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A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour

Nature volume 563, pages 117–120 (2018)Cite this article

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Abstract

The cultural transmission of behaviour depends on the ability of the pupil to identify and emulate an appropriate tutor1,2,3,4. How the brain of the pupil detects a suitable tutor and encodes the behaviour of the tutor is largely unknown. Juvenile zebra finches readily copy the songs of the adult tutors that they interact with, but not the songs that they listen to passively through a speaker5,6, indicating that social cues generated by the tutor facilitate song imitation. Here we show that neurons in the midbrain periaqueductal grey of juvenile finches are selectively excited by a singing tutor and—by releasing dopamine in the cortical song nucleus HVC—help to encode the song representations of the tutor used for vocal copying. Blocking dopamine signalling in the HVC of the pupil during tutoring blocked copying, whereas pairing stimulation of periaqueductal grey terminals in the HVC with a song played through a speaker was sufficient to drive copying. Exposure to a singing tutor triggered the rapid emergence of responses to the tutor song in the HVC of the pupil and a rapid increase in the complexity of the song of the pupil, an early signature of song copying7,8. These findings reveal that a dopaminergic mesocortical circuit detects the presence of a tutor and helps to encode the performance of the tutor, facilitating the cultural transmission of vocal behaviour.

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Fig. 1: Recordings of PAG activity.
Fig. 2: Imaging of DA in the HVC.
Fig. 3: Chemical blockade and optogenetic activation of DA signalling in HVC.
Fig. 4: Changes in HVC activity and song features after live tutoring.

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Data availability

The datasets generated and analysed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank J. Hatfield for constructing AAV2/9-CAG-GRABDA1h; S. Nowicki, S. Peters, C. Sturdy, F. Wang and S. Soderling for critical discussion and for reading earlier versions of this manuscript. This work was supported by JSPS Postdoctoral Fellowship for Research Abroad (M.T.), the National Basic Research Program of China 973 Program Grant 2015CB856402 (Y.L.), the American BRAIN Initiative project 1U01NS103558-01 (Y.L.), NIH Grant 1R01-NS-099288 (R.M.) and NSF IOS-1354962 (R.M.).

Reviewer information

Nature thanks O. Tchernichovski, L. Zweifel and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Duke University, Durham, NC, USA

    Masashi Tanaka & Richard Mooney

  2. State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China

    Fangmiao Sun & Yulong Li

  3. PKU-IDG/McGovern Institute for Brain Research, Beijing, China

    Fangmiao Sun & Yulong Li

  4. Peking-Tsinghua Center for Life Sciences, Beijing, China

    Yulong Li

  5. Graduate School of Life Sciences, Tohoku University, Sendai, Japan

    Masashi Tanaka

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  1. Masashi Tanaka
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Contributions

M.T. and R.M. designed experiments. F.S. and Y.L. developed DA sensors. M.T. performed experiments and analysed data. M.T. and R.M. wrote the manuscript.

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Correspondence to Richard Mooney.

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F.S. and Y.L. have filed patent applications of which the value might be affected by this publication.

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Extended data figures and tables

Extended Data Fig. 1 Distribution of HVC-projecting neurons and Area X-projecting neurons in the midbrain.

