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. Author manuscript; available in PMC: 2008 Oct 1.
Published in final edited form as: J Neurophysiol. 2007 Jul 11;98(4):2099–2109. doi: 10.1152/jn.00916.2006

Song Selectivity in the Pallial-Basal Ganglia Song Circuit of Zebra Finches Raised Without Tutor Song Exposure

Satoshi Kojima 1, Allison J Doupe 1
PMCID: PMC2443789  NIHMSID: NIHMS50329  PMID: 17625059

Abstract

Acoustic experience critically influences auditory cortical development as well as emergence of highly selective auditory neurons in the songbird sensorimotor circuit. In adult zebra finches, these “song-selective” neurons respond better to the bird's own song (BOS) than to songs of other conspecifics. Birds learn their songs by memorizing a tutor's song and then matching auditory feedback of their voice to the tutor song memory. Song-selective neurons in the pallial-basal ganglia circuit called the anterior forebrain pathway (AFP) reflect the development of BOS. However, during learning, they also respond strongly to tutor song and are compromised in their adult selectivity when birds are prevented from matching BOS to tutor, suggesting that selectivity depends on tutor song learning as well as sensorimotor matching of BOS feedback to the tutor song memory. We examined the contribution of sensory learning of tutor song to song selectivity by recording from AFP neurons in birds reared without exposure to adult conspecifics. We found that AFP neurons in these “isolate” birds had highly tuned responses to isolate BOS. The selectivity was as high, and in the striato-pallidal nucleus Area X, even higher than that in normal birds, due to abnormally weak responsiveness to conspecific song. These results demonstrate that sensory learning of tutor song is not necessary for BOS tuning of AFP neurons. Because isolate birds develop their song via sensorimotor learning, our data further illustrate the importance of individual sensorimotor learning for song selectivity and provide insight into possible functions of song-selective neurons.

Introduction

In vocal learners, such as humans and songbirds, the development of their complex vocalizations strongly depends on two types of auditory experience in early life: hearing the adults they will imitate and hearing themselves as they practice (Doupe and Kuhl 1999). In songbirds, a young bird first memorizes the song of an adult conspecific (the tutor) during the sensory phase of learning (Fig. 1A). In the subsequent sensorimotor learning phase, the juvenile begins to sing and refines its vocalizations until they resemble the tutor song (Konishi 1965; Price 1979). Because normal song development in this second phase depends on auditory feedback (Konishi 1965) but not on the continued presence of the tutor, the bird is thought to compare its auditory feedback to the tutor song memory (the “template”) and to use the results of this evaluation to guide song motor development.

Fig. 1.

Fig. 1

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A: time course of zebra finch song learning. The sensory phase ends at approximately posthatch day (PHD) 60; the sensorimotor phase begins at ∼PHD 30 and continues until PHD 90–110. B: simplified schematic view of the 2 major pathways in the song system. The motor pathway nuclei are gray and the anterior forebrain pathway (AFP) nuclei are black; primary auditory stations are indicated in white. DLM, medial nucleus of the dorsolateral thalamus; LMAN, lateral magnocellular nucleus of the anterior nidopallium; NIf, interfacial nucleus of the nidopallium; RA, robust nucleus of the arcopallium.

Auditory neurons within the vocal control system of songbirds appear to reflect the process of song learning. Although these neurons exist throughout the circuit (Coleman and Mooney 2004; Doupe and Konishi 1991; Janata and Margoliash 1999; Margoliash 1983; Margoliash and Fortune 1992; Mooney 2000; Nick and Konishi 2005; Vates et al. 1997; Vicario and Yohay 1993), their development has been studied most extensively in the anterior forebrain pathway (AFP, Fig. 1B), a pallial-basal ganglia circuit that is essential for both sensory and sensorimotor learning (Basham et al. 1996; Bottjer et al. 1984; Scharff and Nottebohm 1991; Sohrabji et al. 1990). By the end of the sensory learning phase and partway through the sensorimotor learning phase (posthatch day 60, PHD 60), auditory neurons in two nuclei of the AFP, Area X and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), have developed selective responsiveness for the bird's own song (BOS) relative to songs of other zebra finches (conspecifics) and temporally altered versions of BOS, even when BOS has been made abnormal by manipulation of the peripheral motor system (Doupe 1997; Solis and Doupe 1997, 1999; Yazaki-Sugiyama and Mooney 2004). This “song selectivity” suggests that these neurons are shaped by the bird hearing its own song during sensorimotor learning.

However, song selectivity appears to be influenced by more than just the sound of the bird's song. For one, when sensorimotor matching of BOS to tutor song is chronically disrupted by denervation of the vocal organ (syrinx), BOS selectivity is compromised (Solis and Doupe 2000): neurons in Area X of such birds have a lower degree of selectivity for BOS than do normal adults, and LMAN neurons with auditory responses of any kind are found with a much lower frequency than in normal adults. In contrast, neurons in adult birds that successfully mimic tutor song after presumably reinnervating the syrinx, exhibit normal adult selectivity for BOS. Thus during sensorimotor learning, the development of selectivity for complex stimuli such as BOS may be influenced by how well the bird can match its motor output to the internal tutor song model.

In addition, by PHD 60, many of the highly BOS selective neurons in Area X and LMAN also respond strongly to the tutor song (Doupe 1997; Solis and Doupe 1997, 1999; Yazaki-Sugiyama and Mooney 2004), even when it differs markedly from BOS (Solis and Doupe 1999). This raises the possibility that, in addition to depending on successful sensorimotor learning, the development of BOS selectivity requires the sensory learning of tutor song template.

Therefore to test whether song selectivity obligatorily depends on sensory learning of tutor song, we examined the auditory selectivity of AFP neurons in zebra finches raised in isolation from adult individuals, so that they had not experienced normal tutoring. Although isolate birds do not learn songs of conspecific individuals, their song has many conspecific features, which require hearing to emerge (Eales 1985, 1987; Konishi 1965; Marler and Tamura 1964; Morrison and Nottebohm 1993; Price 1979; Scharff and Nottebohm 1991). Thus isolate birds are thought to develop their song in a sensorimotor learning process, matching their vocalizations to an innate, species-specific template (Adret 2004; Konishi 1965; Marler 1997).

We report here that AFP neurons in birds raised without experience of adult conspecific song develop BOS selectivity comparable with, and in Area X even greater than, that in normally reared birds. These results indicate that song selectivity can develop in the AFP in the absence of sensory learning of tutor song and with sensorimotor matching likely limited to innate information about song rather than to a learned template. Together with the existing evidence on how tightly song selectivity follows the motor development of BOS (Doupe 1997; Nick and Konishi 2005; Roy and Mooney 2007; Solis and Doupe 1997, 1999; Yazaki-Sugiyama and Mooney 2004), our data provide further support for the critical importance of song sensorimotor learning to the properties of song-selective neurons.

