EC1) controlled by an electrostatic speaker driver (TDT ED1). The output of the system at each ear was calibrated in situ using a condenser microphone (Brüel and Kjær 4134, Nærum, Denmark) and a DI-2200 spectrum analyser (Diagnostic Instruments, Livingston, Scotland, UK). The maximum output of the system was flat from 0.3 to 5 kHz (
100 ± 7 dB SPL) and 5 to 40 kHz (90 ± 5 dB SPL), with a notch at 22–23 kHz with a slope of 15 dB/octave. Second and third harmonic components in the signal were 45 dB or more below the level of the fundamental at the highest output level. Because of the nonlinearities of the loudspeaker output, all values are expressed as dB SPL. The highest frequency produced by our system was limited to 40 kHz. Action potentials were amplified (10,000 times) with a Bioamp amplifier (TDT) and filtered (0.5–3 kHz; TDT DB4) before being processed in a spike discriminator (TDT SD1). The spike times were stored on a computer.
Once a single unit was isolated, its characteristic frequency (CF) and threshold were determined by an automated procedure that consisted of the randomized presentation of pure tones across a matrix of frequency and intensity values that extended beyond the visually estimated response area. The standard duration of these stimuli was 75 ms. For duration-sensitive neurons, it was set at the neuron's estimated best duration. For the experiments in which duration was varied, stimuli were pure tones at the neuron's CF, typically 10–20 dB above threshold, and a rise-fall time of 1 or 2 ms. Stimuli were presented to the ear contralateral to the IC from which recordings were obtained. Stimulus duration was varied randomly among 10 or 20 stepwise values starting at 2–5 ms and extending up to 100–200 ms. To avoid confounds associated with spectral artifacts, we did not test durations <2 ms. Each duration was presented 10 times. The data obtained were analyzed and plotted using commercial software (Microsoft Excel, Sigmaplot, and SPSS).
To determine whether a neuron was sensitive to sound duration, we plotted response probability as a function of duration. Response probability (also referred to as spike probability) was defined as the number of presentations (or trials) of a given stimulus for which there was at least one stimulus-evoked action potential, divided by the total number of presentations for that stimulus. For neurons with spontaneous activity, response probability was calculated after subtracting the spontaneous rate. This measure was used instead of spike counts to distinguish long-pass duration sensitivity from simple systematic increases in spike count with increased duration in units with sustained discharge patterns. A neuron was considered to be duration sensitive if, at any point, the response probability function dropped below 50% of the maximum. For long-pass or short-pass neurons, the cut-off duration was defined as the point at which the probability function dropped below 50% of the maximum; if this point was between two tested durations, it was calculated by linear interpolation. For band-pass neurons, which had cut-offs at both long and short durations, the best duration was defined as that at which spike probability was maximal. Because we were unable to test durations <2 ms, it is possible that those neurons that we classified as short pass were actually band-pass, or that they might have had band-pass characteristics at some sound levels (Fremouw et al. 2005).
Selected recording sites and other landmarks were marked with electrolytic lesions. These marks were used to reconstruct electrode tracks and to confirm the locations of the recorded units. For histological examination of the brain, the animal was administered a lethal dose of pentobarbital sodium (Nembutal; 60 mg/kg in saline, ip) and perfused transcardially with Ringer solution followed by fixative (1% paraformaldehyde and 1% glutaraldehyde in 0.1 M phosphate buffer; pH 7.4). The brain was immersed in a 30% sucrose solution for 2–3 days before being cut into 40-µm-thick transverse sections using a freezing microtome. Sections were stained with cresyl violet. Neurons were assigned to the IC subdivisions according to the parcellation scheme of Malmierca et al. (1993).
