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Previous Article | Next Article
Volume 16, Number 21, Issue of November 1, 1996 pp. 6987-6998
Copyright ©1996 Society for NeuroscienceHierarchical Organization of Auditory Temporal Context Sensitivity
Michael S. Lewicki and Benjamin J. Arthur Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125
ABSTRACT
Some of the most complex auditory neurons known are contained in the songbird forebrain nucleus HVc. These neurons are highly sensitive to auditory temporal context: they respond strongly to the bird's own song, but respond weakly or not at all when the sequence of the song syllables is altered. It is not known whether this property arises de novo in HVc or whether it is relayed from the properties of neurons in afferent nuclei. To address this issue, we recorded from neurons in both HVc and its afferent nuclei, collectively called field L. Experimental tests were designed to determine the degree of auditory context sensitivity in field L and HVc. Tests were also performed to compare the responses to individual syllables and syllable combinations to see whether these responses could account for the response seen to the entire song.
Our results show a substantial increase in the auditory temporal context sensitivity between field L and HVc. Most field L neurons respond equally well both to normal song and to temporally manipulated versions of the same song. A few field L neurons show sensitivity to local temporal structure, such as the sequence of syllable pairs. In contrast, HVc neurons are highly dependent on the song's local and global temporal structure. This shows that HVc neurons can integrate auditory context over periods much longer than neurons in field L and suggests that additional mechanisms are required to explain the marked sensitivity of HVc neurons to the temporal structure of the bird's own song.
Key words: hierarchical organization; auditory response properties; neural integration; context sensitivity; order sensitivity; song system; field L; HVc
INTRODUCTION
Neurons selective for complex stimuli occur in high-order brain areas in most sensory systems, such as face-selective neurons in the macaque monkey (Gross et al., 1972
; Perrett et al., 1992
Song-specific neurons respond exclusively or preferentially to the individual bird's own (autogenous) song (Margoliash, 1983
The circuitry by which song selectivity is established is not known. The song nucleus HVc is the first known site containing song-specific neurons (Margoliash, 1986
Fig. 1. A simplified diagram of the song system. Dashed lines indicate indistinct anatomical borders. Areas L1, L2a, L2b, and L3 are collectively called field L. The primary source of auditory input to HVc (via the shelf) is areas L1 and L3 (Kelley and Nottebohm, 1979
[View Larger Version of this Image (19K GIF file)]
As a population, field L neurons show no preference for the autogenous song over other songs (Margoliash, 1986
MATERIALS AND METHODS
Surgery. Experiments were performed on 25 adult (older than 120 d) male zebra finches (Taeniopygia guttata) raised in our own colony. A few days before the experiment, birds were anesthetized with Equithesin [0.03-0.04 ml intramuscular injection (0.85 gm of chloral hydrate, 0.21 gm of pentobarbital, 0.42 gm of MgSO4, 2.2 ml of 100% ethanol, 8.6 ml of propylene glycol, filled to a total volume of 20 ml with water); all chemicals were purchased from Sigma (St. Louis, MO)], and a small metal post, used to immobilize the head during later physiological recordings, was cemented to the skull with dental cement. One or two days later, the birds were anesthetized with urethane (65-90 µl of a 20% solution, Sigma) for physiological recordings.Electrodes were lowered through a craniotomy that was made small (400 µm diameter) so as to minimize brain edema and pulsation. If neurons were isolated in field L, the next electrode track was made into HVc and vice versa so as to maximize the number of single neurons from field L and HVc in each bird. Extracellular recordings were obtained with parylene-coated tungsten electrodes with impedances (at 1.0 kHz) ranging from 1 to 10 M
(AM Systems, Everett, WA).