Methods

Animals and Isolation protocols

Experiments used adult male zebra finches (Taeniopygia guttata). The care and treatment of experimental animals was reviewed and approved by the animal care and use committee at the University of California, San Francisco (UCSF). Birds to be isolated were initially raised in sound-attenuating chambers with their parents, and siblings from the same clutch, until PHD 9–11. After this day, the male parent was removed. At PHD ∼30, the young birds were removed from the female parent and the siblings and housed alone in individual sound-attenuating chambers. Normal control birds were raised in individual cages in the colony with their parents and siblings; opaque dividers between cages visually isolated control birds from other conspecifics, which allows them rich song exposure but limits their song learning to the visible tutor (Eales 1989; Price 1979). Control birds were removed from their parents at PHD ∼60 and housed in cages with their brothers and/or other conspecifics.

Electrophysiology

Extracellular signals of single LMAN and Area X neurons during song playback were recorded as described by Solis and Doupe (1999), in isolate birds at 216–774 days of age and in normal control birds at 151–427 days of age. Two to 7 days prior to the experiment, birds were prepared for neurophysiological recording by affixing a head post to the skull under Equithesin anesthesia (see Solis and Doupe 1999 for components) and marking the location of the song nuclei on the skull (see Solis and Doupe 1997; for details) or creating a craniotomy that was sealed with bone wax. On the day of the experiment, they were anesthetized with a 20% solution of urethan (60–85 μl im; Sigma, St. Louis, MO) or sedated with 0.5% (5 mg/ml) diazepam (10–30 μl im; Abott Laboratories, North Chicago, IL), secured in the stereotaxic apparatus by the head post, and placed in a double-walled anechoic sound-attenuating chamber. Body temperature was maintained at ∼40°C with a temperature controller. Extracellular activity recorded with tungsten electrodes (1–5 MΩ) was amplified and filtered between 300 Hz and 5 kHz (A-M Systems, Everett, WA). Some neurons with high signal-to-noise ratios (approximately >10) without any background units were isolated with an on-line window discriminator (FHC, Bowdoinham, ME). For most sites, one or at most two neurons were sorted off-line from a waveform with high signal to noise, containing a small number of units, using spike-sorting software developed by M. Lewicki (Caltech) and B. Wright (UCSF). Briefly, spike models were constructed from spike waveforms recorded during and before the stimulus presentation, and spikes were then classified using the spike models with a template-matching algorithm based on Bayesian probability theory (Lewicki 1994). All neurons were judged to be single units based on inspection of the waveforms and by analysis of interspike interval (ISI) violations: any sites where occurrence of ISIs <0.7 ms constituted >1.0% of total ISI occurrences were discarded.

Electrolytic lesions were made at selected locations for reconstructing recording sites. At the end of each experiment, the bird was killed with Metofane (methoxyflurane) (Pitman-Moore, Mundelein, IL) or Isoflurane [2-chloro-2-(difluoromethoxy-1,1,1-trifluoro-ethane] (Abott Laboratories) and transcardially perfused with 0.9% saline, followed by 3.7% formaldehyde in 0.025 M phosphate buffer. Brains were postfixed, and 40-μm sections were cut with a freezing microtome. Sections were stained with cresyl violet, and electrode tracks and lesions were identified. Neural recording sites where we did not make any lesions were identified in reference to the lesion sites on the same electrode tracks. Only neurons histologically confirmed in this manner to be in LMAN or Area X were analyzed.

Stimuli

The songs of the isolate birds and of the normal control birds were recorded as described by Solis and Doupe (1999) at 2–9 days before the neurophysiological recordings. Prior to the final song recording, isolate songs were recorded two to three times at intervals of 1 wk to 4 mo to make sure that the songs were crystallized. Once songs were crystallized, a song of the type that was most frequently produced was chosen by visual inspection of the spectrograms and by listening to the songs. Most bird's own song (BOS) stimuli had several introductory notes followed by two song motifs as shown in Fig. 2. During neural recordings, stimuli were presented from a speaker positioned 20 cm from the bird. Search stimuli included BOS and the father's song at different peak volumes (75, 65, 55, 45 dB), and broad-band noise bursts (65 dB at peak volume, 500-ms or 1-s duration). At most sites, the stimulus intensity at which BOS or the father's song evoked the strongest responses was determined by examining average response amplitude in peristimulus time histograms (PSTHs) of spike rasters displayed on-line, and song selectivity was then examined by playing all the stimuli at that intensity (usually 65–75 dB). Stimulus types included two to four different songs of normal zebra finches (conspecifics), songs of other isolate birds (isolated conspecifics), at least one song of Bengalese finches and/or white-crowned sparrows (heterospecific songs), BOS, and temporally reversed version of BOS (reverse BOS). Stimuli were presented in a random, interleaved fashion. Intertrial interval was randomly varied within a range of 5–12 s. An effort was made to present each neuron with 15–30 trials of each stimulus type.

Fig. 2.

Fig. 2

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A: songs of a father from nest 67, its normally reared offspring (pupil) and 4 additional siblings reared in isolation from the father (is01-03 and is05). Sonograms plot frequency vs. time, and the energy in each frequency band is indicated by its darkness. For each bird, introductory notes and the subsequent 2 motifs are shown except for is01, which sang only 1 motif in most bouts. Song motif is indicated by a bar underneath the sonogram. B: songs of a father from nest 27 and its isolation-reared offspring, is04. *, examples of relatively soft syllables with short neighboring intervals and poorly defined syllable boundaries. Conventions are as in A. C: distributions of syllable durations in isolate and normal birds' songs. Bin size is 10 ms.

Data analysis

We analyzed only neurons that had an average firing rate during at least one of the auditory stimuli that was significantly different from the background rate (2-tailed paired t-test with Bonferroni correction, P < 0.01). The response strength (RS) of a neuron to a stimulus was calculated as the difference between the firing rate during the stimulus and the background rate. The period of stimulus presentation was offset by estimates of the latency determined in prior studies, 35 ms for Area X and 50 ms for LMAN. The background firing rate was defined as the mean firing rate of a 2-s period preceding stimulus presentation. For each neuron, the RS to a stimulus was measured for each trial and then averaged across trials to obtain a mean RS. For presentation of conspecific songs, heterospecific songs, and songs of isolated conspecifics, data from different stimuli but of the same stimulus type were also averaged to obtain the mean RS of a neuron to a particular stimulus type.

The selectivity of an individual neuron for one song stimulus (A) over another song stimulus (B) was quantified using the d′A-B measure (Green and Swets 1966) as described by Solis and Doupe (1997), where

d′A−B=2(RS¯A−RS¯B)σA2+σB2.

In this equation, RS¯A and RS¯B are the mean RS to stimulus A and B, respectively, and σ2 is the variance of each RS. If d′A-B is positive, then stimulus A elicited a greater response than stimulus B. A neuron was considered selective for stimulus A over stimulus B if it had a d′A-B value ≥0.5.

We also used an additional measure, the selectivity index (SI) (Doupe 1997; Solis and Doupe 1997; Volman 1996), which focuses less on absolute discriminability and more on the relative difference in the strength of the average responses between two stimuli. The SI quantifies responsiveness to one stimulus relative to the other by comparing the mean RS to each stimulus in ratio form (and thus is normalized by response magnitude)

SI=RS¯ARS¯A+RS¯B

SI will approach 1.0 if a response to stimulus A is much stronger than a response to stimulus B and will be close to 0.5 if the two responses are comparable. When a particular RS¯B had a negative value, it was considered to be zero for calculating SI, and thus the SI would be one regardless of RS¯A.

