Song selectivity in the pallial-basal ganglia song circuit of zebra finches raised without tutor song exposure

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.

Fig. 1

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.

Fig. 2

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.

Fig. 3

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

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.

Fig. 5

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.

Fig. 6

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 SI_BOS-HET is 0.018.

Fig. 7

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.