The anatomical locations of the recording sites were determined from reference marks consisting of two or more electrolytic lesions (
2 to
Spike analysis. Extracellular waveforms containing action potentials of different shapes were sorted using a new real-time software spike discrimination algorithm (Lewicki, 1994
Stimuli. Before each experiment, the autogenous song was recorded, digitized, and analyzed on a DSP Sona-graph 5500 (Kay Elemetrics, Pinebrook, NJ) and on a computer using custom software (written by M.S.L., Dr. Larry Proctor, and Dr. James Mazer). The bird's own song was used as a search stimulus in both field L and HVc. Well isolated single neurons were selected for further analysis only if they demonstrated a significant response to song. Because the purpose of the present study was to compare the relative sensitivity to temporal structure between the field L areas and HVc, the general selectivity of the song responsive cells was not determined. Previous studies have shown that most (>90%) song-responsive HVc cells respond more to the bird's own song than to other songs of the same species (Margoliash, 1986
Some of the stimuli used in these experiments were constructed by manipulating the order of syllables and subsyllables in the autogenous song. Four stimuli were used in the tests for context sensitivity: forward song, reversed song (the song played backward), subsyllables in reverse order, and syllables in reverse order. Syllable boundaries were defined as points where the song's amplitude falls to zero. Subsyllable boundaries were defined as places where the sonogram of the song indicated an abrupt change in spectral composition. Typically, this was a change in the harmonic pattern or a change in the direction of the frequency modulation. An example of these divisions is shown in Figure 2. An envelope (3 msec rise-fall) was placed around each syllable and subsyllable to remove any transients. All stimuli were presented in free field conditions in a sound-attenuating chamber (Acoustic Systems, Austin, TX) with a calibrated speaker (JBL, Northridge, CA). The frequency response of the speaker, as measured from the bird's position in the stereotaxic apparatus inside the chamber, was flat to within 8 dB between 500 and 8000 Hz. Stimuli were presented with a peak amplitude between 60 and 70 dB SPL.
Fig. 2. An illustration of the procedure for selecting syllable pairs for performing the tests for temporal combination sensitivity. The graphs show the response of an HVc cell in response to the forward song (a) and to the syllables in reverse order (b). The top of each graph shows the spike rasters. The sonogram and oscillogram of the stimulus are shown below. The solid and dotted vertical lines indicate the syllable and subsyllable boundaries, respectively. This divides the song into segments that are numbered from left to right, counting both syllables and the silent periods in between the syllables. The numbers below the oscillogram indicate the segment numbers referred to in the table. The table shows the song segments that had the greatest difference (in terms of the p value of a paired t test) between the response in the forward song and the response to the song with the syllables in reverse order. Entries with few spikes were omitted. In this example, there were 58 total spikes during segment 12 during the forward song. The same syllable elicited only 34 spikes in the context of the syllable-reversed song. Thus, segments 10-12 (2 syllables, separated by a silent segment) would be selected for presentation in isolation to test for temporal combination sensitivity.
[View Larger Version of this Image (47K GIF file)]
An automated procedure was developed to select syllable pairs for which a neuron would be likely to show order and combination sensitivity. This procedure is illustrated in Figure 2. Syllable pairs were selected by comparing the response to each syllable when presented as part of the forward song to the same syllable as part of a song constructed by playing the syllables in reverse order. The syllables (or subsyllables) with the greatest statistically different responses (by a paired t test) and the syllables (or subsyllables) preceding them were selected to test for temporal combination sensitivity. This yielded two syllables, A and B (and the intervening silent period), which were presented in the following combinations: A, B, AB, BA, AA, and BB. Syllables at the beginning of the song were not considered, because significant differences can result simply from an onset response. Sometimes more than two syllables were necessary to evoke a response, in which case the set of syllables was divided into two groups and manipulated as above.
The trials for both types of experimental tests were either interleaved or randomized. No difference was observed between these conditions. During the collections to measure the response to syllables and syllable pairs, the response to forward song was also measured. Cells that did not show a stable response to forward song were omitted from the analysis. The collection duration was 5 sec for the song stimuli and between 2 and 3 sec for syllables. For all trials, a delay of at least 2 sec was inserted between each stimulus with an additional random delay of up to 500 msec to minimize the effect of any periodicity in the noise or in successive responses. This yielded an effective interstimulus interval between 4 and 6.5 sec for song stimuli and between 3 and 3.5 sec for syllables.
Data analysis. The response of a cell to autogenous song and the synthetic songs was measured by the average spike rate during the stimulus presentation minus the spontaneous rate. The variation of the response is reported as mean ± SEM. For shorter stimuli, such as single syllables, the time course of the response of HVc neurons can be highly variable from neuron to neuron: some neurons respond during the stimulus, and others respond well after the stimulus has ended. This variability makes it difficult to determine exactly when and how much a cell responded. We determined the regions of significant response automatically by calculating where the spike rate differed significantly from background by sliding a 50 msec window from the start of the stimulus (plus latency) to the end of the collection. Because a standard t test can inaccurately report significant response regions when most or all of the window counts across trials are zero, we determined statistical significance using a Poisson model that takes into account the window size. Excitatory and inhibitory regions were analyzed separately.