For the neural data of normal control birds, we had data that were newly collected for the current study (55 Area X neurons from 10 birds and 15 LMAN neurons from 4 birds) as well as data originally collected for a previous paper (Solis and Doupe 2000) (34 Area X neurons from 13 birds and 14 LMAN neurons from 6 birds). Although Solis and Doupe (2000) did not determine optimal amplitude for song playback and only used a fixed volume for each stimulus ranging from 64 to 73 dB, we found that for most neurons their amplitude range was in the saturated range of the response-stimulus amplitude curve that we determined in this study. Moreover, neither spontaneous firing rate, auditory responsiveness, nor BOS selectivity were significantly different between the two groups of data (unpaired t-test, P > 0.05): for Area X neurons, spontaneous firing rates (Hz) of the current and previous study were 44.7 ± 4.1 (mean ± SE) and 39.5 ± 4.8, respectively; RS to BOS (spike/s) were 11.3 ± 1.0 and 8.5 ± 1.2; d′BOS-CON was 1.83 ± 0.77 and 1.55 ± 1.73; for LMAN neurons, spontaneous firing rates (Hz) were 2.5 ± 0.8 and 2.1 ± 0.5; RS to BOS (spike/s) were 4.7 ± 1.0 and 2.8 ± 0.8; d′BOS-CON was 2.11 ± 0.25 and 1.80 ± 0.17. Given this equivalence, we combined these data for analysis in the present study.

In the great majority of cells recorded from both isolate and normal birds (isolates: 72/79 neurons; normal birds: 112/117 neurons), auditory responses were recorded under urethan anesthesia; the other seven isolate and five normal bird neurons were recorded under diazepam sedation. We included both urethan and diazepam data in the analyses because similar properties of auditory responses in the two drug conditions were reported for recordings in the upstream nucleus HVC (Cardin and Schmidt 2003, 2004; Lewicki and Arthur 1996; Margoliash and Fortune 1992; Mooney 2000; Theunissen and Doupe 1998; Volman 1996), and also because we observed no significant difference in auditory responses or song selectivity between the two agents in our preliminary experiments in Area X of normal birds (3 birds, 32 sites with urethan, 33 sites with diazepam, data not shown).

Song analysis

To quantify the difference in temporal structure of isolate song from that of normal song, we compared the number of syllables in song motifs and the syllable durations. In most birds (6 of 10 isolate birds; 7 of 10 normal control birds), syllable boundaries were defined by inspection of song oscillograms as points where the song envelope fell to background level. For the songs of the other seven birds (4 isolate and 3 normal control birds), we developed a more automated and quantitative approach to segmentation: syllable/note boundaries were defined as points where the song's envelope crossed a threshold, which was set as 5–10 times the RMS amplitude of the background noise. Then, silent intervals <2 ms were discarded, and the notes before and after the short intervals were combined into one syllable. For straightforward songs with clearly defined syllables, this method resulted in the same segmentation as the visual inspection. We measured the syllable durations in the first motif of the BOS stimuli that were used in the extracellular recordings in the current study. The number of syllables in a motif was measured for each song and the mean and variance of syllable number across all the different songs in a group (normal or isolate) were calculated.

Results

Songs of isolate birds

Consistent with previous reports (Aamodt et al. 1995; Livingston et al. 2000; Morrison and Nottebohm 1993; Price 1979; Volman and Khanna 1995), all the male zebra finches (n = 10 birds) isolated from conspecific adults by 9–11 days of age developed stereotyped songs composed of several repetitions of an introductory note followed by one or more renditions of a song motif (Fig. 2, A and B). The songs had abnormal acoustic features including broadband noise notes, upward sweeps, an abundance of call-like notes (harmonic stacks), abnormally long and short syllables, and many relatively soft syllables with short neighboring intervals and poorly defined syllable boundaries (Fig. 2B, *). Using our segmentation of the songs (see methods), the distributions of syllable durations of all the isolate songs that were used in the extracellular recordings had significantly greater variance than that of normal birds' songs (Fig. 2C and Table 1; F-test for equality of variance, P < 0.005). The higher variance of syllable duration in isolate birds is consistent with a previous report by Price (1979). Also the number of syllables in a motif was larger in isolate songs than in normal birds' songs. Visual inspection of the spectrograms of the songs showed no sharing of song notes between the songs of isolate birds and of their fathers except for the generic call-like notes. This contrasted with the songs of normally raised birds, which usually contained many song notes copied from the father's song (Fig. 2A, pupil). Thus our isolate birds appeared to have no evidence for an influence of father's song on their song development.

Table 1. Temporal properties of songs from isolate and normal birds.

Isolate Bird Normal Bird
Syllable duration (ms)
 Mean (range) 78.06 (3.7–520.0) 89.8 (13.4–360.0)
 Median 54.25 77.16
 S.D. 76.62** 54.94
Number of syllables
 Mean (range) 10.30 (5–19)* 6.4 (3–12)
 Median 9.5 6.0
 S.D. 4.27 2.67
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Means and SD of syllable durations were calculated from the songs of isolate and normal birds. Asterisks indicate significant differences between isolate's and normal bird's songs: *P < 0.05; **P < 0.005. Comparisons of mean values were made using the unpaired t test (parametric) or the Mann-Whitney U-test (non-parametric). Comparisons of SD were made using the F-test for equality of variance. n = 10 for normal and isolated birds.

Song selectivity of Area X neurons in isolate birds

Extracellular recording of single Area X neurons from isolate birds revealed that these cells had a strong preference for BOS over other song stimuli. We recorded 46 Area X neurons from 10 isolate birds that responded significantly to at least one of the stimuli we played to the birds. One Area X neuron that had a significant inhibitory response to BOS and no significant responses to any other stimuli was excluded from the analyses.

Figure 3 shows a typical neuron with relatively high spontaneous firing that responded substantially more to BOS than to the father's song or to a song of an isolate conspecific (a sibling of the experimental bird). On average, the mean response strength (RS; difference between the firing rate during the stimulus and the background rate) of all the auditory neurons in Area X was significantly greater to BOS than to the other stimulus types we played: father's song, reversed version of BOS (reverse BOS), songs of isolated conspecifics (isolate CON), songs of normally reared conspecifics (normal CON), and heterospecific song (HET) (Fig. 4A, one-way ANOVA and Tukey-Kramer HSD test, P < 0.05). The song selectivity of individual Area X neurons is illustrated with a scatter plot in Fig. 4B where the mean RS to BOS of each cell is plotted against its mean RS to isolate CON. All the points lie above the diagonal line, indicating stronger responses to BOS than to isolate CON; the difference between BOS and isolate CON responses was significant in the majority of individual neurons (30/42, filled circles, paired t-test with Bonferroni correction, α value for significance = 0.01). We also quantified the preferences of individual neurons with a measure of discriminability, d′ (see methods). Neurons were considered to prefer stimulus A over stimulus B if they had d′A-B ≥0.5. The d′BOS-father, d′BOS-reverse BOS, and d′BOS-normal CON of all the Area X neurons recorded are shown in Fig. 4C. For all the stimulus types that we compared with BOS, d′ values were ≥0.5 in most Area X neurons (39/43 cells for d′BOS-father; 42/45 cells for d′BOS-reverse BOS; 38/42 cells for d′BOS-isolate CON; 44/46 cells for d′BOS-normal CON; 42/45 cells for d′BOS-HET). These results indicate strong preferences for BOS over the other stimulus types in Area X neurons of isolate birds.