a, From left to right, a maximum-projected image of serial sagittal sections visualized with a confocal microscope, showing a lateral part of the PAG (lPAG) (approximately 1.0 mm lateral of the midline), a medial part of the PAG (mPAG, approximately 0.2 mm lateral of the midline), SNc (approximately 1.2 mm lateral of the midline) and VTA (approximately 0.2 mm lateral of the midline), each of which was labelled with dextran injected into the HVC (green) and an antibody against TH (pseudo-coloured magenta). Similar results were obtained in four independently repeated experiments. R, rostral; V, ventral. b, Proportion of HVC-projecting neurons in the PAG and VTA/SNc. χ2 test; \({\chi }_{1}^{2}=406.54\), P < 0.001, n = 4 hemispheres from three birds. c, Proportion of TH+ neurons in HVC-projecting neuron subsets in the PAG and the VTA/SNc. χ2 test; \({\chi }_{1}^{2}=204.62\), P < 0.001, n = 4 hemispheres from three birds. d, From left to right, a maximum-projected image of serial sagittal sections visualized with a confocal microscope, showing the PAG (approximately 0.6 mm lateral of the midline), SNc (approximately 0.6 mm lateral of the midline) and VTA (approximately 0.2 mm lateral), each of which was labelled with dextran injected into Area X (green) and an antibody against TH (pseudo-coloured magenta). Similar results were obtained in three independently repeated experiments. e, Proportion of double-labelled neurons (dextran and TH) in PAG and SNc/VTA in birds that received injection of dextran into Area X. χ2 test; \({\chi }_{1}^{2}=493.92\), P < 0.001, n = 3 hemispheres from three birds. f, Proportion of Area-X-projecting neurons in the PAG and VTA/SNc. χ2 test; \({\chi }_{1}^{2}=472.07\), P < 0.001, n = 3 hemispheres from three birds. g, Proportion of TH+ neurons in Area-X-projecting neuron subsets in the PAG and VTA/SNc. χ2 test; \({\chi }_{1}^{2}=55.14\), P < 0.001, n = 3 hemispheres from three birds. Data are mean ± s.e.m.

Extended Data Fig. 2 Juvenile male PAG activity in response to song playback in the presence of a female bird and live songs of a male bird.

a, Tutor-naive juvenile male finch PAG activity aligned to the onset of 35 presentations of song playback in the presence of an adult female bird. Top, averaged sound spectrogram. Middle, spike raster plot. Bottom, mean firing rate. Blue vertical bar marks song onset. b, Mean firing rate of neurons in the juvenile PAG during presentation of song playback in the presence of an adult female bird, normalized to baseline firing rate. Student’s two-sided paired t-test; t7 = 0.620, P = 0.555; n = 8 neurons from two birds. c, Neuron activity in the PAG of the juvenile during a live tutor song bout. Top, sound spectrogram. Middle, voltage recording. Bottom, firing rate. Blue bar, song motif. d, Juvenile PAG unit activity aligned to the offset (blue vertical bar) of the song bouts of a live tutor (red bar, live song), shown as in a. e, A maximum-projected image of serial sagittal sections visualized with a confocal microscope, showing the site of tetrode recordings in the PAG (around 0.8 mm lateral of the midline). f, Juvenile PAG unit activity aligned to the onset (blue vertical bar) of the song motifs (syllables denoted by black horizontal bars) of a live tutor, shown as in a. Note that the tutor often sings multiple motifs within a single bout, thus some motifs precede (and follow) the alignment time. Data are mean ± s.e.m.

Extended Data Fig. 3 Effects of 6-OHDA injection into the HVC on DA fibres in the HVC and surrounding regions and on noradrenergic/adrenergic fibres in the HVC.

a, From left to right, a maximum-projected image of serial sagittal sections visualized with a confocal microscope, showing the HVC with TH immunolabelling (approximately 2.4 mm lateral of the midline), the HVC shelf and nidopallium caudolateral (NCL) just ventral of the HVC with TH immunolabelling (approximately 2.4 mm lateral of the midline), and the HVC with DBH immunolabelling (approximately 2.4 mm lateral of the midline) in control birds, which received an injection of vehicle into the HVC. Similar results were obtained in five independently repeated experiments (orientation is similar to b). b, From left to right, a maximum-projected image of serial sagittal sections visualized with a confocal microscope, showing the HVC with TH immunolabelling (approximately 2.4 mm lateral of the midline), the HVC shelf and NCL just ventral to the HVC with TH immunolabelling (approximately 2.4 mm lateral of the midline), and the HVC with DBH immunolabelling (approximately 2.4 mm lateral of the midline) in birds that received an injection of 6-OHDA into the HVC two days before tissue fixation. Similar results were obtained in four independently repeated experiments. D, dorsal; R, rostral. c, Density of TH+ fibres in the HVC of control birds (n = 5 hemispheres from three birds) was higher than the density in birds that received injections of 6-OHDA two days before fixation (Tukey–Kramer test; P = 0.002; n = 4 hemispheres from two birds), and also higher than the density in birds that received injections of 6-OHDA around 60 days before fixation, as in Fig. 3b, c (Tukey–Kramer test; P = 0.002; n = 6 hemispheres from four birds). d, Density of TH+ fibres in the HVC shelf and NCL in control birds (n = 5 hemispheres from three birds), birds that received an injection of 6-OHDA two days before fixation (n = 4 hemispheres from two birds), and birds that received an injection of 6-OHDA around 60 days before fixation, as in Fig. 3b, c (n = 6 hemispheres from four birds). e, Density of DBH+ fibres in HVC in control birds (n = 4 hemispheres from two birds) and birds that received an injection of 6-OHDA two days before injection (n = 4 hemispheres from two birds) was not significantly different. Student’s two-sided unpaired t-test; t7 = 0.379, P = 0.716. Data are mean ± s.e.m.