The statistical significance of the sensitivity to syllable order was determined by comparing the total spike counts in the significant response regions of syllable pairs AB and BA using a t test. The significance of the sensitivity to syllable combinations was determined using a t test to compare the sum of the spike counts in the regions of syllables A and B to the spike counts from the regions of AB.
RESULTS
We recorded from 52 well isolated neurons in HVc and 56 neurons in the field L areas that had a significant response to song (shown in Fig. 3). In the areas of field L, there were 8 well isolated units in L1, 11 in L2a, 10 in L2b, 16 in L3, and 11 that bordered two or more field L regions. Neurons that were on the border between field L and non-field L areas, such as caudal neostriatum (NC) and ventral hyperstriatum (HV), were omitted from the analysis. Both phasic and tonic responses were seen in each of the areas. Cells in HVc sometimes responded with bursts of action potentials. Bursting was rarely observed in field L.
Fig. 3. The anatomical sites of the neurons analyzed in this study (note that because spikes were sorted using a software discrimination algorithm, some sites may contain more than one isolated neuron). The upper diagram shows the sites in HVc, and the lower diagram shows the sites in field L. The average medial-lateral position was 2.3 mm (range 1.8-2.65) for HVc and 1.5 mm (range 1.1-1.9) for field L. Area L2a of the field L complex as well as HVc can be clearly identified in cresyl violet-stained sections. The dashed lines indicate the approximate anatomical areas as described by Fortune and Margoliash (1992)
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Comparison of context sensitivity in HVc and field L
The first set of experiments compares auditory context sensitivity in field L and HVc. A cell is sensitive to the auditory temporal context if the response at one point depends on previous parts of the stimulus. For example, if a cell's response was determined solely by spectral structure, then reversing the song should have little effect on the response, because playing the song backward alters the temporal structure but not the spectral structure. The response of song-specific neurons to autogenous song is often abolished if the song is played backward (Margoliash, 1983The extent of the temporal context sensitivity was estimated by reversing the order of segments of different lengths, i.e., by comparing the response to forward song with the responses to reversed song, subsyllables in reverse order, and syllables in reverse order. This preserves the local spectral and temporal structure within each segment, but alters the global auditory context in which each segment occurs.
The response of a typical HVc neuron is shown in Figure 4a. This particular neuron shows a strong response to forward song (22.78 ± 4.32 spikes/sec) and is slightly inhibited by the reversed song (
Fig. 4. The response of representative cells from HVc (a) and field L (b) to autogenous song and three manipulations of the song's temporal structure. The graphs show the spike rasters and peristimulus time histograms of the response recorded from two well isolated units. The oscillograms of the stimuli are shown below each histogram.
[View Larger Version of this Image (31K GIF file)]
Fig. 5. The bar graphs show the number of times the response to forward song differed significantly from the response to reversed song (r), to subsyllables in reverse order (rss), or to syllables in reverse order (rs).
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Neurons in field L showed much less sensitivity to manipulations of the auditory temporal context than neurons in HVc. Neurons in all areas of field L responded strongly throughout the forward song, the reversed song, and to the syllables and subsyllables in reverse order. The response of a typical field L neuron (in area L3) is shown in Figure 4b. The differences between the response to forward and the temporally altered songs is much less than in HVc (forward song, 19.07 ± 0.74 spikes/sec; reversed song, 16.17 ± 1.18 spikes/sec; subsyllables in reverse order, 15.29 ± 0.76 spikes/sec; syllables in reverse order, 14.10 ± 0.55 spikes/sec). A majority of field L cells (41/56) show no significant difference (p > 0.01) between the response to the forward song and the response to any of the three temporally altered songs. These data are summarized in the bar plots in Figure 5.
Of the field L subdivisions, only L3 contained neurons that showed a significant difference in response between the forward song and the syllable-reversed song (6/16). Both L1 and L3 had neurons that showed a significant difference between the forward song and subsyllable-reversed song (1/8 and 4/16, respectively). All subdivisions of field L had neurons that showed a significant difference between the forward and reversed song (L2a, 3/11; L2b, 2/10; L1, 1/8; L3, 5/16).