Fig. 3.

Fig. 3

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Bird's own song (BOS)-selective responses of an Area X neuron recorded from an isolate bird. A: raster plots and peristimulus time histograms (PSTHs) show the greater responses of a single Area X neuron to BOS than to father's song and isolate conspecific song, which here is the bird's brother's song; 20 trials of each song were presented. Bin size of the PSTHs is 30 ms. A raw extracellular recording trace of the first trial of each raster plot is shown at the top. Songs are shown underneath each PSTH as sonograms (frequency vs. time) and oscillograms (amplitude waveform vs. time). B: overlaid waveforms of 100 spike events that were randomly chosen from the BOS recording shown in A. C: histogram of interspike intervals calculated from the spike events in the BOS recording shown in A. Note that the horizontal axis has a logarithmic scale.

Fig. 4.

Fig. 4

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Group data of Area X auditory responses in isolate birds. A: mean response strength (RS) to BOS, father's song, reverse BOS, isolate conspecific song (isolate CON), normal conspecific song (normal CON), and heterospecific song (HET) in all the auditory neurons recorded. One site with significant inhibitory responses to BOS is excluded from the analysis. Error bars denote SE for all the subsequent figures. Asterisks, significant differences after paired comparisons of the mean RS to BOS and the other song stimuli (P < 0.05, one-way ANOVA and Tukey-Kramer HSD test). B: mean RS to BOS of each Area X neuron is plotted against the mean RS to isolate CON. The diagonal line marks where cells would lie if the RS to the 2 stimuli were equal; filled circle, neurons with significantly greater responses to 1 of the stimuli vs. the other (paired t-test with Bonferroni correction, α value for significance = 0.01). C: cumulative distribution of preferences of individual Area X neurons for BOS over the songs of the father (circles), reverse BOS (triangles), and isolate CON (squares) as quantified with d′ values. The cells in the area between the 2 dashed lines (−0.5 < d < 0.5) are considered to respond equally to the songs being compared. D: mean RS to father's song of each neuron is plotted against the mean RS to isolate CON. Conventions are as in B. E: histogram showing the distribution of spontaneous firing rates of all the isolate auditory Area X neurons recorded. F: mean RS to BOS (filled circles), father's song (shaded triangles), and isolate CON (open squares) in individual neurons, plotted against spontaneous firing rate.

Although isolate birds' song did not share notes with their father's song (Fig. 2), this does not rule out the possibility that the isolate birds may have a memory of the father's song that influences the tuning of AFP neurons given the fact that these birds were exposed to their father until 10 days after hatching. However, Area X neurons in isolate birds were showed no selective for their father's song. The group mean RS to father's song was not significantly different from that to other song stimuli except BOS, and most (39/42) neurons showed no significant difference in RS between father's song and isolate CON (Fig. 4D). The highly similar distributions of d′BOS-father and of d′BOS-reverse BOS and d′BOS-isolate CON in Fig. 4C also indicate little selectivity for father's song. Thus Area X neurons in isolate birds had strong preferences for BOS and virtually absent preferences for father's song or other song stimuli, corresponding to their highly limited auditory experience.

Area X is known to have heterogeneous cell populations, containing low-firing rate striatal neurons (spiny neurons), high-firing rate pallidal-like neurons (aspiny fast-firing neurons), presumptive cholinergic neurons, and other small interneurons (Farries and Perkel 2002). Our Area X neurons had spontaneous firing rates in a wide range (3.8–103.3 Hz) and can be divided into two major classes based on spontaneous activity (Fig. 4E). Nonetheless, BOS evoked stronger responses than father's song and isolate CON over the entire range of firing rates (Fig. 4F), suggesting that the different firing rate classes show no obvious difference in song selectivity.

Song selectivity of LMAN neurons in isolate birds

As in Area X, LMAN neurons of isolate birds (n = 29 neurons in 6 birds) had high selectivity for BOS over the other stimulus types (Fig. 5, A–C). Auditory neurons in LMAN had relatively low spontaneous firing rates (2.3 ± 0.4 Hz, range: 0.1–10.7 Hz; see Fig. 5A) and showed significantly greater mean RS to BOS than to other stimuli (Fig. 5D, one-way ANOVA and Tukey-Kramer HSD test, P < 0.05). All the individual neurons had larger mean RS to BOS than to isolate CON (Fig. 5E), and the difference between those responses was significant in the majority of neurons (20/26 cells, filled circles, paired t-test with Bonferroni correction). Many LMAN neurons also showed d′ values ≥0.5 for BOS over the other stimulus types (25/28 cells for d′BOS-father; 27/29 cells for d′BOS-reverse BOS; 24/26 cells for d′BOS-isolate CON; 28/29 cells for d′BOS-normal CON; 25/29 cells for d′BOS-HET, Fig. 5F).

Fig. 5.

Fig. 5

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Song selectivity of LMAN neurons recorded from isolate birds. All conventions are as in Figs. 3 and 4. A: raster plots and PSTHs show the greater response of a single LMAN neuron to BOS than to father's song and isolate conspecific song, which is the bird's brother's song; 20 trials of each song were presented. B: overlaid waveforms of 100 spike events that were randomly chosen from the BOS recording shown in A. C: histogram of interspike invervals calculated from the spike events in the BOS recording shown in A. D: mean RS to BOS, father's song, reverse BOS, isolate CON, normal CON, and HET in all the auditory LMAN neurons recorded. Asterisks, significant differences after paired comparisons of the mean RS to BOS and the other song stimuli (P < 0.05, one-way ANOVA and Tukey-Kramer HSD test). E: mean RS to BOS of each LMAN neuron is plotted against the mean RS to isolate CON. ●, neurons with significantly greater responses to one of the stimuli vs. the other (paired t-test with Bonferroni correction, α value for significance = 0.01). F: cumulative distribution of preferences of individual Area X neurons for BOS over the songs of the father (○), reverse BOS (△), and isolate CON (□), as quantified with d′ values. G: mean RS to father's song of each neuron is plotted against the mean RS to isolate CON.

As with Area X neurons, LMAN neurons in isolate birds were not selective for their father's song. The group mean RS to father's song was not significantly different from that of isolate CON (Fig. 5D), and this was also true for the RS values of individual neurons in all but one neuron (Fig. 5G). The very similar distributions of d′BOS-father and of d′BOS-reverse BOS and d′BOS-CON in Fig. 5F likewise indicate little selectivity for father's song. Thus both LMAN neurons and Area X neurons of isolate birds are strongly and exclusively selective for BOS.

Comparison of isolate song selectivity to that of normal birds

In normal adult birds, neurons in both Area X and LMAN have high selectivity for BOS relative to conspecific and heterospecific songs. Area X neurons differ slightly from those in LMAN, however: they tend to have significant responses to a variety of conspecific songs in addition to BOS (albeit lower than to BOS) and are less likely than LMAN neurons to be significantly inhibited by non-BOS songs (Doupe 1997). In contrast to normal birds, Area X neurons in adult birds raised with a deficit in sensorimotor learning created by denervating the syrinx have abnormally low BOS selectivity due to unusually low BOS responses along with higher than usual responses to conspecific and reversed songs (Solis and Doupe 2000); LMAN in these birds is compromised as well with markedly low auditory responsiveness to any stimuli. Consistent with the idea that disruption of sensory learning due to a lack of tutor song exposure might also affect song selectivity, a previous preliminary report had suggested that AFP neurons in isolate birds were not highly song-selective (Maekawa 1998). However, we found that AFP neurons in isolate birds had BOS selectivity as high as, and in the case of Area X, even higher than that in normal birds.