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RESULTS |
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; Pérez-González et al. 2005) and were consequently excluded from all analyses. Of the remaining 155 neurons, 84 (54.2%) showed some form of duration sensitivity. By far the most common form of duration sensitivity was long-pass filtering. Long-pass neurons were defined as those with a 50% cut-off on the short-duration side, but a higher probability of firing at all longer durations tested. Neurons with long-pass sensitivity comprised 41.3% of all IC neurons from which we recorded and 76.2% of duration-sensitive neurons. Long-pass neurons’ cut-off durations ranged from 5 to 60 ms. An example of a long-pass neuron is shown in Fig. 1, A and B. This neuron had no spontaneous activity. It was completely unresponsive to durations less than 35 ms. From this point, the response probability gradually increased until reaching the 50% cut-off at 60 ms and a plateau at 80 ms. This neuron’s response took the form of a sparse sustained discharge. Figure 1B shows that the response probability and sound duration were positively correlated until the neuron reached its maxi-mum probability of firing. First-spike latency was extremely variable across trials but was always >35 ms. Figure 1C shows the response from another neuron with a sustained discharge pattern, but this neuron was not duration sensitive (all pass). Although the number of spikes per trial was positively correlated with sound duration, as would be the case if recording from an auditory nerve fiber, there was no duration tested at which the neuron failed to respond reliably. The spike probability function of this neuron (Fig. 1D) was high (>70%) and essentially flat across all of the durations tested.
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15 ms. Once the duration exceeded the cut-off, the number of spikes per stimulus remained constant and response probability remained flat with further increases in duration. Response latency was consistently 15 ms, about the same as the cut-off duration. For comparison, Fig. 2, C and D, shows the response of an onset responder that was not duration sensitive (all pass). This neuron responded with one spike on every trial, even at the shortest duration tested. The spike probability was 1.0 for all durations.
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28 ms at 5 dB above threshold, changing to 5 ms or less at 25 dB above threshold. Over this range, latency also changed from 35 ms at 5 dB above threshold to 12 ms at 25 dB above threshold. The level-dependent changes shown by this neuron were typical of those whose cut-off durations shifted to shorter values. For the neurons in this category, the mean decrease in cut-off duration was 35 ms (range, 3–92 ms). The mean decrease in latency was 18 ms (range, 3.6–28.3 ms). Two of these neurons lost their duration sensitivity at higher sound levels.
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10 ms at 20 dB above threshold to 30 ms at 40 dB above threshold. In addition, latency lengthened from 25 ms at 20 dB above threshold to 45 ms at 40 dB above threshold. The other neuron (data not shown) displayed a smaller change in cut-off duration (from 42 to 47 ms) but a similar increase in latency (from 45 to 58 ms). The cut-off durations of the remaining three neurons did not change with sound level. Figure 6 shows a scatter plot of cut-off durations versus first-spike latency for 48 long-pass duration-sensitive neurons at 20 dB above threshold. All but one of these neurons had first-spike latencies that were longer than their cut-off durations, as would be expected if latencies depended on energy integration or the same inhibitory input that set the cut-off duration. Sustained responders had a large range of latencies (10–68 ms) and cut-off durations (4.5–60.5 ms), with a strong positive correlation between latency and cut-off duration (R2 = 0.88). Transient responders, on the other hand, all had relatively short latencies (12–24 ms) and cut-off durations (4.5–15 ms). When calculated in a case by case basis, the latency for transient responders was 7.4 ms longer than the cut-off duration on average, whereas for sustained neurons it was 8.3 ms longer.
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25 and 160 ms, with the most reliable response at 55 ms. This neuron was typical of band-pass units in that it responded at the offset of the sound, so latency relative to sound onset varied as a function of sound duration.
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Seven neurons in our sample (4.5% of all IC neurons, 8.4% of duration-sensitive neurons) had responses that we classified as mixed. Three of these had "band-reject" responses to stimulus duration, responding most reliably to both short and long durations but poorly to sounds of intermediate durations. An example of such a neuron is shown in Fig. 8, A and B. This neuron had a sparse response to durations of 80 ms and longer and a robust response to durations <10 ms, but little or no response to durations in between. Band-reject duration tuning of this sort has been described in the chinchilla (Chen 1998), where it was suggested that the decreased response to intermediate durations was caused by neural inhibition.