Although both field L and HVc contained cells that were significantly dependent on the temporal order, the difference in response rates between the forward song and the altered songs for these cells was much greater in HVc. This difference in the response properties of the two populations can be summarized by plotting the response of the forward song against the response of altered songs. Figure 6 shows that responses of the population of field L neurons was largely the same for all four types of stimuli, but the response of many neurons in HVc compared to forward song is greatly reduced or inhibited when the temporal structure of the forward song is altered. Each graph plots the response to forward song against the response to the three temporally altered songs. In HVc, many of the neurons responded much more to the forward song than to the temporally altered songs. This is indicated on the graph in Figure 6a by the large number of points above the line y = x (solid line). The further a point is above the line, the greater difference in response. If a neuron shows no sensitivity to auditory context, the responses to forward and the temporally altered stimuli would be the same, and the points would fall near the line y = x (solid line). This is indeed the case for the field L data shown in Figure 6b.
Fig. 6. The graphs show summary data for HVc (a) and field L (b). Response is defined as the average spikes/sec during stimulus minus the spontaneous rate. The response to the forward song is plotted against the response to the altered song. The solid diagonal line is y = x. a, Many neurons in HVc show a large dependence on the song's temporal structure. b, In field L, however, the response to the altered song is typically similar in magnitude to the response to forward song.
[View Larger Version of this Image (19K GIF file)]
HVc neurons clearly show greater sensitivity to the auditory temporal context than field L neurons. The difference between the HVc and field L responses is statistically significant for forward versus reversed song (p < 0.001, unpaired t test), forward versus subsyllables in reverse order (p < 0.001), and forward versus syllables in reverse order (p < 0.05). A one-way ANOVA indicated no statistical differences (p > 0.2, F test) among any of the field L areas between the forward song and the temporally altered stimuli. Because there are relatively few neurons in each of the field L subdivisions, these tests do not rule out the possibility that more subtle differences among these areas do exist.
Another way to see the difference between HVc and field L response properties is to look at the time course of the responses. Figure 7 shows the average response to the forward song and the three altered songs for HVc and field L neurons. The plots were generated by computing for each cell the response in 50 msec time windows over the duration of the collection. The average response was computed by normalizing the time axis so that the song was from 0.0 and 1.0 and then averaging the response rates across cells. The average response plots show that both HVc and field L neurons have an onset response. For HVc cells, the average response to forward song builds up during the course of the song, whereas the response attenuates during the course of reverse song and the subsyllables and syllables in reverse order. For field L neurons, the average response to the forward song and the three altered songs is roughly the same. Neurons typically have a strong onset response and accommodate at the same rate over the course of all four types of stimuli.
Fig. 7. The graphs show the average response for HVc and field L areas, with the time axis normalized so that the song was from 0.0 to 1.0 (see text). a, The average response of HVc cells builds up during the course of the forward song, but only has an onset response to the other stimuli. b, The average responses in field L were the same for all manipulations of the song with a strong onset response in all cases.
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Comparison of order and combination sensitivity in HVc and field L
The second part of this study addresses the question of whether the auditory context sensitivity observed in song-specific neurons can be accounted for by the response measured for syllables presented in isolation. A cell is said to be combination-sensitive if the response to a syllable pair AB is greater than the sum of the responses to syllables A and B presented in isolation (Margoliash, 1983Figure 8a shows an example of a TCS neuron in HVc. The syllables A and B were selected using the automated procedure described in Materials and Methods. Because the response to AB is significantly greater than the response to BA (p < 0.001, paired t test), this cell shows order sensitivity. The cell also shows combination sensitivity, because the response to AB is significantly greater than the sum of the responses to A and B presented in isolation (p < 0.001). It is possible that the response to the pair AB could be explained by a nonspecific facilitation. For example, syllable A may facilitate the response to any subsequent stimulus. Conversely, it is also possible that any auditory stimulus facilitates the response to B. To test for these possibilities, the present study also measured the responses to repetitions of each syllable, AA and BB. This cell shows no response to either, which provides further evidence that the cell is indeed selective for the syllable combination AB.