Figure 6 illustrates this result with a comparison of responsiveness and selectivity of Area X neurons between isolate and normal birds (89 neurons from 23 birds) (combined data from Solis and Doupe 2000 and the present study) (see methods for comparison of the 2 groups). Auditory responses to BOS in isolate birds were as strong as in normal birds (Fig. 6A; two-way ANOVA, P < 0.0001; unpaired t-test with Bonferroni correction, α value for significance = 0.013, P = 0.16). Area X neurons in isolate birds, however, had virtually no responses to reverse BOS, normal CON, and HET, and therefore these responses were much lower than those in normal birds (Fig. 6A, P < 0.001 for reverse BOS; P < 0.0001 for normal CON; P < 0.01 for HET). This pattern of lower responses to non-BOS stimuli but not to BOS in isolate birds was observed over the entire range of spontaneous firing rates in the Area X neurons (Fig. 6, B and C), indicating that the different responsiveness to non-BOS stimuli between isolate and normal birds is not due to different fractions of cell types collected between the two groups.

Fig. 6.

Fig. 6

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BOS selectivity of Area X neurons in isolate birds relative to that found in normal birds. A: histograms compare the mean RS to different stimulus types (BOS, reverse BOS, normal CON, and HET) measured from Area X neurons in isolate birds (■) and normal birds (□). *, significant differences between isolate and normal birds (two-way ANOVA and paired t-test with Bonferroni correction, α value for significance = 0.013, P < 0.01). Isolate birds had significantly smaller mean RS to non-BOS stimuli than normal birds. B: mean RS to BOS in individual neurons from isolate (▲) and normal (□) birds plotted against spontaneous firing rate. C: mean RS to normal CON in individual neurons from isolate and normal birds plotted against spontaneous firing rate. Note that the majority of neurons in normal birds have positive mean RS, whereas most neurons in isolate birds have virtually no responses to CON. D: degree of BOS selectivity in Area X neurons of isolate (■) and normal (□) birds, quantified using the d′ values for BOS over normal CON, reverse BOS, and HET. *, significant differences between isolate and normal birds (two-way ANOVA and paired t-test with Bonferroni correction, α value for significance = 0.017, P < 0.012). The P values for d′BOS-normal CON and d′BOS-HET are 0.021 and 0.13, respectively. E: BOS selectivity quantified using the selectivity index (SI). *, significant differences between isolate and normal birds (two-way ANOVA and paired t-test with Bonferroni correction, α value for significance = 0.017, P < 0.01). The P value for SIBOS-HET is 0.018.

Along with the lower responses to non-BOS songs, we found higher selectivity for BOS relative to other songs in isolate Area X neurons (Fig. 6D): the mean d′BOS-reverse BOS was significantly greater in isolate birds than in normal birds (two-way ANOVA, P < 0.0001; unpaired t-test with Bonferroni correction, α value for significance = 0.017, P < 0.012) and the mean d′BOS-normal CON and the mean d′BOS-HET had the same trend, although the differences were not significant (P = 0.021 and 0.13, respectively). When we quantified the selectivity using a measure that quantifies average responsiveness to one stimulus relative to the other (see methods), the selectivity index (SI), the difference between isolate birds and normal birds was even more evident (Fig. 6E): the mean SIBOS-reverse BOS and SIBOS-CON were significantly greater in isolate birds than in normal birds (two-way ANOVA, P < 0.0001; unpaired t-test with Bonferroni correction, α value for significance = 0.017, P < 0.01 for SIBOS-reverse BOS, P < 0.0001 for SIBOS-CON); the mean SIBOS-HET revealed the same trend but was not significantly different between the two groups (P = 0.018). Together, these results demonstrate that song selectivity in Area X neurons does not require sensory learning of tutor song and may also reflect birds' experience of songs other than BOS and tutor song with normally reared birds showing a broader range of responsiveness to non-BOS stimuli.

LMAN neurons in isolate birds, like those in isolate Area X, had responses to BOS similar in strength to those of normal birds (29 neurons from 10 birds; Fig. 7, A and B). However, in contrast to Area X, responses to the other songs in isolate LMAN neurons were not lower than that in normal birds: normal LMAN neurons were already sharply tuned to BOS with virtually no excitatory responses to non-BOS stimuli and thus were similar to isolate LMAN neurons in this respect (Fig. 7, A and C). Because of this response property in LMAN of normal birds, BOS selectivity relative to the other song types was not higher in isolate birds than in normal birds: the mean d′ or SI values for BOS relative to the other song stimuli (reverse BOS, normal CON, or HET) in LMAN were not significantly different between the two groups of birds (Fig. 7, D and E). Thus deprivation of conspecific song experience had little effect on song selectivity in LMAN neurons, which contrasts with higher selectivity in Area X neurons.

Fig. 7.

Fig. 7

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BOS selectivity of LMAN neurons in isolate birds relative to that found in normal birds. All conventions are as in Fig. 6. A: histograms of the mean RS to different stimulus types in LMAN neurons of isolate and normal birds. No significant difference was found in mean RS between isolate and normal birds. B and C: mean RS to BOS (B) and normal CON (C) in individual neurons from isolate (▲) and normal (□) birds plotted against spontaneous firing rate. The distributions of neurons from isolate and normal birds overlap for both BOS and normal CON at all firing rates. D and E: degree of BOS selectivity of LMAN neurons in isolate and normal birds, quantified using the d′ values (D) and selectivity index (E). No significant difference in BOS selectivity relative to any other stimulus types was found between isolate and normal birds.

In LMAN of adult birds that were raised with a denervated syrinx and thus did not successfully mimic their tutor song, auditory neurons were encountered at a much lower frequency than in normal birds (Solis and Doupe 2000). In isolate birds, however, auditory responsiveness of LMAN neurons was not compromised and was as high as that of normal birds: of the 9 isolate birds in which LMAN was sampled, auditory responses were obtained from 6 birds (67.0%), comparable to 4/8 normal birds (50.0%; here we used only data collected for the current study). Of the 52 LMAN neurons recorded in the isolate birds, 29 neurons yielded auditory responses (55.8%). This frequency at which we encountered auditory neurons in isolate birds was not significantly different from that in normal birds, where 15/25 neurons showed auditory responses (60.0%, χ2 test, P = 0.81). Together with the selectivity data, these results support the idea that normal auditory selectivity of LMAN neurons can develop without sensory learning of tutor song.

Discussion

This study demonstrates that sensory learning of tutor song is not obligatory for the emergence of song selectivity in AFP neurons. In birds raised in isolation from adult conspecific song, AFP neurons developed selectivity for BOS relative to other song stimuli as high as that in normal birds, and in Area X higher than in normal birds, due to normal BOS responses and abnormally weak responses to non-BOS stimuli. Together with the existing evidence for the dependence of song neural selectivity on song sensorimotor learning, this result stresses the critical role of sensorimotor learning of BOS in shaping song-selective neurons. Moreover, our data suggest that a lack of conspecific experience can even sharpen BOS selectivity.