Extended Data Fig. 4 Ablation of DA terminals in the HVC did not affect song rate but decreased song imitation to the level of birds raised in isolation from a tutor.

a, The song rates of 90-day-old birds that received an injection of vehicle (n = 7), 6-OHDA at around 30 days of age (n = 7), and 6-OHDA at around 45 days of age (n = 6) were not significantly different. One-way ANOVA; F2,17 = 0.283, P = 0.757. b, Spectrograms from a 90-day-old bird that was raised in isolation from a tutor (top) and from a 90-day-old bird that was normally tutored but received an injection of 6-OHDA into the HVC at 30 days of age (bottom). c, Similarity of 90-day-old untutored (Isolated) adult zebra finch songs to songs of unrelated adult zebra finches that had been normally tutored (n = 3) was not significantly different from tutor song similarity of 90-day-old pupils that received an injection of 6-OHDA into the HVC at approximately 30 days of age (n = 7; Student’s two-sided unpaired t-test; t9 = 0.013, P = 0.990), but was significantly different from tutor song similarity of 90-day-old pupils that received an injection of vehicle at around 30 days of age (n = 7; Student’s two-sided unpaired t-test; t9 = 3.028, P = 0.014), or from tutor song similarity of 90-day-old pupils that received an injection of 6-OHDA into the HVC at around 45 days of age (n = 6; Student’s two-sided unpaired t-test; t8 = 3.314, P = 0.011). The song data from birds injected with 6-OHDA into the HVC at around 30 days of age is the same as in Fig. 3e; song similarity data from birds injected into the HVC with vehicle at around 30 days of age or 6-OHDA at around 45 days of age are not shown here but are shown in Fig. 3f. Data are mean ± s.e.m.

Extended Data Fig. 5 Effects of infusing DA blockers into either the HVC or CM, or infusing muscimol into the PAG on song copying.