Fig. 8. To the left of each set of histograms are the sonogram and oscillogram of the stimuli, which are syllables selected from the autogenous song. a, A temporal combination-sensitive (TCS) neuron from HVc. b, A field L TCS neuron.
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In field L, temporal combination sensitivity was also observed despite the lack of strong sensitivity to syllable order of the whole autogenous song as reported in the previous section. Figure 8b shows an example of a TCS neuron in field L. This cell shows order sensitivity, because the response to the syllable pair AB was significantly greater (18.03 ± 2.52 spikes/sec, p < 0.001) than the response to BA (6.23 ± 2.21 spikes/sec). This cell was also combination-sensitive, because the response to AB was significantly greater than the response to the sum of the responses to A and B in isolation (p < 0.001). The response to AB cannot be accounted for by facilitation by syllable A because the syllable pair AA produces no response. This cell, however, did show significant facilitation by syllable B (p = 0.018), because the response to BB was greater than twice the response to syllable B when presented alone. The other two examples of temporal combination sensitivity seen in field L (data not shown) showed strong responses to individual syllables and syllable pairs (but still satisfied the criteria listed above). None of the temporal combination sensitive units in HVc responded to individual syllables in isolation.
Tests for order and combination sensitivity were performed on 31 and 42 well isolated neurons in HVc and field L, respectively. All of these cells showed a significant response to autogenous song as determined from the tests for temporal context sensitivity described in the previous section. Cells that did not show a significant response to the selected syllable pair AB when presented in isolation were not analyzed. There were 26 neurons in HVc and 27 in field L that showed a significant response to a syllable pair AB in isolation. Most of the syllable pairs selected for HVc neurons produced a significant response (26/31) compared to 27/42 in field L. This difference arises because several field L neurons had a relatively weak, but statistically significant, response to autogenous song. Subsequently, these neurons did not produce a significant response to isolated syllables. Most of the HVc neurons responded more strongly to autogenous song and also to the syllables presented in isolation. The results of the syllable tests on the population of HVc and field L neurons are summarized in Figure 9. A greater percentage of HVc units showed some sensitivity, but in both areas there were instances of order and combination sensitivity.
Fig. 9. The tests for order and combination sensitivity were performed on cells that showed a significant response to forward song. For each set of tests, a pair of syllables (AB) was selected that was likely to show order sensitivity (see Materials and Methods). The bars indicate the percentage of cells that satisfied the listed conditions given a significant response to the syllable pair AB. Order, The response to AB is significantly greater than the response to BA; Comb, the response to the syllable combination AB is significantly greater than the response to A or B when presented in isolation; TCS, the cell showed both order and combination sensitivity. The incidence of TCS is low but not inconsistent with previous studies.
[View Larger Version of this Image (33K GIF file)]
The data were also analyzed for significant responses to the syllable pairs in reverse order. Twenty cells in HVc and 29 cells in field L showed a significant response to the syllable pair BA in isolation. Of these, one HVc cell showed significant reverse order sensitivity (BA > AB) compared to 4 in field L. In HVc, 2 cells showed significant reverse combination sensitivity (BA > B + A) compared to 3 cells in field L. No cells in HVc showed both of these properties, whereas 1 cell did in field L. The number of HVc cells showing significant order or combination sensitivity for the reverse order, BA, was lower than for the normal order, AB (20 vs 26). In field L, there were roughly equal numbers for both the reverse and normal order (29 vs 27).
Not all of the cells that showed auditory context sensitivity also showed order or combination sensitivity. In HVc, tests for order and combination sensitivity were performed on 13 cells that showed a significant difference between the response to the forward song and the response to the syllable- or subsyllable-reversed songs. Of these, only 7 cells were sensitive to the temporal order and/or combination of the syllables, despite large differences in response between the forward and syllable-reversed songs. In field L, order and combination tests were performed on 4 cells that showed significant sensitivity to the syllable or subsyllable order. Three of these showed either order or combination sensitivity, and the other showed significant facilitation.