High BOS selectivity of AFP neurons in isolate birds and possible functions of AFP song selectivity

A variety of evidence suggests that AFP song-selective neurons can independently develop sensitivity to both BOS and tutor song, at least transiently. At PHD 60, AFP neurons show stronger and more temporally sensitive responses to both these stimuli than to other conspecific songs (Solis and Doupe 1997; Yazaki-Sugiyama and Mooney 2004), even when BOS has been manipulated to be very different from the tutor song (Solis and Doupe 1999). An obligatory requirement for tutor exposure and for subsequent matching of BOS to the sensory memory of tutor song was further suggested by the impaired song selectivity evident both in preliminary experiments in birds raised in isolation (Maekawa 1998) and in birds chronically prevented from matching their song to the tutor song (Solis and Doupe 2000). Our results clearly demonstrate, however, that despite the presumed lack of an acquired song template in isolate birds, maximal development of BOS selectivity does not require sensory learning of tutor song. The findings here provide further evidence that BOS selectivity is strongly shaped by the bird's experience of its own song during learning and support the idea that song-selective neurons represent an auditory version of the bird's current song (Margoliash 1983; Nick and Konishi 2005; Solis and Doupe 1997, 1999; Volman 1993; Yazaki-Sugiyama and Mooney 2004).

Our results also speak to several further functions that have been suggested for song-selective neurons. For one, the dual tuning to BOS and tutor song at PHD 60 and the compromised responses of AFP neurons in adult birds raised with a denervated syrinx (Solis and Doupe 2000) raised the possibility that AFP neurons are important in the comparison of BOS to the tutor template: that is, they might develop strong BOS-selective responses only when auditory feedback of the bird's own vocalizations is close enough to the tutor song target to evoke activation of both BOS- and tutor-tuned inputs. In this respect, AFP song-selective neurons may be comparable with their counterparts in mammalian basal ganglia-cortical circuits, which have been shown to acquire responses predictive of or dependent on reward (for recent reviews, see Hikosaka et al. 2006; Salzman et al. 2005; Schultz et al. 2003). Isolate birds are also thought to match their vocalizations to a template, one that is innate and species-specific (Adret 2004; Konishi 1965; Marler 1997). Thus although isolate birds do not learn any songs during the sensory phase, they may nonetheless experience successful matching to a song template during sensorimotor learning, which could result in high BOS selectivity. To be certain of this, however, it would be necessary to know more about the nature of the innate template.

A second possible function of song-selective neurons is that they represent a neural mapping between auditory feedback and vocal motor output, which may be necessary for song learning. This has been suggested by accumulating evidence that song selectivity is not a purely sensory property but is found of necessity in neurons with both sensory and motorrelated responses. A specific relationship between sensory and motor responses that may reflect such a sensorimotor mapping has been described in the premotor song nucleus RA (the robust nucleus of the arcopallium), where playback of a set of syllables evokes a song-selective firing pattern that resembles the premotor activity for the next syllable in the song (Dave and Margoliash 2000). The AFP, like mammalian corticalbasal ganglia circuitry (Graybiel et al. 1994; Hikosaka et al. 2000), has both auditory responses and premotor activity (Hessler and Doupe 1999a,b; Leonardo 2004), and thus could also be involved in developing a sensorimotor map during learning. Syringeally denervated birds may have impaired AFP song selectivity because they cannot create a reliable relationship between motor commands and auditory feedback. In contrast, isolate birds are able both to control and to hear their vocalizations as normal birds do, so that they should have normal sensorimotor mapping, which may explain their strong BOS selectivity.

Higher BOS selectivity of AFP neurons in isolate birds and effects of sensory experience

Not only was BOS selectivity in isolate AFP neurons not compromised by tutor song deprivation, it was in fact higher than in normal birds in Area X, which includes both striatal and pallidal neurons. This increased selectivity was the result of weaker responses to non-BOS song stimuli in isolate birds compared with controls, whereas BOS responses did not differ between the two groups. This could reflect the unusual and variable structure of isolate songs, which may result in lower overall acoustic similarity both between isolate and normal songs and among isolate birds than among normal songs. Such lower acoustic similarity may have weakened conspecific responses of Area X neurons tuned to isolate BOS and thus increased neural BOS selectivity relative to conspecific songs.

Alternatively, the increased selectivity of isolate Area X neurons may reflect their different, highly impoverished experience of conspecific song. Isolate birds were raised in sound-attenuating chambers without hearing any other adult zebra finch songs, whereas normal birds were raised in a colony where they could hear their siblings and other conspecifics. Thus the isolate birds' sensory experience of song was narrowly focused on BOS, and this may have decreased their responses to non-BOS song stimuli. If so, it suggests that the responsiveness of song neurons in normal birds includes a component shaped by the sounds of other birds in addition to BOS and tutor song. Examination of song selectivity in birds exposed to a tutor (and thus with acoustically normal BOS) but otherwise in isolation from conspecific song might be informative in distinguishing effects of passive sensory experience of others from effects of sensory experience of BOS on Area X neuron responsiveness.

Unlike Area X, responses to non-BOS song stimuli in the pallial nucleus LMAN of isolate birds were not different from those of normal birds, and thus BOS selectivity was not different between the two experimental groups. In general, LMAN neurons of normal birds are more narrowly responsive to BOS and much less likely than Area X neurons to show excitatory responses to non-BOS stimuli (Doupe 1997). Our result that conspecific song deprivation has differential effects on neurons in Area X and its pallial target LMAN appears to reflect this different responsiveness to conspecific songs between the two nuclei in normal birds: the already narrowly BOS-tuned LMAN neurons would be less susceptible to isolation from conspecific songs than the more broadly tuned Area X neurons.

The neural dynamics underlying the differential conspecific responsiveness between nuclei in this pallial-basal ganglia circuit remain unclear. The differences may reflect changes in AFP firing properties from Area X to LMAN due to strong inhibitory synapses in the thalamic nucleus DLM (the medial part of the dorsolateral anterior thalamic nucleus), where a postinhibitory rebound spike is thought to participate in the synaptic transmission of auditory responses (Luo and Perkel 1999; Person and Perkel 2005). The large difference in spontaneous firing rate between most LMAN neurons and the high firing Area X neurons could also contribute to the different conspecific responsiveness between the two nuclei. Because LMAN neurons have very low spontaneous activity, only strong synaptic inputs such as BOS responses may be able to evoke suprathreshold postsynaptic potentials and subsequent spike firing.

The functional role of the differential conspecific responsiveness and the resulting differences in BOS selectivity between Area X and LMAN is a matter for speculation. The stronger conspecific responsiveness of Area X neurons could be useful for a comparison between conspecific song and BOS, which has been hypothesized to involve the AFP (Scharff et al. 1998). Alternatively the very high BOS selectivity seen in LMAN may simply be emerging gradually along the AFP circuit. To understand the function of the different degrees of song selectivity in AFP nuclei, as well as the function of song selectivity in song learning more generally, further studies of song auditory responses in relation to premotor song activity in awake birds will be required.