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35 and 80 ms where spike probability dropped to zero. Even at the maxima, however, the spike probability for this neuron was low. Maximal spike probability for other neurons with multipeaked duration sensitivity varied considerably but was typically <1.0 (range, 0.4–0.8). Figure 9 summarizes the distribution of neuron classes based on their patterns of duration selectivity. Long-pass duration sensitivity was by far the most common type observed, followed by band-pass, whereas only a few of the other types were found. Figure 10 shows the relation between neuron discharge patterns and their sensitivity to sound duration. Neurons that were insensitive to duration responded with a variety of temporal discharge patterns. The majority of neurons with transient and pauser discharge patterns were insensitive to duration, whereas the majority of units with sustained responses were long-pass. Offset responses were typical of band-pass units, but were also occasionally seen in long-pass and short-pass units. Interestingly, all of the units that responded at sound offset exhibited some form of duration sensitivity.
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250 ms. Interestingly, this unit was an offset responder. Thus we cannot entirely rule out the possibility that some off responders that were classified as long-pass using stimuli up to 200 ms could actually be band-pass with best durations >200 ms. One neuron (data not shown) had a multipeaked duration sensitivity function that included peaks at durations between 200 and 400 ms. The remaining three units were not duration sensitive, and their filtering properties did not change at durations >100 ms (Fig. 11, E and F).
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To determine whether duration-sensitive neurons are confined to a particular region within the IC, we plotted the locations of 56 neurons at marked sites within the subdivisions of the IC. The results are shown in Fig. 12. Eighty percent of neurons in the central nucleus of the IC (CNIC) were insensitive to the duration of the stimulus. However, the CNIC was also the only region in which we found short-pass neurons. In contrast, more than one-half of all neurons in the dorsal cortex of the IC (DCIC) and external cortex of the IC (ECIC) were duration sensitive. In the DCIC, more than one-half of all neurons were long pass. In the ECIC, there was a relatively high percentage of band-pass neurons. Band-pass neurons were found only in the DCIC or the ECIC and multipeaked neurons only in the ECIC.
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DISCUSSION |
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The population of duration-sensitive neurons found in the IC of the rat closely resembles that of the mouse (Brand et al. 2000). Both species have a high proportion of long-pass neurons, accounting for 40% of all units sampled in the rat and 38% in the mouse (Brand et al. 2000). Moreover, band-pass and short-pass neurons comprised <10% of all IC neurons in rats and 17% in mice (Brand et al. 2000). Bats have nearly opposite ratios of these response types. In the bat species that have been studied, band-pass and short-pass neurons comprised approximately one-third to two-thirds of all IC neurons, and long-pass neurons were in the minority (Ehrlich et al. 1997; Faure et al. 2003; Fremouw et al. 2005; Fuzessery and Hall 1999; Galazyuk and Feng 1997; Mora and Kössl 2004).
The durations to which most neurons in the rat and mouse are selective are considerably longer than those in bats. Figure 13 compares the range of cut-off durations and best durations of IC neurons in the rat and the big brown bat, Eptesicus fuscus, a species typical of the bats that have been studied. In the rat, the range of durations to which band-pass neurons are tuned extends to >120 ms. In contrast, best durations of band-pass neurons in the bat IC typically range from 1 to 25 ms, with the majority under 10 ms (Ehrlich et al. 1997; Fuzessery and Hall 1999; Galazyuk and Feng 1997; Mora and Kössl 2004). Bat echolocation calls typically range from 20 to <1 ms (Simmons 1989). Although echolocation calls are short, communication calls in Eptesicus may be longer in duration, ranging 
100 ms (Gould 1971). Although not as common as in the rat or mouse, long-pass duration-sensitive neurons are also found in the bat, where they respond to sounds longer than those used for echolocation (Faure et al. 2003). The close match between band-pass duration tuning and the durations of bats' echolocation calls suggests that the large number of band-pass neurons in the bat represents a specialization for echolocation, whereas long-pass neurons may be used for processing communication sounds and therefore be the more primitive characteristic.