DISCUSSION
The neural circuitry that gives rise to the complex auditory response properties of song-specific neurons is not known. These results show that there is a substantial increase in the auditory temporal context sensitivity associated with the progression from the areas of field L to HVc. Neurons in field L typically respond equally well to autogenous song and to the temporally manipulated versions of the song. In contrast, neurons in HVc are highly dependent on the song's temporal structure. They respond strongly to the forward song but weakly to the reversed song and to the song with the syllables or subsyllables in reverse order. These results extend previous findings that neuronal preference for autogenous song is observed in HVc but not in field L (Margoliash, 1986The response of song-specific units in HVc depends on auditory temporal context that extends beyond a single syllable. FM sensitivity alone is insufficient to account for the context-sensitive properties of these neurons. Previous studies comparing the context sensitivity of HVc and field L neurons used only forward and reverse song (Margoliash, 1986
Earlier studies suggested that the responses of field L neurons could be accounted for by the sensitivity to short-term spectro-temporal structure, such as amplitude and frequency modulation (Schafer et al., 1992
One explanation for the temporal context sensitivity of HVc song-specific units is in terms of the neural sensitivity to syllable order and combinations. In this model, sensitivity to the order of the syllables in the autogenous song results either from sensitivity to the order of particular syllable combinations or from integrating the output of such neurons. Several HVc neurons, however, showed strong sensitivity to the order of the syllables in the whole song, but were not sensitive to either the order or the combination of syllable pairs when presented in isolation. These data show that HVc neurons integrate auditory context over periods greater than the duration of syllable pairs, which supports the conclusions reached by earlier studies (Margoliash and Fortune, 1992
These findings suggest that there is a hierarchical arrangement of the temporal tuning properties in the song system auditory pathway. At the simplest level, field L neurons can be sensitive to amplitude and frequency modulation, which requires integrating just a few milliseconds of auditory temporal context. This work showed that field L neurons can also show nonlinear tuning properties such as sensitivity to combinations of syllables. This requires integration on the order of tens of milliseconds and also a nonlinear mechanism for combination sensitivity. The increase in auditory temporal context sensitivity from field L to HVc, however, represents a significant computation, because it is the first known location in the songbird auditory pathway where neurons are sensitive to much longer periods of temporal context, often as much as several hundred milliseconds. The hierarchical organization continues beyond HVc to the auditory nuclei in the anterior forebrain, where neurons become increasingly selective for autogenous song (Doupe and Konishi, 1991
A hierarchical arrangement of response properties would be expected, because L2a and L2b, which are the main recipients of thalamic auditory projections, project to L1 and L3, which in turn project to the shelf (Kelley and Nottebohm, 1979
The present data show highly significant differences between field L and HVc, but they are insufficient to allow meaningful comparisons between the different subareas of field L. These need to be studied in greater detail, but we can summarize the trends observed in the present study. All field L areas and HVc contained some neurons that were sensitive to the local temporal structure, as evidenced from the differences in response between the forward and reversed song. Only L1, L3, and HVc contained neurons that showed significant sensitivity to the order of the syllables or subsyllables in the autogenous song. Dramatic dependencies on the auditory temporal structure of autogenous song, in some cases having little or no response to the song with syllables in reverse order, were only observed in HVc.
New anatomical results suggest that there could be additional auditory pathways between field L and HVc, parallel to those studied here. A recent report showed that NIf, which sends projections throughout HVc, receives auditory inputs via the caudolateral hyperstriatum ventrale (clHV), which has reciprocal connections with all of the field L areas and also sends projections to the shelf (Vates et al., 1996
The hierarchical organization suggested by the studies presented here agrees with behavioral data from HVc lesion studies. In male songbirds, it is difficult to separate any perceptual roles HVc might have from its crucial role in song production. Female songbirds, however, need to discriminate their own species' song from those of other species. Brenowitz (1991)
The mechanisms that give rise to the dramatic increase in sensitivity in HVc are still unknown. Some initial studies have been made (Lewicki and Konishi, 1995
Sensitivity to auditory temporal structure has been observed in other systems, such as the cat (Weinberger and McKenna, 1988
FOOTNOTES
Received March 14, 1996; revised July 8, 1996; accepted July 24, 1996.
This work was supported by a National Institutes of Health Research Training Grant, a Caltech Engineering Research Center fellowship (M.S.L.), and a National Science Foundation graduate fellowship (B.J.A.). We thank Allison Doupe, Mark Konishi, James Mazer, and Marc Schmidt for valuable comments on this manuscript.
Correspondence should be addressed to Dr. Michael Lewicki, The Salk Institute, Computational Neurobiology Laboratory, 10010 North Torrey Pines Road, La Jolla, CA 92037.
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