Effects of adult song deprivation on the song auditory and vocal control systems may differ

Song selectivity does not originate in the AFP—it is already robustly present in HVC (Margoliash 1983; Margoliash and Fortune 1992; Mooney 2000; Nick and Konishi 2005), and even in the interfacial nucleus of the nidopallium (NIf), although less strongly (Coleman and Mooney 2004; Janata and Margoliash 1999). Selectivity likely emerges gradually through a hierarchy of telencephalic auditory and early song system areas. The primary auditory area Field L is the main structure transmitting auditory information from the thalamus to this hierarchy (Fortune and Margoliash 1995; Karten 1968; Katz and Gurney 1981; Vates et al. 1996; Wild et al. 1993). Our results from the very high-level song neurons of the AFP raise the question of whether a similar resilience to tutor and conspecific song deprivation exists at all levels of this network including Field L. Strikingly, studies of Field L in European starlings deprived of adult song in early life (Cousillas et al. 2004) show marked effects: Field L had highly abnormal properties, including altered tonotopy and a large nonselective auditory area. This result contrasts strongly with the normal BOS selectivity of AFP neurons observed in isolate zebra finches, and raises the possibility that isolate zebra finches have the same abnormalities in Field L neurons as isolate starlings do but nonetheless develop normal song selectivity. Given the importance of sensorimotor learning to shaping song-selective neurons, song-selective neurons in the AFP and elsewhere may be able to emerge using less organized auditory information, as long as this information relates systematically to song output.

Consistent with possible abnormalities in Field L, isolate zebra finches have deficits in processing of sounds (Sturdy et al. 2001). In contrast, disruption of AFP function has been shown to impair discrimination between BOS and conspecific songs but not between conspecific and heterospecific songs (Scharff et al. 1998). This suggests that the AFP song neurons may be specialized to monitor the bird's own vocalizations. If song-selective neurons function in such perception, our results suggest that isolate birds would have intact perception of self versus other. Investigating the joint changes in Field L and the song system in response to altered sensory experience should provide insights into the hierarchical emergence of song selectivity and into the function of both these sets of areas in auditory perception and song learning.

Acknowledgments

Grants: This work was supported by National Institutes of Health Grants MH-055987 and NS-34835 to A. J. Doupe and Japan Society for the Promotion of Science for Young Scientists Research Fellowship 7202 to S. Kojima.