a, Schematic showing infusion of DA blockers into the HVC. b, From top to bottom, sound spectrograms of a song of a tutor bird, a 90-day-old pupil that received an infusion of vehicle during tutoring sessions, a 90-day-old pupil that received infusions of both D1- and D2-type DA blockers (DA blockers) during tutoring sessions, a 90-day-old pupil bird that received an infusion of a D1-type blocker during tutoring sessions, and a 90-day-old pupil that received infusions of both D1- and D2-type DA blockers after tutoring sessions. c, Developmental changes in tutor song similarity of pupils that received infusions of both D1- and D2-type DA blockers (DA blockers) into the HVC during tutoring sessions (top, n = 5), a D1-type blocker into HVC during tutoring sessions (middle, n = 5), or DA blockers into the HVC immediately after tutoring sessions (bottom, n = 5). Asterisks indicate P < 0.050; Tukey–Kramer test (see Methods). d, Proportion of time that juvenile birds attended to the tutor during tutoring sessions was not significantly different between birds that received infusions of vehicle (n = 3) or DA blockers into HVC (n = 4) (Tukey–Kramer test; P = 0.871). By contrast, the attention time of juvenile birds that received infusion of muscimol into the PAG (n = 3) was lower than that of control birds (Tukey–Kramer test; P = 0.001) and that of birds that received an injection of DA blockers into the HVC (Tukey–Kramer test; P < 0.001). e, Singing rates of the tutor bird to pupils that received vehicle into the HVC (n = 5) were not different from that to pupils that received injection of DA blockers into the HVC (n = 5) or muscimol into the PAG (n = 3). One-way ANOVA; F2,10 = 0.776, P = 0.486. f, Schematic showing infusion of muscimol into the PAG. g, A sound spectrogram of a song of a 90-day-old pupil that received an infusion of muscimol into the PAG during tutoring sessions. A sound spectrogram of the tutor song is shown in b. h, Tutor song similarity of pupil birds that received infusion of vehicle into the HVC and birds that received an infusion of muscimol blockers into PAG were significantly different (Tukey–Kramer test; vehicle, n = 5; muscimol into the PAG, n = 3; at 90 days of age, P = 0.007). i, Schematic showing infusion of DA blockers into the CM (DA blockers possibly diffused into both the medial and lateral CM). j, A sound spectrogram of a song of a 90-day-old pupil that received an infusion of DA blockers into the CM during tutoring sessions. A sound spectrogram of the tutor song is shown in b. k, Tutor song similarity of pupil birds that received an infusion of vehicle into the HVC and birds that received infusion of DA blockers into the CM were not significantly different (Tukey–Kramer test; vehicle, n = 5; DA blockers into the CM, n = 3; at 90 days of age; P = 1.000). c, h, k, Horizontal red dashed lines show song similarity between 90-day-old untutored birds and unrelated adult male zebra finches that had been raised with normal exposure to a tutor (see Extended Data Fig. 4b, c). Data are mean ± s.e.m.

Extended Data Fig. 6 Infusion of DA blockers into Area X in juvenile males did not disrupt song copying.

a, Schematic (top) and schedule (bottom) of infusion of DA blockers into Area X. b, Sound spectrograms of a song of a tutor (top), a 90-day-old bird that received an infusion of vehicle into Area X during tutoring sessions (middle), and a 90-day-old bird that received an infusion of DA blockers into Area X during tutoring sessions (bottom). c, Tutor song similarity of pupil birds that received an infusion of vehicle into Area X and birds that received infusion of DA blockers into Area X were not significantly different. Tukey–Kramer test; vehicle, n = 4, DA blockers, n = 4; at 90 days of age; P = 1.000. The horizontal red dashed line shows song similarity between 90-day-old untutored birds and unrelated adult male zebra finches that had been raised with normal exposure to a tutor (see Extended Data Fig. 4b, c). Data are mean ± s.e.m.

Extended Data Fig. 7 Optogenetic activation of PAGHVC terminals paired with song playback.

a, Schematic (left) and schedule (right) of optogenetic stimulation of PAGHVC terminals paired with song playback. b, Sound spectrograms of song playback used in tutoring sessions (top), a song of a 90-d pupil ‘tutored’ by song playback without viral injections but with laser illumination over HVC (top middle), and 90-day-old pupils that had received optogenetic activation of PAGHVC terminals paired with song playback (bottom middle and bottom). c, From left to right, a maximum-projected image of serial sagittal sections of the PAG (left, approximately 0.5 mm lateral of the midline), showing PAG neurons expressing both ChR2 (green) and TH (pseudo-coloured magenta) (arrows), SNc (middle, approximately 0.8 mm lateral of the midline) and VTA (right, approximately 0.3 mm lateral of the midline). Similar results were obtained in six independently repeated experiments. d, Multiunit activity in the PAG, showing the time-locked response to laser stimulation at 2 Hz (top) and 20Hz (bottom). e, Schematic of optogenetic stimulation of PAGHVC terminals paired with song playback while infusing DA blockers into HVC. f, Tutor song similarity of pupils that received activation of PAGHVC terminals paired with song playback while infusing DA blockers into the HVC (red, n = 3) was not different from control birds shown in Fig. 3j (Tukey–Kramer test; at 90 days of age; P = 1.000), but lower than that received activation of PAGHVC terminals paired with song playback shown in Fig. 3j (Tukey–Kramer test; at 90 days of age; P = 0.019). g, A sound spectrogram of the song of a 90-day-old pupil that had received optogenetic activation of PAGHVC terminals paired with song playback while infusing DA blockers into the HVC. A sound spectrogram of the song playback used in tutoring sessions is shown in b. Data are mean ± s.e.m.