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; Kaltwasser 1990). Long-pass neuron cut-off durations were distributed over a fairly wide range, from 5 to 60 ms, indicating that a subset of these neurons would be unresponsive to short-duration calls such as the "broadband" signals emitted during exploration or the "short" and "wave-like modulated" calls emitted during sexual behavior. These cells would presumably be responsive to infant calls as well as the "screams" and "frequency step" calls emitted during agonistic behavior (Kaltwasser 1990).
Our finding that most band-pass and long-pass neurons were located outside the central nucleus of the IC also seems different from the situation in the bat, where most duration-sensitive neurons, at least band-pass ones, are found in the caudal half of the central nucleus (Ehrlich et al. 1997). The finding that the rat has a high proportion of long-pass neurons in the dorsal part of the IC is consistent with the idea that neurons in this region have longer integration times because of the influence of cascaded intrinsic projections within the IC itself (Miller et al. 2005) and/or descending input from the cortex (Caicedo and Herbert 1993; Saldaña et al. 1996; reviewed in Malmierca 2003).
Previous studies in which inhibition was blocked (Casseday et al. 1994, 2000; Fuzessery and Hall 1999) provide convincing evidence that duration sensitivity of all types can be created through the interaction of excitation and inhibition within the IC. However, there is also evidence that inhibition may not be directly responsible for the duration tuning of all IC neurons (Fuzessery and Hall 1999). The fact that latencies of long-pass neurons were always longer than their cut-off duration, and the average latency of long-pass neurons was longer than the average latency of those that were not sensitive to duration, is consistent with the idea that the duration of a single onset-evoked inhibitory input determines both the cut-off duration and response latency of long-pass neurons (Fig. 14, A and B) (Brand et al. 2000; Faure et al. 2003). For neurons with sustained responses and paradoxical latency shift (Sullivan 1982), whose cut-off durations shifted to longer values with increasing sound level, this clearly seems to be the case. For these neurons, the relative strength and duration of a transient, onset-evoked inhibitory input apparently grew at a faster rate than that of a sustained, onset-evoked excitatory input (Fig. 14C). Previous studies have shown that, in many IC neurons, inhibition precedes excitation (e.g., Covey et al. 1996; Kuwada et al. 1997), and that such inhibition can cause paradoxical latency shift (Covey et al. 1996).
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; Kuwada et al. 1997) and that blocking inhibition causes a lowering of threshold in some IC neurons (LeBeau et al. 2001; Vater et al. 1992). An equally plausible alternative explanation would be that these neurons were integrating subthreshold excitatory inputs over a period as long as 90 ms, possibly through projections from a cascaded system of delay lines within the IC (Miller et al. 2005) or convergence of ascending inputs with descending excitatory projections from outside the IC. In this case, increases in sound amplitude would result in larger, longer lasting excitatory postsynaptic potentials (EPSPs), allowing temporal summation to occur. The finding that blocking inhibition in some IC neurons in the pallid bat did not abolish their duration tuning is consistent with this hypothesis, and suggests that duration sensitivity may arise through multiple mechanisms. Moreover, the relative prevalence of each mechanism may vary across species. For long-pass neurons with transient responses, a transient onset-evoked inhibition could not easily create a long-pass response, because it would presumably have the same effect regardless of stimulus duration. However, if transient inhibition were evoked by the offset of the stimulus, it could eliminate responses to sounds with durations shorter than the latency of the excitatory input, while permitting responses to sounds at all longer durations. The latency of an offset response (relative to the onset of the stimulus) is equal to the duration of the stimulus plus the latency of the inhibition relative to sound offset. Based on the data in Fig. 6, the average value for the theoretical 50% cut-off duration at which the latency of the offset inhibition becomes long enough to permit a response to onset-evoked transient excitation is 7.3 ± 3.1 ms, a perfectly plausible value for latency in the rat IC.