References

  1. Aamodt SM, Nordeen EJ, Nordeen KW. Early isolation from conspecific song does not affect the normal developmental decline of N-methyl-d-aspartate receptor binding in an avian song nucleus. J Neurobiol. 1995;27:76–84. doi: 10.1002/neu.480270108. [DOI] [PubMed] [Google Scholar]
  2. Adret P. In search of the song template. Ann NY Acad Sci. 2004;1016:303–324. doi: 10.1196/annals.1298.005. [DOI] [PubMed] [Google Scholar]
  3. Basham ME, Nordeen EJ, Nordeen KW. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch. Neurobiol Learning Mem. 1996;66:295–304. doi: 10.1006/nlme.1996.0071. [DOI] [PubMed] [Google Scholar]
  4. Bottjer SW, Miesner EA, Arnold AP. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science. 1984;224:901–903. doi: 10.1126/science.6719123. [DOI] [PubMed] [Google Scholar]
  5. Cardin JA, Schmidt MF. Song system auditory responses are stable and highly tuned during sedation, rapidly modulated and unselective during wakefulness, and suppressed by arousal. J Neurophysiol. 2003;90:2884–2899. doi: 10.1152/jn.00391.2003. [DOI] [PubMed] [Google Scholar]
  6. Cardin JA, Schmidt MF. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J Neurophysiol. 2004;91:2148–2163. doi: 10.1152/jn.00918.2003. [DOI] [PubMed] [Google Scholar]
  7. Coleman MJ, Mooney R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J Neurosci. 2004;24:7251–7265. doi: 10.1523/JNEUROSCI.0947-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cousillas H, Richard JP, Mathelier M, Henry L, George I, Hausberger M. Experience-dependent neuronal specialization and functional organization in the central auditory area of a songbird. Eur J Neurosci. 2004;19:3343–3352. doi: 10.1111/j.0953-816X.2004.03376.x. [DOI] [PubMed] [Google Scholar]
  9. Dave AS, Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science. 2000;290:812–816. doi: 10.1126/science.290.5492.812. [DOI] [PubMed] [Google Scholar]
  10. Doupe AJ. Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J Neurosci. 1997;17:1147–1167. doi: 10.1523/JNEUROSCI.17-03-01147.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doupe AJ, Konishi M. Song-selective auditory circuits in the vocal control system of the zebra finch. Proc Natl Acad Sci USA. 1991;88:11339–11343. doi: 10.1073/pnas.88.24.11339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Doupe AJ, Kuhl PK. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci. 1999;22:567–631. doi: 10.1146/annurev.neuro.22.1.567. [DOI] [PubMed] [Google Scholar]
  13. Eales LA. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim Behav. 1985;33:1293–1300. [Google Scholar]
  14. Eales LA. Song learning in female-raised zebra finches: another look at the sensitive phase. Anim Behav. 1987;35:1356–1365. [Google Scholar]
  15. Eales LA. The influences of visual and vocal interaction on song learning in zebra finches. Anim Behav. 1989;37:507–508. [Google Scholar]
  16. Farries MA, Perkel DJ. A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J Neurosci. 2002;22:3776–3787. doi: 10.1523/JNEUROSCI.22-09-03776.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fortune ES, Margoliash D. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata) J Comp Neurol. 1995;360:413–441. doi: 10.1002/cne.903600305. [DOI] [PubMed] [Google Scholar]
  18. Graybiel AM, Aosaki T, Flaherty AW, Kimura M. The basal ganglia and adaptive motor control. Science. 1994;265:1826–1831. doi: 10.1126/science.8091209. [DOI] [PubMed] [Google Scholar]
  19. Green DM, Swets JA. Signal Detection Theory and Psychophysics. New York: Wiley; 1966. [Google Scholar]
  20. Hessler NA, Doupe AJ. Singing-related neural activity in a dorsal forebrainbasal ganglia circuit of adult zebra finches. J Neurosci. 1999a;19:10461–10481. doi: 10.1523/JNEUROSCI.19-23-10461.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hessler NA, Doupe AJ. Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci. 1999b;2:209–211. doi: 10.1038/6306. [DOI] [PubMed] [Google Scholar]
  22. Hikosaka O, Nakamura K, Nakahara H. Basal ganglia orient eyes to reward. J Neurophysiol. 2006;95:567–584. doi: 10.1152/jn.00458.2005. [DOI] [PubMed] [Google Scholar]
  23. Hikosaka O, Takikawa Y, Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev. 2000;80:953–978. doi: 10.1152/physrev.2000.80.3.953. [DOI] [PubMed] [Google Scholar]
  24. Janata P, Margoliash D. Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci. 1999;19:5108–5118. doi: 10.1523/JNEUROSCI.19-12-05108.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Karten HJ. The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res. 1968;11:134–153. doi: 10.1016/0006-8993(68)90078-4. [DOI] [PubMed] [Google Scholar]
  26. Katz LC, Gurney ME. Auditory responses in the zebra finch's motor system for song. Brain Res. 1981;211:192–197. doi: 10.1016/0006-8993(81)91073-8. [DOI] [PubMed] [Google Scholar]
  27. Konishi M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Zeitsch Tierpsychol. 1965;22:770–783. [PubMed] [Google Scholar]
  28. Leonardo A. Experimental test of the birdsong error-correction model. Proc Natl Acad Sci USA. 2004;101:16935–16940. doi: 10.1073/pnas.0407870101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lewicki MS. Bayesian modelling and classification of neural signals. Neural Comput. 1994;6:1005–1030. [Google Scholar]
  30. Lewicki MS, Arthur BJ. Hierarchical organization of auditory temporal context sensitivity. J Neurosci. 1996;16:6987–6998. doi: 10.1523/JNEUROSCI.16-21-06987.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Livingston FS, White SA, Mooney R. Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches. Nat Neurosci. 2000;3:482–488. doi: 10.1038/74857. [DOI] [PubMed] [Google Scholar]
  32. Luo M, Perkel DJ. A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. J Neurosci. 1999;19:6700–6711. doi: 10.1523/JNEUROSCI.19-15-06700.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Maekawa M. Response selectivity of neurons in the forebrain song control nucleus of the zebra finch reared in abnormal acoustic environment. Soc Neurosci Abstr. 1998;23:78.10. [Google Scholar]
  34. Margoliash D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci. 1983;3:1039–1057. doi: 10.1523/JNEUROSCI.03-05-01039.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Margoliash D, Fortune ES. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J Neurosci. 1992;12:4309–4326. doi: 10.1523/JNEUROSCI.12-11-04309.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Marler P. Three models of song learning: evidence from behavior. J Neurobiol. 1997;33:501–516. [PubMed] [Google Scholar]
  37. Marler P, Tamura M. Culturally transmitted patterns of vocal behavior in sparrows. Science. 1964;146:1483–1486. doi: 10.1126/science.146.3650.1483. [DOI] [PubMed] [Google Scholar]
  38. Mooney R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J Neurosci. 2000;20:5420–5436. doi: 10.1523/JNEUROSCI.20-14-05420.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Morrison RG, Nottebohm F. Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. J Neurobiol. 1993;24:1045–1064. doi: 10.1002/neu.480240805. [DOI] [PubMed] [Google Scholar]
  40. Nick TA, Konishi M. Neural auditory selectivity develops in parallel with song. J Neurobiol. 2005;62:469–481. doi: 10.1002/neu.20115. [DOI] [PubMed] [Google Scholar]
  41. Person AL, Perkel DJ. Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron. 2005;46:129–140. doi: 10.1016/j.neuron.2004.12.057. [DOI] [PubMed] [Google Scholar]
  42. Price PH. Developmental determinants of structure in zebra finch song. J Comp Phys Psych. 1979;93:268–277. [Google Scholar]
  43. Roy A, Mooney R. Auditory plasticity in a basal ganglia-forebrain pathway during decrystallization of adult birdsong. J Neurosci. 2007;27:6374–6387. doi: 10.1523/JNEUROSCI.0894-07.2007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Salzman CD, Belova MA, Paton JJ. Beetles, boxes and brain cells: neural mechanisms underlying valuation and learning. Curr Opin Neurobiol. 2005;15:721–729. doi: 10.1016/j.conb.2005.10.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Scharff C, Nottebohm F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J Neurosci. 1991;11:2896–2913. doi: 10.1523/JNEUROSCI.11-09-02896.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Scharff C, Nottebohm F, Cynx J. Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. J Neurobiol. 1998;36:81–90. [PubMed] [Google Scholar]
  47. Schultz W, Tremblay L, Hollerman JR. Changes in behavior-related neuronal activity in the striatum during learning. Trends Neurosci. 2003;26:321–328. doi: 10.1016/S0166-2236(03)00122-X. [DOI] [PubMed] [Google Scholar]
  48. Sohrabji F, Nordeen EJ, Nordeen KW. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav Neural Biol. 1990;53:51–63. doi: 10.1016/0163-1047(90)90797-a. [DOI] [PubMed] [Google Scholar]
  49. Solis MM, Doupe AJ. Anterior forebrain neurons develop selectivity by an intermediate stage of birdsong learning. J Neurosci. 1997;17:6447–6462. doi: 10.1523/JNEUROSCI.17-16-06447.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Solis MM, Doupe AJ. Contributions of tutor and bird's own song experience to neural selectivity in the songbird anterior forebrain. J Neurosci. 1999;19:4559–4584. doi: 10.1523/JNEUROSCI.19-11-04559.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Solis MM, Doupe AJ. Compromised neural selectivity for song in birds with impaired sensorimotor learning. Neuron. 2000;25:109–121. doi: 10.1016/s0896-6273(00)80875-2. [DOI] [PubMed] [Google Scholar]
  52. Sturdy CB, Phillmore LS, Sartor JJ, Weisman RG. Reduced social contact causes auditory perceptual deficits in zebra finces, Taeniopygia guttata. Anim Behav. 2001;62:1207–1218. [Google Scholar]
  53. Theunissen FE, Doupe AJ. Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. J Neurosci. 1998;18:3786–3802. doi: 10.1523/JNEUROSCI.18-10-03786.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Vates GE, Broome BM, Mello CV, Nottebohm F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taeniopygia guttata) J Comp Neurol. 1996;366:613–642. doi: 10.1002/(SICI)1096-9861(19960318)366:4<613::AID-CNE5>3.0.CO;2-7. [DOI] [PubMed] [Google Scholar]
  55. Vates GE, Vicario DS, Nottebohm F. Reafferent thalamo-“cortical” loops in the song system of oscine songbirds. J Comp Neurol. 1997;380:275–290. [PubMed] [Google Scholar]
  56. Vicario DS, Yohay KH. Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch. J Neurobiol. 1993;24:488–505. doi: 10.1002/neu.480240407. [DOI] [PubMed] [Google Scholar]
  57. Volman SF. Development of neural selectivity for birdsong during vocal learning. J Neurosci. 1993;13:4737–4747. doi: 10.1523/JNEUROSCI.13-11-04737.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Volman SF. Quantitative assessment of song-selectivity in the zebra finch “high vocal center”. J Comp Physiol [A] 1996;178:849–862. doi: 10.1007/BF00225832. [DOI] [PubMed] [Google Scholar]
  59. Volman SF, Khanna H. Convergence of untutored song in group-reared zebra finches (Taeniopygia guttata) J Comp Psychol. 1995;109:211–221. doi: 10.1037/0735-7036.109.3.211. [DOI] [PubMed] [Google Scholar]
  60. Wild JM, Karten HJ, Frost BJ. Connections of the auditory forebrain in the pigeon (Columbia livia) J Comp Neurol. 1993;337:32–62. doi: 10.1002/cne.903370103. [DOI] [PubMed] [Google Scholar]
  61. Yazaki-Sugiyama Y, Mooney R. Sequential learning from multiple tutors and serial retuning of auditory neurons in a brain area important to birdsong learning. J Neurophysiol. 2004;92:2771–2788. doi: 10.1152/jn.00690.2004. [DOI] [PubMed] [Google Scholar]

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