Extended Data Fig. 8 Action potential activity of HVC neurons in juvenile male zebra finches before and after their first exposure to live tutor songs.

a–c, Action potential activity of an HVC neuron to tutor song playback before exposure to a singing tutor (a), to live tutor songs (b) and to tutor song playback after exposure to live tutor songs (c). Top, sound spectrogram. Bottom, voltage recording. Bottom right, 50 action potentials (grey) and their mean (black). Circle, individual action potential; blue bar, tutor song motif. d, Spontaneous firing rates (FR spont) of HVC neurons of juvenile males before and after exposure to live tutor songs. Student’s two-sided paired t-test; mean firing rate before, 1.6 ± 0.3 Hz; mean firing rate after, 1.6 ± 0.4 Hz; t34 = 0.794, P = 0.433, n = 35 neurons from four birds. e, Firing rates of juvenile male HVC neurons during playback of tutor songs (FR during playback) before and after exposure to live tutor songs. Student’s two-sided paired t-test; mean firing rate before, 2.0 ± 0.6 Hz; mean firing rate after, 2.1 ± 0.6 Hz; t34 = 0.468, P = 0.643, n = 35 neurons from four birds. f, Changes in firing rates (ΔFR) of juvenile HVC neurons in response to playback of tutor songs before and after exposure to live tutor songs. Student’s two-sided paired t-test; ΔFR before, 0.5 ± 0.4 Hz; ΔFR after, 0.5 ± 0.2 Hz; t34 = 0.079, P = 0.937, n = 35 neurons from four birds.

Extended Data Fig. 9 Song rates of juvenile birds before and after their first tutoring sessions.

a, Ratio of song bouts produced before and after the first tutoring session in control birds (black, n = 6) and in birds that received an injection of 6-OHDA into the HVC several days before the tutoring session or that were infused with DA blockers into the HVC immediately before and during the tutoring session (red, n = 6). Data are mean ± s.e.m.

Extended Data Fig. 10 Summary diagram.

a, The presence of a singing tutor (that is, a suitable model) activates auditory afferent neurons and DA-releasing PAG afferent neurons to HVC, leading to potentiation and stabilization of auditory synapses in HVC. This plastic change results in temporally precise coding of the tutor song and increases the occurrence of bursting activity in the HVC, while also rapidly altering temporal and spectral features of the vocalization of a pupil in a manner that drives successful imitation of the tutor song. b, Playback of an adult male song without social cues (that is, extraneous sound) only activates auditory afferent neurons in the HVC. The activation of these auditory inputs by itself can neither alter HVC activity nor drive song learning, similar to the condition in which DA signalling in the HVC of the pupil is blocked during the exposure of a juvenile to a live, singing tutor.

Supplementary information

Supplementary Table

This file contains Summary of sample size, which shows the sample size for each experiment.

Reporting Summary

Video 1: Social interaction of a pupil with vehicle in HVC.

Social interaction of a juvenile bird that received infusion of vehicle into HVC during a tutoring session.

Video 2: Social interaction of a pupil with DA blockers in HVC.

Social interaction of a juvenile bird that received infusion of DA blockers into HVC during a tutoring session.

Video 3: Social interaction of a pupil with muscimol in PAG.

Social interaction of a juvenile bird that received infusion of muscimol into PAG during a tutoring session.

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Tanaka, M., Sun, F., Li, Y. et al. A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour. Nature 563, 117–120 (2018). https://doi.org/10.1038/s41586-018-0636-7

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