The observation that band-pass neurons were typically offset responders is consistent with previous studies showing that transient onset-evoked excitation and sustained inhibition followed by an excitatory rebound at sound offset is responsible for this response pattern (Casseday et al. 1994, 2000; Faure et al. 2003). To further support this view, all of the offset responders in this study showed some kind of duration sensitivity. Although the number of offset neurons in our sample is relatively small (7), the same finding has been published in other species, including the mouse (Brand et al. 2000) and chinchilla (Chen 1998). In the bat, up to 80% of duration sensitive neurons are offset responders (Fremouw et al. 2005), a finding that is consistent with the observation that the majority of duration-sensitive neurons in the bat have band-pass tuning (Ehrlich et al. 1997). It seems this relationship also holds in regions outside the IC. For example, in the dorsal zone of the auditory cortex of the cat, 24/28 offset neurons were described as duration sensitive (He et al. 1997). Therefore it seems to be a highly consistent finding, both across species and across sound levels, that a majority of offset responders are sensitive to stimulus duration. The conclusion to be drawn from considering all of these data together is that duration sensitivity in the IC takes many forms and may arise through diverse mechanisms but that these mechanisms are consistent across species.
Although it is tempting to think of duration sensitivity as an independent filtering mechanism that creates "feature detectors" selective for biologically relevant sound durations, we must also consider the possibility that it is but one component of a larger scale mechanism underlying the filtering and analysis of complex temporal sequences of natural sounds. The fact that duration-tuned neurons in the bat experience suppression analogous to forward and backward masking when presented with sounds of different durations (Faure et al. 2003) suggests that their responses are also determined by the temporal context in which a given sound occurs.
In the rat, we found that most duration-sensitive neurons were located in the cortical areas of the IC. This finding was surprising because, in the bat, they have been reported only in the CNIC, mainly in the caudal portion (Ehrlich et al. 1997). In the other studies, either the recordings were performed only in the CNIC (Ehrlich et al. 1997; Faure et al. 2003; Fremouw et al. 2005) or there was no precise indication of the location (Brand et al. 2000; Chen 1998; Fuzessery and Hall 1999; Mora and Kössl 2004; Pinheiro et al. 1991), so the opportunities for comparison are limited. There are some anatomical differences that may explain the different distribution of the duration-sensitive neurons in the rat and bat. In E. fuscus, the bat in which duration-tuned neurons were localized, the "cortical" areas surrounding the CNIC are not nearly as prominent as they are in rats. In Eptesicus the "pericentral area" is quite small (<200 µm thickness) and includes regions that would presumably correspond to both the ECIC and DCIC in rats (Casseday and Covey 1992; Covey and Carr 2005). Even though we cannot rule out a sampling bias caused by the relatively larger size of the cortical areas in the rat, it is still significant that only 20% of the CNIC units in our sample had any kind of duration sensitivity, whereas the percentage was much higher in the cortical areas. This finding suggests that duration-sensitive neurons in the rat may be important for orienting to sounds of specific durations.
The finding that all of the different types of duration-sensitive neurons that have been described in other species are present in the rat IC reinforces the idea that duration tuning is an emergent property in the midbrain of all vertebrate species and that it arises through multiple mechanisms and takes multiple forms. The selectivity of rat IC neurons for relatively long durations that correspond to those within the rat's vocalization repertoire suggests that there are species-specific adjustments in latencies, discharge patterns, and synaptic strengths that optimize the range of sound duration sensitivity in each species to produce filtering properties that are important for behaviors that depend on analyzing the temporal pattern of sound.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. Covey, Dept. of Psychology, Box 351525, Univ. of Washington, Seattle, WA 98195 (E-mail: ecovey{at}u.washington.edu)
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ABSTRACT
INTRODUCTION
); dotted line is regression line for sustained responders (
).
